调控小鼠肾脏功能的相关中枢核团神经解剖学研究
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摘要
近年来随着有生物活性的能够进行多突触传递的嗜神经示踪病毒的发现、改造与应用,有关调控内脏功能的中枢核团定位和功能认识得以深化,相关中枢核团之间的神经解剖学通路变得更加明晰。本研究运用伪狂犬病毒(pseudorabies virus, PRV)转突触示踪技术和荧光标记技术试图确定中枢神经系统参与调控小鼠肾脏功能的相关神经核团,以及这些核团之间的神经解剖学投射通路。研究方法与结果方法：将嗜神经示踪病毒PRV-614注入19只成年雄性C57BL/6J小鼠的左侧肾脏上极,按照动物的不同生存期限无痛处死后制备冰冻切片,用荧光免疫组织化学技术检测脊髓、脑干(延髓和中脑)中PRV-614感染神经元、色氨酸羟化酶(TPH)和酪氨酸羟化酶(TH)阳性神经元的表达。结果：1.PRV-614经小鼠肾脏注射后第3d,少量的PRV-614感染神经元逆行示踪标记在脊髓T9的IML区。2.注射PRV-614后第4d,少量的PRV-614感染神经元发现在脊髓T8-10的IML区、IC区和CAN区,以及延髓头端腹外侧核。3.注射PRV-614后第5d,较多的PRV-614感染神经元发现在脊髓T7-12的IML区、IC区和CAN区等,延髓头端腹内侧核、延髓头端腹外侧核、延髓中缝核、孤束核、A5区域、蓝斑核及亚蓝斑核等；较少的PRV-614感染神经元发现在中脑PPTg和LDTg区等。4.注射PRV-614后第6d,在脊髓几乎未发现PRV-614感染神经元。较多的PRV-614感染神经元发现在延髓头端腹内侧核、延髓头端腹外侧核、延髓中缝核、A5区域、蓝斑核及亚蓝斑核等,以及中脑PPTg和LDTg区。其中PRV-614感染神经元主要发现在LDTg头端和中间部位,以及PPTg中部和尾部。PRV-614/TPH双重标记神经元主要分布在LDTg头端,而PRV-614/TH神经元分散在LDTg中在3个部位。PRV-614/TPH和PRV-614/TH神经元主要位于PPTg (cPPTg)尾侧。研究总结1.从小鼠肾脏注射的PRV-614经突触逆行传递到达中枢核团具有时空表达特异性。2.主要调节肾脏交感神经活性的脊髓节段范围可能是T8-10,其中T9尤为重要。3.延髓头端腹外侧核是主要调节肾脏TH阳性交感神经活性的中枢核团,而延髓中缝核是主要调节肾脏TPH阳性交感神经活性的中枢核团。4.脑桥中A5区域、蓝斑核及亚蓝斑核是主要调节肾脏TH阳性交感神经活性的中枢核团。5. LDTg头部和PPTg尾部均参与肾脏TH/TPH阳性交感神经活性的调节。
PARTⅠRole of Spinal Cord in Regulation Mouse Kidney:A Virally Mediated Trans-synaptic Tracing StudyTo determine the spinal innervation and neuronal connections is important for studying renal metabolic responses. In this study, the spinal cords of 13 adult male C57BL/6J strain mice were retrogradely mapped using injections of pseudorabies virus (PRV)-614. The virus injected into the kidney was specifically transported to the spinal cord. At 5d after injection of the PRV-614, PRV-614 positive cells were found in the intermediolateral cell column, the intercalates nucleus or the central autonomic nucleus of spinal cord segments T4 to L1, and most PRV-614 labeled cells were found in the T9 segment. Our results revealed neuroanatomic circuits between kidney and the spinal intermediolateral cell column (IML) neurons. PARTⅡTransneuronal Labeling of Brainstem Neuronal Populations by Injection of Pseudorabies Virus into Mice KidneysThe autonomic nervous system is the primary neural mediator of renal catabolic and anabolic responses to internal stimuli. Our understanding of the brainstem neuronal populations that project to kidney is important for studying renal metabolic responses. In this study, the spinal cords and brainstem of 19 adult male C57BL/6J strain mice were retrogradely mapped using injections of pseudorabies virus-614. The virus injected into the kidney was specifically transported to the spinal cord and brainstem through the renal nerve. The rostral ventromedial medulla, rostral ventrolateral medulla, medullary raphe nuclei, A5 region, Locus coeruleus and nucleus subcoeruleus all contributed to the regulation of innervating sympathetic activity within the kidney. Sympathetic outflow to the kidney was regulated by different types of neural populations, including serotonin-, tryptophan hydroxylase-, and tyrosine hydroxylase-positive neurons in the brainstem. Neural circuit tracing could reliably identify medullary neurons that received synaptic inputs originating from renal autonomic afferents. Our results reveal neuroanatomical substrates of the descending serotonergic and catecholaminergic neuronal circuits in the brainstem for the regulation of renal functions. PartⅢLaterodorsal Tegmentum and Pedunculopontine Tegmental Nucleus Circuits Regulate Renal Functions: Neuroanatomical Evidence in Mice ModelsNeurons in the laterodorsal tegmentum (LDTg) and pedunculopontine tegmental nucleus (PPTg) play important roles in central autonomic circuits of the kidney. In this study, we used a combination of retrograde tracers pseudorabies virus (PRV)-614 and fluorescence immunohistochemistry to characterize the neuroanatomic substrate of PPTg and LDTg innervating the kidney in the mouse. PRV-614-infected neurons were retrogradely labeled in the rostral and middle parts of LDTg, and the middle and caudal parts of PPTg after tracer injection in the kidney. PRV-614/TPH double-labeled neurons were mainly localized in the rostral of LDTg, whereas PRV-614/TH neurons were scattered within the three parts of LDTg. PRV-614/TPH and PRV-614/TH neurons were located predominantly in the caudal of PPTg (cPPTg). These data provided direct neuroanatomical foundation for the identification of serotonergic and catecholaminergic projections from the mid-brain tegmentum to the kidney.
PARTⅠRole of Spinal Cord in Regulation Mouse Kidney:A Virally Mediated Trans-synaptic Tracing StudyTo determine the spinal innervation and neuronal connections is important for studying renal metabolic responses. In this study, the spinal cords of 13 adult male C57BL/6J strain mice were retrogradely mapped using injections of pseudorabies virus (PRV)-614. The virus injected into the kidney was specifically transported to the spinal cord. At 5d after injection of the PRV-614, PRV-614 positive cells were found in the intermediolateral cell column, the intercalates nucleus or the central autonomic nucleus of spinal cord segments T4 to L1, and most PRV-614 labeled cells were found in the T9 segment. Our results revealed neuroanatomic circuits between kidney and the spinal intermediolateral cell column (IML) neurons. PARTⅡTransneuronal Labeling of Brainstem Neuronal Populations by Injection of Pseudorabies Virus into Mice KidneysThe autonomic nervous system is the primary neural mediator of renal catabolic and anabolic responses to internal stimuli. Our understanding of the brainstem neuronal populations that project to kidney is important for studying renal metabolic responses. In this study, the spinal cords and brainstem of 19 adult male C57BL/6J strain mice were retrogradely mapped using injections of pseudorabies virus-614. The virus injected into the kidney was specifically transported to the spinal cord and brainstem through the renal nerve. The rostral ventromedial medulla, rostral ventrolateral medulla, medullary raphe nuclei, A5 region, Locus coeruleus and nucleus subcoeruleus all contributed to the regulation of innervating sympathetic activity within the kidney. Sympathetic outflow to the kidney was regulated by different types of neural populations, including serotonin-, tryptophan hydroxylase-, and tyrosine hydroxylase-positive neurons in the brainstem. Neural circuit tracing could reliably identify medullary neurons that received synaptic inputs originating from renal autonomic afferents. Our results reveal neuroanatomical substrates of the descending serotonergic and catecholaminergic neuronal circuits in the brainstem for the regulation of renal functions. PartⅢLaterodorsal Tegmentum and Pedunculopontine Tegmental Nucleus Circuits Regulate Renal Functions: Neuroanatomical Evidence in Mice ModelsNeurons in the laterodorsal tegmentum (LDTg) and pedunculopontine tegmental nucleus (PPTg) play important roles in central autonomic circuits of the kidney. In this study, we used a combination of retrograde tracers pseudorabies virus (PRV)-614 and fluorescence immunohistochemistry to characterize the neuroanatomic substrate of PPTg and LDTg innervating the kidney in the mouse. PRV-614-infected neurons were retrogradely labeled in the rostral and middle parts of LDTg, and the middle and caudal parts of PPTg after tracer injection in the kidney. PRV-614/TPH double-labeled neurons were mainly localized in the rostral of LDTg, whereas PRV-614/TH neurons were scattered within the three parts of LDTg. PRV-614/TPH and PRV-614/TH neurons were located predominantly in the caudal of PPTg (cPPTg). These data provided direct neuroanatomical foundation for the identification of serotonergic and catecholaminergic projections from the mid-brain tegmentum to the kidney.
引文
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1. Sakamoto H. Gastrin-releasing peptide system in the spinal cord mediates masculine sexual function. Anat Sci Int.2011;86(1):19-29.
2. McDonald TJ, Jornvall H, Nilsson G, et al. Characterization of a gastrin releasing peptide from porcine non-antral gastric tissue. Biochem Biophys Res Commun. 1979;90(1):227-33.
3. Patel O, Shulkes A, Baldwin GS. Gastrin-releasing peptide and cancer. Biochim Biophys Acta.2006;1766(1):23-41.
4. Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature.2007;448(7154):700-3.
5. Sun YG, Zhao ZQ, Meng XL, et al. Cellular basis of itch sensation. Science.2009; 325(5947):1531-4.
6. Battey JF, Way JM, Corjay MH, et al. Molecular cloning of the
bombesin/gastrin-releasing peptide receptor from Swiss 3T3 cells. Proc Natl Acad Sci USA.1991;88(2):395-9.
7. Sakamoto H. The neurobiology of psychogenic erectile dysfunction in the spinal cord. JAndrol.2010;31(6):519-26.
8. Sakamoto H, Matsuda K-I, Zuloaga DG, et al. Sexually dimorphic gastrin releasing peptide system in the spinal cord controls male reproductive functions. Nat Neurosci 2008;11(6):634-6.
9. Battey J, Wada E. Two distinct receptor subtypes for mammalian bombesin-like peptides. Trends Neurosci.1991;14(12):524-8.
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11. Morris JA, Jordan CL, Breedlove SM. Sexual differentiation of the vertebrate nervous system. Nat Neurosci.2004;7(10):1034-9.
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14. Sakamoto H, Arii T, Kawata M. High-voltage electron microscopy reveals direct synaptic inputs from a spinal gastrin-releasing peptide system to neurons of the spinal nucleus of bulbocavernosus. Endocrinology.2010;151(1):417-21.
15. Zuloaga DG, Puts DA, Jordan CL, et al. The role of androgen receptors in the masculinization of brain and behavior:what we've learned from the testicular feminization mutation. Horm Behav.2008;53(5):613-26.
16. Giuliano F, Rampin O. Central neural regulation of penile erection. Neurosci Biobehav Rev.2000;24(5):517-33.
17. Sun XQ, Xu C, Leclerc P, et al. Spinal neurons involved in the control of the seminal vesicles:a transsynaptic labeling study using pseudorabies virus in rats. Neuroscience. 2009;158(2):786-97.
18. Mulchahey JJ, Ekhator NN, Zhang H, et al. Cerebrospinal fluid and plasma testosterone levels in post-traumatic stress disorder and tobacco dependence. Psychoneuroendocrinology.2001;26(3):273-85.
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1. Sakamoto H. Gastrin-releasing peptide system in the spinal cord mediates masculine sexual function. Anat Sci Int.2011;86(1):19-29.
2. McDonald TJ, Jornvall H, Nilsson G, et al. Characterization of a gastrin releasing peptide from porcine non-antral gastric tissue. Biochem Biophys Res Commun. 1979;90(1):227-33.
3. Patel O, Shulkes A, Baldwin GS. Gastrin-releasing peptide and cancer. Biochim Biophys Acta.2006;1766(1):23-41.
4. Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature.2007;448(7154):700-3.
5. Sun YG, Zhao ZQ, Meng XL, et al. Cellular basis of itch sensation. Science.2009; 325(5947):1531-4.
6. Battey JF, Way JM, Corjay MH, et al. Molecular cloning of the
bombesin/gastrin-releasing peptide receptor from Swiss 3T3 cells. Proc Natl Acad Sci USA.1991;88(2):395-9.
7. Sakamoto H. The neurobiology of psychogenic erectile dysfunction in the spinal cord. JAndrol.2010;31(6):519-26.
8. Sakamoto H, Matsuda K-I, Zuloaga DG, et al. Sexually dimorphic gastrin releasing peptide system in the spinal cord controls male reproductive functions. Nat Neurosci 2008;11(6):634-6.
9. Battey J, Wada E. Two distinct receptor subtypes for mammalian bombesin-like peptides. Trends Neurosci.1991;14(12):524-8.
10. Sakamoto H, Matsuda K, Zuloaga DG et al. Stress affects a gastrin-releasing peptide system in the spinal cord that mediates sexual function:implications for psychogenic erectile dysfunction. PLoS One.2009;4(1):e4276.
11. Morris JA, Jordan CL, Breedlove SM. Sexual differentiation of the vertebrate nervous system. Nat Neurosci.2004;7(10):1034-9.
12. Sakamoto H, Takanami K, Zuloaga DG, et al. Androgen regulates the sexually dimorphic gastrin-releasing peptide system in the lumbar spinal cord that mediates male sexual function. Endocrinology.2009;150 (8):3672-9.
13. Sakamoto H, Kawata M. Gastrin-releasing peptide system in the spinal cord controls male sexual behaviour. J Neuroendocrinol.2009;21(4):432-5.
14. Sakamoto H, Arii T, Kawata M. High-voltage electron microscopy reveals direct synaptic inputs from a spinal gastrin-releasing peptide system to neurons of the spinal nucleus of bulbocavernosus. Endocrinology.2010;151(1):417-21.
15. Zuloaga DG, Puts DA, Jordan CL, et al. The role of androgen receptors in the masculinization of brain and behavior:what we've learned from the testicular feminization mutation. Horm Behav.2008;53(5):613-26.
16. Giuliano F, Rampin O. Central neural regulation of penile erection. Neurosci Biobehav Rev.2000;24(5):517-33.
17. Sun XQ, Xu C, Leclerc P, et al. Spinal neurons involved in the control of the seminal vesicles:a transsynaptic labeling study using pseudorabies virus in rats. Neuroscience. 2009;158(2):786-97.
18. Mulchahey JJ, Ekhator NN, Zhang H, et al. Cerebrospinal fluid and plasma testosterone levels in post-traumatic stress disorder and tobacco dependence. Psychoneuroendocrinology.2001;26(3):273-85.
19. Liberzon I, Krstov M, Young EA. Stress-restress:effects on ACTH and fast feedback. Psychoneuroendocrinology.1997;22(6):443-53.