NXF3和CaMKIV在精子发生过程中的功能研究
摘要
在世界范围内大约有10%-15%的育龄夫妇正在遭受不育症的折磨。不育症夫妇中40%的男性是不育的,并且随着环境和社会等因素的影响,男性不育的比例正在逐渐增加。男性不育患者大部分为非梗阻性无精症(non-obstructive azoospermia, NOA),其病因不明,对临床治疗极为不利。随着对非梗阻性无精症的深入研究,发现男性不育与血睾屏障(Blood-testis barrier, BTB)的功能异常有关,然而导致血睾屏障功能异常的分子机制仍有待阐明。
位于生精上皮底部的支持细胞(Sertoli cell)通过彼此间的紧密连接构建血睾屏障,为精子发生提供一个稳定的微环境和独特的免疫屏障,并通过有序的开放调节精子生成。血睾屏障开放机制的异常使得精子发生的微环境和免疫屏障受损,进而影响精子生成,导致男性不育。血睾屏障的开放机制受到众多因子的调节,而TGF-β3是调节血睾屏障开放的主要因子之一,因此研究影响TGF-β3的表达和分泌的因素具有重要意义,这也是本文的第一个研究课题。
NXF3属于核输出因子蛋白家族(nuclear RNA export factor family, NXF),本文研究发现NXF3在小鼠睾丸的支持细胞中特异性地表达,并且在附睾头部、区的主细胞中也检测到NXF3的表达。在支持细胞中首次检测到NXF3的表达是小鼠出生后10天,而此时正是小鼠血睾屏障形成之时,因此NXF3极有可能与血睾屏障相关,这引起我们的极大兴趣。由于TGF-β3是参与血睾屏障调节的主要因子之一,我们检测了NXF3和TGF-β3在睾丸中的表达,发现两者之间具有负相关的关系。进一步的实验也证实了这一关系：在用热或CdC12处理小鼠睾丸后发现,NXF3的表达下降,而TGF-β3的表达上升了。随着研究的深入,发现NXF3参与调节TGF-β3转录负反馈的调控进而影响了TGF-β3的表达,即TGF-β信号通路激活后,NXF3增强了Smad2/3途径的活性,从而使TGF-P3的转录受到抑制。通过更详细的研究我们发现了NXF3的结合蛋白：STRAP, TGF-β信号通路的抑制因子。因此NXF3调节TGF-p3的机制得以阐明：TGF-β信号通路激活后,NXF3与STRAP结合,抑制了STRAP与Smad7的结合,影响了TpR1-STRAP-Smad7复合体的形成,使得Smad2/3途径激活从而抑制了TGF-β3的转录,并且Smad2/3途径的下游靶基因Claudin11、WT1、GATA1和p21也受到调控.
拟染色小体(chromatoid body)是雄性圆形精子时期出现的一个特异性结构,在电子显微镜下呈纤维状结构,主要由蛋白质和RNA组成,不含DNA。由于其含有许多RNA结合蛋白、mRNA和nicroRNA,拟染色小体被认为是精子发生过程中的RNA存储和加工中心,参与精子发生过程中的基因表达调控,因此非常引人关注。距1891年拟染色小体首次被报道,至今已有一百多年,有关拟染色小体的研究取得了很大的进展,许多拟染色小体的蛋白和RNA组分被发现,但是拟染色小体的功能和机制仍然不清楚,需要进一步的探究。
本文发现CaMKIV (Ca2+/Calmodulin-dependent Protein Kinase IV, CaMKIV)定位在拟染色小体上,是拟染色小体的一个新的组分。CaMKIV是钙调蛋白激酶家族之一,据报道CaMKIV表达在睾丸的精原细胞和精子细胞中,并且camkiv基因敲除小鼠由于在精子变形过程中组蛋白替换异常而不育。研究发现CaMKIV能够和拟染色小体中的MVH.MIWI和KIF17b相互作用,并且能够促进MVH、MIWI与KIF17b的结合。这是首次报道拟染色小体中蛋白之间的相互作用的调控模式,对理解拟染色小体的结构和功能具有重要意义。
综上所述,本文报道了NXF3调控细胞因子TGF-03在睾丸支持细胞中的表达、分泌的机制,有助于分析非梗阻性无精症患者中血睾屏障异常的原因。同时本文报道了CaMKIV作为拟染色小体的一个新的组分,能够调节拟染色小体中的蛋白质之间的相互作用,有助于拟染色小体的进一步研究。
About10%-15%couples of childbearing in the world are suffering from infertility, male factor infertility accounts for40%of infertile couples, and with the impact of environmental and social factors, the proportion of male infertility is increasing. Most of the infertile man are non-obstructive azoospermia (NOA) remained unexplained and extremely unfavorable for the clinical treatment. With the in-depth study of the non-obstructive azoospermia over the past decades, it's found that male infertility has relationship with blood-testis barrier dysfunction, however, the molecular mechanism which leads to dysfunction of the blood-testis barrier remains to be elucidated.
Blood-testis barrier is constituted by adjacent Sertoli cells in the basal compartment of the seminiferous epithelium through tight junction, provides a stable microenvironment and unique immune barrier for spermatogenesis, and regulates spermatogenesis by "opening" and "closing" orderly. Disruption of the "opening" and "closing" of blood-testis barrier will break the microenvironment and immune barrier, impaire spermatogenesis and lead to male infertility. Many factors take part in the regulation of "opening" and "closing" of blood-testis barrier, and TGF-β3is one of the important factors. It's important to clarify the expression and secretion of TGF-β3and this is the first research program be choosed.
NXF3is one of the nuclear RNA export factor family and its specific expression iwas detected in Sertoli cells of mouse testis, as well as in the principal cells in the segment II of the caput epididymis. The expression of NXF3can be first detected at10dpp, when the mouse blood-testis barrier is constituted, it arouses our great interest that NXF3maybe related to blood-testis barrier. Since TGF-β3is one of the important factors, the expressions of NXF3and TGF-β3were checked and a significant negative correlation was discoverd between the expression levels of TGF-β3and NXF3in the mouse testis. This discovery is confirmed by another experiments, the expression of NXF3was decreased while TGF-β3increased in the CdCl2-or heat-treated testes. With further research, we find that NXF3can affect the expression of TGF-β3through regulating the negative feedback of TGF-β3transcription, that is the activity of Smad2/3passway was promoted by NXF3and then the transcription of TGF-β3was depressed when the TGF-β signal passway activated. The partner of NXF3was found by detailed study, STRAP, an inhibitor of TGF-β signal passway, thus the mechanism of NXF3regulating the expression of TGF-β3could be clarified. That is when TGF-β signal passway activated, NXF3interplays with STRAP and the association of STRAP between Smad7is inhibited, and the protein comlex of TβR1(TD)-STRAP-Smad7is disrupted, so the Smad2/3passway is activated and depressed the transcription of TGF-P3, and also many target genes of the Smad2/3passway are regulated, just as Claudinll, WT1, GATA1and p21.
Chromatoid body is a male specific structure and appears as a filamentous and lobulated granule using electron microscopy. Chromatoid body contains many RNA-binding proteins and RNAs and on the basis of its structural features and composition, it is considered as a specialized form of germplasm or nuage. Thus, chromatoid body is proposed as a RNA processing center of male germ cells and regulates gene expression during spermatogenesis, and has attracted the interesting of many researchers. Over one hundred years has passed since chromatoid body was first described in1891, many proteins and RNAs were found located in chromatoid body, but the function and mechanism of chromatoid body is still unclear.
Ca2+/Calmodulin-dependent Protein Kinase IV (CaMKIV) localizes in chromatoid body and is a new component of chromatoid body reported by this study. It's been reported that CaMKIV was expressed in spermatocyte and spermatid in testis and camkiv knockout mice were sterile for the abnormal of histone proteins transition during elongated sperm. Here we report that CaMKIV can associate with chromatoid body components:MVH, MIWI and KIF17b, most importantly that CaMKIV can promote the interplay of KIF17b between MVH and MIWI. For the first time we report the regulation of proteins association in chromatoid body and this will promote the knowledge of structure and function of chromatoid body.
位于生精上皮底部的支持细胞(Sertoli cell)通过彼此间的紧密连接构建血睾屏障,为精子发生提供一个稳定的微环境和独特的免疫屏障,并通过有序的开放调节精子生成。血睾屏障开放机制的异常使得精子发生的微环境和免疫屏障受损,进而影响精子生成,导致男性不育。血睾屏障的开放机制受到众多因子的调节,而TGF-β3是调节血睾屏障开放的主要因子之一,因此研究影响TGF-β3的表达和分泌的因素具有重要意义,这也是本文的第一个研究课题。
NXF3属于核输出因子蛋白家族(nuclear RNA export factor family, NXF),本文研究发现NXF3在小鼠睾丸的支持细胞中特异性地表达,并且在附睾头部、区的主细胞中也检测到NXF3的表达。在支持细胞中首次检测到NXF3的表达是小鼠出生后10天,而此时正是小鼠血睾屏障形成之时,因此NXF3极有可能与血睾屏障相关,这引起我们的极大兴趣。由于TGF-β3是参与血睾屏障调节的主要因子之一,我们检测了NXF3和TGF-β3在睾丸中的表达,发现两者之间具有负相关的关系。进一步的实验也证实了这一关系：在用热或CdC12处理小鼠睾丸后发现,NXF3的表达下降,而TGF-β3的表达上升了。随着研究的深入,发现NXF3参与调节TGF-β3转录负反馈的调控进而影响了TGF-β3的表达,即TGF-β信号通路激活后,NXF3增强了Smad2/3途径的活性,从而使TGF-P3的转录受到抑制。通过更详细的研究我们发现了NXF3的结合蛋白：STRAP, TGF-β信号通路的抑制因子。因此NXF3调节TGF-p3的机制得以阐明：TGF-β信号通路激活后,NXF3与STRAP结合,抑制了STRAP与Smad7的结合,影响了TpR1-STRAP-Smad7复合体的形成,使得Smad2/3途径激活从而抑制了TGF-β3的转录,并且Smad2/3途径的下游靶基因Claudin11、WT1、GATA1和p21也受到调控.
拟染色小体(chromatoid body)是雄性圆形精子时期出现的一个特异性结构,在电子显微镜下呈纤维状结构,主要由蛋白质和RNA组成,不含DNA。由于其含有许多RNA结合蛋白、mRNA和nicroRNA,拟染色小体被认为是精子发生过程中的RNA存储和加工中心,参与精子发生过程中的基因表达调控,因此非常引人关注。距1891年拟染色小体首次被报道,至今已有一百多年,有关拟染色小体的研究取得了很大的进展,许多拟染色小体的蛋白和RNA组分被发现,但是拟染色小体的功能和机制仍然不清楚,需要进一步的探究。
本文发现CaMKIV (Ca2+/Calmodulin-dependent Protein Kinase IV, CaMKIV)定位在拟染色小体上,是拟染色小体的一个新的组分。CaMKIV是钙调蛋白激酶家族之一,据报道CaMKIV表达在睾丸的精原细胞和精子细胞中,并且camkiv基因敲除小鼠由于在精子变形过程中组蛋白替换异常而不育。研究发现CaMKIV能够和拟染色小体中的MVH.MIWI和KIF17b相互作用,并且能够促进MVH、MIWI与KIF17b的结合。这是首次报道拟染色小体中蛋白之间的相互作用的调控模式,对理解拟染色小体的结构和功能具有重要意义。
综上所述,本文报道了NXF3调控细胞因子TGF-03在睾丸支持细胞中的表达、分泌的机制,有助于分析非梗阻性无精症患者中血睾屏障异常的原因。同时本文报道了CaMKIV作为拟染色小体的一个新的组分,能够调节拟染色小体中的蛋白质之间的相互作用,有助于拟染色小体的进一步研究。
About10%-15%couples of childbearing in the world are suffering from infertility, male factor infertility accounts for40%of infertile couples, and with the impact of environmental and social factors, the proportion of male infertility is increasing. Most of the infertile man are non-obstructive azoospermia (NOA) remained unexplained and extremely unfavorable for the clinical treatment. With the in-depth study of the non-obstructive azoospermia over the past decades, it's found that male infertility has relationship with blood-testis barrier dysfunction, however, the molecular mechanism which leads to dysfunction of the blood-testis barrier remains to be elucidated.
Blood-testis barrier is constituted by adjacent Sertoli cells in the basal compartment of the seminiferous epithelium through tight junction, provides a stable microenvironment and unique immune barrier for spermatogenesis, and regulates spermatogenesis by "opening" and "closing" orderly. Disruption of the "opening" and "closing" of blood-testis barrier will break the microenvironment and immune barrier, impaire spermatogenesis and lead to male infertility. Many factors take part in the regulation of "opening" and "closing" of blood-testis barrier, and TGF-β3is one of the important factors. It's important to clarify the expression and secretion of TGF-β3and this is the first research program be choosed.
NXF3is one of the nuclear RNA export factor family and its specific expression iwas detected in Sertoli cells of mouse testis, as well as in the principal cells in the segment II of the caput epididymis. The expression of NXF3can be first detected at10dpp, when the mouse blood-testis barrier is constituted, it arouses our great interest that NXF3maybe related to blood-testis barrier. Since TGF-β3is one of the important factors, the expressions of NXF3and TGF-β3were checked and a significant negative correlation was discoverd between the expression levels of TGF-β3and NXF3in the mouse testis. This discovery is confirmed by another experiments, the expression of NXF3was decreased while TGF-β3increased in the CdCl2-or heat-treated testes. With further research, we find that NXF3can affect the expression of TGF-β3through regulating the negative feedback of TGF-β3transcription, that is the activity of Smad2/3passway was promoted by NXF3and then the transcription of TGF-β3was depressed when the TGF-β signal passway activated. The partner of NXF3was found by detailed study, STRAP, an inhibitor of TGF-β signal passway, thus the mechanism of NXF3regulating the expression of TGF-β3could be clarified. That is when TGF-β signal passway activated, NXF3interplays with STRAP and the association of STRAP between Smad7is inhibited, and the protein comlex of TβR1(TD)-STRAP-Smad7is disrupted, so the Smad2/3passway is activated and depressed the transcription of TGF-P3, and also many target genes of the Smad2/3passway are regulated, just as Claudinll, WT1, GATA1and p21.
Chromatoid body is a male specific structure and appears as a filamentous and lobulated granule using electron microscopy. Chromatoid body contains many RNA-binding proteins and RNAs and on the basis of its structural features and composition, it is considered as a specialized form of germplasm or nuage. Thus, chromatoid body is proposed as a RNA processing center of male germ cells and regulates gene expression during spermatogenesis, and has attracted the interesting of many researchers. Over one hundred years has passed since chromatoid body was first described in1891, many proteins and RNAs were found located in chromatoid body, but the function and mechanism of chromatoid body is still unclear.
Ca2+/Calmodulin-dependent Protein Kinase IV (CaMKIV) localizes in chromatoid body and is a new component of chromatoid body reported by this study. It's been reported that CaMKIV was expressed in spermatocyte and spermatid in testis and camkiv knockout mice were sterile for the abnormal of histone proteins transition during elongated sperm. Here we report that CaMKIV can associate with chromatoid body components:MVH, MIWI and KIF17b, most importantly that CaMKIV can promote the interplay of KIF17b between MVH and MIWI. For the first time we report the regulation of proteins association in chromatoid body and this will promote the knowledge of structure and function of chromatoid body.
引文
Angst, B.D., Marcozzi, C., and Magee, A.I. (2001). The cadherin superfamily:diversity in form and function. J Cell Sci 114,629-641.
Anton, E. (1983). Association of Golgi vesicles containing acid phosphatase with the chromatoid body of rat spermatids. Experientia 39,393-394.
Asada, M., Irie, K., Morimoto, K., Yamada, A., Ikeda, W., Takeuchi, M., and Takai, Y. (2003). ADIP, a novel Afadin- and alpha-actinin-binding protein localized at cell-cell adherens junctions. J Biol Chem 278,4103-4111.
Barad, O., Meiri, E., Avniel, A., Aharonov, R., Barzilai, A., Bentwich, I., Einav, U., Gilad, S., Hurban, P., Karov, Y., et al. (2004). MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 14,2486-2494.
Bazzoni, G. (2003). The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 15, 525-530.
Benda, C. (1891). Neue mitteilungen uber die entwickelung der genitaldrtisen und die metamorphose der samenzellen (Histogenese der Spermatozoen). Verh Berliner Physiol Ges Arch Anat Physiol 1891,549-522.
Bernstein, E., and Allis, C.D. (2005). RNA meets chromatin. Genes Dev 19,1635-1655.
Bhasin, S., de Kretser, D.M., and Baker, H.W. (1994). Clinical review 64:Pathophysiology and natural history of male infertility. J Clin Endocrinol Metab 79,1525-1529.
Biggiogera, M., Fakan, S., Leser, G., Martin, T.E., and Gordon, J. (1990). Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26,150-158.
Bloom, G.P., Fromm, D., Rosenberg, S., and Goldman, H. (1976). Attempted retrograde cannulation of the ampulla:a probable cause of mass in the pancreas. Ann Surg 183,107-108.
Bouchard, M.J., Dong, Y., McDermott, B.M., Jr., Lam, D.H., Brown, K.R., Shelanski, M., Bellve, A.R., and Racaniello, V.R. (2000). Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions. Mol Cell Biol 20,2865-2873.
Braun, R.E. (1998). Post-trans crip tional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9,483-489.
Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310,486-489.
Buzzard, J.J., Wreford, N.G., and Morrison, J.R. (2003). Thyroid hormone, retinoic acid, and testosterone suppress proliferation and induce markers of differentiation in cultured rat sertoli cells. Endocrinology 144,3722-3731.
Cai, H., Ren, Y., Li, X.X., Yang, J.L., Zhang, C.P., Chen, M., Fan, C.H., Hu, X.Q., Hu, Z.Y., Gao, F., et al. (2011). Scrotal heat stress causes a transient alteration in tight junctions and induction of TGF-beta expression. Int J Androl 34,352-362.
Cameron, D.F., Snydle, F.E., Ross, M.H., and Drylie, D.M. (1980). Ultrastructural alterations in the adluminal testicular compartment in men with varicocele. Fertil Steril 33,526-533.
Carmell, M.A., Xuan, Z., Zhang, M.Q., and Hannon, G.J. (2002). The Argonaute family:tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16, 2733-2742.
Cheng, C.Y., and Mruk, D.D. (2002). Cell junction dynamics in the testis:Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82,825-874.
Cheng, C.Y., Wong, E.W., Yan, H.H., and Mruk, D.D. (2010). Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium:new insights and advances. Mol Cell Endocrinol 315,49-56.
Chennathukuzhi, V., Morales, C.R., El-Alfy, M., and Hecht, N.B. (2003). The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP-responsive element modulator-regulated mRNAs in male germ cells. Proc Natl Acad Sci U S A100,15566-15571.
Chuma, S., Hiyoshi, M., Yamamoto, A., Hosokawa, M., Takamune, K., and Nakatsuji, N. (2003). Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120,979-990.
Clermont, Y. (1963). The cycle of the seminiferous epithelium in man. Am J Anat 112,35-51.
Coller, J., and Parker, R. (2005). General translational repression by activators of mRNA decapping. Cell 122,875-886.
Cooke, H.J., and Saunders, P.T. (2002). Mouse models of male infertility. Nat Rev Genet 3,790-801.
Cote, J., and Richard, S. (2005). Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 250,28476-28483.
Cougot, N., Babajko, S., and Seraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165,31-40.
Cruzalegui, F.H., and Means, A.R. (1993). Biochemical characterization of the multifunctional Ca2+/calmodulin-dependent protein kinase type IV expressed in insect cells. J Biol Chem 268, 26171-26178.
Cyr, D.G., Gregory, M., Dube, E., Dufresne, J., Chan, P.T., and Hermo, L. (2007). Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J Androl 9,463-475.
Daniel, J.M., and Reynolds, A.B. (1997). Tyrosine phosphorylation and cadherin/catenin function. Bioessays 19,883-891.
Datta, P.K., Chytil, A., Gorska, A.E., and Moses, H.L. (1998). Identification of STRAP, a novel WD domain protein in transforming growth factor-beta signaling. J Biol Chem 273,34671-34674.
Datta, P.K., and Moses, H.L. (2000). STRAP and Smad7 synergize in the inhibition of transforming growth factor beta signaling. Mol Cell Biol 20,3157-3167.
Deng, W., and Lin, H. (2002). miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2,819-830.
Dunson, D.B., Baird, D.D., and Colombo, B. (2004). Increased infertility with age in men and women. Obstet Gynecol 103,51-56.
Dym, M. (1994). Basement membrane regulation of Sertoli cells. Endocr Rev 15,102-115.
Dym, M., and Fawcett, D.W. (1970). The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3,308-326.
Ebnet, K., Suzuki, A., Ohno, S., and Vestweber, D. (2004). Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 117,19-29.
Fabris, F., Casonato, A., Randi, M.L., and Girolami, A. (1980). Plasma and platelet beta-thromboglobulin levels in patients with May-Hegglin anomaly. Haemostasis 9,126-130.
Fawcett, D.W., Eddy, E.M., and Phillips, D.M. (1970). Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 2,129-153.
Figueroa, J., and Burzio, L.O. (1998). Polysome-like structures in the chromatoid body of rat spermatids. Cell Tissue Res 291,575-579.
Filipowicz, W., Jaskiewicz, L., Kolb, F.A., and Pillai, R.S. (2005). Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15,331-341.
Florin, A., Maire, M., Bozec, A., Hellani, A., Chater, S., Bars, R., Chuzel, F., and Benahmed, M. (2005). Androgens and postmeiotic germ cells regulate claudin-11 expression in rat Sertoli cells. Endocrinology 146,1532-1540.
Foresta, C., Moro, E., and Ferlin, A. (2001). Y chromosome microdeletions and alterations of spermatogenesis. Endocr Rev 22,226-239.
Franca, L.R., Ogawa, T., Avarbock, M.R., Brinster, R.L., and Russell, L.D. (1998). Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 59,1371-1377.
Fukuhara, T., Shimizu, K., Kawakatsu, T., Fukuyama, T., Minami, Y., Honda, T., Hoshino, T., Yamada, T., Ogita, H., Okada, M., et al. (2004). Activation of Cdc42 by trans interactions of the cell adhesion molecules nectins through c-Src and Cdc42-GEF FRG. J Cell Biol 166,393-405.
Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., and Tsukita, S. (1993). Occludin:a novel integral membrane protein localizing at tight junctions. J Cell Biol 123,1777-1788.
Gliki, G., Ebnet, K., Aurrand-Lions, M., Imhof, B.A., and Adams, R.H. (2004). Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431,320-324.
Gonsalves, J., Sun, F., Schlegel, P.N., Turek, P.J., Hopps, C.V., Greene, C., Martin, R.H., and Pera, R.A. (2004). Defective recombination in infertile men. Hum Mol Genet 13,2875-2883.
Goodenough, D.A., Goliger, J.A., and Paul, D.L. (1996). Connexins, connexons, and intercellular communication. Annu Rev Biochem 65,475-502.
Gooding, J.M., Yap, K.L., and Ikura, M. (2004). The cadherin-catenin complex as a focal point of cell adhesion and signalling:new insights from three-dimensional structures. Bioessays 26,497-511.
Gow, A., Southwood, C.M., Li, J.S., Pariali, M., Riordan, G.P., Brodie, S.E., Danias, J., Bronstein, J.M., Kachar, B., and Lazzarini, R.A. (1999). CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99,649-659.
Griswold, M.D. (1995). Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52, 211-216.
Grivna, S.T., Pyhtila, B., and Lin, H. (2006). MTWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 103, 13415-13420.
Gruter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K., and Izaurralde, E. (1998). TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1,649-659.
Guillaud, L., Wong, R., and Hirokawa, N. (2008). Disruption of KIF17-Mintl interaction by CaMKII-dependent phosphorylation:a molecular model of kinesin-cargo release. Nat Cell Biol 10, 19-29.
Haley, B., and Zamore, P.D. (2004). Kinetic analysis of the RNAi enzyme complex. Nat Struct Mol Biol 11,599-606.
Haraguchi, C.M., Mabuchi, T., Hirata, S., Shoda, T., Hoshi, K., Akasaki, K., and Yokota, S. (2005). Chromatoid bodies:aggresome-like characteristics and degradation sites for organelles of spermiogenic cells. J Histochem Cytochem 53,455-465.
Head, J.R., and Kresge, C.K. (1985). Reaction of the chromatoid body with a monoclonal antibody to a rat histocompatibility antigen. Biol Reprod 33,1001-1008.
Hellani, A., Ji, J., Mauduit, C., Deschildre, C., Tabone, E., and Benahmed, M. (2000). Developmental and hormonal regulation of the expression of oligodendrocyte-specific protein/claudin 11 in mouse testis. Endocrinology 141,3012-3019.
Hermann, F. (1889). Beitrage zur Histologie des Hodens. Arch mikr Anat 34,58-105.
Herold, A., Suyama, M., Rodrigues, J.P., Braun, I.C., Kutay, U., Carmo-Fonseca, M., Bork, P., and Izaurralde, E. (2000). TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol 20,8996-9008.
Hess, R.A., Miller, L.A., Kirby, J.D., Margoliash, E., and Goldberg, E. (1993). Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol Reprod 48,1299-1308.
Hinton, B.T., and Palladino, M.A. (1995). Epididymal epithelium:its contribution to the formation of a luminal fluid microenvironment. Microsc Res Tech 30,67-81.
Hirabayashi, S., Tajima, M., Yao, I., Nishimura, W., Mori, H., and Hata, Y. (2003). JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 23, 4267-4282.
Hunter, D., Anand-Ivell, R., Danner, S., and Ivell, R. (2012). Models of in vitro spermatogenesis. Spermatogenesis 2,32-43.
Janecki, A., Jakubowiak, A., and Steinberger, A. (1991). Regulation of transepithelial electrical resistance in two-compartment Sertoli cell cultures:in vitro model of the blood-testis barrier. Endocrinology 129,1489-1496.
Jin, L., Guzik, B.W., Bor, Y.C., Rekosh, D., and Hammarskjold, M.L. (2003). Tap and NXT promote translation of unspliced mRNA. Genes Dev 17,3075-3086.
Johnson, K. J., and Boekelheide, K. (2002). Dynamic testicular adhesion junctions are immunologically unique. Ⅰ. Localization of p120 catenin in rat testis. Biol Reprod 66,983-991.
Johnson, K.J., Patel, S.R., and Boekelheide, K. (2000). Multiple cadherin superfamily members with unique expression profiles are produced in rat testis. Endocrinology 141,675-683.
Jonk, L.J., Itoh, S., Heldin, C.H., ten Dijke, P., and Kruijer, W. (1998). Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J Biol Chem 273,21145-21152.
Jun, L., Frints, S., Duhamel, H., Herold, A., Abad-Rodrigues, J., Dotti, C., Izaurralde, E., Marynen, P., and Froyen, G. (2001). NXF5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation. Curr Biol 11,1381-1391.
Kang, Y.B., and Cullen, B.R. (1999). The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev 13, 1126-1139.
Katahira, J., Strasser, K., Podtelejnikov, A., Mann, M, Jung, J.U., and Hurt, E. (1999). The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. Embo J 18, 2593-2609.
Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D. Kaufman, R.J., Golan, D.E., and Anderson, P. (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169,871-884.
Kleene, K.C. (1993). Multiple controls over the efficiency of translation of the mRNAs encoding transition proteins, protamines, and the mitochondrial capsule selenoprotein in late spermatids in mice. Dev Biol 159,720-731.
Komori, K., Tsujimura, A., Miura, H., Shin, M., Takada, T., Honda, M., Matsumiya, K., and Fujioka, H. (2004). Serial follow-up study of serum testosterone and antisperm antibodies in patients with non-obstructive azoospermia after conventional or microdissection testicular sperm extraction. Int J Androl 27,32-36.
Kopera, I.A., Bilinska, B., Cheng, C.Y., and Mruk, D.D. (2010). Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365,1593-1605.
Kotaja, N., Bhattacharyya, S.N., Jaskiewicz, L., Kimmins, S., Parvinen, M., Filipowicz, W., and Sassone-Corsi, P. (2006a). The chromatoid body of male germ cells:similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 103, 2647-2652.
Kotaja, N., Kimmins, S., Brancorsini, S., Hentsch, D., Vonesch, J.L., Davidson, Ⅰ., Parvinen, M., and Sassone-Corsi, P. (2004). Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1,249-254.
Kotaja, N., Lin, H., Parvinen, M., and Sassone-Corsi, P. (2006b). Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119,2819-2825.
Kotaja, N., Macho, B., and Sassone-Corsi, P. (2005). Microtubule-independent and protein kinase A-mediated function of kinesin KIF17b controls the intracellular transport of activator of CREM in testis (ACT). J Biol Chem 280,31739-31745.
Kotaja, N., and Sassone-Corsi, P. (2007). The chromatoid body:a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8,85-90.
Krawetz, S.A. (2005). Paternal contribution:new insights and future challenges. Nat Rev Genet 6, 633-642.
Krimer, D.B., and Esponda, P. (1980). Presence of polysaccharides and proteins in the chromatoid body of mouse spermatids. Cell Biol Int Rep 4,265-270.
Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., et al. (2004). Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131,839-849.
Lamb, D.J., Kessler, M.J., Shewach, D.S., Steinberger, A., and Sanborn, B.M. (1982). Characterization of Sertoli cell RNA synthetic activities in vitro at selected times during sexual maturation. Biol Reprod 27,374-382.
Landon, G.V., and Pryor, J.P. (1981). The blood-testis barrier in men of diverse fertility status:an ultrastructural study. Virchows Arch A Pathol Anat Histol 392,355-364.
Law, G.L., and Griswold, M.D. (1994). Activity and form of sulfated glycoprotein 2 (clusterin) from cultured Sertoli cells, testis, and epididymis of the rat. Biol Reprod 50,669-679.
Lee, H., Ogawa, H., Fujioka, M., and Gerton, G.L. (1994). Guanidinoacetate methyltransferase in the mouse:extensive expression in Sertoli cells of testis and in microvilli of caput epididymis. Biol Reprod 50,152-162.
Lee, N.P., Mruk, D., Lee, W.M., and Cheng, C.Y. (2003). Is the cadherin/catenin complex a functional unit of cell-cell actin-based adherens junctions in the rat testis? Biol Reprod 68,489-508.
Lee, N.P., Mruk, D.D., Conway, A.M., and Cheng, C.Y. (2004). Zyxin, axin, and Wiskott-Aldrich syndrome protein are adaptors that link the cadherin/catenin protein complex to the cytoskeleton at adherens junctions in the seminiferous epithelium of the rat testis. J Androl 25,200-215.
Lee, N.P., Wong, E.W., Mruk, D.D., and Cheng, C.Y. (2009). Testicular cell junction:a novel target for male contraception. Curr Med Chem 16,906-915.
Lenhossek, M. (1898). Untersuchungen uber Spermatogenese. Arch Micr Anat 51,215-318.
Li, Y., Friel, P.J., Robinson, M.O., McLean, D.J., and Griswold, M.D. (2002). Identification and characterization of testis-and epididymis-specific genes:cystatin SC and cystatin TE-1. Biol Reprod 67,1872-1880.
Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R.,3rd, Parker, R., and Hannon, G.J. (2005a). A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7,1261-1266.
Liu, J., Valencia-Sanchez, M.A., Hannon, G.J., and Parker, R. (2005b). MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7,719-723.
Lui, W.Y., and Cheng, C.Y. (2007). Regulation of cell junction dynamics by cytokines in the testis:a molecular and biochemical perspective. Cytokine Growth Factor Rev 18,299-311.
Lui, W.Y., Lee, W.M., and Cheng, C.Y. (2001). Transforming growth factor-beta3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology 142,1865-1877.
Lui, W.Y., Lee, W.M., and Cheng, C.Y. (2003a). TGF-betas:their role in testicular function and Sertoli cell tight junction dynamics. Int J Androl 26,147-160.
Lui, W.Y., Wong, C.H., Mruk, D.D., and Cheng, C.Y. (2003b). TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway:an in vivo study. Endocrinology 144,1139-1142.
Macho, B., Brancorsini, S., Fimia, G.M., Setou, M., Hirokawa, N., and Sassone-Corsi, P. (2002). CREM-dependent transcription in male germ cells controlled by a kinesin. Science 298, 2388-2390.
Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A., et al. (1998). Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142,117-127.
McLachlan, R.I., Rajpert-De Meyts, E., Hoei-Hansen, C.E., de Kretser, D.M., and Skakkebaek, N.E. (2007). Histological evaluation of the human testis-approaches to optimizing the clinical value of the assessment:mini review. Hum Reprod 22,2-16.
Meng, J., Holdcraft, R.W., Shima, J.E., Griswold, M.D., and Braun, R.E. (2005). Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci U S A 102,16696-16700.
Moch, H., Schraml, P., Bubendorf, L., Richter, J., Gasser, T.C., Mihatsch, M.J., and Sauter, G. (1998). Intratumoral heterogeneity of von Hippel-Lindau gene deletions in renal cell carcinoma detected by fluorescence in situ hybridization. Cancer Res 58,2304-2309.
Morita, K., Sasaki, H., Fujimoto, K., Furuse, M., and Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145,379-588.
Moussa, F., Oko, R., and Hermo, L. (1994). The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278,363-378.
Moustakas, A., Souchelnytskyi, S., and Heldin, C.H. (2001). Smad regulation in TGF-beta signal transduction. J Cell Sci 114,4359-4369.
Mruk, D.D., and Cheng, C.Y. (2004). Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25,747-806.
Mruk, D.D., and Cheng, C.Y. (2010). Tight junctions in the testis:new perspectives. Philos Trans R Soc Lond B Biol Sci 365,1621-1635.
Mruk, D.D., Silvestrini, B., and Cheng, C.Y. (2008). Anchoring junctions as drug targets:role in contraceptive development. Pharmacol Rev 60,146-180.
Mueller, S., Rosenquist, T.A., Takai, Y., Bronson, R.A., and Wimmer, E. (2003). Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration. Biol Reprod 69,1330-1340.
Nagamori, Ⅰ., Cruickshank, V.A., and Sassone-Corsi, P. (2012). Regulation of an RNA granule during spermatogenesis:acetylation of MVH in the chromatoid body of germ cells. J Cell Sci.
Nakao, A., Afrakhte, M., Moren, A., Nakayama, T., Christian, J.L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N.E., Heldin, C.H., et al. (1997). Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389,631-635.
Namiki, M. (2000). Genetic aspects of male infertility. World J Surg 24,1176-1179.
Noce, T., Okamoto-Ito, S., and Tsunekawa, N. (2001). Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 26,131-136.
Olsen, L.C., Aasland, R., and Fjose, A. (1997). A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66,95-105.
Ou, J.P., and Zhuang, G.L. (2003). Effect of antisperm antibodies on assisted reproduction. Zhonghua Nan Ke Xue 9,214-217.
Ozaki-Kuroda, K., Nakanishi, H., Ohta, H., Tanaka, H., Kurihara, H., Mueller, S., Irie, K., Ikeda, W., Sakai, T., Wimmer, E., et al. (2002). Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12,1145-1150.
Page, D.C., Silber, S., and Brown, L.G. (1999). Men with infertility caused by AZFc deletion can produce sons by intracytoplasmic sperm injection, but are likely to transmit the deletion and infertility. Hum Reprod 14,1722-1726.
Palermo, G., Joris, H., Devroey, P., and Van Steirteghem, A.C. (1992). Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340,17-18.
Pan, J., Eckardt, S., Leu, N.A., Buffone, M.G., Zhou, J., Gerton, G.L., McLaughlin, K.J., and Wang, P.J. (2009). Inactivation of Nxf2 causes defects in male meiosis and age-dependent depletion of spermatogonia. Dev Biol 330,167-174.
Paniagua, R., Nistal, M., Amat, P., and Rodriguez, M.C. (1985). Presence of ribonucleoproteins and basic proteins in the nuage and intermitochondrial bars of human spermatogonia. J Anat 143, 201-206.
Parvinen, M., and Parvinen, L.M. (1979). Active movements of the chromatoid body. A possible transport mechanism for haploid gene products. J Cell Biol 80,621-628.
Peinado, H., Portillo, F., and Cano, A. (2004). Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 48,365-375.
Perez-Moreno, M., Jamora, C., and Fuchs, E. (2003). Sticky business:orchestrating cellular signals at adherens junctions. Cell 112,535-548.
Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309,1573-1576.
Rao, M.K., Pham, J., Imam, J.S., MacLean, J.A., Murali, D., Furuta, Y., Sinha-Hikim, A.P., and Wilkinson, M.F. (2006). Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 20,147-152.
Reymond, N., Fabre, S., Lecocq, E., Adelaide, J., Dubreuil, P., and Lopez, M. (2001). Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectinl/PRRl through V domain interaction. J Biol Chem 276,43205-43215.
Rossi, J.J. (2005). RNAi and the P-body connection. Nat Cell Biol 7,643-644.
Rouelle-Rossier, V.B., Biggiogera, M., and Fakan, S. (1993). Ultrastructural detection of calcium and magnesium in the chromatoid body of mouse spermatids by electron spectroscopic imaging and electron energy loss spectroscopy. J Histochem Cytochem 41,1155-1162.
Russell, L. (1977). Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148,313-328.
Saitou, M., Furuse, M., Sasaki, H., Schulzke, J.D., Fromm, M., Takano, H., Noda, T., and Tsukita, S. (2000). Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11,4131-4142.
Sasaki, M., Takeda, E., Takano, K., Yomogida, K., Katahira, J., and Yoneda, Y. (2005). Molecular cloning and functional characterization of mouse Nxf family gene products. Genomics 85, 641-653.
Sassone-Corsi, P. (1997). Transcriptional checkpoints determining the fate of male germ cells. Cell 88, 163-166.
Sassone-Corsi, P. (2002). Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296,2176-2178.
Satoh-Horikawa, K., Nakanishi, H., Takahashi, K., Miyahara, M., Nishimura, M., Tachibana, K., Mizoguchi, A., and Takai, Y. (2000). Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J Biol Chem 275,10291-10299.
Saunders, P.T., Millar, M.R., Maguire, S.M., and Sharpe, R.M. (1992). Stage-specific expression of rat transition protein 2 mRNA and possible localization to the chromatoid body of step 7 spermatids by in situ hybridization using a nonradioactive riboprobe. Mol Reprod Dev 33,385-391.
Segref, A., Sharma, K., Doye, V., Hellwig, A., Huber, J., Luhrmann, R., and Hurt, E. (1997). Mex67p, a novel factor for nuclear inRNA export, binds to both poly(A)(+) RNA and nuclear pores. Embo J 16,3256-3271.
Sen, G.L., and Blau, H.M. (2005). Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat Cell Biol 7,633-636.
Serjeantson, S. (1975). Marriage patterns and fertility in three Papua New Guinean populations. Hum Biol 47,399-413.
Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300,805-808.
Shibata, N., Tsunekawa, N., Okamoto-Ito, S., Akasu, R., Tokumasu, A., and Noce, T. (2004). Mouse RanBPM is a partner gene to a germline specific RNA helicase, mouse vasa homolog protein. Mol Reprod Dev 67,1-7.
Siu, M.K., and Cheng, C.Y. (2004a). Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 26,978-992.
Siu, M.K., and Cheng, C.Y. (2004b). Interactions of proteases, protease inhibitors, and the betal integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 70,945-964.
Siu, M.K., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2003). Adhering junction dynamics in the testis are regulated by an interplay of beta 1-integrin and focal adhesion complex-associated proteins. Endocrinology 144,2141-2163.
Soderstrom, K.O., and Parvinen, M. (1976). Incorporation of (3H)uridine by the chromatoid body during rat spermatogenesis. J Cell Biol 70,239-246.
Sontheimer, E.J. (2005). Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol 6, 127-138.
Sun, F., Turek, P., Greene, C, Ko, E., Rademaker, A., and Martin, R.H. (2007). Abnormal progression through meiosis in men with nonobstructive azoospermia. Fertil Steril 87,565-571.
Tachibana, K., Nakanishi, H., Mandai, K., Ozaki, K., Ikeda, W., Yamamoto, Y., Nagafuchi, A., Tsukita, S., and Takai, Y. (2000). Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J Cell Biol 150,1161-1176.
Takahashi, K., Nakanishi, H., Miyahara, M., Mandai, K., Satoh, K., Satoh, A., Nishioka, H., Aoki, J., Nomoto, A., Mizoguchi, A., et al. (1999). Nectin/PRR:an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol 145,539-549.
Takai, Y., Irie, K., Shimizu, K., Sakisaka, T., and Ikeda, W. (2003). Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci 94,655-667.
Takai, Y., and Nakanishi, H. (2003). Nectin and afadin:novel organizers of intercellular junctions. J Cell Sci 116,17-27.
Takano, K., Miki, T., Katahira, J., and Yoneda, Y. (2007). NXF2 is involved in cytoplasmic mRNA dynamics through interactions with motor proteins. Nucleic Acids Res 35,2513-2521.
Tan, W., Zolotukhin, A.S., Bear, J., Patenaude, D.J., and Felber, B.K. (2000). The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA-Publ RNA Soc 6,1762-1772.
Tan, W., Zolotukhin, A.S., Tretyakova, I., Bear, J., Lindtner, S., Smulevitch, S.V., and Felber, B.K. (2005). Identification and characterization of the mouse nuclear export factor (Nxf) family members. Nucleic Acids Res 33,3855-3865.
Tanaka, S.S., Toyooka, Y., Akasu, R., Katoh-Fukui, Y., Nakahara, Y., Suzuki, R., Yokoyama, M., and Noce, T. (2000). The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 14,841-853.
Tang, X.M., Lalli, M.F., and Clermont, Y. (1982). A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am J Anat 163,283-294.
Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., and Parker, R. (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11,371-382.
Thorne-Tjomsland, G., Clermont, Y., and Hermo, L. (1988). Contribution of the Golgi apparatus components to the formation of the acrosomic system and chromatoid body in rat spermatids. Anat Rec 221,591-598.
Toyooka, Y., Tsunekawa, N., Takahashi, Y., Matsui, Y., Satoh, M., and Noce, T. (2000). Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93,139-149.
Tretyakova, Ⅰ., Zolotukhin, A.S., Tan, W., Bear, J., Propst, F., Ruthel, G., and Felber, B.K. (2005). Nuclear export factor family protein participates in cytoplasmic mRNA trafficking. J Biol Chem 250,31981-31990.
Tsai-Morris, C.H., Sheng, Y., Lee, E., Lei, K.J., and Dufau, M.L. (2004). Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis. Proc Natl Acad Sci U S A 101,6373-6378.
Turksen, K., and Troy, T.C. (2004). Barriers built on claudins. J Cell Sci 117,2435-2447.
Vagin, V.V., Wohlschlegel, J., Qu, J., Jonsson, Z., Huang, X., Chuma, S., Girard, A., Sachidanandam, R., Hannon, G.J., and Aravin, A.A. (2009). Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23, 1749-1762.
Vanmarsenille, L., Verbeeck, J., Belet, S., Roebroek, A.J., Van de Putte, T., Nevelsteen, J., Callaerts-Vegh, Z., D'Hooge, R., Marynen, P., and Froyen, G. (2013). Generation and characterization of an Nxf7 knockout mouse to study NXF5 deficiency in a patient with intellectual disability. PLoS One 8, e64144.
Ventela, S., Toppari, J., and Parvinen, M. (2003). Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat:mechanisms of haploid gene product sharing. Mol Biol Cell 14,2768-2780.
Walt, H., and Armbruster, B.L. (1984). Actin and RNA are components of the chromatoid bodies in spermatids of the rat. Cell Tissue Res 236,487-490.
Werner, G., and Werner, K. (1995). Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids. J Submicrosc Cytol Pathol 27,325-330.
Wheelock, M.J., and Johnson, K..R. (2003a). Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15,509-514.
Wheelock, M.J., and Johnson, K.R. (2003b). Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 19,207-235.
Wieser, R., Wrana, J.L., and Massague, J. (1995). GS domain mutations that constitutively activate T beta R-Ⅰ, the downstream signaling component in the TGF-beta receptor complex. EMBO J 14, 2199-2208.
Wilkie, G.S., Zimyanin, V., Kirby, R., Korey, C., Francis-Lang, H., Van Vactor, D., and Davis, Ⅰ. (2001). Small bristles, the Drosophila ortholog of NXF-1, is essential for mRNA export throughout development. RNA 7,1781-1792.
Wine, R.N., and Chapin, R.E. (1999). Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 20,198-213.
Wong, C.H., and Cheng, C.Y. (2005). Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis:a review of recent data. Dev Biol 286,1-15.
Wong, C.H., Mruk, D.D., Lui, W.Y., and Cheng, C.Y. (2004). Regulation of blood-testis barrier dynamics:an in vivo study. J Cell Sci 117,783-798.
Wong, E.W., and Cheng, C.Y. (2009). Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 278,309-353.
Wu, J.Y., and Means, A.R. (2000). Ca(2+)/calmodulin-dependent protein kinase IV is expressed in spermatids and targeted to chromatin and the nuclear matrix. J Biol Chem 275,7994-7999.
Xia, W., and Cheng, C.Y. (2005). TGF-beta3 regulates anchoring junction dynamics in the seminiferous epithelium of the rat testis via the Ras/ERK signaling pathway:An in vivo study. Dev Biol 280,321-343.
Xia, W., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2005a). Cytokines and junction restructuring during spermatogenesis--a lesson to learn from the testis. Cytokine Growth Factor Rev 16, 469-493.
Xia, W., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2006). Differential interactions between transforming growth factor-beta3/TbetaRl, TAB1, and CD2AP disrupt blood-testis barrier and Sertoli-germ cell adhesion. J Biol Chem 281,16799-16813.
Xia, W., Wong, C.H., Lee, N.P., Lee, W.M., and Cheng, C.Y. (2005b). Disruption of Sertoli-germ cell adhesion function in the seminiferous epithelium of the rat testis can be limited to adherens junctions without affecting the blood-testis barrier integrity:an in vivo study using an androgen suppression model. J Cell Physiol 205,141-157.
Xia, W., Wong, E.W., Mruk, D.D., and Cheng, C.Y. (2009). TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins:a new concept of BTB regulation during spermatogenesis. Dev Biol 327, 48-61.
Yagi, T., and Takeichi, M. (2000). Cadherin superfamily genes:functions, genomic organization, and neurologic diversity. Genes Dev 14,1169-1180.
Yan, H.H., and Cheng, C.Y. (2005). Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci U S A102,11722-11727.
Yang, J., Bogerd, H.P., Wang, P.J., Page, D.C., and Cullen, B.R. (2001). Two closely related human nuclear export factors utilize entirely distinct export pathways. Mol Cell 8,397-406.
Yokota, S. (2008). Historical survey on chromatoid body research. Acta Histochem Cytochem 41, 65-82.
Yomogida, K., Ohtani, H., Harigae, H., Ito, E., Nishimune, Y., Engel, J.D., and Yamamoto, M. (1994). Developmental stage-and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 120,1759-1766.
Yu, Z., Raabe, T., and Hecht, N.B. (2005). MicroRNA Mirnl22a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod 73,427-433.
Zamore, P.D., and Haley, B. (2005). Ribo-gnome:the big world of small RNAs. Science 309, 1519-1524.
Zhang, X., Wheeler, D., Tang, Y., Guo, L., Shapiro, R.A., Ribar, T.J., Means, A.R., Billiar, T.R., Angus, D.C., and Rosengart, M.R. (2008). Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages. J Immunol 181,5015-5023.
Zhou, J., Pan, J., Eckardt, S., Leu, N.A., McLaughlin, K.J., and Wang, P.J. (2011). Nxf3 is expressed in Sertoli cells, but is dispensable for spermatogenesis. Mol Reprod Dev 78,241-249.
Anton, E. (1983). Association of Golgi vesicles containing acid phosphatase with the chromatoid body of rat spermatids. Experientia 39,393-394.
Asada, M., Irie, K., Morimoto, K., Yamada, A., Ikeda, W., Takeuchi, M., and Takai, Y. (2003). ADIP, a novel Afadin- and alpha-actinin-binding protein localized at cell-cell adherens junctions. J Biol Chem 278,4103-4111.
Barad, O., Meiri, E., Avniel, A., Aharonov, R., Barzilai, A., Bentwich, I., Einav, U., Gilad, S., Hurban, P., Karov, Y., et al. (2004). MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 14,2486-2494.
Bazzoni, G. (2003). The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 15, 525-530.
Benda, C. (1891). Neue mitteilungen uber die entwickelung der genitaldrtisen und die metamorphose der samenzellen (Histogenese der Spermatozoen). Verh Berliner Physiol Ges Arch Anat Physiol 1891,549-522.
Bernstein, E., and Allis, C.D. (2005). RNA meets chromatin. Genes Dev 19,1635-1655.
Bhasin, S., de Kretser, D.M., and Baker, H.W. (1994). Clinical review 64:Pathophysiology and natural history of male infertility. J Clin Endocrinol Metab 79,1525-1529.
Biggiogera, M., Fakan, S., Leser, G., Martin, T.E., and Gordon, J. (1990). Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26,150-158.
Bloom, G.P., Fromm, D., Rosenberg, S., and Goldman, H. (1976). Attempted retrograde cannulation of the ampulla:a probable cause of mass in the pancreas. Ann Surg 183,107-108.
Bouchard, M.J., Dong, Y., McDermott, B.M., Jr., Lam, D.H., Brown, K.R., Shelanski, M., Bellve, A.R., and Racaniello, V.R. (2000). Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions. Mol Cell Biol 20,2865-2873.
Braun, R.E. (1998). Post-trans crip tional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9,483-489.
Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310,486-489.
Buzzard, J.J., Wreford, N.G., and Morrison, J.R. (2003). Thyroid hormone, retinoic acid, and testosterone suppress proliferation and induce markers of differentiation in cultured rat sertoli cells. Endocrinology 144,3722-3731.
Cai, H., Ren, Y., Li, X.X., Yang, J.L., Zhang, C.P., Chen, M., Fan, C.H., Hu, X.Q., Hu, Z.Y., Gao, F., et al. (2011). Scrotal heat stress causes a transient alteration in tight junctions and induction of TGF-beta expression. Int J Androl 34,352-362.
Cameron, D.F., Snydle, F.E., Ross, M.H., and Drylie, D.M. (1980). Ultrastructural alterations in the adluminal testicular compartment in men with varicocele. Fertil Steril 33,526-533.
Carmell, M.A., Xuan, Z., Zhang, M.Q., and Hannon, G.J. (2002). The Argonaute family:tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis. Genes Dev 16, 2733-2742.
Cheng, C.Y., and Mruk, D.D. (2002). Cell junction dynamics in the testis:Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82,825-874.
Cheng, C.Y., Wong, E.W., Yan, H.H., and Mruk, D.D. (2010). Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium:new insights and advances. Mol Cell Endocrinol 315,49-56.
Chennathukuzhi, V., Morales, C.R., El-Alfy, M., and Hecht, N.B. (2003). The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP-responsive element modulator-regulated mRNAs in male germ cells. Proc Natl Acad Sci U S A100,15566-15571.
Chuma, S., Hiyoshi, M., Yamamoto, A., Hosokawa, M., Takamune, K., and Nakatsuji, N. (2003). Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120,979-990.
Clermont, Y. (1963). The cycle of the seminiferous epithelium in man. Am J Anat 112,35-51.
Coller, J., and Parker, R. (2005). General translational repression by activators of mRNA decapping. Cell 122,875-886.
Cooke, H.J., and Saunders, P.T. (2002). Mouse models of male infertility. Nat Rev Genet 3,790-801.
Cote, J., and Richard, S. (2005). Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 250,28476-28483.
Cougot, N., Babajko, S., and Seraphin, B. (2004). Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165,31-40.
Cruzalegui, F.H., and Means, A.R. (1993). Biochemical characterization of the multifunctional Ca2+/calmodulin-dependent protein kinase type IV expressed in insect cells. J Biol Chem 268, 26171-26178.
Cyr, D.G., Gregory, M., Dube, E., Dufresne, J., Chan, P.T., and Hermo, L. (2007). Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J Androl 9,463-475.
Daniel, J.M., and Reynolds, A.B. (1997). Tyrosine phosphorylation and cadherin/catenin function. Bioessays 19,883-891.
Datta, P.K., Chytil, A., Gorska, A.E., and Moses, H.L. (1998). Identification of STRAP, a novel WD domain protein in transforming growth factor-beta signaling. J Biol Chem 273,34671-34674.
Datta, P.K., and Moses, H.L. (2000). STRAP and Smad7 synergize in the inhibition of transforming growth factor beta signaling. Mol Cell Biol 20,3157-3167.
Deng, W., and Lin, H. (2002). miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2,819-830.
Dunson, D.B., Baird, D.D., and Colombo, B. (2004). Increased infertility with age in men and women. Obstet Gynecol 103,51-56.
Dym, M. (1994). Basement membrane regulation of Sertoli cells. Endocr Rev 15,102-115.
Dym, M., and Fawcett, D.W. (1970). The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3,308-326.
Ebnet, K., Suzuki, A., Ohno, S., and Vestweber, D. (2004). Junctional adhesion molecules (JAMs): more molecules with dual functions? J Cell Sci 117,19-29.
Fabris, F., Casonato, A., Randi, M.L., and Girolami, A. (1980). Plasma and platelet beta-thromboglobulin levels in patients with May-Hegglin anomaly. Haemostasis 9,126-130.
Fawcett, D.W., Eddy, E.M., and Phillips, D.M. (1970). Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 2,129-153.
Figueroa, J., and Burzio, L.O. (1998). Polysome-like structures in the chromatoid body of rat spermatids. Cell Tissue Res 291,575-579.
Filipowicz, W., Jaskiewicz, L., Kolb, F.A., and Pillai, R.S. (2005). Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15,331-341.
Florin, A., Maire, M., Bozec, A., Hellani, A., Chater, S., Bars, R., Chuzel, F., and Benahmed, M. (2005). Androgens and postmeiotic germ cells regulate claudin-11 expression in rat Sertoli cells. Endocrinology 146,1532-1540.
Foresta, C., Moro, E., and Ferlin, A. (2001). Y chromosome microdeletions and alterations of spermatogenesis. Endocr Rev 22,226-239.
Franca, L.R., Ogawa, T., Avarbock, M.R., Brinster, R.L., and Russell, L.D. (1998). Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 59,1371-1377.
Fukuhara, T., Shimizu, K., Kawakatsu, T., Fukuyama, T., Minami, Y., Honda, T., Hoshino, T., Yamada, T., Ogita, H., Okada, M., et al. (2004). Activation of Cdc42 by trans interactions of the cell adhesion molecules nectins through c-Src and Cdc42-GEF FRG. J Cell Biol 166,393-405.
Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S., and Tsukita, S. (1993). Occludin:a novel integral membrane protein localizing at tight junctions. J Cell Biol 123,1777-1788.
Gliki, G., Ebnet, K., Aurrand-Lions, M., Imhof, B.A., and Adams, R.H. (2004). Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431,320-324.
Gonsalves, J., Sun, F., Schlegel, P.N., Turek, P.J., Hopps, C.V., Greene, C., Martin, R.H., and Pera, R.A. (2004). Defective recombination in infertile men. Hum Mol Genet 13,2875-2883.
Goodenough, D.A., Goliger, J.A., and Paul, D.L. (1996). Connexins, connexons, and intercellular communication. Annu Rev Biochem 65,475-502.
Gooding, J.M., Yap, K.L., and Ikura, M. (2004). The cadherin-catenin complex as a focal point of cell adhesion and signalling:new insights from three-dimensional structures. Bioessays 26,497-511.
Gow, A., Southwood, C.M., Li, J.S., Pariali, M., Riordan, G.P., Brodie, S.E., Danias, J., Bronstein, J.M., Kachar, B., and Lazzarini, R.A. (1999). CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99,649-659.
Griswold, M.D. (1995). Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52, 211-216.
Grivna, S.T., Pyhtila, B., and Lin, H. (2006). MTWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 103, 13415-13420.
Gruter, P., Tabernero, C., von Kobbe, C., Schmitt, C., Saavedra, C., Bachi, A., Wilm, M., Felber, B.K., and Izaurralde, E. (1998). TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1,649-659.
Guillaud, L., Wong, R., and Hirokawa, N. (2008). Disruption of KIF17-Mintl interaction by CaMKII-dependent phosphorylation:a molecular model of kinesin-cargo release. Nat Cell Biol 10, 19-29.
Haley, B., and Zamore, P.D. (2004). Kinetic analysis of the RNAi enzyme complex. Nat Struct Mol Biol 11,599-606.
Haraguchi, C.M., Mabuchi, T., Hirata, S., Shoda, T., Hoshi, K., Akasaki, K., and Yokota, S. (2005). Chromatoid bodies:aggresome-like characteristics and degradation sites for organelles of spermiogenic cells. J Histochem Cytochem 53,455-465.
Head, J.R., and Kresge, C.K. (1985). Reaction of the chromatoid body with a monoclonal antibody to a rat histocompatibility antigen. Biol Reprod 33,1001-1008.
Hellani, A., Ji, J., Mauduit, C., Deschildre, C., Tabone, E., and Benahmed, M. (2000). Developmental and hormonal regulation of the expression of oligodendrocyte-specific protein/claudin 11 in mouse testis. Endocrinology 141,3012-3019.
Hermann, F. (1889). Beitrage zur Histologie des Hodens. Arch mikr Anat 34,58-105.
Herold, A., Suyama, M., Rodrigues, J.P., Braun, I.C., Kutay, U., Carmo-Fonseca, M., Bork, P., and Izaurralde, E. (2000). TAP (NXF1) belongs to a multigene family of putative RNA export factors with a conserved modular architecture. Mol Cell Biol 20,8996-9008.
Hess, R.A., Miller, L.A., Kirby, J.D., Margoliash, E., and Goldberg, E. (1993). Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol Reprod 48,1299-1308.
Hinton, B.T., and Palladino, M.A. (1995). Epididymal epithelium:its contribution to the formation of a luminal fluid microenvironment. Microsc Res Tech 30,67-81.
Hirabayashi, S., Tajima, M., Yao, I., Nishimura, W., Mori, H., and Hata, Y. (2003). JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGI-1. Mol Cell Biol 23, 4267-4282.
Hunter, D., Anand-Ivell, R., Danner, S., and Ivell, R. (2012). Models of in vitro spermatogenesis. Spermatogenesis 2,32-43.
Janecki, A., Jakubowiak, A., and Steinberger, A. (1991). Regulation of transepithelial electrical resistance in two-compartment Sertoli cell cultures:in vitro model of the blood-testis barrier. Endocrinology 129,1489-1496.
Jin, L., Guzik, B.W., Bor, Y.C., Rekosh, D., and Hammarskjold, M.L. (2003). Tap and NXT promote translation of unspliced mRNA. Genes Dev 17,3075-3086.
Johnson, K. J., and Boekelheide, K. (2002). Dynamic testicular adhesion junctions are immunologically unique. Ⅰ. Localization of p120 catenin in rat testis. Biol Reprod 66,983-991.
Johnson, K.J., Patel, S.R., and Boekelheide, K. (2000). Multiple cadherin superfamily members with unique expression profiles are produced in rat testis. Endocrinology 141,675-683.
Jonk, L.J., Itoh, S., Heldin, C.H., ten Dijke, P., and Kruijer, W. (1998). Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J Biol Chem 273,21145-21152.
Jun, L., Frints, S., Duhamel, H., Herold, A., Abad-Rodrigues, J., Dotti, C., Izaurralde, E., Marynen, P., and Froyen, G. (2001). NXF5, a novel member of the nuclear RNA export factor family, is lost in a male patient with a syndromic form of mental retardation. Curr Biol 11,1381-1391.
Kang, Y.B., and Cullen, B.R. (1999). The human Tap protein is a nuclear mRNA export factor that contains novel RNA-binding and nucleocytoplasmic transport sequences. Genes Dev 13, 1126-1139.
Katahira, J., Strasser, K., Podtelejnikov, A., Mann, M, Jung, J.U., and Hurt, E. (1999). The Mex67p-mediated nuclear mRNA export pathway is conserved from yeast to human. Embo J 18, 2593-2609.
Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D. Kaufman, R.J., Golan, D.E., and Anderson, P. (2005). Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169,871-884.
Kleene, K.C. (1993). Multiple controls over the efficiency of translation of the mRNAs encoding transition proteins, protamines, and the mitochondrial capsule selenoprotein in late spermatids in mice. Dev Biol 159,720-731.
Komori, K., Tsujimura, A., Miura, H., Shin, M., Takada, T., Honda, M., Matsumiya, K., and Fujioka, H. (2004). Serial follow-up study of serum testosterone and antisperm antibodies in patients with non-obstructive azoospermia after conventional or microdissection testicular sperm extraction. Int J Androl 27,32-36.
Kopera, I.A., Bilinska, B., Cheng, C.Y., and Mruk, D.D. (2010). Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365,1593-1605.
Kotaja, N., Bhattacharyya, S.N., Jaskiewicz, L., Kimmins, S., Parvinen, M., Filipowicz, W., and Sassone-Corsi, P. (2006a). The chromatoid body of male germ cells:similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci U S A 103, 2647-2652.
Kotaja, N., Kimmins, S., Brancorsini, S., Hentsch, D., Vonesch, J.L., Davidson, Ⅰ., Parvinen, M., and Sassone-Corsi, P. (2004). Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1,249-254.
Kotaja, N., Lin, H., Parvinen, M., and Sassone-Corsi, P. (2006b). Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119,2819-2825.
Kotaja, N., Macho, B., and Sassone-Corsi, P. (2005). Microtubule-independent and protein kinase A-mediated function of kinesin KIF17b controls the intracellular transport of activator of CREM in testis (ACT). J Biol Chem 280,31739-31745.
Kotaja, N., and Sassone-Corsi, P. (2007). The chromatoid body:a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8,85-90.
Krawetz, S.A. (2005). Paternal contribution:new insights and future challenges. Nat Rev Genet 6, 633-642.
Krimer, D.B., and Esponda, P. (1980). Presence of polysaccharides and proteins in the chromatoid body of mouse spermatids. Cell Biol Int Rep 4,265-270.
Kuramochi-Miyagawa, S., Kimura, T., Ijiri, T.W., Isobe, T., Asada, N., Fujita, Y., Ikawa, M., Iwai, N., Okabe, M., Deng, W., et al. (2004). Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131,839-849.
Lamb, D.J., Kessler, M.J., Shewach, D.S., Steinberger, A., and Sanborn, B.M. (1982). Characterization of Sertoli cell RNA synthetic activities in vitro at selected times during sexual maturation. Biol Reprod 27,374-382.
Landon, G.V., and Pryor, J.P. (1981). The blood-testis barrier in men of diverse fertility status:an ultrastructural study. Virchows Arch A Pathol Anat Histol 392,355-364.
Law, G.L., and Griswold, M.D. (1994). Activity and form of sulfated glycoprotein 2 (clusterin) from cultured Sertoli cells, testis, and epididymis of the rat. Biol Reprod 50,669-679.
Lee, H., Ogawa, H., Fujioka, M., and Gerton, G.L. (1994). Guanidinoacetate methyltransferase in the mouse:extensive expression in Sertoli cells of testis and in microvilli of caput epididymis. Biol Reprod 50,152-162.
Lee, N.P., Mruk, D., Lee, W.M., and Cheng, C.Y. (2003). Is the cadherin/catenin complex a functional unit of cell-cell actin-based adherens junctions in the rat testis? Biol Reprod 68,489-508.
Lee, N.P., Mruk, D.D., Conway, A.M., and Cheng, C.Y. (2004). Zyxin, axin, and Wiskott-Aldrich syndrome protein are adaptors that link the cadherin/catenin protein complex to the cytoskeleton at adherens junctions in the seminiferous epithelium of the rat testis. J Androl 25,200-215.
Lee, N.P., Wong, E.W., Mruk, D.D., and Cheng, C.Y. (2009). Testicular cell junction:a novel target for male contraception. Curr Med Chem 16,906-915.
Lenhossek, M. (1898). Untersuchungen uber Spermatogenese. Arch Micr Anat 51,215-318.
Li, Y., Friel, P.J., Robinson, M.O., McLean, D.J., and Griswold, M.D. (2002). Identification and characterization of testis-and epididymis-specific genes:cystatin SC and cystatin TE-1. Biol Reprod 67,1872-1880.
Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R.,3rd, Parker, R., and Hannon, G.J. (2005a). A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7,1261-1266.
Liu, J., Valencia-Sanchez, M.A., Hannon, G.J., and Parker, R. (2005b). MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7,719-723.
Lui, W.Y., and Cheng, C.Y. (2007). Regulation of cell junction dynamics by cytokines in the testis:a molecular and biochemical perspective. Cytokine Growth Factor Rev 18,299-311.
Lui, W.Y., Lee, W.M., and Cheng, C.Y. (2001). Transforming growth factor-beta3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology 142,1865-1877.
Lui, W.Y., Lee, W.M., and Cheng, C.Y. (2003a). TGF-betas:their role in testicular function and Sertoli cell tight junction dynamics. Int J Androl 26,147-160.
Lui, W.Y., Wong, C.H., Mruk, D.D., and Cheng, C.Y. (2003b). TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway:an in vivo study. Endocrinology 144,1139-1142.
Macho, B., Brancorsini, S., Fimia, G.M., Setou, M., Hirokawa, N., and Sassone-Corsi, P. (2002). CREM-dependent transcription in male germ cells controlled by a kinesin. Science 298, 2388-2390.
Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A., et al. (1998). Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142,117-127.
McLachlan, R.I., Rajpert-De Meyts, E., Hoei-Hansen, C.E., de Kretser, D.M., and Skakkebaek, N.E. (2007). Histological evaluation of the human testis-approaches to optimizing the clinical value of the assessment:mini review. Hum Reprod 22,2-16.
Meng, J., Holdcraft, R.W., Shima, J.E., Griswold, M.D., and Braun, R.E. (2005). Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci U S A 102,16696-16700.
Moch, H., Schraml, P., Bubendorf, L., Richter, J., Gasser, T.C., Mihatsch, M.J., and Sauter, G. (1998). Intratumoral heterogeneity of von Hippel-Lindau gene deletions in renal cell carcinoma detected by fluorescence in situ hybridization. Cancer Res 58,2304-2309.
Morita, K., Sasaki, H., Fujimoto, K., Furuse, M., and Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145,379-588.
Moussa, F., Oko, R., and Hermo, L. (1994). The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278,363-378.
Moustakas, A., Souchelnytskyi, S., and Heldin, C.H. (2001). Smad regulation in TGF-beta signal transduction. J Cell Sci 114,4359-4369.
Mruk, D.D., and Cheng, C.Y. (2004). Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 25,747-806.
Mruk, D.D., and Cheng, C.Y. (2010). Tight junctions in the testis:new perspectives. Philos Trans R Soc Lond B Biol Sci 365,1621-1635.
Mruk, D.D., Silvestrini, B., and Cheng, C.Y. (2008). Anchoring junctions as drug targets:role in contraceptive development. Pharmacol Rev 60,146-180.
Mueller, S., Rosenquist, T.A., Takai, Y., Bronson, R.A., and Wimmer, E. (2003). Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration. Biol Reprod 69,1330-1340.
Nagamori, Ⅰ., Cruickshank, V.A., and Sassone-Corsi, P. (2012). Regulation of an RNA granule during spermatogenesis:acetylation of MVH in the chromatoid body of germ cells. J Cell Sci.
Nakao, A., Afrakhte, M., Moren, A., Nakayama, T., Christian, J.L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N.E., Heldin, C.H., et al. (1997). Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389,631-635.
Namiki, M. (2000). Genetic aspects of male infertility. World J Surg 24,1176-1179.
Noce, T., Okamoto-Ito, S., and Tsunekawa, N. (2001). Vasa homolog genes in mammalian germ cell development. Cell Struct Funct 26,131-136.
Olsen, L.C., Aasland, R., and Fjose, A. (1997). A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66,95-105.
Ou, J.P., and Zhuang, G.L. (2003). Effect of antisperm antibodies on assisted reproduction. Zhonghua Nan Ke Xue 9,214-217.
Ozaki-Kuroda, K., Nakanishi, H., Ohta, H., Tanaka, H., Kurihara, H., Mueller, S., Irie, K., Ikeda, W., Sakai, T., Wimmer, E., et al. (2002). Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12,1145-1150.
Page, D.C., Silber, S., and Brown, L.G. (1999). Men with infertility caused by AZFc deletion can produce sons by intracytoplasmic sperm injection, but are likely to transmit the deletion and infertility. Hum Reprod 14,1722-1726.
Palermo, G., Joris, H., Devroey, P., and Van Steirteghem, A.C. (1992). Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340,17-18.
Pan, J., Eckardt, S., Leu, N.A., Buffone, M.G., Zhou, J., Gerton, G.L., McLaughlin, K.J., and Wang, P.J. (2009). Inactivation of Nxf2 causes defects in male meiosis and age-dependent depletion of spermatogonia. Dev Biol 330,167-174.
Paniagua, R., Nistal, M., Amat, P., and Rodriguez, M.C. (1985). Presence of ribonucleoproteins and basic proteins in the nuage and intermitochondrial bars of human spermatogonia. J Anat 143, 201-206.
Parvinen, M., and Parvinen, L.M. (1979). Active movements of the chromatoid body. A possible transport mechanism for haploid gene products. J Cell Biol 80,621-628.
Peinado, H., Portillo, F., and Cano, A. (2004). Transcriptional regulation of cadherins during development and carcinogenesis. Int J Dev Biol 48,365-375.
Perez-Moreno, M., Jamora, C., and Fuchs, E. (2003). Sticky business:orchestrating cellular signals at adherens junctions. Cell 112,535-548.
Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E., and Filipowicz, W. (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309,1573-1576.
Rao, M.K., Pham, J., Imam, J.S., MacLean, J.A., Murali, D., Furuta, Y., Sinha-Hikim, A.P., and Wilkinson, M.F. (2006). Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 20,147-152.
Reymond, N., Fabre, S., Lecocq, E., Adelaide, J., Dubreuil, P., and Lopez, M. (2001). Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectinl/PRRl through V domain interaction. J Biol Chem 276,43205-43215.
Rossi, J.J. (2005). RNAi and the P-body connection. Nat Cell Biol 7,643-644.
Rouelle-Rossier, V.B., Biggiogera, M., and Fakan, S. (1993). Ultrastructural detection of calcium and magnesium in the chromatoid body of mouse spermatids by electron spectroscopic imaging and electron energy loss spectroscopy. J Histochem Cytochem 41,1155-1162.
Russell, L. (1977). Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148,313-328.
Saitou, M., Furuse, M., Sasaki, H., Schulzke, J.D., Fromm, M., Takano, H., Noda, T., and Tsukita, S. (2000). Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11,4131-4142.
Sasaki, M., Takeda, E., Takano, K., Yomogida, K., Katahira, J., and Yoneda, Y. (2005). Molecular cloning and functional characterization of mouse Nxf family gene products. Genomics 85, 641-653.
Sassone-Corsi, P. (1997). Transcriptional checkpoints determining the fate of male germ cells. Cell 88, 163-166.
Sassone-Corsi, P. (2002). Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296,2176-2178.
Satoh-Horikawa, K., Nakanishi, H., Takahashi, K., Miyahara, M., Nishimura, M., Tachibana, K., Mizoguchi, A., and Takai, Y. (2000). Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J Biol Chem 275,10291-10299.
Saunders, P.T., Millar, M.R., Maguire, S.M., and Sharpe, R.M. (1992). Stage-specific expression of rat transition protein 2 mRNA and possible localization to the chromatoid body of step 7 spermatids by in situ hybridization using a nonradioactive riboprobe. Mol Reprod Dev 33,385-391.
Segref, A., Sharma, K., Doye, V., Hellwig, A., Huber, J., Luhrmann, R., and Hurt, E. (1997). Mex67p, a novel factor for nuclear inRNA export, binds to both poly(A)(+) RNA and nuclear pores. Embo J 16,3256-3271.
Sen, G.L., and Blau, H.M. (2005). Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat Cell Biol 7,633-636.
Serjeantson, S. (1975). Marriage patterns and fertility in three Papua New Guinean populations. Hum Biol 47,399-413.
Sheth, U., and Parker, R. (2003). Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300,805-808.
Shibata, N., Tsunekawa, N., Okamoto-Ito, S., Akasu, R., Tokumasu, A., and Noce, T. (2004). Mouse RanBPM is a partner gene to a germline specific RNA helicase, mouse vasa homolog protein. Mol Reprod Dev 67,1-7.
Siu, M.K., and Cheng, C.Y. (2004a). Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 26,978-992.
Siu, M.K., and Cheng, C.Y. (2004b). Interactions of proteases, protease inhibitors, and the betal integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 70,945-964.
Siu, M.K., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2003). Adhering junction dynamics in the testis are regulated by an interplay of beta 1-integrin and focal adhesion complex-associated proteins. Endocrinology 144,2141-2163.
Soderstrom, K.O., and Parvinen, M. (1976). Incorporation of (3H)uridine by the chromatoid body during rat spermatogenesis. J Cell Biol 70,239-246.
Sontheimer, E.J. (2005). Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol 6, 127-138.
Sun, F., Turek, P., Greene, C, Ko, E., Rademaker, A., and Martin, R.H. (2007). Abnormal progression through meiosis in men with nonobstructive azoospermia. Fertil Steril 87,565-571.
Tachibana, K., Nakanishi, H., Mandai, K., Ozaki, K., Ikeda, W., Yamamoto, Y., Nagafuchi, A., Tsukita, S., and Takai, Y. (2000). Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J Cell Biol 150,1161-1176.
Takahashi, K., Nakanishi, H., Miyahara, M., Mandai, K., Satoh, K., Satoh, A., Nishioka, H., Aoki, J., Nomoto, A., Mizoguchi, A., et al. (1999). Nectin/PRR:an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with Afadin, a PDZ domain-containing protein. J Cell Biol 145,539-549.
Takai, Y., Irie, K., Shimizu, K., Sakisaka, T., and Ikeda, W. (2003). Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization. Cancer Sci 94,655-667.
Takai, Y., and Nakanishi, H. (2003). Nectin and afadin:novel organizers of intercellular junctions. J Cell Sci 116,17-27.
Takano, K., Miki, T., Katahira, J., and Yoneda, Y. (2007). NXF2 is involved in cytoplasmic mRNA dynamics through interactions with motor proteins. Nucleic Acids Res 35,2513-2521.
Tan, W., Zolotukhin, A.S., Bear, J., Patenaude, D.J., and Felber, B.K. (2000). The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA-Publ RNA Soc 6,1762-1772.
Tan, W., Zolotukhin, A.S., Tretyakova, I., Bear, J., Lindtner, S., Smulevitch, S.V., and Felber, B.K. (2005). Identification and characterization of the mouse nuclear export factor (Nxf) family members. Nucleic Acids Res 33,3855-3865.
Tanaka, S.S., Toyooka, Y., Akasu, R., Katoh-Fukui, Y., Nakahara, Y., Suzuki, R., Yokoyama, M., and Noce, T. (2000). The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 14,841-853.
Tang, X.M., Lalli, M.F., and Clermont, Y. (1982). A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am J Anat 163,283-294.
Teixeira, D., Sheth, U., Valencia-Sanchez, M.A., Brengues, M., and Parker, R. (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11,371-382.
Thorne-Tjomsland, G., Clermont, Y., and Hermo, L. (1988). Contribution of the Golgi apparatus components to the formation of the acrosomic system and chromatoid body in rat spermatids. Anat Rec 221,591-598.
Toyooka, Y., Tsunekawa, N., Takahashi, Y., Matsui, Y., Satoh, M., and Noce, T. (2000). Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93,139-149.
Tretyakova, Ⅰ., Zolotukhin, A.S., Tan, W., Bear, J., Propst, F., Ruthel, G., and Felber, B.K. (2005). Nuclear export factor family protein participates in cytoplasmic mRNA trafficking. J Biol Chem 250,31981-31990.
Tsai-Morris, C.H., Sheng, Y., Lee, E., Lei, K.J., and Dufau, M.L. (2004). Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis. Proc Natl Acad Sci U S A 101,6373-6378.
Turksen, K., and Troy, T.C. (2004). Barriers built on claudins. J Cell Sci 117,2435-2447.
Vagin, V.V., Wohlschlegel, J., Qu, J., Jonsson, Z., Huang, X., Chuma, S., Girard, A., Sachidanandam, R., Hannon, G.J., and Aravin, A.A. (2009). Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23, 1749-1762.
Vanmarsenille, L., Verbeeck, J., Belet, S., Roebroek, A.J., Van de Putte, T., Nevelsteen, J., Callaerts-Vegh, Z., D'Hooge, R., Marynen, P., and Froyen, G. (2013). Generation and characterization of an Nxf7 knockout mouse to study NXF5 deficiency in a patient with intellectual disability. PLoS One 8, e64144.
Ventela, S., Toppari, J., and Parvinen, M. (2003). Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat:mechanisms of haploid gene product sharing. Mol Biol Cell 14,2768-2780.
Walt, H., and Armbruster, B.L. (1984). Actin and RNA are components of the chromatoid bodies in spermatids of the rat. Cell Tissue Res 236,487-490.
Werner, G., and Werner, K. (1995). Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids. J Submicrosc Cytol Pathol 27,325-330.
Wheelock, M.J., and Johnson, K..R. (2003a). Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15,509-514.
Wheelock, M.J., and Johnson, K.R. (2003b). Cadherins as modulators of cellular phenotype. Annu Rev Cell Dev Biol 19,207-235.
Wieser, R., Wrana, J.L., and Massague, J. (1995). GS domain mutations that constitutively activate T beta R-Ⅰ, the downstream signaling component in the TGF-beta receptor complex. EMBO J 14, 2199-2208.
Wilkie, G.S., Zimyanin, V., Kirby, R., Korey, C., Francis-Lang, H., Van Vactor, D., and Davis, Ⅰ. (2001). Small bristles, the Drosophila ortholog of NXF-1, is essential for mRNA export throughout development. RNA 7,1781-1792.
Wine, R.N., and Chapin, R.E. (1999). Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 20,198-213.
Wong, C.H., and Cheng, C.Y. (2005). Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis:a review of recent data. Dev Biol 286,1-15.
Wong, C.H., Mruk, D.D., Lui, W.Y., and Cheng, C.Y. (2004). Regulation of blood-testis barrier dynamics:an in vivo study. J Cell Sci 117,783-798.
Wong, E.W., and Cheng, C.Y. (2009). Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 278,309-353.
Wu, J.Y., and Means, A.R. (2000). Ca(2+)/calmodulin-dependent protein kinase IV is expressed in spermatids and targeted to chromatin and the nuclear matrix. J Biol Chem 275,7994-7999.
Xia, W., and Cheng, C.Y. (2005). TGF-beta3 regulates anchoring junction dynamics in the seminiferous epithelium of the rat testis via the Ras/ERK signaling pathway:An in vivo study. Dev Biol 280,321-343.
Xia, W., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2005a). Cytokines and junction restructuring during spermatogenesis--a lesson to learn from the testis. Cytokine Growth Factor Rev 16, 469-493.
Xia, W., Mruk, D.D., Lee, W.M., and Cheng, C.Y. (2006). Differential interactions between transforming growth factor-beta3/TbetaRl, TAB1, and CD2AP disrupt blood-testis barrier and Sertoli-germ cell adhesion. J Biol Chem 281,16799-16813.
Xia, W., Wong, C.H., Lee, N.P., Lee, W.M., and Cheng, C.Y. (2005b). Disruption of Sertoli-germ cell adhesion function in the seminiferous epithelium of the rat testis can be limited to adherens junctions without affecting the blood-testis barrier integrity:an in vivo study using an androgen suppression model. J Cell Physiol 205,141-157.
Xia, W., Wong, E.W., Mruk, D.D., and Cheng, C.Y. (2009). TGF-beta3 and TNFalpha perturb blood-testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins:a new concept of BTB regulation during spermatogenesis. Dev Biol 327, 48-61.
Yagi, T., and Takeichi, M. (2000). Cadherin superfamily genes:functions, genomic organization, and neurologic diversity. Genes Dev 14,1169-1180.
Yan, H.H., and Cheng, C.Y. (2005). Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci U S A102,11722-11727.
Yang, J., Bogerd, H.P., Wang, P.J., Page, D.C., and Cullen, B.R. (2001). Two closely related human nuclear export factors utilize entirely distinct export pathways. Mol Cell 8,397-406.
Yokota, S. (2008). Historical survey on chromatoid body research. Acta Histochem Cytochem 41, 65-82.
Yomogida, K., Ohtani, H., Harigae, H., Ito, E., Nishimune, Y., Engel, J.D., and Yamamoto, M. (1994). Developmental stage-and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 120,1759-1766.
Yu, Z., Raabe, T., and Hecht, N.B. (2005). MicroRNA Mirnl22a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod 73,427-433.
Zamore, P.D., and Haley, B. (2005). Ribo-gnome:the big world of small RNAs. Science 309, 1519-1524.
Zhang, X., Wheeler, D., Tang, Y., Guo, L., Shapiro, R.A., Ribar, T.J., Means, A.R., Billiar, T.R., Angus, D.C., and Rosengart, M.R. (2008). Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages. J Immunol 181,5015-5023.
Zhou, J., Pan, J., Eckardt, S., Leu, N.A., McLaughlin, K.J., and Wang, P.J. (2011). Nxf3 is expressed in Sertoli cells, but is dispensable for spermatogenesis. Mol Reprod Dev 78,241-249.