精原干细胞在转基因小鼠生产中的研究进展
|
摘要
精原干细胞(spermatogonial stem cells, SSCs)是雄性动物体内的一类生殖干细胞,可以增殖分化形成大量生殖细胞,修饰精原干细胞基因组是生产转基因动物的有效方法之一。精原干细胞介导转基因小鼠的研究比较系统,本研究对精原干细胞的分离纯化以及体内外介导精原干细胞制备转基因小鼠的方法进行系统阐述和比较,为利用该方法研究其他转基因动物提供借鉴。本研究还讨论了基因编辑技术修饰精原干细胞,产生转基因动物在基因功能研究和疾病模型构建方面的研究前景。
Spermatogonial stem cells(SSCs) is a kind of genital stem cells in male animals, which could proliferate and differentiate to form a large number of germ cells. Therefore, modifying the genome of spermatogonial stem cells is one of the effective strategies to produce transgenic animals. The studies on SSCs-mediated transgenic mice are fairly systematic. In this review, the methods of isolating and purifying SSCs and producing transgenic mice mediated by SSCs in vitro and in vivo were systematically described and compared, which could provide reference for the studies on other transgenic animals. Additionally, the study discussed gene editing technology used for modifying SSCs, which could be applied in gene function research and disease model building of transgenic animals.
Spermatogonial stem cells(SSCs) is a kind of genital stem cells in male animals, which could proliferate and differentiate to form a large number of germ cells. Therefore, modifying the genome of spermatogonial stem cells is one of the effective strategies to produce transgenic animals. The studies on SSCs-mediated transgenic mice are fairly systematic. In this review, the methods of isolating and purifying SSCs and producing transgenic mice mediated by SSCs in vitro and in vivo were systematically described and compared, which could provide reference for the studies on other transgenic animals. Additionally, the study discussed gene editing technology used for modifying SSCs, which could be applied in gene function research and disease model building of transgenic animals.
引文
An J.H.,2014,The mechanism of histone methyltransferase ES-ET in the survival of murine spermatogonial stem cells,Dissertation for Ph.D.,Northwest A&F University,Supervisor:Zeng X.W.,pp.8(安俊辉,2014,组蛋白甲基化酶ESET调控小鼠精原干细胞存活的机理研究,博士学位论文,西北农林科技大学,导师:曾文先,pp.8)
Aloisio G.M.,Nakada Y.,Saatcioglu H.D.,Pe觡a C.G.,Baker M.D.,Tarnawa E.D.,Mukherjee J.,Manjunath H.,Bugde A.,Sengupta A.L.,Amatruda J.F.,Cuevas I.,Hamra F.K.,and Castrillon D.H.,2014,PAX7 expression defines germline stem cells in the adult testis,J.Clin.Invest,124(9):3929-3944
Brinster R.L.,and Avarbock M.R.,1994,Germline transmission of donor haplotype following spermatogonial transplantation,Proc.Natl.Acad.Sci.USA,91(24):11303-11307
Chen S.R.,and Liu Y.X.,2015,Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli cell signaling,Reproduction,149(4):R159-R167
Choi N.Y.,Park Y.S.,Ryu J.S.,Lee H.J.,Arauzo-Bravo M.J.,Ko K.,Han D.W.,S choler H.R.,and Ko K.,2014,A novel feeder-free culture system for expansion of mouse spermatogonial stem cells,Mol.Cells,37(6):473-479
De Rooij D.G.,2006,Rapid expansion of the spermatogonial stem cell tool box,Proc.Natl.Acad.Sci.USA,103(21):7939-7940
De Rooij D.G.,2009,The spermatogonial stem cell niche,Microsc.Res.Tech.,72(8):580-585
Dai J.J.,Li X.,Wu C.F.,Zhang S.S.,Zhang T.Y.,and Zhang D.F.,2014,Effect of different transfection reagents and injection methods in mice testicular injection on the expression of exogenous gene,Shengwugongcheng Xuebao(Chinese Journal of Biotechnology),30(10):1522-1530(戴建军,李翔,吴彩凤,张树山,张廷宇,张德福,2014,小鼠睾丸注射不同转染试剂和注射方法对外源基因表达的影响,生物工程学报,30(10):1522-1530)
Ganguli N.,Wadhwa N.,Usmani A.,Kunj N.,Ganguli N.,Sarkar R.K.,Ghorai S.M.,and Majumdar S.S.,2016,An efficient method for generating a germ cell depleted animal model for studies related to spermatogonial stem cell transplantation,Stem Cell Research&Therapy,7(1):142
Goodyear S.,and Brinster R.,2017,Culture and expansion of primary undifferentiated spermatogonial stem cells,Cold Spring Harb.Protoc.,(4):t94193
Goodyear S.,and Brinster R.,2017,Spermatogonial stem cell transplantation to the testis,Cold Spring Harb Protoc.,2017(4):t94235
He Y.N.,Chen X.L.,Zhu H.B.,and Wang D.,2015,Developments in techniques for the isolation,enrichment,main culture conditions and identification of spermatogonial stem cells,Cytotechnology,67(6):921-930
He Z.P.,Kokkinaki M.,Jiang J.J.,Dobrinski I.,and Dym M.,2010,Isolation,characterization,and culture of human spermatogonia,Biol.Reprod,82(2):363-372
Helsel A.R.,Oatley M.J.,and Oatley J.M.,2017,Glycolysis-optimized conditions enhance maintenance of regenerative integrity in mouse spermatogonial stem cells during long-term culture,Stem Cell Reports,8(5):1430-1441
Honaramooz A.,Behboodi E.,Hausler C.L.,Blash S.,Ayres S.,Azuma C.,Echelard Y.,and Dobrinski I.,2005,Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation,J.Androl.,26(6):698-705
Kadam P.,Van Saen D.,and Goossens E.,2017,Can mesenchymal stem cells improve spermatogonial stem cell transplantation efficiency Andrology,Stem Cell Research&Therapy,5(1):2-9
Kanatsu-Shinohara M.,Mori Y.,and Shinohara T.,2013,Enrichment of mouse spermatogonial stem cells based on aldehyde dehydrogenase activity,Biol.Reprod.,89(6):140
Kanatsu-Shinohara M.,Morimoto H.,and Shinohara T.,2016,Enrichment of mouse spermatogonial stem cells by the stem cell dye CDy1,Biol.Reprod.,94(1):1-10
Kanatsu-Shinohara M.,Onoyama I.,Nakayama K.I.,and Shinohara T.,2014,Skp1-Cullin-F-box(SCF)-type ubiquitin ligase FBXW7 negatively regulates spermatogonial stem cell self-renewal,Proc.Natl.Acad.Sci.USA,111(24):8826-8831
Kanatsu-Shinohara M.,Toyokuni S.,and Shinohara T.,2005,Genetic selection of mouse male germline stem cells in vitro:offspring from single stem cells,Biol.Reprod,72(1):236-240
Kim Y.,Selvaraj V.,Dobrinski I.,Lee H.,McEntee M.C.,and Travis A.J.,2006,Recipient preparation and mixed germ cell isolation for spermatogonial stem cell transplantation in domestic cats,J.Androl.,27(2):248-256
Li J.T.,Zhang P.H.,Qu X.W.,Li Z.S.,and Li S.W.,2016,Rhodiola polysaccharide effect on spermatogonial stem cell proliferation in vitro,Zhongguo Zuzhigongcheng Yanjiu(Chinese Journal of Tissue Engineering Research),20(10):1501-1507(李俊涛,张培海,曲晓伟,李郑生,李松伟,2016,红景天多糖对精原干细胞体外增殖的影响,中国组织工程研究,20(10):1501-1507)
Li C.H.,Yan L.Z.,Ban W.Z.,Tu Q.,Wu Y.,Wang L.,Bi R.,Ji S.,Ma Y.H.,Nie W.H.,Lv L.B.,Yao Y.G.,Zhao X.D.,and Zheng P.,2017,Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring,Cell Res.,27(2):241-252
Liang P.P.,Xu Y.W.,Zhang X.Y.,Ding C.H.,Huang R.H.,Zhang Z.Z.,Lv J.,Xie X.W.,Chen Y.X.,Li Y.J.,Sun Y.,Bai Y.F.,Songyang Z.,Ma W.B.,Zhou C.Q.,and Huang J.J.,2015,CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes,Protein Cell,6(5):363-372
Lin Z.,Bao J.,Kong Q.,Bai Y.,Luo F.,Songyang Z.,Wu Y.,and Huang J.,2016,Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan,Theriogenology,89:365-373
Ma W.,An L.,Wu Z.,Wang X.,Guo M.,Miao K.,Ma W.,and Tian J.,2011,Efficient and safe recipient preparation for transplantation of mouse spermatogonial stem cells:pretreat ing testes with heat shock,Biol.Reprod,85(4):670-677
Nagano M.,Brinster C.J.,Orwig K.E.,Ryu B.Y.,Avarbock M.R.,and Brinster R.L.,2001,Transgenic mice produced by retroviral transduction of male germ-line stem cells,Proc.Natl.Acad.Sci.USA,98(23):13090-13095
Nagano M.,Ryu B.Y.,Brinster C.J.,Avarbock M.R.,and Brinster R.L.,2003,Maintenance of mouse male germ line stem cells in vitro,Biol.Reprod,68(6):2207-2214
Oatley M.J.,Kaucher A.V.,Racicot K.E.,and Oatley J.M.,2011,Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice,Biol.Reprod.,85(2):347-356
Ohtsuka M.,Miura H.,Nakaoka H.,Kimura M.,Sato M.,and I-noko H.,2012,Targeted transgenesis through pronuclear injection of improved vectors into in vitro fertilized eggs,Transgenic Res.,21(1):225-226
Palmiter R.D.,Brinster R.L.,Hammer R.E.,Trumbauer M.E.,Rosenfeld M.G.,Birnberg N.C.,and Evans R.M.,1982,Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes,Nature,300(5893):611-615
Phillips B.T.,Gassei K.,and Orwig K.E.,2010,Spermatogonial stem cell regulation and spermatogenesis,Philos.Trans.RSoc.Lond B Biol.Sci.,365(1546):1663-1678
Ren W.Q.,Zhang Z.P.,Wang X.Z.,Lv J.Y.,Xu X.T.,Jiang J.H.,Zhai M.S.,and Shi K.W.,2013,Effects of SC1(pluripotin)on isolation and culture of embryonic stem cells from Kunming mouse,Zhongguo Shouyi Xuebao(Chinese Journal of Veterinary Science),33(7):1132-1136(任卫青,张志平,王新庄,吕婧玉,许晓婷,蒋金航,翟明胜,石凯文,2013,SC1(pluripotin)对昆明小鼠胚胎干细胞分离培养的影响,中国兽医学报,33(7):1132-1136)
Sachs C.,Robinson B.D.,Andres-Martin L.,Webster T.,Gilbert M.,Lo H.Y.,Rafii S.,Ng C.K.,and Seandel M.,2014,Evaluation of candidate spermatogonial markers ID4 and GPR125in testes of adult human cadaveric organ donors,Andrology,2(4):607-614
Takashima S.,Kanatsu-Shinohara M.,Tanaka T.,Morimoto H.,Inoue K.,Ogonuki N.,Jijiwa M.,Takahashi M.,Ogura A.,and Shinohara T.,2015,Functional differences between GDNF-dependent and FGF2-dependent mouse spermatogonial stem cell self-renewal,Stem Cell Reports,4(3):489-502
Watanabe S.,Kanatsu-Shinohara M.,Ogonuki N.,Matoba S.,Ogura A.,and Shinohara T.,2017,Adeno-associated virus-me diated delivery of genes to mouse spermatogonial stem cellsdagger,Biol.Reprod,96(1):221-231
Wu Y.X.,Zhou H.,Fan X.Y.,Zhang Y.,Zhang M.,Wang Y.H.,Xie Z.F.,Bai M.Z.,Yin Q.,Liang D.,Tang W.,Liao J.Y.,Zhou C.K.,Liu W.J.,Zhu P.,Guo H.S.,Pan H.,Wu C.L.,Shi H.J.,Wu L.G.,Tang F.C.,and Li J.S.,2015,Correction of a genetic disease by CRISPR-Cas9-mediated gene editing in mouse spermatogonial stem cells,Cell Res.,25(1):67-79
Wang H.J.,Ma X.,Zhao M.,Du X.Y.,Li Y.C.,and Chen Z.W.,2013,Transfection efficiency of lentiviral vector-based SMGTfor dog testicular germ cells in vivo,Shiyan Dongwu Kexue(Laboratory Animal Science),30(1):6-10(王洪军,马啸,赵明,杜小燕,李益琛,陈振文,2013,慢病毒载体转染犬睾丸生殖细胞,实验动物科学,30(1):6-10)
Wang J.H.,Xie Q.Q.,Fan C.Y.,Fang F.G.,Zhou J.,Cao H.G.,and Zhang X.R.,2015,Establishment of transplantation model for spermatogonial stem cells in Kunming mice with busulfan treatment,Xibeinonglin Keji Daxue Xuebao(Zirankexue Ban)(Journal of Northwest A&F University(Nat.Sci.Ed.)),43(8):51-56(王菊花,解倩倩,范彩云,方富贵,周杰,曹鸿国,章孝荣,2015,白消安注射法建立昆明小鼠精原干细胞移植受体模型,西北农林科技大学学报(自然科学版),43(8):51-56)
Xie C.,Yu M.J.,Xui N.,Wang L.B.,Li W.J.,and Zhao Y.B.,2010,Testis injection of exogenous DNA results in expression in mouse sperm,Dongwuxue Zazhi(Chinese Journal of Zoology),40(2):151-157(谢畅,于明举,惠楠,王岭斌,李文杰,赵永聚,2010,通过睾丸内注射转染外源DNA在小鼠精子的表达,动物学杂志,40(2):151-157)
Xie J.J.,Yao X.L.,Song R.G.,Lv X.K.,Zhang R.X.,Wang L.H.,and Shi L.,2016,Enrichment and identification of spermatogonial stem cells from sheep testis,Heilongjiang Dong wu Fanzhi(Heilongjiang Journal of Animal Reproduction),24(4):12-15(谢静静,姚晓磊,宋瑞高,吕小康,张瑞鑫,王莉宏,石磊,2016,绵羊精原干细胞的分离纯化与鉴定,黑龙江动物繁殖,24(4):12-15)
Xin Y.,Zhang T.,Zhang Y.Y.,and Zhang Z.Y.,2014,Production of transgenic mice by lentivirus mediated spermatognoial stem cells in vivo,Xibeinonglin Keji Daxue Xuebao(Ziran Kexue Ban)(Journal of Northwest A&F University(Natural Science Edition)),42(6):15-20(辛颖,张涛,张优优,张智英,2014,慢病毒活体介导精原干细胞生产转基因小鼠,西北农林科技大学学报(自然科学版),42(6):15-20)
Yomogida K.,Yagura Y.,and Nishimune Y.,2002,Electroporated transgene-rescued spermatogenesis in infertile mutant mice with a sertoli cell defect,Biol.Reprod,67(3):712-717
Zheng Y.,Zhang Y.Q.,Qu R.F.,He Y.,Tian X.,and Zeng W.X.,2014,Spermatogonial stem cells from domestic animals:progress and prospects,Reproduction,147(3):R65-R74
Zohni K.,Zhang X.,Tan S.L.,Chan P.,and Nagano M.,2012,CD9 is expressed on human male germ cells that have a long-term repopulation potential after transplantation into mouse testes,Biol.Reprod.,87(2):27
Zhang W.X.,Han G.Y.,Wang R.,Li S.,and Han X.F.,2009,Separation and purification of rat spermatogonial stem cells,Zhengzhou Daxue Xuebao(Joumal of Zhengzhou University(Medical Sciences)),44(3):497-500(张卫星,韩广业,王瑞,李松,韩雪飞,2009,大鼠精原干细胞的分离纯化,郑州大学学报(医学版),44(3):497-500)
Aloisio G.M.,Nakada Y.,Saatcioglu H.D.,Pe觡a C.G.,Baker M.D.,Tarnawa E.D.,Mukherjee J.,Manjunath H.,Bugde A.,Sengupta A.L.,Amatruda J.F.,Cuevas I.,Hamra F.K.,and Castrillon D.H.,2014,PAX7 expression defines germline stem cells in the adult testis,J.Clin.Invest,124(9):3929-3944
Brinster R.L.,and Avarbock M.R.,1994,Germline transmission of donor haplotype following spermatogonial transplantation,Proc.Natl.Acad.Sci.USA,91(24):11303-11307
Chen S.R.,and Liu Y.X.,2015,Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli cell signaling,Reproduction,149(4):R159-R167
Choi N.Y.,Park Y.S.,Ryu J.S.,Lee H.J.,Arauzo-Bravo M.J.,Ko K.,Han D.W.,S choler H.R.,and Ko K.,2014,A novel feeder-free culture system for expansion of mouse spermatogonial stem cells,Mol.Cells,37(6):473-479
De Rooij D.G.,2006,Rapid expansion of the spermatogonial stem cell tool box,Proc.Natl.Acad.Sci.USA,103(21):7939-7940
De Rooij D.G.,2009,The spermatogonial stem cell niche,Microsc.Res.Tech.,72(8):580-585
Dai J.J.,Li X.,Wu C.F.,Zhang S.S.,Zhang T.Y.,and Zhang D.F.,2014,Effect of different transfection reagents and injection methods in mice testicular injection on the expression of exogenous gene,Shengwugongcheng Xuebao(Chinese Journal of Biotechnology),30(10):1522-1530(戴建军,李翔,吴彩凤,张树山,张廷宇,张德福,2014,小鼠睾丸注射不同转染试剂和注射方法对外源基因表达的影响,生物工程学报,30(10):1522-1530)
Ganguli N.,Wadhwa N.,Usmani A.,Kunj N.,Ganguli N.,Sarkar R.K.,Ghorai S.M.,and Majumdar S.S.,2016,An efficient method for generating a germ cell depleted animal model for studies related to spermatogonial stem cell transplantation,Stem Cell Research&Therapy,7(1):142
Goodyear S.,and Brinster R.,2017,Culture and expansion of primary undifferentiated spermatogonial stem cells,Cold Spring Harb.Protoc.,(4):t94193
Goodyear S.,and Brinster R.,2017,Spermatogonial stem cell transplantation to the testis,Cold Spring Harb Protoc.,2017(4):t94235
He Y.N.,Chen X.L.,Zhu H.B.,and Wang D.,2015,Developments in techniques for the isolation,enrichment,main culture conditions and identification of spermatogonial stem cells,Cytotechnology,67(6):921-930
He Z.P.,Kokkinaki M.,Jiang J.J.,Dobrinski I.,and Dym M.,2010,Isolation,characterization,and culture of human spermatogonia,Biol.Reprod,82(2):363-372
Helsel A.R.,Oatley M.J.,and Oatley J.M.,2017,Glycolysis-optimized conditions enhance maintenance of regenerative integrity in mouse spermatogonial stem cells during long-term culture,Stem Cell Reports,8(5):1430-1441
Honaramooz A.,Behboodi E.,Hausler C.L.,Blash S.,Ayres S.,Azuma C.,Echelard Y.,and Dobrinski I.,2005,Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation,J.Androl.,26(6):698-705
Kadam P.,Van Saen D.,and Goossens E.,2017,Can mesenchymal stem cells improve spermatogonial stem cell transplantation efficiency Andrology,Stem Cell Research&Therapy,5(1):2-9
Kanatsu-Shinohara M.,Mori Y.,and Shinohara T.,2013,Enrichment of mouse spermatogonial stem cells based on aldehyde dehydrogenase activity,Biol.Reprod.,89(6):140
Kanatsu-Shinohara M.,Morimoto H.,and Shinohara T.,2016,Enrichment of mouse spermatogonial stem cells by the stem cell dye CDy1,Biol.Reprod.,94(1):1-10
Kanatsu-Shinohara M.,Onoyama I.,Nakayama K.I.,and Shinohara T.,2014,Skp1-Cullin-F-box(SCF)-type ubiquitin ligase FBXW7 negatively regulates spermatogonial stem cell self-renewal,Proc.Natl.Acad.Sci.USA,111(24):8826-8831
Kanatsu-Shinohara M.,Toyokuni S.,and Shinohara T.,2005,Genetic selection of mouse male germline stem cells in vitro:offspring from single stem cells,Biol.Reprod,72(1):236-240
Kim Y.,Selvaraj V.,Dobrinski I.,Lee H.,McEntee M.C.,and Travis A.J.,2006,Recipient preparation and mixed germ cell isolation for spermatogonial stem cell transplantation in domestic cats,J.Androl.,27(2):248-256
Li J.T.,Zhang P.H.,Qu X.W.,Li Z.S.,and Li S.W.,2016,Rhodiola polysaccharide effect on spermatogonial stem cell proliferation in vitro,Zhongguo Zuzhigongcheng Yanjiu(Chinese Journal of Tissue Engineering Research),20(10):1501-1507(李俊涛,张培海,曲晓伟,李郑生,李松伟,2016,红景天多糖对精原干细胞体外增殖的影响,中国组织工程研究,20(10):1501-1507)
Li C.H.,Yan L.Z.,Ban W.Z.,Tu Q.,Wu Y.,Wang L.,Bi R.,Ji S.,Ma Y.H.,Nie W.H.,Lv L.B.,Yao Y.G.,Zhao X.D.,and Zheng P.,2017,Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring,Cell Res.,27(2):241-252
Liang P.P.,Xu Y.W.,Zhang X.Y.,Ding C.H.,Huang R.H.,Zhang Z.Z.,Lv J.,Xie X.W.,Chen Y.X.,Li Y.J.,Sun Y.,Bai Y.F.,Songyang Z.,Ma W.B.,Zhou C.Q.,and Huang J.J.,2015,CRISPR/Cas9-mediated gene editing in human tripronuclear zygotes,Protein Cell,6(5):363-372
Lin Z.,Bao J.,Kong Q.,Bai Y.,Luo F.,Songyang Z.,Wu Y.,and Huang J.,2016,Effective production of recipient male pigs for spermatogonial stem cell transplantation by intratesticular injection with busulfan,Theriogenology,89:365-373
Ma W.,An L.,Wu Z.,Wang X.,Guo M.,Miao K.,Ma W.,and Tian J.,2011,Efficient and safe recipient preparation for transplantation of mouse spermatogonial stem cells:pretreat ing testes with heat shock,Biol.Reprod,85(4):670-677
Nagano M.,Brinster C.J.,Orwig K.E.,Ryu B.Y.,Avarbock M.R.,and Brinster R.L.,2001,Transgenic mice produced by retroviral transduction of male germ-line stem cells,Proc.Natl.Acad.Sci.USA,98(23):13090-13095
Nagano M.,Ryu B.Y.,Brinster C.J.,Avarbock M.R.,and Brinster R.L.,2003,Maintenance of mouse male germ line stem cells in vitro,Biol.Reprod,68(6):2207-2214
Oatley M.J.,Kaucher A.V.,Racicot K.E.,and Oatley J.M.,2011,Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice,Biol.Reprod.,85(2):347-356
Ohtsuka M.,Miura H.,Nakaoka H.,Kimura M.,Sato M.,and I-noko H.,2012,Targeted transgenesis through pronuclear injection of improved vectors into in vitro fertilized eggs,Transgenic Res.,21(1):225-226
Palmiter R.D.,Brinster R.L.,Hammer R.E.,Trumbauer M.E.,Rosenfeld M.G.,Birnberg N.C.,and Evans R.M.,1982,Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes,Nature,300(5893):611-615
Phillips B.T.,Gassei K.,and Orwig K.E.,2010,Spermatogonial stem cell regulation and spermatogenesis,Philos.Trans.RSoc.Lond B Biol.Sci.,365(1546):1663-1678
Ren W.Q.,Zhang Z.P.,Wang X.Z.,Lv J.Y.,Xu X.T.,Jiang J.H.,Zhai M.S.,and Shi K.W.,2013,Effects of SC1(pluripotin)on isolation and culture of embryonic stem cells from Kunming mouse,Zhongguo Shouyi Xuebao(Chinese Journal of Veterinary Science),33(7):1132-1136(任卫青,张志平,王新庄,吕婧玉,许晓婷,蒋金航,翟明胜,石凯文,2013,SC1(pluripotin)对昆明小鼠胚胎干细胞分离培养的影响,中国兽医学报,33(7):1132-1136)
Sachs C.,Robinson B.D.,Andres-Martin L.,Webster T.,Gilbert M.,Lo H.Y.,Rafii S.,Ng C.K.,and Seandel M.,2014,Evaluation of candidate spermatogonial markers ID4 and GPR125in testes of adult human cadaveric organ donors,Andrology,2(4):607-614
Takashima S.,Kanatsu-Shinohara M.,Tanaka T.,Morimoto H.,Inoue K.,Ogonuki N.,Jijiwa M.,Takahashi M.,Ogura A.,and Shinohara T.,2015,Functional differences between GDNF-dependent and FGF2-dependent mouse spermatogonial stem cell self-renewal,Stem Cell Reports,4(3):489-502
Watanabe S.,Kanatsu-Shinohara M.,Ogonuki N.,Matoba S.,Ogura A.,and Shinohara T.,2017,Adeno-associated virus-me diated delivery of genes to mouse spermatogonial stem cellsdagger,Biol.Reprod,96(1):221-231
Wu Y.X.,Zhou H.,Fan X.Y.,Zhang Y.,Zhang M.,Wang Y.H.,Xie Z.F.,Bai M.Z.,Yin Q.,Liang D.,Tang W.,Liao J.Y.,Zhou C.K.,Liu W.J.,Zhu P.,Guo H.S.,Pan H.,Wu C.L.,Shi H.J.,Wu L.G.,Tang F.C.,and Li J.S.,2015,Correction of a genetic disease by CRISPR-Cas9-mediated gene editing in mouse spermatogonial stem cells,Cell Res.,25(1):67-79
Wang H.J.,Ma X.,Zhao M.,Du X.Y.,Li Y.C.,and Chen Z.W.,2013,Transfection efficiency of lentiviral vector-based SMGTfor dog testicular germ cells in vivo,Shiyan Dongwu Kexue(Laboratory Animal Science),30(1):6-10(王洪军,马啸,赵明,杜小燕,李益琛,陈振文,2013,慢病毒载体转染犬睾丸生殖细胞,实验动物科学,30(1):6-10)
Wang J.H.,Xie Q.Q.,Fan C.Y.,Fang F.G.,Zhou J.,Cao H.G.,and Zhang X.R.,2015,Establishment of transplantation model for spermatogonial stem cells in Kunming mice with busulfan treatment,Xibeinonglin Keji Daxue Xuebao(Zirankexue Ban)(Journal of Northwest A&F University(Nat.Sci.Ed.)),43(8):51-56(王菊花,解倩倩,范彩云,方富贵,周杰,曹鸿国,章孝荣,2015,白消安注射法建立昆明小鼠精原干细胞移植受体模型,西北农林科技大学学报(自然科学版),43(8):51-56)
Xie C.,Yu M.J.,Xui N.,Wang L.B.,Li W.J.,and Zhao Y.B.,2010,Testis injection of exogenous DNA results in expression in mouse sperm,Dongwuxue Zazhi(Chinese Journal of Zoology),40(2):151-157(谢畅,于明举,惠楠,王岭斌,李文杰,赵永聚,2010,通过睾丸内注射转染外源DNA在小鼠精子的表达,动物学杂志,40(2):151-157)
Xie J.J.,Yao X.L.,Song R.G.,Lv X.K.,Zhang R.X.,Wang L.H.,and Shi L.,2016,Enrichment and identification of spermatogonial stem cells from sheep testis,Heilongjiang Dong wu Fanzhi(Heilongjiang Journal of Animal Reproduction),24(4):12-15(谢静静,姚晓磊,宋瑞高,吕小康,张瑞鑫,王莉宏,石磊,2016,绵羊精原干细胞的分离纯化与鉴定,黑龙江动物繁殖,24(4):12-15)
Xin Y.,Zhang T.,Zhang Y.Y.,and Zhang Z.Y.,2014,Production of transgenic mice by lentivirus mediated spermatognoial stem cells in vivo,Xibeinonglin Keji Daxue Xuebao(Ziran Kexue Ban)(Journal of Northwest A&F University(Natural Science Edition)),42(6):15-20(辛颖,张涛,张优优,张智英,2014,慢病毒活体介导精原干细胞生产转基因小鼠,西北农林科技大学学报(自然科学版),42(6):15-20)
Yomogida K.,Yagura Y.,and Nishimune Y.,2002,Electroporated transgene-rescued spermatogenesis in infertile mutant mice with a sertoli cell defect,Biol.Reprod,67(3):712-717
Zheng Y.,Zhang Y.Q.,Qu R.F.,He Y.,Tian X.,and Zeng W.X.,2014,Spermatogonial stem cells from domestic animals:progress and prospects,Reproduction,147(3):R65-R74
Zohni K.,Zhang X.,Tan S.L.,Chan P.,and Nagano M.,2012,CD9 is expressed on human male germ cells that have a long-term repopulation potential after transplantation into mouse testes,Biol.Reprod.,87(2):27
Zhang W.X.,Han G.Y.,Wang R.,Li S.,and Han X.F.,2009,Separation and purification of rat spermatogonial stem cells,Zhengzhou Daxue Xuebao(Joumal of Zhengzhou University(Medical Sciences)),44(3):497-500(张卫星,韩广业,王瑞,李松,韩雪飞,2009,大鼠精原干细胞的分离纯化,郑州大学学报(医学版),44(3):497-500)