Testosterone prevents synaptic loss in the perineal motoneuron pool in the spinal cord in male rats exposed to chronic stress

Stress

Volumn 8, Issue 2, 2005, Pages 133-140

  Matsumoto, Akira ^a  

^a JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Onuf's nucleus; Restraint stress; Spinal nucleus of the bulbocavernosus; Synaptic plasticity; Testosterone

Indexed keywords

ANDROGEN; CHOLERA TOXIN; HORSERADISH PEROXIDASE; TESTOSTERONE; TETRAMETHYLBENZIDINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; COPULATION; HORMONAL THERAPY; IMMOBILIZATION STRESS; MALE; MOTONEURON; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SPINAL CORD; STRESS; SYNAPTIC MEMBRANE; TESTOSTERONE BLOOD LEVEL;

ANIMALS; DISEASE MODELS, ANIMAL; MALE; MOTOR NEURONS; RATS; RATS, WISTAR; SPINAL CORD; STRESS, PSYCHOLOGICAL; SYNAPSES; TESTOSTERONE;

EID: 22144480092     PISSN: 10253890     EISSN: None     Source Type: Journal    
DOI: 10.1080/10253890500140642     Document Type: Article

References (71)

1. Al-Shamma HA, Arnold AP. 1995. Importance of target innervation in recovery from axotomy-induced loss of androgen receptor in rat perineal motoneurons. J Neurobiol 28:341-353.
2. Al-Shamma HA, Arnold AP. 1997. Brain-derived neurotrophic factor regulates expression of androgen receptors in perineal motoneurons. Proc Natl Acad Sci USA 94:1521-1526.
3. Araki I, Harada Y, Kuno M. 1991. Target-dependent hormonal control of neuron size in the rat spinal nucleus of the bulbocavernosus. J Neurosci 11:3025-3033.
4. Arnold AP, Breedlove SM. 1985. Organizational and activational effects of sex steroids on brain and behavior: A reanalysis. Horm Behav 19:423-442.
5. Bidzinska B, Petraglia F, Anigioni S, Genazzani AD, Riscuolo M, Ficarra G, Gallinelli A, Trentini GP, Genazzani AR. 1993. Effect of different chronic intermittent stressors and acetyl-I-carnitine on hypothalamic beta-endorphin and GnRH and plasma testosterone levels in male rats. Neuroendocrinology 57:985-990.
6. Breedlove SM. 1986. Cellular analysis of hormone influence on motoneuronal development and function. J Neurobiol 17:157-176.
7. Breedlove SM, Arnold AP. 1980. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
8. Breedlove SM, Arnold AP. 1981. Sexually dimorphic motor nucleus in the rat lumbar spinal cord: Response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res 225:297-307.
9. Collu R, Gibb W, Ducharme GR. 1984. Role of catecholamines in the inhibitory effect of immobolization stress on testosterone secretion in rats. Biol Reprod 30:416-422.
10. Conrad CD, Magarinos AM, LeDoux JE, McEwen BS. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 113:902-913.
11. Conrad CD, Jackson JL, Wise LS. 2004. Chronic stress enhances ibotenic acid-induced damage selectively within the hippocampal CA3 region of male, but not female rats. Neuroscience 125:759-767.
12. Cook SC, Wellman CL. 2004. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60:236-248.
13. Dallman MF, Viau VG, Bhatnagar S, Gomez F, Laugero K, Bell ME. 2002. Corticotropin-releasing factor, corticosteroids, stress, and sugar: Energy balance, the brain, and behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, brain and behavior. Vol. 1. San Diego: Elsevier Science, p 571-631.
14. D'Aquila PS, Brain P, Willner P. 1994. Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol Behav 56:861-867.
15. Dube JY, Lesage R, Tremble RR. 1976. Androgen and estrogen binding in rat skeletal and perineal muscles. Can J Biochem 54:50-55.
16. Evans RM. 1988. The steroid and thyroid hormone receptor superfamily. Science 240:889-895.
17. Gibson SJ, Polak JM, Katagiri T, Su H, Weller RO, Brownell DB, Holland S, Hughes JT, Kikuyama S, Ball J, Bloom SR, Steiner TJ, De Belleroche J, Clifford Rose F. 1988. A comparison of the distributions of eight peptides in spinal cord from normal controls and cases of motor neurone disease with special reference to Onuf's nucleus. Brain Res 474:255-278.
18. Gonzalez-Quijano M, Ariznavarreta C, Martin A, Tresguerres J, Lopez-Calderon A. 1991. Naltrexone does not reverse the inhibitory effect of chronic restraint on gonadotropin secretion in the intact male rat. Neuroendocrinology 54:447-453.
19. Gray G, Smith E, Damassa D, Ehrenkranz J, Davidson J. 1978. Neuroendocrine mechanisms meditating the suppression of circulating testosterone levels associated with chronic stress in male rats. Neuroendocrinology 25:247-256.
20. Hart BL, Leedy MG. 1985. Neurological bases of male sexual behavior. A comparative study. In: Adler N, Pfaff D, Goy RW, editors. Handbook of behavioral neurobiology, Vol. 7. Reproduction. New York: Plenum Press, p 373-422.
21. Johnson H, Hokfelt T, Ulfhake B. 1996. Decreased expression of trkB and trkC mRNAs in spinal motoneurons of aged rats. Eur J Neurosci 8:494-499.
22. Katagiri T, Gibson SJ, Su HC, Polak JM. 1986. Composition and central projections of the pudendal nerve in the rat investigated by combined peptide immunocytochemistry and retrograde fluorescent labelling. Brain Res 372:313-322.
23. Kawano M, Sugita O, Inagaki S, Furuyama T, Takagi H. 1993. Neuropeptide Y innervation in the spinal nucleus of bulbocavernosus of the rat. Neurosci Lett 152:158-160.
24. Kojima M, Matsuura T, Tanaka A, Amagi T, Imanishi J, Sano Y. 1985. Characteristic distribution of noradrenergic terminals on the anterior horn motoneuron innervating the perineal striated muscles in the rat. An immunoelectron-microscopic study. Anat Embryol 171:267-273.
25. Konishi A, Itoh K, Sugimoto T, Yasui Y, Kaneko T, Takeda M, Mizuno M. 1985. Leucine-enkephalin-like immunoreactive afferent fibers to pudendal motoneuron in the cat. Neurosci Lett 61:109-113.
26. Kurz EM, Sengelaub DR, Arnold AP. 1986. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232:395-398.
27. Leedy MG, Bresnahan JC, Beattie MS. 1987. Testosterone induced plasticity of synaptic inputs to adult mammalian motoneurons. Brain Res 424:386-390.
28. Leedy MG, Bresnahan JC, Beattie MS. 1991. Ultrastructural analysis of TH and 5-HT input to the SNB of the male rats. Soc Neurosci Abstr 17:469.
29. Lemann W, Spaer CB, Rye DB, Wainer BH. 1985. Stabilization of TMB reaction product for electron microscopic retrograde and anterograde fiber tracing. Brain Res Bull 14:277-281.
30. Leslie M, Forger NG, Breedlove SM. 1991. Does androgen affect axonal transport of cholera toxin HRP in spinal motoneurons? Neurosci Lett 126:199-202.
31. Magarinos AM, McEwen BS. 1995. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69:89-98.
32. Magarinos AM, McEwen BS, Flugge G, Fuchs E. 1996. Chronic psychological stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16:3534-3540.
33. Magarinos AM, Garcia Verdugo JM, McEwen BS. 1997. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci USA 94:14002-14008.
34. Matsumoto A. 1991. Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology 16:25-40.
35. Matsumoto A. 1992a. Hormonally induced synaptic plasticity in the adult neuroendocrine brain. Zool Sci 9:679-695.
36. Matsumoto A. 1992b. Sex steroid induction of synaptic reorganization in adult neuro-endocrine brain. Rev Neurosci 3:287-306.
37. Matsumoto A. 1997. Hormonally induced neuronal plasticity in the adult motoneurons. Brain Res Bull 44:539-547.
38. Matsumoto A. 1998. Synaptic changes in the perineal motoneurons of aged male rats. J Comp Neurol 400:103-109.
39. Matsumoto A. 2001. Androgen stimulates neuronal plasticity in the perineal motoneurons of aged male rats. J Comp Neurol 430:389-395.
40. Matsumoto A, Prins PG. 1998. Age-dependent changes in androgen receptor immuno-reactivity in motoneuron of the spinal nucleus of the bulbocavernosus of male rats. Neurosci Lett 243:29-32.
41. Matsumoto A, Prins GS. 2002. Androgenic regulation of expression of androgen receptor protein in the perineal motoneurons of aged male rats. J Comp Neurol 443:383-387.
42. Matsumoto A, Micevych PE, Arnold AP. 1988. Androgen regulates synaptic input to motoneurons of the adult rat spinal cord. J Neurosci 8:4168-4176.
43. Matsumoto A, Arai Y, Urano A, Hyodo H. 1995. Molecular basis of neuronal plasticity to gonadal steroids. Funct Neurol 10:59-76.
44. Matsumoto A, Arai Y, Prins PG. 1996. Androgenic regulation of androgen receptor immunoreactivity in motoneurons of the spinal nucleus of the bulbocavernosus of male rats. J Neuroendocrinol 8:552-559.
45. McEwen BS. 2002. Sex, stress and the hippocampus: Allostasis, allostatic load and the aging process. Neurobiol Aging 23:921-939.
46. McKenna KE, Nadelhaft I. 1986. The organization of the pudendal nerve in the male and female rat. J Comp Neurol 268:532-549.
47. Mesulam M-M. 1978. Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117.
48. Micevych PE, Coquelin A, Arnold AP. 1986. Immunohistochemical distribution of substance P, serotonin, and methionine enkephalin in sexually dimorphic nuclei of the rat lumbar spinal cord. J Comp Neurol 248:235-244.
49. Monder C, Sakai RP, Miroff Y, Blanchard DC, Blanchard RJ. 1994. Reciprocal changes in plasma corticosterone and testosterone in stressed male rats maintained in a visible burrow system: Evidence for a meditating role of testicular 11β-hydroxysteroid dehydrogenase. Endocrinology 134:1193-1198.
50. Popper P, Ulibarri C, Micevych PE. 1992. The role of target muscles in the expression of calcitonin-gene-related peptide mRNA in the spinal nucleus of the bulbocavernosus. Brain Res Mol Brain Res 13:43-51.
51. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR, McEwen BS, Morrison JH. 2004. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125:1-6.
52. Rajaoferta N, Passagia J-G, Marlier L, Poulat P, Pellas F, Sandillon F, Verschere B, Gouy BD, Geffard M, Privat A. 1992. Serotoninergic, noradrenergic, and peptidergic innervation of Onuf's nucleus of normal and transected spinal cords of baboons (Papio papio). J Comp Neurol 318:1-17.
53. Ramirez-Leon V, Ulfhake B. 1993. GABA-like immunoreactive innervation and dendro-dendritic contacts in the ventrolateral dendritic bundle in the cat S1 spinal cord segment: An electron microscopic study. Exp Brain Res 97:1-12.
54. Rand M, Breedlove SM. 1995. Androgen alters the dendrite arbors of SNB motoneuron by acting upon their target muscles. J Neurosci 15:4408-4416.
55. Retana-Marquez S, Salazar ED, Velazquez-Moctezuma J. 1996. Effect of acute and chronic stress on masculine sexual behavior in the rat. Psychoneuroendocrinology 21:39-50.
56. Retana-Marquez S, Bonilla-Jaime H, Vazquez-Palacios G, Martinez-Garcia R, Velazquez-Moctezuma J. 2003. Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm Behav 44:327-337.
57. Sachs BD, Meisel RL. 1988. The physiology of male sexual behavior. In: Knobil E, Neil JD, Ewing LL, Greenward GS, Markert CL, Pfaff DW, editors. The physiology of reproduction. Vol. 2. New York: Raven Press, p 1393-1485.
58. Schroder HD. 1980. Organization of the motoneuron innervating the pelvic muscles of the male rat. J Comp Neurol 192:567-587.
59. Sousa N, Almeida OFX, Holsboer F, Paula-Barbosa MM, Madeira MD. 1998. Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 2:237-250.
60. Sousa N, Lukoyanov NV, Madeira MD, Almeida OFX, Paula-Barbosa MM. 2000. Reorganization of the morphology of hippocampal neunte and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97:253-266.
61. Tashiro T, Ruda MA. 1988. Immunohistochemical identification of axons containing coexistent serotonin and substance P in the cat lumber spinal cord. Peptides 9:383-391.
62. Tashiro T, Satoda T, Matsushima R, Mizuno N. 1989a. Convergence of serotonin-, enkephalin- and substance P-like immunoreactive afferent fibers on single pudendal motoneurons in Onuf's nucleus of the cat: A light microscope study combining the triple immunochemical staining technique with the retrograde HRP-tracing method. Brain Res 481:392-398.
63. Tashiro T, Satoda T, Matsushima R, Mizuno N. 1989b. Possible origins of substance P-like immunoreactive axons within Onuf's nucleus of the cat. Brain Res 497:177-182.
64. Truss M, Beato M. 1993. Steroid hormone receptors: Interaction with deoxyribonucleic acid and transcription factors. Endocr Rev 14:459-479.
65. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM. 1989. Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 9:1705-1711.
66. Wagner CK, Clemens LG. 1993. Neurophysin-containing pathway from the paraventricular nucleus of the hypothalamus to a sexually dimorphic nucleus in lumbar spinal cord. J Comp Neurol 336:106-116.
67. Watanabe Y, Gould E, McEwen BS. 1992. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588:341-345.
68. Wellman CL. 2001. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 49:245-253.
69. Woolley CS, Gould E, McEwen BS. 1990. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225-231.
70. Yamamoto KR. 1985. Steroid receptor regulated transcription of specific genes and gene network. Annu Rev Genet 19:209-252.
71. Yang L-Y, Arnold AP. 2000. BDNF regulation of androgen receptor expression in axotomized SNB motoneurons of adult male rats. Brain Res 852:127-139.