Steroid metabolism in the mammalian brain: 5Alpha-reduction and aromatization

Brain Research Bulletin

Volumn 44, Issue 4, 1997, Pages 365-375

  Celotti, Fabio ^a   Negri Cesi, Paola ^a   Poletti, Angelo ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

3Alpha hydroxy steroid dehydrogenase; 5Alpha reductase; Aromatase; Brain; Metabolism; Steroid anesthesia

Indexed keywords

17BETA (N,N DIETHYLCARBAMOYL) 4 METHYL 4 AZA 5ALPHA ANDROSTAN 3 ONE; 3ALPHA HYDROXYSTEROID DEHYDROGENASE; 4 AMINOBUTYRIC ACID A RECEPTOR; AROMATASE; FINASTERIDE; PROGESTERONE; STEROID 5ALPHA REDUCTASE; STEROID 5ALPHA REDUCTASE INHIBITOR;

ANESTHESIA; AROMATIZATION; ARTICLE; BRAIN; CELLULAR DISTRIBUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEROID METABOLISM;

3-ALPHA-HYDROXYSTEROID DEHYDROGENASE (B-SPECIFIC); 3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; AROMATASE; BRAIN; FEMALE; HUMANS; MALE; MAMMALS; ORGAN SPECIFICITY; RECEPTORS, GABA-A; STEROIDS; TESTOSTERONE 5-ALPHA-REDUCTASE;

EID: 0030699924     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(97)00216-5     Document Type: Article

References (93)

1. Abe-Dohmae S., Tanaka R., Harada N. Cell-type and region-specific expression of aromatase mRNA in cultured brain cell. Mol. Brain Res. 24:1994;153-158.
2. Andersson S., Berman D. M., Jenkins E. P., Russell D. W. Deletion of steroid 5alpha-reductase 2 gene in male pseudohermaphroditism. Nature. 354:1991;159-161.
3. Andersson S., Bishop R. W., Russell D. W. Expression and regulation of steroid 5alpha-reductase, an enzyme essential for male sexual differentiation. J. Biol. Chem. 264:1989;16249-16255.
4. Balthazart J., Foidart A., Harada N. Immunocytochemical localization of aromatase in the brain. Brain Res. 514:1990;327-333.
5. +. Biochemistry. 33:1996;10702-10711.
6. A receptors. J. Neurochem. 7:1995;171-177.
7. Callard G. V. Aromatization in brain and pituitary. Celotti F., Naflolin F., Martini L. Metabolism of Hormonal Steroids in the Neuroendrocrine structures. 1984;79-102 Raven Press, New York.
8. Celotti F., Massa R., Martini L. Metabolism of sex steroids in the central nervous system. DeGroot L. J. Endocrinology. Vol. 1:1979;41-53 Grune and Stratton, New York.
9. Celotti F., Melcangi R., Martini L. The 5alpha-reductase in the brain Molecular aspects and relation to brain function . Front. Neuroendocrinol. 13:1992;163-215.
10. Celotti F., Melcangi R. C., Negri-Cesi P., Ballabio M., Martini L. Differential distribution of the 5alpha-reductase in the central nervous system of the rat and the mouse Are the white matter structures of the brain target tissues for testosterone action? J. Steroid Biochem. 26:1987;125-129.
11. Celotti F., Melcangi R. C., Negri-Cesi P., Poletti A. Testosterone metabolism in brain cells and membranes. J. Steroid Biochem. Mol. Biol. 40:1991;675-678.
12. Cheng K. C. Molecular cloning of rat liver 3alpha-hydroxysteroid dehydrogenase and identification of structurally related proteins from rat lung and kidney. J. Steroid Biochem. Mol. Biol. 43:1992;1083-1088.
13. Cheng, K. C.; Lee, J.; Khanna, M; Quin, K. N. Distribution and ontogeny of 3alpha-hydroxysteriod dehydrogenase in the rat brain. J. Steroid Biochem. Mol. Biol. 50:85-89; 1994.
14. Cheng K. C., White P. C., Quin K. N. Molecular cloning and expression of rat liver 3alpha-hydroxysteroid dehydrogenase. Mol. Endocrinol. 5:1991;823-828.
15. Collado, P.; Segovia, S.; Cales, J. M.; Perez Laso, C.; Rodriuez Zafra, M.; Giullamon, A.; Valencia, A. Female's DHT controls sex differences in the rat bed nucleus of the accessory olfactory tract. Neuroreport 3:327-329; 1992.
16. Corbin J. C., Graham-Lorence S., McPhaul M., Mason J. I., Mendelson C. R., Simpson E. R. Isolation of a full-length cDNA insert encoding human aromatase system cytochrome P-450 and its expression in nonsteroidogenic cells. Proc. Natl. Acad. Sci. USA. 85:1988;8948-8952.
17. Corbin C. J., Kalhil M. W., Conley A. J. Functional ovarian and placental isoforms of porcine aromatase. Mol. Cell. Endocrinol. 113:1995;29-37.
18. Döhler K. D., Srivastava S. S., Shryne J. E., Jarzab B., Sipos A., Gorski R. Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is inhibited by postnatal treatment with an estrogen antagonist. Neuroendocrinology. 38:1984;297-301.
19. Eicheler W. J., Tuohimaa P., Vilja P., Adermann K., Frossman W.-G., Aumüller G. Immunocytochemical localization of human 5alpha-reductase 2 with polyclonal antibodies in androgen target and non-target human tissues. J. Histochem. Cytochem. 42:1994;667-675.
20. Gaston, K; Fried, M. The isolation of transcription factors from lambdaGT11 cDNA expression libraries: Human steroid 5alpha-reductase 1 as sequence-specific DNA binding activity. Nucleic Acid Res. 20:6297-6301; 1992.
21. Goldstain L. A., Sengelaub D. R. Timing and duration of dihydrotestosterone treatment affect the development of motoneuron number and morphology in a sexually dimorphic rat spinal nucleus. J. Comp. Neurol. 326:1992;147-157.
22. Gonzalez M. I., Leret M. L. Role of monoamines in the male differentiation of the brain induced by androgen aromatization. Pharmacol. Biochem. Behav. 41:1992;733-737.
23. Goy R., McEwen B. S. Sexual differentiation of the brain. 1980;MIT Press, Cambridge.
24. A receptor complex. J. Pharmacol. Exp. Ther. 241:1987;346-353.
25. Hauser K. F., McLusky N. J., Toran-Allerand C. D. Androgen action in fetal spinal cultures Metabolic and morphologic aspects . Brain Res. 406:1987;62-72.
26. Honda S., Harada N., Takagi Y. Novel exon 1 of the aromatase gene specific for aromatase transcripts in human brain. Biochem. Biophys. Res. Commun. 198:1994;1153-1160.
27. Johnston I. G., Rush S. J., Gurd J. W. , Brown, I. R. Molecular cloning of a novel mRNA using an antibody directed against synaptic glycoproteins. J. Neurosci. Res. 32:1992;159-166.
28. Jurman M. E., Erulkar S. D., Krieger N. R. Testosterone 5alpha-reductase in spinal cord of Xenopus laevis. J. Neurochem. 38:1982;657-661.
29. Karavolas H. J., Hodges D. Neuroendocrine metabolism of progesterone and related progestins. Chadwick D., Widdows K. Steroids and neuronal activity. 1990;22-55 John Wiley & Sons, Ciba Foundation Symposium 153. Chichester.
30. Katz M. D., Cai L., Zhu Y., Herrera C., DeFillo-Ricart M., Shackleton C. H. L., Imperato-McGinley J. The biochemical and phenotypic characterization of females homozygous for 5alpha-reductase-2 deficiency. J. Clin. Endocrinol. Metab. 80:1995;3160-3167.
31. Khanna, M; Quin, K. N.; Cheng, K. C. Distribution of 3alpha-hydroxysteriod dehydrogenase and molecular cloning of multiple cDNAs encoding structurally related proteins in humans. J. Steroid Biochem. Mol. Biol. 53:41-46; 1995.
32. Koenig H. L., Schumacher M., Ferzaz B. , Do Thi, A. N.; Ressouches, A.; Guennoun, R.; Jung-Testas, I.; Robel, P.; Akwa, Y.; Baulieu, E. E. Progesterone and myelin formation by Schwann cells. Science. 268:1995;1500-1503.
33. Krieger N. R., Scott R. G. 3alpha-hydroxysteroid dehydrogenase in rat brain. J. Neurochem. 42:1984;887-890.
34. Labrie F., Sugimoto Y., Luu-The V., Simard J., Lachance Y., Bachvarov D., Leblanc G. ; Durocher, F; Paquet N. Structure of human type 2 5alpha-reductase gene. Endocrinology. 131:1992;1571-1573.
35. Lauber M. E., Lichtensteigher W. Pre- and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization. Endocrinology. 135:1994;1661-1668.
36. Lauber M. E., Lichtensteiger W. Ontogeny of 5alpha reductase (type 1) messenger ribonucleic acid expression in rat brain Early presence in germinal zones . Endocrinology. 137:1996;2718-2730.
37. Lephart E. D. Pituitary and brain 5alpha-reductase messenger RNA levels in control, castrated, and dihydrotestosterone-treated rats. Mol. Cell. Neurosci. 4:1993;526-531.
38. Lephart E. D. Brain 5alpha-reductase cellular, enzymatic, and molecular perspectives and implications for biological function . Mol. Cell. Neurosci. 4:1993;473-484.
39. Levy M. A., Brandt M., Sheedy K. M., Holt D. A., Heaslip J. I., Trill J. J., Ryan P. J., Morris R. A., Garrison L. M., Bergsma D. J. Cloning, expression and functional characterization of type 1 and type 2 steroid 5alpha-reductases from Cynomolgus monkey Comparison with human and rat isoenzymes . J. Steroid Biochem. Mol. Biol. 52:1995;307-319.
40. Lopez-Solache I., Luu-The V., Seralini G.E., Labrie F. Heterogeneity of rat type 1 5alpha-reductase cDNA Cloning, expression and regulation by pituitary implants and dihydrotestosterone . Biochem. Biophys. Acta. 1305:1966;139-144.
41. MacLusky N. J., Clark C. R., Shanabroug M., Naftolin F. Metabolism of androgens in the spinal cord of the rat. Brain Res. 422:1987;83-91.
42. MacLusky N. J., Naftolin F. Sexual differentiation of the central nervous system. Science. 211:1981;1294-1302.
43. Mahendroo M. S., Cala K. M., Russell D. W. 5alpha-reduced androgens play a key role in murine parturition. Mol. Endocrinol. 10:1996;380-392.
44. Majewska M. D., Harrison N. L., Schwartz R.D., Barker J. L., Paul S. M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science. 232:1986;1004-1007.
45. Matsumoto A., Micevych P. E., Arnold P. Androgen regulates synaptic input to motoneurones of the adult rat spinal cord. J. Neurosci. 8:1988;4168-4176.
46. McCarthy M. M., Schlenker E. H., Pfaff D. W. Enduring consequences of neonatal treatment with antisense oligodeoxynucleotides to estrogen receptor messenger ribinucleic acid on sexual differentiation of rat brain. Endocrinology. 331:1993;433-439.
47. McEwen B., Gould E. Adrenal steroid influences on the survival of hippocampal neurons. Biochem. Pharmacol. 40:1990;2393-2402.
48. Melcangi C. R., Celotti F., Ballabio M., Castano P., Massarelli R., Poletti A., Martini L. 5alpha-reductase activity in isolated and cultured neuronal and glial cells of the rat. Brain Res. 516:1990;229-236.
49. Melcangi R. C., Celotti F., Ballabio M., Castano P., Poletti A., Milani S., Martini L. Ontogenetic development of the 5alpha-reductase in the rat brain Cerebral cortex, hypothalamus, purified myelin and isolated oligodendrocyte . Dev. Brain. Res. 44:1988;181-188.
50. Melcangi R. C., Celotti F., Ballabio M., Poletti A., Castano P., Martini L. Testosterone 5alpha-reductase activity in the rat brain is highly concentrated in white matter structures and in purified myelin sheats of axons. J. Steroid Biochem. 31:1988;173-180.
51. Melcangi R. C., Celotti F., Ballabio M., Poletti A., Martini L. Testosterone metabolism in peripheral nerves presence of the 5alpha-reductase-3alpha-hydroxysteroid-dehydrogenase enzymatic system in the sciatic nerve of adult and aged rats . J. Steroid Biochem. 35:1990;145-148.
52. Melcangi, R. C.; Celotti, F., Castano, P.; Martini L. Differential localization of the 5alpha-reductase and 3alpha-hydroxysteroid-dehydrogenase in neuronal and glial cultures. Endocrinology 132:1252-1259; 1993.
53. Melcangi R. C., Celotti F., Martini L. Progesterone 5alpha-reduction in neuronal and in different types of glial cell cultures Type 1 and 2 astrocytes and oligodentrocytes . Brain Res. 639:1994;202-206.
54. Mellon S. H. Neurosteroids Biochemistry, modes of action, and clinical relevance . J. Clin. Endocrinol. Metab. 78:1994;1003-1008.
55. Mendelson W. B., Martin J. V., Perlis M., Wagner R., Majewska M. D., Paul S. M. Sleep induction by an adrenal steroid in the rat. Psycopharmacology (Berlin). 93:1987;226-229.
56. Milewich, L.; Mendonca, B. B.; Arnhold, I.; Wallace, A. N; Donaldson, M. D. C.; Wilson, J. D.; Russell, D. W. Women with steroid 5alpha-reductase 2 deficiency have normal concentrations of plasma 5alpha-dihydroprogesterone during the luteal phase. J. Clin. Endocrinol. Metab. 80:3136-3139; 1995.
57. Morishima A., Grumbach M. M., Simpson E. R., Fisher C. R., Qin K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J. Clin. Endocrinol. Metab. 80:1995;3689-3698.
58. Negri-Cesi P., Melcangi R. C., Celotti F., Martini L. Aromatase activity in cultured brain cells Difference between neurons and glia . Brain Res. 589:1992;327-332.
59. Negri-Cesi P., Poletti A., Celotti F. Metabolism of steroids in the brain A new insight in the role of 5alpha-reductase and aromatase in the brain differentiation and functions . J. Steroid Biochem. Mol. Biol. 58:1996;455-466.
60. Normington K., Russell D. W. Tissue distribution and kinetic characteristics of rat steroid 5alpha-reductase isozymes. J. Biol. Chem. 267:1992;19548-19554.
61. Paul S. M., Purdy R. H. Neuroactive steroids. FASEB J. 6:1992;2311-2322.
62. Pawlovski J. E., Huizinga M., Penning T. M. Cloning and sequencing of the cDNA for rat liver 3alpha-hydroxysteroid/dihydrodiol dehydrogenase. J. Biol. Chem. 266:1991;8820-8825.
63. Pelletier G., Lu-The V., Labrie F. Immunocytochemical localization of 5alpha-reductase in rat brain. Mol. Cell. Neurosci. 5:1994;394-399.
64. Penning T. M. 3alpha-hydroxysteroid dehydrogenase Three dimensional structure and gene regulation . J. Endocrinol. 150:1996;S175-S187.
65. Penning, T.; Pawlowski, J. E.; Schlegel, B. P; Jez, J. M.; Lin, H.-K.; Hoog, S. S; Bennett, M. J.; Lewis, M. Mammalian 3alpha-hydroxysteroid dehydrogenases. Steroids 61:508-523; 1996.
66. Penning T., Sharp R. B., Krieger N. R. Purification properties of 3alpha-hydroxysteroid dehydrogenase from rat brain cytosol Inhibition by nonsteroidal anti-inflammatory drugs and progestins . J. Biol. Chem. 260:1985;15266-15272.
67. Poletti A., Celotti F., Melcangi R. C., Ballabio M., Martini L. Kinetics properties of the 5alpha-reductase of testosterone in purified myelin, in the subcortical white matter and in the cerebral cortex of the male rat brain. J. Steroid Biochem. 35:1990;97-101.
68. Poletti A., Celotti F., Motta M., Martini L. Characterization and subcellular localization of rat 5alpha-reductases type 1 and type 2 expressed in yeast Saccharomyces cerevisiae. Biochem. J. 314:1996;1047-1052.
69. Poletti, A.; Celotti, F.; Rumio, C.; Rabuffetti, M.; Martini, L. Identification of type 1 5alpha-reductase in myelin membranes of male and female rat brain. Mol. Cell. Endocrinol. 129:181-190; 1997.
70. Poletti A., Negri-Cesi P., Melcangi R. C., Colciago A., Martini L., Celotti F. Expression of androgen activating enzymes in cultured cells of developing rat brain. J. Neurochem. 68:1997;1298-1303.
71. Poletti, A.; Negri-Cesi, P.; Rabuffetti, M.; Celotti, F.; Martini, L. Transient expression in the late fetal and early post-natal life of type 2 5alpha-reductase isozyme in the rat brain. 10th International Congress of Endocrinology (ICE'96), San Francisco, USA, 1996. abs. P2-575.
72. Poletti, A.; Rabuffetti, M.; Celotti, F. 5Alpha-reductase in the brain. In: Gennazzani, F.; Petraglia, F.; Purdy, R. H; eds. The brain: Source and targets for sex steroid hormones. New York: Parthenon Publishing Group: 1996:123-133.
73. Robel P., Baulieu E. E. Neurosteroids Biosynthesis and function . TEM. 5:1994;1-8.
74. Roselli C. E., Resko J. A. Aromatase activity in the rat brain Hormonal regulation and sex differences . J. Steroid Biochem. Mol. Biol. 44:1993;499-508.
75. Russell D. W., Wilson J. D. Steroid 5alpha- reductase Two genes/two enzymes . Annu. Rev. Biochem. 63:1994;25-61.
76. Sanghera M. K., Simpson E. R., McPhaul M.J., Kozlowski G., Conley A. J., Lephard E. D. Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies. Endocrinology. 129:1991;2834-2844.
77. Schlinger B. A., Amur-Umarjee S., Shen P., Campagnoni T., Arnold A.P. Neuronal and non-neuronal aromatase in primary cultures of developing zebra finch telencephalon. J. Neurosci. 14:1994;7541-7552.
78. Selye H. Anaestetic effect of steroid hormones. Proc. Soc. Exp. Biol. Med. 46:1941;116-121.
79. Selye H. Correlation between the chemical structure and the pharmacological actions of the steroids. Endocrinology. 30:1942;437-453.
80. Shinoda K. Brain aromatization and its associated structures. Endocr. J. 41:1994;115-138.
81. Sholl, S. A., Goy, R. W.; Kim, K. L. 5alpha-reductase, aromatase, and androgen receptor levels in the monkey brain during fetal development. Endocrinology 124:627-634; 1989.
82. Simpson E. R., Mahendroo M. S., Means G. D., Kilgore M. W., Hinshelwood M. M., Graham-Lorence S., Amameh B., Ito Y., Fisher C. R., Dodson M. M., Mendelson C. R., Bulun S. E. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr. Rev. 15:1994;342-355.
83. Smith E. P., Boyd J., Frank G. R., Takahashi H., Cohen R. M., Specker B., Williams T. C., Lubahn D.B., Korach K. S. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331:1994;1056-1061.
84. Sodersen P., Eneroth P., Hansson T. Oestradiol synergize with 5alpha-dihydrotestosterone or 3 alpha-but not 3 beta-androstanediol in inducing sexual behavior in castrated rats. J. Endocrinol. 119:1988;461-465.
85. Thigpen A. E., Silver R. I., Guileyardo J.M., Casey M. L., McConnel J. D., Russell D. W. Tissue distribution and ontogenity of steroid 5alpha-reductase isozyme expression. J. Clin. Invest. 92:1993;903-910.
86. Tonjes R., Docke F., Dorner G. Effects of neonatal intracerebral implantation of sex steroids on sexual behaviour, social play, and gonadotropin secretion. Exp. Clin. Endocrinol. 90:1987;257-263.
87. Tsuruo Y., Ishimura K., Fujita H., Osawa Y. Immunocytochemical localization of aromatase-containing neurons in the rat brain during pre- and postnatal development. Cell Tissue Res. 278:1994;29-39.
88. Tsuruo Y., Miyamoto T., Kitagawa K., Futaki S., Ishimura K. Immunohistochemical presence of 5alpha-reductase rat type1-containing cells in the rat brain. Brain Res. 722:1996;207-211.
89. Valencia A., Collado P., Cales J. M., Segovia S., Perez Laso C.;, Rodriuez Zafra M.; Giullamon A. Postnatal administration of dihydrotestosterone to the male rat abolishes sexual dimorism in the accessory olfactory bulb A volumetric study . Dev. Brain Res. 68:1992;132-135.
90. Wilson J. D., Griffin J. E., Russell D. W. Steroid 5alpha-reductase 2 deficiency. Endocr. Rev. 14:1993;577-593.
91. Yamada-Mouri N., Hirata S., Hayashi M., Kato J. Analysis of the expression and the first exon of aromatase mRNA in monkey brain. J. Steroid Biochem. Mol. Biol. 55:1995;17-23.
92. Yamada-Mouri, N.; Hirata, S.; Kato, J.; Hoshi, K. Expression and distribution of cortical type aromatase mRNA variant in the adult rat brain. J. Steroid Biochem. Mol. Biol. 60:325-329; 1997.
93. Yu W. A. Administration of testosterone attenuates neuronal loss following axotomy in the brain-stem nuclei of female rats. J. Neurosci. 9:1989;3908-3914.