Motoneuron injury and repair: New perspectives on gonadal steroids as neurotherapeutics

Journal of Molecular Neuroscience

Volumn 28, Issue 1, 2006, Pages 53-64

  Tetzlaff, Julie E ^a   Huppenbauer, Christopher B ^a   Tanzer, Lisa ^a   Alexander, Thomas D ^a   Jones, Kathryn J ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Estrogen; Facial motoneurons; Hamster; Immortalized mouse spinal motoneurons; Mouse; Testosterone

Indexed keywords

ANDROSTANOLONE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; NEURITIN; NEUROPROTECTIVE AGENT; PROTEIN; SEX HORMONE; STEROID RECEPTOR; SURVIVAL MOTOR NEURON PROTEIN; TESTOSTERONE PROPIONATE; UNCLASSIFIED DRUG;

CELL CULTURE; CELL VIABILITY; FACIAL NERVE INJURY; HAMSTER; HEAT SHOCK; MOTONEURON; MOTOR NEURON DISEASE; NERVE CELL PLASTICITY; NERVE FIBER TRANSECTION; NERVE REGENERATION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PROTEIN EXPRESSION; REVIEW; STRESS; TREATMENT OUTCOME;

ANIMALS; AXOTOMY; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FACIAL NERVE; GONADAL STEROID HORMONES; HEAT; MEMBRANE PROTEINS; MOTOR NEURONS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROPROTECTIVE AGENTS; RNA-BINDING PROTEINS;

CRICETINAE;

EID: 33646873698     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1385/JMN:28:1:53     Document Type: Review

References (107)

1. Anderson K. and Talbot K. (2003) Spinal muscular atrophies reveal motor neuron vulnerability to defects in ribonucleoprotein handling. Curr. Opin. Neurol. 16, 595-599.
2. Azcoitia I., Sierra A., and Garcia-Segura L. M. (1999) Neuroprotective effects of estradiol in the adult rat hippocampus: interaction with insulin-like growth factor-I signalling. J. Neurosci. Res. 58, 815-822.
3. Baba N., Koji T., Itoh M., and Mizuno A. (1999) Reciprocal changes in the expression of Bcl-2 and Bax in hypoglossal nucleus after axotomy in adult rats: possible involvement in the induction of neuronal cell death. Brain Res. 827, 122-129.
4. Baron-Delage S., Abadie A., Echaniz-Laguna A., Melki J., and Beretta L. (2000) Interferons and IRF-1 induce expression of the survival motor neuron (SMN) genes. Mol. Med. 6, 957-968.
5. Behl C. (2002) Oestrogen as a neuroprotective hormone. Nat. Rev. Neurosci. 3, 433-442.
6. Benten W. P., Guo Z., Krucken J., and Wunderlich F. (2004) Rapid effects of androgens in macrophages. Steroids 69, 585-590.
7. Cantallops I., Haas K., and Cline H. T. (2000) Postsynaptic CPG15 promotes synaptic maturation and presynaptic axon arbor elaboration in vivo. Nat. Neurosci. 3, 1004-1011.
8. Castoria G., Lombardi M., Barone M. V., Bilancio A., Di Domenico M., De Falco A., et al. (2004) Rapid signalling pathway activation by androgens in epithelial and stromal cells. Steroids 69, 517-522.
9. Chambraud B., Berry M., Redeuilh G., Chambon P., and Baulieu E. E. (1990) Several regions of human estrogen receptor are involved in the formation of receptor-heat shock protein 90 complexes. J. Biol. Chem. 265, 20686-20691.
10. Clancy A. N., Whitman C., Michael R. P., and Albers H. E. (1994) Distribution of androgen receptor-like immunoreactivity in the brains of intact and castrated male hamsters. Brain Res. Bull. 33, 325-332.
11. Claus P., Bruns A. F., and Grothe C. (2004) Fibroblast growth factor-2 23 is binding directly to the survival of motoneuron protein and is associated with small nuclear RNAs. Biochem. J. 384, 559-565.
12. Corriveau R. A., Shatz C. J., and Nedivi E. (1999) Dynamic regulation of cpg15 during activity-dependent synaptic development in the mammalian visual system. J. Neurosci. 19, 7999-8008.
13. Cragg B. G. (1970) What is the signal for chromatolysis? Brain Res. 23, 1-21.
14. Dhandapani K. M., Hadman M., De Sevilla L., Wade M. F., Mahesh V. B., and Brann D. W. (2003) Astrocyte protection of neurons: role of transforming growth factor-beta signaling via a c-Jun-AP-1 protective pathway. J. Biol. Chem. 278, 43,329-43,339.
15. Di Giovanni S., Faden A. I., Yakovlev A., Duke-Cohan J. S., Finn T., Thouin M., et al. (2005) Neuronal plasticity after spinal cord injury: identification of a gene cluster driving neurite outgrowth. FASEB J. 19, 153, 154.
16. Dong L., Wang W., Wang F., Stoner M., Reed J. C., Harigai M., et al. (1999) Mechanisms of transcriptional activation of bcl-2 gene expression by 17beta-estradiol in breast cancer cells. J. Biol. Chem. 274, 32099-32107.
17. Drengler S. M., Handa R. J., and Jones K. J. (1996a) Sex differences in androgen receptor mRNA levels and regulation in hamster facial motoneurons. Brain Res. Mol. Brain Res. 35, 131-138.
18. Drengler S. M., Handa R. J., and Jones K. J. (1996b) Regulation of androgen receptor mRNA expression in hamster facial motoneurons: differential effects of non-aromatizable and aromatizable androgens. Brain Res. Mol. Brain Res. 41, 8-15.
19. Fan L. and Simard L. R. (2002) Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development. Hum. Mol. Genet. 11, 1605-1614.
20. Fargo K. N. and Sengelaub D. R. (2004) Testosterone manipulation protects motoneurons from dendritic atrophy after contralateral motoneuron depletion. J. Comp. Neurol. 469, 96-106.
21. Forger N. G., Wagner C. K., Contois M., Bengston L., and MacLennan A. J. (1998) Ciliary neurotrophic factor receptor alpha in spinal motoneurons is regulated by gonadal hormones. J. Neurosci. 18, 8720-8729.
22. Fujino T., Lee W. C., and Nedivi E. (2003) Regulation of cpg15 by signaling pathways that mediate synaptic plasticity. Mol. Cell. Neurosci. 24, 538-554.
23. Garcia-Ovejero D., Veiga S., Garcia-Segura L. M., and Doncarlos L. L. (2002) Glial expression of estrogen and androgen receptors after rat brain injury. J. Comp. Neurol. 450, 256-271.
24. Garcia-Segura L. M., Azcoitia I., and DonCarlos L. L. (2001) Neuroprotection by estradiol. Prog. Neurobiol. 63, 29-60.
25. Grafstein B. (1975) The nerve cell body response to axotomy. Exp. Neurol. 48, 32-51.
26. Gubitz A. K., Feng W., and Dreyfuss G. (2004) The SMN complex. Exp. Cell. Res. 296, 51-56.
27. Guerra B., Diaz M., Alonso R., and Marin R. (2004) Plasma membrane oestrogen receptor mediates neuroprotection against beta-amyloid toxicity through activation of Raf-1/MEK/ERK cascade in septal-derived cholinergic SN56 cells. J. Neurochem. 91, 99-109.
28. Han P. J., Shukla S., Subramanian P. S., and Hoffman P. N. (2004) Cyclic AMP elevates tubulin expression without increasing intrinsic axon growth capacity. Exp. Neurol. 189, 293-302.
29. Hua Y. and Zhou J. (2004) Rpp20 interacts with SMN and is re-distributed into SMN granules in response to stress. Biochem. Biophys. Res. Commun. 314, 268-276.
30. Huppenbauer C. B., Tanzer L., DonCarlos L. L., and Jones K. J. (2005) Gonadal steroid attenuation of developing hamster facial motoneuron loss by axotomy: equal efficacy of testosterone, dihydrotestosterone, and 17-beta estradiol. J. Neurosci. 25, 4004-4013.
31. Jensen E. V., Greene G. L., Closs L. E., DeSombre E. R., and Nadji M. (1982) Receptors reconsidered: a 20-year perspective. Recent Prog. Horm. Res. 38, 1-40.
32. Jones K. J. (1993) Gonadal steroids and neuronal regeneration. A therapeutic role. Adv. Neurol. 59, 227-240.
33. Jones K. J. (1988) Steroid hormones and neurotrophism: relationship to nerve injury. Metab. Brain Dis. 3, 1-18.
34. Jones K. J., Alexander T. D., Brown T. J., and Tanzer L. (2000) Gonadal steroid enhancement of facial nerve regeneration: role of heat shock protein 70. J. Neurocytol. 29, 341-349.
35. Jones K. J. and Lavelle A. (1986) Differential effects of axotomy on immature and mature hamster facial neurons: a time course study of initial nucleolar and nuclear changes. J. Neurocytol. 15, 197-206.
36. Jones K. J. and Oblinger M. M. (1994) Androgenic regulation of tubulin gene expression in axotomized hamster facial motoneurons. J. Neurosci. 14, 3620-3627.
37. Jones K. J., Brown T. J., and Damaser M. (2001) Neuroprotective effects of gonadal steroids on regenerating peripheral motoneurons. Brain Res. Brain Res. Rev. 37, 372-382.
38. Jones K. J., Durica T. E., and Jacob S. K. (1997) Gonadal steroid preservation of central synaptic input to hamster facial motoneurons following peripheral axotomy. J. Neurocytol. 26, 257-266.
39. Jung-Testas I., Renoir M., Bugnard H., Greene G. L., and Baulieu E. E. (1992) Demonstration of steroid hormone receptors and steroid action in primary cultures of rat glial cells. J. Steroid Biochem. Mol. Biol. 41, 621-631.
40. Kerr D. A., Nery J. P., Traystman R. J., Chau B. N., and Hardwick J. M. (2000) Survival motor neuron protein modulates neuron-specific apoptosis. Proc. Natl. Acad. Sci. U. S. A. 97, 13312-13317.
41. Kinderman N. B. and Jones K. J. (1993) Testosterone enhancement of the nerve cell body response to injury: evidence using in situ hybridization and ribosomal DNA probes. J. Neurosci. 13, 1523-1532.
42. Kinderman N. B., Harrington C. A., Drengler S. M., and Jones K. J. (1998) Ribosomal RNA transcriptional activation and processing in hamster facial motoneurons: effects of axotomy with or without exposure to testosterone. J. Comp. Neurol. 401, 205-216.
43. Kujawa K. A. and Jones K. J. (1990) Testosterone-induced acceleration of recovery from facial paralysis in male hamsters: temporal requirements of hormone exposure. Physiol. Behav. 48, 765-768.
44. Kujawa K. A., Emeric E., and Jones K. J. (1991) Testosterone differentially regulates the regenerative properties of injured hamster facial motoneurons. J. Neurosci. 11, 3898-3906.
45. Kujawa K. A., Jacob J. M., and Jones K. J. (1993) Testosterone regulation of the regenerative properties of injured rat sciatic motor neurons. J. Neurosci. Res. 35, 268-273.
46. Kujawa K. A., Kinderman N. B., and Jones K. J. (1989) Testosterone-induced acceleration of recovery from facial paralysis following crush axotomy of the facial nerve in male hamsters. Exp. Neurol. 105, 80-85.
47. Kujawa K. A., Tanzer L., and Jones K. J. (1995) Inhibition of the accelerative effects of testosterone on hamster facial nerve regeneration by the antiandrogen flutamide. Exp. Neurol. 133, 138-143.
48. La Bella V., Cisterni C., Salaun D., and Pettmann B. (1998) Survival motor neuron (SMN) protein in rat is expressed as different molecular forms and is developmentally regulated. Eur. J. Neurosci. 10, 2913-2923.
49. Langub M. C. Jr. and Watson R. E. Jr. (1992) Estrogen receptor-immunoreactive glia, endothelia, and ependyma in guinea pig preoptic area and median eminence: electron microscopy. Endocrinology 130, 364-372.
50. LaVelle A. and LaVelle F., eds. (1984) Neuronal Reaction to Injury During Development, Academic Press, New York.
51. Lee W. C. and Nedivi E. (2002) Extended plasticity of visual cortex in dark-reared animals may result from prolonged expression of cpg15-like genes. J. Neurosci. 22, 1807-1815.
52. Lefebvre S., Burglen L., Reboullet S., Clermont O., Burlet P., Viollet L., et al. (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80, 155-165.
53. Lefebvre S., Burlet P., Liu Q., Bertrandy S., Clermont O., Munnich A., et al. (1997) Correlation between severity and SMN protein level in spinal muscular atrophy. Nat. Genet. 16, 265-269.
54. Lieberman A. R. (1971) The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14, 49-124.
55. Liu Q. and Dreyfuss G. (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15, 3555-3565.
56. Lu M. L., Schneider M. C., Zheng Y., Zhang X., and Richie J. P. (2001) Caveolin-1 interacts with androgen receptor. A positive modulator of androgen receptor mediated transactivation. J. Biol. Chem. 276, 13442-13451.
57. MacLusky N. J., Chalmers-Redman R., Kay G., Ju W., Nethrapalli I. S., and Tatton W. G. (2003) Ovarian steroids reduce apoptosis induced by trophic insufficiency in nerve growth factor-differentiated PC12 cells and axotomized rat facial motoneurons. Neuroscience 118, 741-754.
58. Majumder S., Varadharaj S., Ghoshal K., Monani U., Burghes A. H., and Jacob S. T. (2004) Identification of a novel cyclic AMP-response element (CRE-II) and the role of CREB-1 in the cAMP-induced expression of the survival motor neuron (SMN) gene. J. Biol. Chem. 279, 14803-14811.
59. Marron T. U., Guerini V., Rusmini P., Sau D., Brevini T. A., Martini L., and Poletti A. (2005) Androgen-induced neurite outgrowth is mediated by neuritin in motor neurones. J. Neurochem. 92, 10-20.
60. McWhorter M. L., Monani U. R., Burghes A. H., and Beattie C. E. (2003) Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J. Cell. Biol. 162, 919-931.
61. Meister G., Eggert C., and Fischer U. (2002) SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol. 12, 472-478.
62. Mitra S. W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H. A., Hayashi S., et al. (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144, 2055-2067.
63. Monani U. R., Sendtner M., Coovert D. D., Parsons D. W., Andreassi C., Le T. T., et al. (2000) The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum. Mol. Genet. 9, 333-339.
64. Mor G., Nilsen J., Horvath T., Bechmann I., Brown S., Garcia-Segura L. M., and Naftolin F. (1999) Estrogen and microglia: a regulatory system that affects the brain. J. Neurobiol. 40, 484-496.
65. Most S. P. (2004) Facial nerve recovery in bcl2 overexpression mice after crush injury. Arch. Facial Plast. Surg. 6, 82-87.
66. Murashov A. K., Islamov R. R., McMurray R. J., Pak E. S., and Weidner D. A. (2004) Estrogen increases retrograde labeling of motoneurons: evidence of a nongenomic mechanism. Am. J. Physiol. Cell Physiol. 287, C320-326.
67. Naeve G. S., Ramakrishnan M., Kramer R., Hevroni D., Citri Y., and Theill L. E. (1997) Neuritin: a gene induced by neural activity and neurotrophins that promotes neuritogenesis. Proc. Natl. Acad. Sci. U. S. A. 94, 2648-2653.
68. Naghdi N. and Asadollahi A. (2004) Genomic and nongenomic effects of intrahippocampal microinjection of testosterone on long-term memory in male adult rats. Behav. Brain Res. 153, 1-6.
69. Navascues J., Berciano M. T., Tucker K. E., Lafarga M., and Matera A. G. (2004) Targeting SMN to Cajal bodies and nuclear gems during neuritogenesis. Chromosoma 112, 398-409.
70. Nedivi E., Fieldust S., Theill L. E., and Hevron D. (1996) A set of genes expressed in response to light in the adult cerebral cortex and regulated during development. Proc. Natl. Acad. Sci. U. S. A. 93, 2048-2053.
71. Nedivi E., Hevroni D., Naot D., Israeli D., and Citri Y. (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363, 718-722.
72. Nedivi E., Javaherian A., Cantallops I., and Cline H. T. (2001) Developmental regulation of CPG15 expression in Xenopus. J. Comp. Neurol. 435, 464-473.
73. Nedivi E., Wu G. Y., and Cline H. T. (1998) Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. Science 281, 1863-1866.
74. Pagliardini S., Giavazzi A., Setola V., Lizier C., Di Luca M., DeBiasi S., and Battaglia G. (2000) Subcellular localization and axonal transport of the survival motor neuron (SMN) protein in the developing rat spinal cord. Hum. Mol. Genet. 9, 47-56.
75. Papakonstanti E. A., Kampa M., Castanas E., and Stournaras C. (2003) A rapid, nongenomic, signaling pathway regulates the actin reorganization induced by activation of membrane testosterone receptors. Mol. Endocrinol. 17, 870-881.
76. Pellizzoni L., Kataoka N., Charroux B., and Dreyfuss G. (1998) A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 95, 615-624.
77. Perillo B., Sasso A., Abbondanza C., and Palumbo G. (2000) 17beta-estradiol inhibits apoptosis in MCF-7 cells, inducing bcl-2 expression via two estrogen-responsive elements present in the coding sequence. Mol. Cell. Biol. 20, 2890-2901.
78. Pratt W. B. and Toft D. O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18, 306-360.
79. Raivich G., Bohatschek M., Da Costa C., Iwata O., Galiano M., Hristova M., et al. (2004) The AP-1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43, 57-67.
80. Rakotoarivelo C., Petite D., Lambard S., Fabre C., Rouleau C., Lumbroso S., et al. (2004) Receptors to steroid hormones and aromatase are expressed by cultured motoneurons but not by glial cells derived from rat embryo spinal cord. Neuroendocrinology 80, 284-297.
81. Razandi M., Oh P., Pedram A., Schnitzer J., and Levin E. R. (2002) ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions. Mol. Endocrinol. 16, 100-115.
82. Razandi M., Pedram A., Greene G. L., and Levin E. R. (1999) Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol. Endocrinol. 13, 307-319.
83. Razandi M., Pedram A., Park S. T., and Levin E. R. (2003) Proximal events in signaling by plasma membrane estrogen receptors. J. Biol. Chem. 278, 2701-2712.
84. Remage-Healey L. and Bass A. H. (2004) Rapid, hierarchical modulation of vocal patterning by steroid hormones. J. Neurosci. 24, 5892-5900.
85. Ribotta M. G., Menet V., and Privat A. (2004) Glial scar and axonal regeneration in the CNS: lessons from GFAP and vimentin transgenic mice. Acta Neurochir. Suppl. 89, 87-92.
86. Rossoll W., Jablonka S., Andreassi C., Kroning A. K., Karle K., Monani U. R., and Sendtner M. (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol. 163, 801-812.
87. Rossoll W., Kroning A. K., Ohndorf U. M., Steegborn C., Jablonka S., and Sendtner M. (2002) Specific interaction of Smn, the spinal muscular atrophy determining gene product, with hnRNP-R and gry-rbp/hnRNP-Q: a role for Smn in RNA processing in motor axons? Hum. Mol. Genet. 11, 93-105.
88. Singh M., Setalo G. Jr., Guan X., Warren M., and Toran-Allerand C. D. (1999) Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19, 1179-1188.
89. Sortino M. A., Chisari M., Merlo S., Vancheri C., Caruso M., Nicoletti F., et al. (2004) Glia mediates the neuroprotective action of estradiol on beta-amyloid-induced neuronal death. Endocrinology 145, 5080-5086.
90. Streit W. J. (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40, 133-139.
91. Sumner C. J., Huynh T. N., Markowitz J. A., Perhac J. S., Hill B., Coovert D. D., et al. (2003) Valproic acid increases SMN levels in spinal muscular atrophy patient cells. Ann. Neurol. 54, 647-654.
92. Takuma K., Baba A., and Matsuda T. (2004) Astrocyte apoptosis: implications for neuroprotection. Prog. Neurobiol. 72, 111-127.
93. Tanzer L. and Jones K. J. (1997) Gonadal steroid regulation of hamster facial nerve regeneration: effects of dihydrotestosterone and estradiol. Exp. Neurol. 146, 258-264.
94. Tanzer L. and Jones K. J. (2004) Neurotherapeutic action of testosterone on hamster facial nerve regeneration: temporal window of effects. Horm. Behav. 45, 339-344.
95. Tanzer L., Sengelaub D. R., and Jones K. J. (1999) Estrogen receptor expression in the facial nucleus of adult hamsters: does axotomy recapitulate development? J. Neurobiol. 39, 438-446.
96. Tetzlaff J. E., Tanzer L. and Jones K. J. (2005a) Mechanisms of gonadal steroid-induced neuroprotection. Part I: Androgenic and estrogenic effects on mouse facial motoneuron survival and functional recovery following facial nerve injury, in review.
97. Tetzlaff J. E., Tanzer L. and Jones K. J. (2005b) Mechanisms of gonadal steroid-induced neuroprotection. Part II: Androgenic and estrogenic effects on facial motoneuron survival following heat shock in vitro, in review.
98. Wang Z. M., Dai C. F., Kanoh N., Chi F. L., and Li K. Y. (2002) Apoptosis and expression of BCL-2 in facial motoneurons after facial nerve injury. Otol. Neurotol. 23, 397-404.
99. Wehner K. A., Ayala L., Kim Y., Young P. J., Hosler B. A., Lorson C. L., et al. (2002) Survival motor neuron protein in the nucleolus of mammalian neurons. Brain Res. 945, 160-173.
100. Wise P. M. (2002) Estrogens and neuroprotection. Trends Endocrinol. Metab. 13, 229-230.
101. Yang L. Y., Verhovshek T., and Sengelaub D. R. (2004) Brain-derived neurotrophic factor and androgen interact in the maintenance of dendritic morphology in a sexually dimorphic rat spinal nucleus. Endocrinology 145, 161-168.
102. Young P. J., Day P. M., Zhou J., Androphy E. J., Morris G. E., and Lorson C. L. (2002) A direct interaction between the survival motor neuron protein and p53 and its relationship to spinal muscular atrophy. J. Biol. Chem. 277, 2852-2859.
103. Yu W. H. (1982) Effect of testosterone on the regeneration of the hypoglossal nerve in rats. Exp. Neurol. 77, 129-141.
104. Yu W. H. and Cao C. G. (1992) Testosterone fails to rescue motoneurons from axotomy-induced death in young rats. Neuroreport 3, 1042-1044.
105. Yu W. H. and McGinnis M. Y. (2001) Androgen receptors in cranial nerve motor nuclei of male and female rats. J. Neurobiol. 46, 1-10.
106. Yu W. H. and Srinivasan R. (1981) Effect of testosterone and 5 alpha-dihydrotestosterone on regeneration of the hypoglossal nerve in rats. Exp. Neurol. 71, 431-435.
107. Zhang H. L., Pan F., Hong D., Shenoy S. M., Singer R. H., and Bassell G. J. (2003) Active transport of the survival motor neuron protein and the role of exon-7 in cytoplasmic localization. J. Neurosci. 23, 6627-6637.