Synergistic effects of testosterone metabolites on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus

Journal of Neurobiology

Volumn 33, Issue 1, 1997, Pages 1-10

  Burke, K A ^a   Widows, M R ^b   Sengelaub, D R ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

BHRP; Castration; Dendrites; Dihydrotestosterone; Estrogen; Soma size

Indexed keywords

ANDROSTANOLONE PROPIONATE; CHOLERA TOXIN; ESTRADIOL BENZOATE; HORSERADISH PEROXIDASE; TESTOSTERONE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; CONTROLLED STUDY; DENDRITE; HORMONAL REGULATION; MALE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SPINAL CORD; SPINAL CORD MOTONEURON;

ANIMALS; AXONAL TRANSPORT; CHOLERA TOXIN; DENDRITES; DIHYDROTESTOSTERONE; ESTRADIOL; HORSERADISH PEROXIDASE; MALE; MOTOR NEURONS; ORCHIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 0030926102     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199707)33:1<1::AID-NEU1>3.0.CO;2-7     Document Type: Article

References (66)

1. AL-SHAMMA, H. A. and ARNOLD, A. P. (1996). Brainderived neurotrophic factor regulates expression of androgen receptor in perineal motoneurons. Soc. Neurosci Absr. 22:559.
2. ARNOLD, A. P. (1984). Androgen regulation of motoneuron size and number. Trends Neurosci. 7:239-242.
3. ARNOLD, A. P. and GORSKI, R. A. (1984). Gonadal steroid induction of structural sex differences in the central nervous system. Annu. Rev. Neurosci. 7:431-442.
4. ARNOLD, A. P., BBOTTJER, S. W., NORDEEN, E. J., NORDEEN, K. W., and SENGELAUB, D. R. (1987). Hormones and critical periods in behavioral and neural development. In: Imprinting and Cortical Plasticity, J. P. Rauschecker and P. Marier, Eds. John Wiley, New York, pp. 55-97.
5. BAUM, M. J. and VREEBURG, J. T. M. (1973). Copulation in castrated male rats following combined treatment with estradiol and dihydrotestosterone. Science 182:283-285.
6. BREEDLOVE, S. M. and ARNOLD A. P. (1980). Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
7. BREEDLOVE, S. M. and ARNOLD, A. P. (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.
8. BREEDLOVE, S. M. and ARNOLD, A. P. (1983a). Hormonal control of a developing neuromuscular system: I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide. J. Neurosci. 3:417-423.
9. BREEDLOVE, S. M. and ARNOLD, A. P. (1983b). Hormonal control of a developing neuromuscular system: II. Sensitive periods for the androgen-induced masculinization of the rat spinal nucleus of the bulbocavernosus. J. Neurosci. 3:424-432.
10. BREEDLOVE, S. M., JACOBSON, C. D., GORSKI, R. A., and ARNOLD, A. P. (1982). Masculinization of the female rat spinal cord following a single neonatal injection of testosterone propionate but not estradiol benzoate. Brain Res. 237:173-181.
11. BROT M. D., DEVRIES, G. J., and DORSA, D. M. (1993). Local implants of testosterone metabolites regulate vasopressin mRNA in sexually dimorphic nuclei of the rat brain. Peptides 14:933-940.
12. BURKE, K. A. and SENGELAUB, D. R. (1995). Development of motoneuron morphology in the spinal nucleus of the bulbocavernosus after spinal transection. Soc. Neurosci Absr. 21:40.
13. CIHAK, R., GUTMAN, E., and HANZLIKOVA, V. (1970). Involution and hormone-induced persistence of the muscle sphincter (levator) ani in female rats. J. Anat. (Lond.) 106:93-110.
14. CORPÉCHOT, C., BAULIEU, E. E., and ROBEL, P. (1981). Testosterone, dihydrotestosterone and androstanediols in plasma, testes and prostates of rats during development. Acta Endocrinol. 96:127-135.
15. DUBE, J. Y., LESAGE, R., and TREMBLAY, R. R. (1976). Androgen and estrogen binding in rat skeletal and perineal muscles. Can. J. Biochem. 54:50-55.
16. FERREIRA, A. and CACERES, A. (1991). Estrogen-enhanced neunte growth: evidence for a selective induction of tau and stable microtubules. J. Neurosci. 11:392-400.
17. FORGER, N. G. and BREEDLOVE, S. M. (1987). Seasonal variation in striated muscle mass and motoneuron morphology. J. Neurobiol. 18:155-165.
18. GARCIA-SERUGA, L. M., OLMOS, G., TRANQUE, P., and NAFTOLIN, F. (1987). Rapid effects of gonadal steroids upon hypothalamic neuronal membrane ultrastructure. J. Steroid Biochem. 27:615-623.
19. GOLDSTEIN, L. A., KURZ, E. M., and SENGELAUB, D. R. (1990). Androgen regulation of dendritic growth and retraction in the development of a sexually dimorphic spinal nucleus. J. Neurosci. 10:935-946.
20. GOLDSTEIN, L. A., MILLS, A. C., and SENGELAUB, D. R. (1996). Motoneuron development after deafferentation. I. Dorsal rhizotomy does not alter growth in the spinal nucleus of the bulbocavernosus (SNB). Dev. Brain Res. 91:11-19.
21. GOLDSTEIN, L. A. and SENGELAUB, D. R. (1992). Timing and duration of dihydrotestosterone treatment affect the development of motoneuron number and morphology in a sexually dimorphic rat spinal nucleus. J. Comp. Neurol. 326:147-157.
22. GOLDSTEIN, L. A. and SENGELAUB, D. R. (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.
23. GRIESBECK, O., PARSADANIAN, A. S., SENDTNER, M., and THOENEN, H. (1995). Expression of neurotrophins in skeletal muscle: Quantitative comparison and significance for motoneuron survival and maintenance of function. J. Neurosci. Res. 42:21-33.
24. HANDA, R. J., ROSELLI, C. E., HORTON, L., and RRESKO, J. A. (1987a). The quantitative distribution of cytosolic androgen receptors in microdissected areas of the male rat brain: effects of estrogen treatment. Endocrinology 121:233-240.
25. HANDA, R. J., STADELMAN, H. L., and RRESKO, J. A. (1987b) Effect of estrogen on androgen receptor dynamics in female rat pituitary. Endocrinology 121:84-89.
26. HART, B. L. (1979). Sexual behavior and penile reflexes of neonatally castrated male rats treated in infancy with estrogen and dihydrotestosterone. Hormone Behav. 13:256-268.
27. HART, B. L. and MELESE-D'HOSPITAL, P. Y. (1983). Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol. Behav. 31:802-813.
28. HAYES, K. J. (1965). The so-called 'levator ani' of the rat. Acta Endocrinol. 48:337-347.
29. HAYS, T. C., GOLDSTEIN, L. A., MILLS, A. C., and SENGELAUB, D. R. (1996). Motoneuron development after deafferentation: II. Dorsal rhizotomy does not block estrogen-supported growth in the dorsolateral nucleus (DLN). Dev. Brain. Res. 91:20-28.
30. JORDAN, C. L., WATAMURA, S., and ARNOLD, A. P. (1995). Androgenic, not estrogenic, steroids alter neuromuscular synapse elimination in the rat levator ani. Dev. Brain Res. 84:225-232.
31. KOLIATSOS, V. E., CLATTERBUCK, R. E., WINSLOW, J. W., CAYOUNETTE, M. H., and PRICE, D. L. (1993). Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359-367.
32. KOLIATSOS, V. E., PRICE, D. L., and CLATTERBUCK, R. E. (1994). Motor neurons in Onuf's nucleus and its rat homologues express the p75 nerve growth factor receptor: sexual dimorphism and regulation by axotomy. J. Comp. Neurol. 345:510-527.
33. KURZ, E. M., BREWER, R. G., and SENGELAUB, D. R. (1991). Hormonally mediated plasticity of motoneuron morphology in the adult rat spinal cord: a cholera toxin-HRP study. J. Neurobiol. 22:976-988.
34. KURZ, E. M., BURKE, K. A., WIDOWS, M. R., and SENGELAUB, D. R. (1996). Synergistic effects of testosterone metabolites on dendritic growth in a sexually dimorphic rat spinal nucleus. Soc. Neurosci. Abstr. (in press).
35. KURZ, E. M., SENGELAUB, D. R., and ARNOLD, A. P. (1986). Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science 232:395-398.
36. LARSSON, K., SODERSTEN, P., and BEYER, C. (1973). Induction of male sexual behavior by oestradiol benzoate in combination with dihydrotestosterone J. Endocrinol. 57:563-564.
37. LEE, J. H., JORDAN, C. L., and ARNOLD, A. P. (1989). Critical period for androgenic regulation of soma size of sexually dimorphic motoneurons in rat lumbar spinal cord. Neurosci. Lett. 98:79-84.
38. LUSTIG, R. H., SUDOL, M., PFAFF, D. W., and FEDEROFF, H. J. (1991). Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Mol. Brain Res. 11:125-132.
39. LUSTIG, R. H. (1994). Sex hormone modulation of neural development in vitro. Hormone Behav. 28:383-395.
40. LUSTIG, R. H., HUA, P., SMITH, L. S., WANG, C., and CHANG, C. (1994). An in vitro model for the effects of androgen on neurons employing androgen receptor-transfected PC-12 cells. Mol. Cell. Neurosci. 5:587-596.
41. MACLUSKY, N. J. and NAFTOLIN, F. (1981). Sexual differentiation of the central nervous system. Science 211:1294-1303.
42. MARTY, S., CARROLL, P., CELLERINO, A., CASTREN, E., STAIGER, V., THOENEN, H., and UNDHOLM, D. (1996). Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidul neurons, including Cajal-Retzius cells, in organotypic slice cultures. J. Neurosci. 16:657-687.
43. MCALLISTER, A. K., LO, D. C., and KATZ, L. C. (1995). Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791-803.
44. MCEWEN, B. S. (1983). Gonadal steroid influences on brain development and sexual differentiation. Int. Rev. Physiol. 27:99-145.
45. MCKENNA, K. E. and NADELHAFT, I. (1986). Organization of the pudendal nerve in the male and female rat. J. Comp. Neurol. 248:532-549.
46. MESULAM, M. M. (1982). Tracing Neural Connections with Horseradish Peroxidase. John Wiley and Sons, Chichester.
47. PAJUNEN, A. E. L, ISOMAA, V. V., JANNE, O. A., and BARDIN, C. W. (1982). Androgenic regulation of ornithine decarboxylase activity in mouse kidney and its relationship to changes in cytosol and nuclear androgen receptor concentrations. J. Biol. Chem. 257:8190-8198.
48. RAND, M. N. and BREEDLOVE, S. M. (1995). Androgen alters the dendritic arbors of SNB motoneurons by acting upon their target muscles. J. Neurosci. 15:4408-4416.
49. ROSELLI, C. E. and FASASI, T. A. (1992). Estradiol increases the duration of nuclear androgen receptor occupation in the preoptic area of the male rat treated with dihydrotestosterone. J. Steroid Biochem. Mol. Biol. 42:161-168.
50. SACHS, B. D. (1982). Role of striated penile muscle in penile reflexes, copulation, and induction of pregnancy in the rat. J. Reprod. Fertil. 66:433-443.
51. SENGELAUB, D. R. (1989). Cell generation, migration, death, and growth in neural systems mediating social behavior. In: Advances in Comparative and Environmental Physiology 3: Molecular and Cellular Basis of Social Behavior in Vertebrates, J. Balthazart, Ed. Springer-Verlag, Berlin, pp. 239-267.
52. SCHRODER, H. D. (1980). Organization of the motoneurons innervating the pelvic muscles of the male rat. J. Comp. Neurol. 192:567-587.
53. SHEN, P., ARNOLD, A. P., and MICEVYCH, P. E. (1990). Supraspinal projections to the ventromedial lumbar spinal cord in adult male rats. J. Comp. Neurol. 300:263-272.
54. SHUGRUE, P. J. and DORSA, D. M. (1994). Estrogen and androgen differentially modulate the growth-associated protein GAP-43 (Neuromodulin) messenger ribonucleic acid in postnatal rat brain. Endocrinology 134:1321-1328.
55. SODERSTEN, P., ENEROTH, P., HANSSON, T., MODE, A., JOHANSSON, D., NASLUND, B., LIANG, T., and GUSTAFSSON, J.-A. (1986). Activation of sexual behavior in castrated rats: the role of oestradiol. J. Endocrinol. 111:455-462.
56. SODERSTEN, P. and GUSTAFSSON, J. A. (1980). A way in which estradiol might play a role in the sexual behavior of male rats. Hormone Behav. 14:271-274.
57. SOHRABJI, F., MIRANDA, R. C., and TORAN-ALLERAND, C. D. (1994). Ovarian hormones differentially regulate estrogen and nerve growth factor mRNAs in adult sensory neurons. J. Neurosci. 14:459-471.
58. SUMNER, B. E. H. and WATSON, W. E. (1971). Retraction and expansion of the dendritic tree of motor neurons of adult rats induced in vivo. Nature 233:273-275.
59. TAYLOR, S. R., WIDOWS, M. R., and SENGELAUB, D. R. (1995). Estrogenic influence and possible site of action in development of motoneuron morphology in a sexually dimorphic rat spinal nucleus. Soc. Neurosci. Abstr. 21:40.
60. TOBET, S. A., Fox, T. O. (1992). Sex differences in neuronal morphology influenced hormonally throughout life. In: A. A. Gerall, H. Moltz, and I. L. Ward. Eds. Handbook of Behavioral Neurobiology, Vol. 11. Plenum Press, New York, pp. 41-83.
61. TOBIN, C. and JOUBERT, Y. (1991). Testosterone-induced development of the rat levator ani muscle. Dev. Biol. 146:131-138.
62. TORAN-ALLERAND, C. D. (1996). Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? J. Steroid Biochem. Molec. Biol. 56:169-178.
63. VOYVODIC, J. T. (1987). Development and regulation of dendrites in the rat superior cervical ganglion. J. Neurosci. 7:904-912.
64. WAGNER, C. K. and CLEMENS, L. G. (1991). Projections of the paraventricular nucleus of the hypothalamus to the sexually dimorphic lumbosacral region of the spinal cord. Brain Res. 539:254-262.
65. 3H-estradiol in the male rat. J. Neuroendocrinol. 5:545-551.
66. YAWO, H. (1987). Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy. J. Neurosci. 7:3703-3711.