Androgenic, but not estrogenic, protection of motoneurons from somal and dendritic atrophy induced by the death of neighboring motoneurons

Developmental Neurobiology

Volumn 67, Issue 8, 2007, Pages 1094-1106

  Fargo, Keith N ^a   Sengelaub, Dale R ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Dendrites; Morphology; Neuroprotection; Steroids

Indexed keywords

ANDROSTANOLONE; ESTRADIOL; TESTOSTERONE;

ANIMAL CELL; ARTICLE; ATROPHY; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; MALE; MOTONEURON; MOTONEURON NUCLEUS; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATIC CELL;

ANIMALS; ATROPHY; CELL DEATH; DENDRITES; DIHYDROTESTOSTERONE; ESTRADIOL; MALE; MOTOR NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TESTOSTERONE;

EID: 34548354845     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20454     Document Type: Article

References (74)

1. Ahlbom E, Prins GS, Ceccatelli S. 2001. Testosterone protects cerebellar granule cells from oxidative stress-induced cell death through a receptor mediated mechanism. Brain Res 892:255-262.
2. Balice-Gordon RJ, Breedlove SM, Bernstein S, Lichtman JW. 1990. Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: In Vivo observations in the androgen-sensitive bulbocavernosus muscle of mice. J Neurosci 10:2660-2671.
3. Bermant G, Davidson JM. 1974. Biological Bases of Sexual Behavior. New York: Harper & Row, 306 p.
4. Bialek M, Zaremba P, Borowicz KK, Czuczwar SJ. 2004. Neuroprotective role of testosterone in the nervous system. Pol J Pharmacol 56:509-518.
5. Bleisch WV, Harrelson A. 1989. Androgens modulate end-plate size and ACh receptor density at synapses in rat levator ani muscle. J Neurobiol 20:189-202.
6. Bleisch WV, Harrelson AL, Luine VN. 1982. Testosterone increases acetylcholine receptor number in the "levator ani" muscle of the rat. J Neurobiol 13:153-161.
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. Breedlove SM, Arnold AP. 1983. Sex differences in the pattern of steroid accumulation by motoneurons of the rat lumbar spinal cord. J Comp Neurol 215:211-216.
10. Burke KA, Kuwajima M, Sengelaub DR. 1999. Aromatase inhibition reduces dendritic growth in a sexually dimorphic rat spinal nucleus. J Neurobiol 38:301-312.
11. Burke KA, Widows MR, Sengelaub DR. 1997. Synergistic effects of testosterone metabolites on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. J Neurobiol 33:1-10.
12. Coggeshall RE. 1992. A consideration of neural counting methods. Trends Neurosci 15:9-13.
13. Doherty JG, Burns AS, O'Ferrall DM, Ditunno JF Jr. 2002. Prevalence of upper motor neuron vs. lower motor neuron lesions in complete lower thoracic and lumbar spinal cord injuries. J Spinal Cord Med 25:289-292.
14. Dube JY, Lesage R, Tremblay RR. 1976. Androgen and estrogen binding in rat skeletal and perineal muscles. Can J Biochem 54:50-55.
15. Fargo KN, Foster AM, Harty MW, Sengelaub DR. 2003. Estrogen alters excitability but not morphology of a sexually dimorphic neuromuscular system in adult rats. J Neurobiol 56:66-77.
16. Fargo KN, Sengelaub DR. 2004a. Exogenous testosterone prevents motoneuron atrophy induced by contralateral motoneuron depletion. J Neurobiol 60:348-359.
17. Fargo KN, Sengelaub DR. 2004b. Testosterone manipulation protects motoneurons from dendritic atrophy after contralateral motoneuron depletion. J Comp Neurol 469:96-106.
18. Fargo KN, Sengelaub DR. 2005. Testosterone treatment prevents deficits in motor activation caused by partial loss of motoneurons. Program No. 672.8. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
19. Forger NG, Breedlove SM. 1987. Seasonal variation in mammalian striated muscle mass and motoneuron morphology. J Neurobiol 18:155-165.
20. Forger NG, Fishman RB, Breedlove SM. 1992. Differential effects of testosterone metabolites upon the size of sexually dimorphic motoneurons in adulthood. Horm Behav 26:204-213.
21. Forger NG, Wagner CK, Contois M, Bengston L, MacLennan AJ. 1998. Ciliary neurotrophic factor receptor α in spinal motoneurons is regulated by gonadal hormones. J Neurosci 18:8720-8729.
22. Foster AM, Sengelaub DR. 2004. Hormone sensitivity of muscle activation in the sexually dimorphic SNB/BC neuromuscular system of the rat. Neurosci Lett 359:41-44.
23. Goldstein LA, Kurz EM, Kalkbrenner AE, Sengelaub DR. 1993. Changes in dendritic morphology of rat spinal motoneurons during development and after unilateral target deletion. Dev Brain Res 73:151-163.
24. Goldstein LA, Kurz EM, Sengelaub DR. 1990. Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus. J Neurosci 10:935-946.
25. Goldstein LA, Sengelaub DR. 1993. Motoneuron morphology in the dorsolateral nucleus of the rat spinal cord: Normal development and androgenic regulation. J Comp Neurol 338:588-600.
26. Goldstein LA, Sengelaub DR. 1994. Differential effects of dihydrotestosterone and estrogen on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. J Neurobiol 25:878-892.
27. Hammond J, Le Q, Goodyer C, Gelfand M, Trifiro M, LeBlanc A. 2001. Testosterone-mediated neuroprotection through the androgen receptor in human primary neurons. J Neurochem 77:1319-1326.
28. Hart BL, Melese-D'Hospital PY. 1983. Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol Behav 31:807-813.
29. Hebbeler SL, Sengelaub DR. 2003. Development of a sexually dimorphic neuromuscular system in male rats after spinal transection: Morphologic changes and implications for estrogen sites of action. J Comp Neurol 467:80-96.
30. Hebbeler SL, Verhovshek T, Sengelaub DR. 2001. Ovariectomy attenuates dendritic growth in hormone-sensitive spinal motoneurons. J Neurobiol 48:301-314.
31. Hebbeler SL, Verhovshek T, Sengelaub DR. 2002. N- methyl-D-aspartate receptor blockade inhibits estrogenic support of dendritic growth in a sexually dimorphic rat spinal nucleus. J Comp Neurol 451:142-152.
32. Hedge GA, Colby HD, Goodman RL. 1987. Clinical Endocrine Physiology. Philadelphia: W. B. Saunders, 400 p.
33. Henderson VW, Reynolds DW. 2002. Protective effects of estrogen on aging and damaged neural systems. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, Brain and Behavior. San Diego: Academic Press, pp 821-837.
34. Hoffman GE, Merchenthaler I, Zup SL. 2006. Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine 29:217-231.
35. Holmes GM, Sachs BD. 1992. Erectile function and bulbospongiosus EMG activity in estrogen-maintained castrated rats vary with behavioral context. Horm Behav 26:406-419.
36. Huppenbauer CB, Tanzer L, DonCarlos LL, Jones KJ. 2005. Gonadal steroid attenuation of developing hamster facial motoneuron loss by axotomy: Equal efficacy of testosterone, dihydrotestosterone, and 17-β estradiol. J Neuroscience 25:4004-4013.
37. Jones KJ. 1993. Gonadal steroids as promoting factors in axonal regeneration. Brain Res Bull 30:491-498.
38. Jones KJ, Brown TJ, Damaser M. 2001. Neuroprotective effects of gonadal steroids on regenerating peripheral motoneurons. Brain Res Rev 37:372-382.
39. Kalb RG. 1994. Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120:3063-3071.
40. Kujawa KA, Emeric E, Jones KJ. 1991. Testosterone differentially regulates the regenerative properties of injured hamster facial motoneurons. J Neurosci 11:3898-3906.
41. Kujawa KA, Jones KJ. 1990. Testosterone-induced acceleration of recovery from facial paralysis in male hamsters: Temporal requirements of hormone exposure. Physiol Behav 48:765-768.
42. Kujawa KA, Kinderman NB, Jones KJ. 1989. Testosterone-induced acceleration of recovery from facial paralysis following crush axotomy of the facial nerve in male hamsters. Exp Neurol 105:80-85.
43. Kurz EM, Brewer RG, Sengelaub DR. 1991. Hormonally mediated plasticity of motoneuron morphology in the adult rat spinal cord: A cholera toxin-HRP study. J Neurobiol 22:976-988.
44. Kurz EM, Sengelaub DR, Arnold AP. 1986. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232:395-398.
45. Leslie M, Forger NG, Breedlove SM. 1991. Does androgen affect axonal transport of cholera toxin HRP in spinal motoneurons? Neurosci Lett 126:199-202.
46. Matsumoto A, Arai Y, Hyodo S. 1993. Androgenic regulation of expression of β-tubulin messenger ribonucleic acid in motoneurons of the spinal nucleus of the bulbocavernosus. J Neuroendocrinol 5:357-363.
47. Matsumoto A, Arai Y, Urano A, Hyodo S. 1992. Effect of androgen on the expression of gap junction and β-actin mRNAs in adult rat motoneurons. Neurosci Res 14:133-144.
48. Meisel RL, O'Hanlon JK, Sachs BD. 1984. Differential maintenance of penile responses and copulatory behavior by gonadal hormones in castrated male rats. Horm Behav 18:56-64.
49. Mesulam MM. 1982. Tracing Neural Connections with Horseradish Peroxidase. Chichester: Wiley.
50. Monks DA, Getsios S, MacCalman CD, Watson NV. 2001. N-cadherin is regulated by gonadal steroids in adult sexually dimorphic spinal motoneurons. J Neurobiol 47:255-264.
51. Monks DA, O'Bryant EL, Jordan CL. 2004. Androgen receptor immunoreactivity in skeletal muscle: Enrichment at the neuromuscular junction. J Comp Neurol 473:59-72.
52. National Institutes of Health (NIH) National Library of Medicine. 2006. Amyotrophic Lateral Sclerosis - Genetics Home Reference [WWW document]. Available at URL http://ghr.nlm.nih.gov/condition=amyotrophiclateralsclerosis. Published 28 July 2006, accessed August 2006.
53. Nowacek AS, Sengelaub DR. 2006. Estrogenic support of motoneuron dendritic growth via the neuromuscular periphery in a sexually dimorphic motor system. J Neurobiol 66:962-976.
54. v2.2 calcium channels' functional expression at rat levator ani neuromuscular junction. Neuroscience 134:817-826.
55. Pike CJ. 2001. Testosterone attenuates β-amyloid toxicity in cultured hippocampal neurons. Brain Res 919:160-165.
56. Pozzi P, Bendotti C, Simeoni S, Piccioni F, Guerini V, Marron TU, Martini L, Poletti A. 2003. Androgen 5-α-reductase type 2 is highly expressed and active in rat spinal cord motor neurones. J Neuroendocrinol 15:882-887.
57. Ramsden M, Shin TM, Pike CJ. 2003. Androgens modulate neuronal vulnerability to kainate lesion. Neuroscience 122:573-578.
58. Rand MN, Breedlove SM. 1995. Androgen alters the dendritic arbors of SNB motoneurons by acting upon their target muscles. J Neurosci 15(6):4408-4416.
59. Sachs BD. 1982. Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J Reprod Fertil 66:433-443.
60. Sasaki M, Arnold AP. 1991. Androgenic regulation of dendritic trees of motoneurons in the spinal nucleus of the bulbocavernosus: Reconstruction after intracellular iontophoresis of horseradish peroxidase. J Comp Neurol 308:11-27.
61. Smith ER, Damassa DA, Davidson JM. 1977. Hormone administration: Peripheral and intracranial implants. In: Meyer RD, editor. Methods in Psychobiology. New York: Academic Press, pp 259-279.
62. Stirpe F, Barbieri L, Battelli MG, Soria M, Lappi DA. 1992. Ribosome-inactivating proteins from plants: Present status and future prospects. Biotechnology 10:405-412.
63. Stirpe F, Gasperi-Campani A, Barbieri L, Falasca A, Abbondanza A, Stevens WA. 1983. Ribosome-inactivating proteins from the seeds of Saponaria officinalis L. (soapwort), of Agrostemma githago L. (corn cockle) and from Asparagus officinalis L. (asparagus), and from the latex of Hura crepitans L. (sandbox tree). Biochem J 216:617-625.
64. Tanzer L, Jones KJ. 1997. Gonadal steroid regulation of hamster facial nerve regeneration: Effects of dihydrotestosterone and estradiol. Exp Neurol 146:258-264.
65. Tanzer L, Jones KJ. 2004. Neurotherapeutic action of testosterone on hamster facial nerve regeneration: Temporal window of effects. Horm Behav 45:339-344.
66. Venable JH. 1966. Morphology of the cells of normal, testosterone- deprived and testosterone-stimulated levator ani muscles. Am J Anat 119:271-301.
67. Verhovshek T, Wellman CL, Sengelaub DR. 2005. NMDA receptor binding declines differentially in three spinal motor nuclei during postnatal development. Neurosci Lett 384:122-126.
68. Wainman P, Shipounoff GC. 1941. The effects of castration and testosterone propionate on the striated perineal musculature in the rat. Endocrinology 29:975-978.
69. Watson NV, Freeman LM, Breedlove SM. 2001. Neuronal size in the spinal nucleus of the bulbocavernosus: Direct modulation by androgen in rats with mosaic androgen insensitivity. J Neurosci 21:1062-1066.
70. West MJ, Gundersen HJG. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22.
71. Woolley CS, Cohen RS. 2002. Sex steroids and neuronal growth in adulthood. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, editors. Hormones, Brain and Behavior. San Diego: Academic Press, pp 717-777.
72. Woolley CS, McEwen BS. 1994. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
73. Yang LY, Verhovshek T, Sengelaub DR. 2004. Brain-derived neurotrophic factor and androgen interact in the maintenance of dendritic morphology in a sexually dimorphic rat spinal nucleus. Endocrinology 145(1):161-168.
74. Zup SL, Forger NG. 2002. Testosterone regulates BCL-2 immunoreactivity in a sexually dimorphic motor pool of adult rats. Brain Res 950:312-316.