Development and regeneration of the nervous system: A role for neurosteroids

Developmental Neuroscience

Volumn 18, Issue 1-2, 1996, Pages 6-21

  Schumacher, Michael ^a   Robel, Paul ^a   Baulíeu, Etienne Emile ^a,b  

^a INSERM   (France)

^b PSL Research University   (France)

Author keywords

Astrocytes; Development; Memory; Myelin; Neurosteroids; Oligodendro cytes; Pregnenolone; Progesterone; Regeneration; Schwann cells

Indexed keywords

CHOLESTEROL; NEUROSTEROID; PRASTERONE; PREGNENOLONE; PROGESTERONE; STEROID;

AGING; ANIMAL CELL; ASTROCYTE; CENTRAL NERVOUS SYSTEM; EMBRYO; GLIA CELL; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; MOUSE; MYELIN SHEATH; NERVE CELL LESION; NERVE CELL MEMBRANE; NERVE CELL PLASTICITY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; REVIEW; SCHWANN CELL; SCIATIC NERVE; STEROIDOGENESIS;

EID: 0030036766     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000111391     Document Type: Review

References (136)

1. Akwa Y, Morfin RF, Robel P, Baulieu EE (1992) Neurosteroid metabolism: 7α-Hydroxylation of dehydroepiandrosterone and pregnenolone by rat brain microsomes. Biochem J 288: 959-964.
2. Akwa Y, Sananès NG, Robel P, Baulieu EE, Le Goascogne C (1993a) Astrocytes and neurosteroids: Metabolism of pregnenolone and dehydroepiandrosterone. Regulation by cell density. J Cell Biol 121:135-143.
3. Akwa Y, Schumacher M, Jung-Testas I, Baulieu EE (1993b) Neurosteroids in rat sciatic nerves and Schwann cells. C R Acad Sci (III) (Paris) 316:410-414.
4. Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7: 413-442.
5. Barnea A, Hajibeigi A, Trant JM, Mason JI (1990) Expression of steroid metabolizing enzymes by aggregating fetal brain cells in culture: A model for developmental regulation of the progesterone 5α-reductase pathway. Endocrinology 127:500-502.
6. Baulieu EE (1981) Steroid hormones in the brain: Several mechanisms ?; in Fuxe K, Gustafsson JA, Wetterberg L (eds): Steroid Hormone Regulation of the Brain. Oxford, Pergamon Press, pp 3-14.
7. Baulieu EE (1991) Neurosteroids: A new function in the brain. Biol Cell 71:3-10.
8. Baulieu EE (1995) Studies on dehydroepiandrosterone (DHEA) and its sulphate during aging. C R Acad Sci (III) (Paris) 318:7-11.
9. Baulieu EE, Robel P (1995) Non-genomic mechanisms of action of steroid hormones; in Bock GR, Goode JA (eds): Non-Reproductive Actions of Sex Steroids, Ciba Foundation Symposium 191. Chichester, Wiley, pp 24-42.
10. Bizzozero OA, Good LK (1991) Rapid metabolism of fatty acids covalently bound to myelin proteolipid protein. J Biol Chem 266:17092-17098.
11. Bock GR, Goode JA (eds) (1995) Non-reproductive actions of sex steroids. Ciba Foundation Symposium 191.Chichester, Wiley.
12. Bolin LM, Shooter EM (1993) Neurons regulate Schwann cell genes by diffusible molecules. J Cell Biol 123:237-243.
13. Bologna L, Sharma J, Roberts E (1987) Dehydroepiandrosterone and its sulfated derivative reduce neuronal death and enhance astrocytic differentiation in brain cell cultures. J Neurosci Res 17:225-234.
14. Boujrad N, Ogwuegbu SO, Garnier M, Lee CH, Martin BM, Papadopoulos V (1995) Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 268: 1609-1612.
15. Brann DW, Hendry LB, Mahesh VB (1995) Emerging diversities in the mechanism of action of steroid hormones. J Steroid Biochem Mol Biol 52:113-133.
16. Brockes JP, Fields KL, Raff MC (1979) Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res 165:105-118.
17. 125I]iodoestradiol binding: Neuronal localization of estrogen-binding sites in the developing rat brain. Endocrinology 124:2074-2088.
18. Celotti F, Melcangi RC, Martini L (1992) The 5α-reductase in the brain - molecular aspects and relation to brain function. Front Neuroendocrinol 13:163-215.
19. Chadwick D, Widdows K (eds) (1990) Steroids and neuronal activity, Ciba Foundation Symposium 153. Chichester, Wiley.
20. Cheney DL, Uzunov D, Costa E, Guidotti A (1995) Gas chromatographic-mass fragmentographic quantification of 3α-hydroxy-5α-pregnan-20-one (allopregnanolone) and its precursors in blood and brain of adrenalectomized and castrated rats. J Neurosci 15:4641-4650.
21. Cheng KC, Lee J, Khanna M, Qin KN (1994) Distribution and ontogeny of 3 α-hydroxysteroid dehydrogenase in the rat brain. J Steroid Biochem Mol Biol 50:85-89.
22. Clemens JW, Lala DS, Parker KL, Richards JS (1994) Steroidogenic factor-1 binding and transcriptional activity of the cholesterol side-chain cleavage promoter in rat granulosa cells. Endocrinology 134:1499-1508.
23. Cogate N, Verma L, Zhou JM, Milward E, Rusten R, O'Connor M, Kufta C, Kim J, Hudson L, Dubois-Dalcq M (1994) Plasticity in the adult human oligodendrocyte lineage. J Neurosci 14: 4571-4587.
24. Compagnone NA, Bulfone A, Rubenstein JL, Mellon SH (1995) Expression of the steroidogenic enzyme P450scc in the central and peripheral nervous systems during rodent embryogenesis. Endocrinology 136:2689-2696.
25. Compagnone NA, Mellon SH (1995) Neural expression of the steroidogenic enzyme P450c17, crucial for DHEA production in the embryonic nervous system (abstract). International Symposium on DHEA transformation, Québec, Septembre.
26. Corpéchot C, Robel P, Axelson M, Sjövall J, Baulieu EE (1981) Characterization and measurement of dehydroepiandrosterone sulfate in the rat brain. Proc Natl Acad Sci USA 78: 4704-4707.
27. Corpéchot C, Synguelakis M, Talha S, Axelson M, Sjövall J, Vihko R, Baulieu EE, Robel P (1983) Pregnenolone and its sulfate ester in the rat brain. Brain Res 270:119-125.
28. Corpéchot C, Young J, Calvel M, Wehrey C, Veltz JN, Trouyer G, Mouren M, Prasad VVK, Banner C, Sjövall S, Baulieu EE, Robel P (1993) Neurosteroids: 3α-Hydroxy-5α-prenan-20-one and its precursors in the brain, plasma, and steroidogenic glands of male and female rats. Endocrinology 133:1003-1009.
29. De Nicola AF (1993) Steroid hormones and neuronal regeneration. Adv Neurol 59:199-206.
30. Del Cerro S, Garcia-Estrada J, Garcia-Segura LM (1995) Neuroactive steroids regulate astroglia morphology in hippocampal cultures from adult rats. Glia 14:65-71.
31. Dluzen DE, Ramirez VD (1989) Progesterone effects upon dopamine release from the corpus striatum of female rats. II. Evidence for a membrane site of action and the role of albumin. Brain Res 476:338-344.
32. El-Etr M, Akwa Y, Fiddes RJ, Robel P, Baulieu EE (1995) A progesterone metabolite stimulates the release of gonadotropin-releasing hormone from GT1-1 hypothalamic neurons via the γ-aminobutyric acid type A receptor. Proc Natl Acad Sci USA 92:3769-3773.
33. Eldridge CF, Bartlett M, Bunge RP, Wood PM (1987) Differentiation of axon-related Schwann cells in vitro. I. Ascorbic acid regulates basal lamina assembly and myelin formation. J Cell Biol 105:1023-1034.
34. Fahey JM, Lindquist DG, Pritchard GA, Miller LG (1995) Pregnenolone sulfate potentiation of NMDA-mediated increases in intracellular calcium in cultured chick cortical neurons. Brain Res 669:183-188.
35. Fawcett JW, Keynes RJ (1990) Peripheral nerve regeneration. Annu Rev Neurosci 13:43-60.
36. Flood JF, Morley JE, Roberts E (1992) Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it. Proc Natl Acad Sci USA 89:1567-1571.
37. Flood JF, Roberts E (1988) Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res 448:178-181.
38. Forger NG, Hodges LL, Roberts SL, Breedlove SM (1992) Regulation of motoneuron death in the spinal nucleus of the bulbocavernosus. J Neurobiol 23:1192-1203.
39. Garcia-Segura LM, Chowen JA, Duenas M, Torres-Aleman I, Naftolin F (1994) Gonadal steroids as promoters of neuro-glial plasticity. Psychoneuroendocrinology 19:445-453.
40. Garcia-Segura LM, Duenas M, Busiguina S, Naftolin F, Chowen JA (1995) Gonadal hormone regulation of neuronal-glial interactions in the developing neuroendocrine hypothalamus. J Steroid Biochem Mol Biol 53: 293-298.
41. Giaume C, Marin P, Cordier J, Glowinski J, Premont J (1991) Adrenergic regulation of intracellular communications between cultured striatal astrocytes from the mouse. Proc Natl Acad Sci USA 88:5577-5581.
42. Goujet-Zalc C, Babinet C, Monge M, Timsit S, Gabon F, Gansmuller A, Miura M, Sanchez M, Pournin S, Mikoshiba K, Zalc B (1993) The proximal region of the MBP gene promoter is sufficient to induce oligodendroglial-specific expression in transgenic mice. Eur J Neurosci 5:624-632.
43. Guarneri P, Guarneri R, Cascio C, Pavasant P, Piccoli F, Papadopoulos V (1994) Neurosteroidogenesis in rat retinas. J Neurochem 63:86-96.
44. Guarneri P, Papadopoulos V, Pan BS, Costa E (1992) Regulation of pregnenolone synthesis in C6-2B glioma cells by 4′-chlorodiazepam. Proc Natl Acad Sci USA 89:5118-5122.
45. Guennoun R, Fiddes RJ, Gouézou M, Lombès M, Baulieu EE (1995a) A key enzyme in the biosynthesis of neurosteroids. 3β-hydroxysteroid dehydrogenase/Δ5-Δ4-isomerase (3β-HSD), is expressed in rat brain. Mol Brain Res 30:287-300.
46. Guennoun R, Schumacher M, Gouézou M, Robert F, Shazand K, Robel P, Baulieu EE (1995b) 3β-hydroxysteroid dehydrogenase/Δ5-Δ4-isomerase, a key enzyme in the biosynthesis of neurosteroids, is expressed in the rat nervous system. Soc Neurosci Abstr 423.17, San Diego.
47. Guth L, Zhang Z, Roberts E (1994) Key role for pregnenolone in combination therapy promotes recovery after spinal cord injury. Proc Natl Acad Sci USA 91:12308-12312.
48. Haug M, Ouss-Sehlegel ML, Spetz JF, Brain PF, Simon V, Baulieu EE, Robel P (1989) Suppressive effects of dehydroepiandrosterone and 3-b-methylandrost-5-en-17-one on attack towards lactating female intruders by castrated male mice. Physiol Behav 46:955-959.
49. Hildebrand C, Bowe CM, Nilsson Remahl I (1994) Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibers. Prog Neurobiol 43:85-141.
50. Hu ZY, Bourreau E, Jung-Testas I, Robel P, Baulieu EE (1987) Oligodendrocyte mitochondria convert cholesterol to pregnenolone. Proc Natl Acad Sci USA 84:8215-8229.
51. Ikeda Y, Shen WH, Ingraham HA, Parker KL (1994) Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 8:654-662.
52. 2+ in cultured rat hippocampal neurons. Neurosci Lett 141: 30-34.
53. Isaacson RL, Yoder PE, Varner J (1994) The effects of pregnenolone on acquisition and retention of a food search task. Behav Neural Biol 61:170-176.
54. Jones KJ (1993) Gonadal steroids and neuronal regeneration. A therapeutic role. Adv Neurol 59:227-240.
55. Jung-Testas I, Hu ZY, Robel P, Baulieu EE (1989) Biosynthesis of pregnenolone and progesterone in primary cultures of rat glial cells. Endocrinology 125:2083-2091.
56. Jung-Testas I, Renoir M, Bugnard H, Greene GL, Baulieu EE (1992) Demonstration of steroid hormone receptors and steroid action in primary cultures of rat glial cells. J Steroid Biochem Mol Biol 41:621-631.
57. Jung-Testas I, Renoir JM, Gasc JM, Baulieu EE (1991) Estrogen-inducible progesterone receptor in primary cultures of rat glial cells. Exp Cell Res 193:12-19.
58. Jung-Testas I, Schumacher M, Robel P, Baulieu EE (1994) Actions of steroid hormones and growth factors on glial cells of the central and peripheral nervous system. J Steroid Biochem Mol Biol 48:145-154.
59. Jung-Testas I, Schumacher M, Robel P, Baulieu EE (1995) Schwann cells express progesterone receptors. J Steroid Biochem Mol Biol, in press.
60. Kabbadj K, El-Etr M, Baulieu EE, Robel P (1993) Pregnenolone metabolism in rodent embryonic neurons and astrocytes. Glia 7:170-175.
61. Khanna M, Qin KN, Cheng KC (1995) Distribution of 3α-hydroxysteroid dehydrogenase in rat brain and molecular cloning of multiple cDNAs encoding structurally related proteins in humans. J Steroid Biochem Mol Biol 53: 41-46.
62. Kleitman N, Wood PM, Bunge RP (1991) Tissue culture methods for the study of myelination; in Banker G, Goslin K (eds): Culturing Nerve Cells. London, Bradford Books, pp 337-377.
63. Koenig H, Schumacher M, Ferzaz B, Do Thi AN, Ressouches A, Guennoun R, Jung-Testas I, Robel P, Akwa Y, Baulieu EE (1995) Progesterone synthesis and myelin formation by Schwann cells. Science 268:1500-1503.
64. Korneyev A, Pan BS, Polo A, Romer E, Guidotti A, Costa E (1993) Stimulation of brain pregnenolone synthesis by mitochondrial diazepam binding inhibitor receptor ligands in vivo. J Neurochem 61:1515-1524.
65. Krieger NR, Scott RG (1989) Nonneuronal localization for steroid converting enzyme: 3α-Hydroxysteroid oxidoreductase in olfactory tubercle of rat brain. J Neurochem 52: 1866-1870.
66. Lan NC, Gee KW, Bolger MB, Chen JS (1991) Differential responses of expressed recombinant human γ-ammobutyric acid A receptors to neurosteroids. J Neurochem 57:1818-1821.
67. Le Goascogne C, Gouézou M, Robel P, Defaye G, Chambaz E, Waterman MR, Baulieu EE (1989) The cholesterol side-chain cleavage complex in human brain white matter. J Neuroendocrinology 1:153-156.
68. Le Goascogne C, Robel P, Gouézou M, Sananès N, Baulieu EE, Waterman M (1987) Neurosteroids: Cytochrome P450scc in rat brain. Science 237:1212-1215.
69. Lemke G (1993) The molecular genetics of myelination: An update. Glia 7:263-271.
70. Léna C, Changeux JP (1993) Allosteric modulations of the nicotinic acetylcholine receptor. Trends Neurosci 16:181-186.
71. Levi ADO, Bunge RP, Lofgren JA, Meima L, Hefti F, Nikolics K, Sliwkowski MX (1995) The influence of heregulins on human Schwann cell proliferation. J Neurosci 15:1329-1340.
72. Lubischer JL, Arnold AP (1995) Axotomy of developing rat spinal motoneurons: Cell survival, soma size, muscle recovery, and the influence of testosterone. J Neurobiol 26: 225-240.
73. Luine VN (1985) Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projetion areas of female rats. Exp Neurol 89:484-490.
74. MacLusky NJ, Walters MJ, Clark AS, Toran-Allerand CD (1994) Aromatase in the cerebral cortex, hippocampus, and mid-brain: Ontogeny and developmental implications. Mol Cell Neurosci 5:691-698.
75. Magoffin DA, Kurtz KM, Erickson GF (1990) Insulin-like growth factor-I selectively stimulates cholesterol side-chain cleavage expression in ovarian theca-interstitial cells. Mol Endocrinol 4:489-496.
76. A receptor. Mechanism of action and physiological significance. Prog Neurobiol 38:379-395.
77. Martini L, Melcangi RC, Maggi R (1993) Androgen and progesterone metabolism in the central and peripheral nervous system. J Steroid Biochem Mol Biol 47:195-205.
78. Matsumoto A, Micevych PE, Arnold AP (1988) Androgen regulates synaptic input to motoneurons of the adult rat spinal cord. J Neurosci 8: 4168-4176.
79. Mayo W, Dellu F, Robel P, Cherkaoui J, Le Moal M, Baulieu EE, Simon H (1993) Infusion of neurosteroids into the nucleus basalis magnocellularis affects cognitive processes in the rat. Brain Res 607:324-328.
80. McEwen BS (1991) Steroid hormones are multifunctional messengers to the brain. Trends Endocrinol Metab 2:62-67.
81. McEwen BS, Gould E, Orchinik M, Weiland NG, Woolley CS (1995) Oestrogens and the structural and functional plasticity of neurons: Implications for memory, ageing and neurodegenerative processes; in Bock GR, Goode JA (eds): Non-Reproductive Actions of Sex Steroids, Ciba Foundation Symposium 191. Chichester, Wiley, pp 52-73.
82. Melcangi RC, Ballabio M, Magnaghi V, Celotti F (1995) Metabolism of steroids in pure cultures of neurons and glial cells: role of intracellular signalling. J Steroid Biochem Mol Biol 53: 331-336.
83. Melcangi RC, Celotti F, Ballabio M, Castano P, Poletti A, Milani S, Martini L (1988) Ontogenic development of the 5α-reductase in the rat brain: Cerebral cortex, hypothalamus, purified myelin and isolated oligodendrocytes. Dev Brain Res 44:181-188.
84. Melcangi RC, Celotti F, Martini L (1994) Progesterone 5α-reduction in neuronal and in different types of glial cell cultures: Type 1 and type 2 astrocytes and oligodendrocytes. Brain Res 639:202-206.
85. Mellon SH (1994) Neurosteroids: Biochemistry, modes of action, and clinical relevance. J Clin Endocrinol Metab 78:1003-1008.
86. Mellon SH, Deschepper CF (1993) Neurosteroid biosynthesis: Genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 629:283-292.
87. Mensah-Nyagan AG, Feuilloley M, Dupont E, Do-Rego JL, Leboulenger F, Pelletier G, Vaudry H (1994) Immunocytochemical localization and biological activity of 3β-hydroxysteroid dehydrogenase in the central nervous system of the frog. J Neurosci 14:7306-7318.
88. Messing A, Behringer RR, Hammang JP, Palmiter RD, Brinster RL, Lemke G (1992) P0 promoter directs expression of reporter and toxin genes to Schwann cells of transgenic mice. Neuron 8: 507-520.
89. 3H]norepinephrine release evoked by N-methyl-D-aspartate in the rat hippocampus. Proc Natl Acad Sci USA 92:3774-3778.
90. Morales AJ, Nolan JJ, Nelson JC, Yen SSC (1994) Effects of replacement dose of dehydroepiandrosterone in men and women of advancing age. J Clin Endocrinol Metab 78:1360-1367.
91. Morfin R, Young J, Corpéchot C, Egestad B, Sjövall J, Baulieu EE (1992) Neurosteroids: Pregnenolone in human sciatic nerves. Proc Natl Acad Sci USA 89:6790-6793.
92. Murphy MG, Moak CM, Byczko Z, Macdonald WF (1991) Adenosine-dependent regulation of cyclic AMP accumulation in primary cultures of rat astrocytes and neurons. J Neurosci Res 30:631-640.
93. Naftolin F, Ryan KJ, Davies IJ, Reddy VV, Flores F, Petro Z, Kuhn M, White RJ, Takaoka Y, Wolin L (1975) The transformation of estrogens by central neuroendocrine tissues. Recent Prog Horm Res 31:295-319.
94. Omura T, Morohashi K (1995) Gene regulation of steroidogenesis. J Steroid Biochem Mol Biol 53:19-25.
95. Oonk RB, Krasnow JS, Beattie WG, Richards JS (1989) Cyclic AMP-dependent and -independent regulation of cholesterol side chain cleavage cytochrome P-450 (P-450scc) in rat ovarian granulosa cells and corpora lutea. J Biol Chem 264:21934-21942.
96. Orchinik M, McEwen BS (1993) Novel and classical actions of neuroactive steroids. Neurotransmissions 9:1-6.
97. Orentreich N, Brind JL, Rizer RL, Vogelman JH (1984) Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood. J Clin Endocrinol Metab 59:551-555.
98. Papadopoulos V (1993) Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: Biological role in steroidogenic cell function. Endocr Rev 14:222-240.
99. Papadopoulos V, Brown AS (1995) Role of the peripheral-type benzodiazepine receptor and the polypeptide diazepam binding inhibitor in steroidogenesis. J Steroid Biochem Mol Biol 53:103-110.
100. Papadopoulos V, Guarneri P (1994) Regulation of C6 glioma cell steroidogenesis by adenosine 3′,5′-cyclic monophosphate. Glia 10:75-78.
101. Papadopoulos V, Guarneri P, Krueger KE, Guidotti A, Costa E (1992) Pregnenolone biosynthesis in C6-2B glioma cell mitochondria - regulation by a mitochondrial diazepam binding inhibitor receptor. Proc Natl Acad Sci USA 89: 5113-5117.
102. Pardridge WM (1994) Steroid hormone transport through the blood-brain barrier: Methods and concepts; in De Kloet ER, Sutanto W (eds): Neurobiology of Steroids. Methods in Neurosciences. San Diego, Academic Press, vol 22, pp 3-22.
103. Paul SM, Purdy RH (1992) Neuroactive Steroids. FASEB J 6:2311-2322.
104. Raivich G, Kreutzberg GW (1993) Peripheral nerve regeneration: Role of growth factors and their receptors. Int J Neurosci 11:311-324.
105. Roa BB, Garcia CA, Pentao L, Killian JM, Trask BJ, Suter U, Snipes GJ, Ortiz-Lopez R, Shooter EM, Patel PI (1993) Evidence for a recessive PMP22 point mutation in Charcot-Marie-Tooth disease type 1A. Nat Genet 5:189-194.
106. Robel P, Baulieu EE (1994) Neurosteroids. Biosynthesis and function. Trends Endocrinol Metab 5:1-8.
107. Robel P, Jung-Testas I, Hu ZY, Akwa Y, Sananes N, Kabbadj K, Eychenne B, Sancho MJ, Kang KI, Zucman D, Morfin R, Baulieu EE (1991) Neurosteroids: Biosynthesis and metabolism in cultured rodent glis and neurons; in Costa E, Paul SM (eds): Neurosteroids and Bain function. Fidia Research Foundation Symposium Series, Stuttgart, Thieme, vol 8, pp 147-154.
108. Robel P, Young J, Corpéchot C, Mayo W, Perché F, Haug M, Simon H, Baulieu EE (1995) Biosynthesis and assay of neurosteroids in rats and mice: Functional correlates. J Steroid Biochem Mol Biol 53:335-360.
109. Roof RL, Duvdevani R, Braswell L, Stein DG (1994) Progesterone facilitates cognitive recovery and reduces secondary neuronal loss caused by cortical contusion injury in male rats. Exp Neurol 129:64-69.
110. Roof RL, Duvdevani R, Stein DG (1993) Gender influences outcome of brain injury-progesterone plays a protective role. Brain Res 607: 333-336.
111. Rupprecht R, Reul JMHM, Trapp T, Van Steensel B, Wetzel C, Damm K, Ziegelgänsberger W, Holsboer F (1993) Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11:523-530.
112. Rutkowski JL, Kirk CJ, Lerner MA, Tennekoon GI (1995) Purification and expansion of human Schwann cells in vitro. Nature Med 1:80-83.
113. Sanne JL, Krueger KE (1995) Expression of cytochrome P450 side-chain cleavage enzyme and 3β-hydroxysteroid dehydrogenase in the rat central nervous system: A study by polymerase chain reaction and in situ hybridization. J Neurochem 65:528-536.
114. Sar M, Stumpf WE (1977) Androgen concentration in motor neurons of cranial nerves and spinal cord. Science 197:77-79.
115. Schlinger BA, Arnold AP (1992) Circulating estrogens in a male songbird originate in the brain. Proc Natl Acad Sci USA 89:7650-7653.
116. Schumacher M (1990) Rapid membrane effects of steroid hormones: An emerging concept in neuroendocrinology. Trends Neurosci 13: 359-362.
117. Schumacher M, Akwa Y, Do Thi NA, Ferzaz B, Guennoun R, Koenig H, Baulieu EE (1995) Progesterone synthesized by Schwann cells promotes myelin formation. Soc Neurosci Abstr 135.8, San Diego.
118. Schumacher M, Baulieu EE (1995) Neurosteroids: Synthesis and functions in the central and peripheral nervous system; in Bock GR, Goode JA (eds): Non-Reproductive Actions of Sex Steroids. Ciba Foundation Symposium 191. Chichester, Wiley, pp 90-112.
119. Schumacher M, Jung-Testas I, Robel P, Baulieu EE (1993) Insulin-like growth factor I: A mitogen for rat Schwann cells in the presence of elevated levels of cyclic AMP. Glia 8:232-240.
120. A receptor on the response to a neurosteroid. Eur J Pharmacol 206:77-80.
121. Simerly RB (1993) Distribution and regulation of steroid hormone receptor gene expression in the central nervous system. Adv Neurol 59: 207-226.
122. Singh M, Meyer EM, Millard WJ, Simpkins JW (1994) Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 644:305-312.
123. Singh M, Meyer EM, Simpkins JW (1995) The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 136: 2320-2324.
124. Snipes JG, Suter U, Shooter EM (1993) The genetics of myelin. Curr Opin Neurobiol 3:694-702.
125. Sohrabji F, Miranda RC, Toran-Allerand CD (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14: 459-471.
126. Su TP, London ED, Jaffe JH (1988) Steroid binding at σ receptors suggests a link between endocrine, nervous, and immune systems. Science 240:219-221.
127. Sugawara T, Holt JA, Driscoll D, Strauss JF, Lin D, Miller WL, Patterson D, Clancy KP, Hart IM, Clark BJ, Stocco DM (1995) Human steroidogenic acute regulatory protein: Functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13. Proc Natl Acad Sci USA 92:4778-4782.
128. Topilko P, Schneider-Maunoury S, Levi G, Baron Van Evercooren A, Chennoufi ABY, Seitanidou T, Babinet C, Charnay P (1994) Krox-20 controls myelination in the peripheral nervous system. Nature 371:796-799.
129. Toran-Allerand CD, Miranda RC, Bentham WDL, Sohrabji F, Brown TJ, Hochberg RB, MacLusky NJ (1992) Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA 89: 4668-4672.
130. Torres-Aleman I, Rejas MT, Pons S, Garcia-Segura LM (1992) Estradiol promotes cell shape changes and glial fibrillary acidic protein redistribution in hypothalamic astrocytes in vitro: A neuronal-mediated effects. Glia 6:180-187.
131. Truss M, Beato M (1993) Steroid hormone receptors: Interaction with deoxyribonucleic acid and transcription factors. Endocr Rev 14: 459-479.
132. Valera S, Ballivet M, Bertrand D (1992) Progesterone modulates a neuronal nicotinic acetylcholine receptor. Proc Natl Acad Sci USA 89: 9949-9953.
133. Waterman MR, Kagawa N, Zanger UM, Momoi K, Lund J, Simpson ER (1992) Comparison of cAMP-responsive DNA sequences and their binding proteins associated with expression of the bovine CYP17 and CYP11A and human CYP21B genes. J Steroid Biochem Mol Biol 43:931-935.
134. Young J, Corpéchot C, Haug M, Gobaille S, Baulieu EE, Robel P (1991) Suppressive effects of dehydroepiandrosterone and 3β-methyl-androst-5-en-17-one on attack towards lactating female intruders by castrated male mice. II. Brain neurosteroids. Biochem Biophys Res Commun 174:892-897.
135. Young J, Corpéchot C, Perche M, Haug M, Baulieu EE, Robel P (1994) Neurosteroids: Pharmacological effects of a 3β-hydroxysteroid dehydrogenase inhibitor. Endocrine 2:505-509.
136. Yu WH (1989) Survival of motoneurons following axotomy is enhanced by lactation or by progesterone treatment. Brain Res 491:379-382.