Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: A cellular-level analysis using in situ hybridization

Journal of Comparative Neurology

Volumn 370, Issue 1, 1996, Pages 71-84

  Wagner, Christine K ^a,b   Morrell, Joan I ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

castration; estrogen; sex differences; testosterone

Indexed keywords

AROMATASE; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CASTRATION; CELLULAR DISTRIBUTION; ENZYME ASSAY; ENZYME LOCALIZATION; ENZYME REGULATION; FEMALE; FOREBRAIN; GENE EXPRESSION REGULATION; HORMONAL REGULATION; IN SITU HYBRIDIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RNA ANALYSIS;

ANIMALS; AROMATASE; ESTRADIOL; FEMALE; IN SITU HYBRIDIZATION; MALE; NEURONS; ORCHIECTOMY; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEXUAL MATURATION; TESTIS; TESTOSTERONE;

EID: 0029977498     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960617)370:1<71::AID-CNE7>3.0.CO;2-I     Document Type: Article

References (42)

1. Abdelgadir, S.E., J.A. Resko, S.R. Ojeda, E.D. Lephart, M.J. McPhaul, and C.E. Roselli (1994) Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain. Endocrinology 135:395-401.
2. Balthazart, J., A. Foidart, and N. Harada. (1990a) Immunocytochemical localization of aromatase in the brain. Brain Res. 514:327-333.
3. Balthazart, J., A. Foidart, C. Surlemont, A. Vockel, and N. Harada (1990b) Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: An immunocytochemical study. J. Comp. Neurol. 301:276-288.
4. Balthazart, J., A. Foidart, C. Surlemont, and N. Harada (1991) Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J. Neurobiol. 22:143-157.
5. Bonsall, R.W., A.N. Clancy, and R.P. Michael (1992) Effects of the nonsteroidal aromatase inhibitor, fadrozole, on sexual behavior in male rats. Horm. Behav. 26:240-254.
6. Christensen, L.W. and L.G. Clemens (1974) Intrahypothalamic implants of testosterone or estradiol and resumption of masculine sexual behavior in long-term castrated male rats. Endocrinology 95:984-990.
7. Christensen, L.W. and L.G. Clemens (1975) Blockade of testosterone-induced mounting behavior in the male rat with intracranial application of the aromatization inhibitor, androst-1,4,6-triene-3,17-dione. Endocrinology 97:1545-1551.
8. Davis, P.G. and R.J. Barfield (1979) Activation of masculine sexual behavior by intracranial estradiol benzoate implants in male rats. Neuroendocrinol. 28:217-227.
9. Doody, K.J., E.D. Lephart, D. Stirling, M.C. Lorence, R.R. Magness, M.J. McPhaul, and E.R. Simpson (1991) Expression of mRNA species encoding steroidogenic enzyme in the rat ovary. J. Molec. Endocrinol. 6:153-162.
10. Harada, N. and K. Yamada (1992) Ontogeny of aromatase messenger ribonucleic acid in mouse brain: Fluorometrical quantitation by polymerase chain reaction. Endocrinology 131:2306-2312.
11. Hickey, G.J., S. Chen, M.J. Besman, J.E. Shively, P.F. Hall, D. Gaddy-Kurten, and J.S. Richards (1988) Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in the rat ovarian follicles and corpora lutea: Relationship to estradiol biosynthesis. Endocrinology 122:1426-1436.
12. Hickey, G.J., J.S. Krasnow, W.G. Beattie, and J.S. Richards (1990) Aromatase cytochrome P450 in rat ovarian granulosa cells before and after luteinization: Adenosine 3′, 5′-monophosphate-dependentand independent regulation. Cloning and sequencing of rat aromatase cDNA and 5' genomic DNA. Molec. Endocrinology 4:3-12.
13. Jakab, R.L., T.L. Horvath, C. Leranth, N. Harada, and F. Naftolin (1993) Aromatase immunoreactivity in the rat brain: gonadectomy-sensitive hypothalamic neurons and an unresponsive 'limbic ring' of the lateral septum-bed nucleus-amygdala complex. J. Steroid Biochem. Molec. Biol. 44:481-498.
14. Lauber, M.E. and W. Lichtensteiger (1994) Pre- and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization. Endocrinol. 135:1661-1668.
15. Lephart, E.D., K.G. Peterson, J.F. Noble, F.W. George, and M.J. McPhaul (1990) The structure of cDNA clones encoding the aromatase P-450 isolated from a rat Leydig cell tumor line demonstrates differential processing of aromatase mRNA in rat ovary and a neoplastic cell line. Mol. Cell. Endocrinol. 70:31-40.
16. Lephart, E.D., E.R. Simpson, and M.J. McPhaul (1992a) Ovarian aromatase cytochrome P-450 mRNA levels correlate with enzyme activity and serum estradiol levels in anestrous, pregnant and lactatmg rats. Mol. Cell. Endocrinol. 82:205-214.
17. Lephart, E.D., E.R. Simpson, M.J. McPhaul, M.W. Kilgore, J.D. Wilson, and S.R. Ojeda (1992b) Brain aromatase cytochrome P-450 messenger RNA levels and enzyme activity during prenatal and perinatal development in the rat. Molec. Brain Res. 16:187-192.
18. Lisciotto, C.A. and J.I. Morrell (1993) Circulating gonadal steroid hormones regulate estrogen receptor mRNA in the male rat forebrain. Molec. Brain Res. 20:79-90.
19. Mahendroo, M.S., G.D. Means, C.R. Mendelson, and E.R. Simpson (1991) Tissue-specific expression of human P450 aromatase: The promotor responsible for expression in adipose tissue is different from that utilized in placenta. J. Biol. Chem. 266:11276-11281.
20. McEwen, B.S., I. Leiberburg, C. Chaptal, and L.C. Krey (1977) Aromatization: Important for sexual differentiation of the neonatal rat brain. Horm. Behav. 9:249-263.
21. Means, G.D., M.S. Mahendroo, C.J. Corbin, J.M. Mathis, F.E. Powell, C.R. Mendelson, and E.R. Simpson (1989) Structural analysis of the gene encoding human aromatase cytochrome P-450, the enzyme responsible for estrogen biosynthesis. J. Biol. Chem. 264:19385-19391.
22. Naftolin, F. K.J. Ryan, I.J. Davies, V.V. Reddy, F. Flores, Z. Petor, M. Kuhn, R.J. White, Y. Takaoka, and L. Wolin (1975) The formation of estrogens by central neuroendocrine tissues. Recent Prog. Horm. Res. 31:295-319.
23. Naftolin F., C. Leranth, and J. Balthazart (1990) Ultrastructural localization of aromatase immunoreactivity in hypothalamic neurons. Program of the 72nd Annual Meeting of the Endocrine Society, Atlanta, GA, p 192 (Abstract).
24. Parsons, B., T.C. Rainbow, and B.S. McEwen (1984) Organizational effects of testosterone via aromattization on feminine reproductive behavior and neural progestin receptors in rat brain. Endocrinology 115: 1412-1417.
25. Pfaff, D.W. and M. Keiner (1973) Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J. Comp. Neurol. 151:121-158.
26. Roselli, C.E., W.E. Ellinwood, and J.A. Resko (1984) Regulation of brain aromatase activity in rats. Endocrinology 114:192-200.
27. Roselli, C.E., L.E. Horton, and J.A. Resko (1985) Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117:2471-2477.
28. Roselli, C.E., R.L. Salisbury, and J.A. Resko (1987) Genetic evidence for androgen-dependent and independent control of aromatase activity in the rat brain. Endocrinology 121:2205-2210.
29. Sanghera, M.K., E.R. Simpson, M.J. McPhaul, G. Kozlowski, A.J. Conley, and E.D. Lephart (1991) Immunocytochemical distribution of aromatase P450 in the rat brain using peptide-generated polyclonal antibodies. Endocrinology 129:2834-2844.
30. Schlinger, B.A. and G.V. Callard (1989) Localization of aromatase in synaptosomal and microsomal subfractions of quail (Coturnix coturnix japonica) brain. Neuroendocrinology 49:434-441.
31. Schumacher, M. and J. Balthazart (1987) Neuroanatomical distribution of testosterone metabolizing enzymes in the Japenese quail. Brain Res. 422:137-148.
32. Selmanoff, M.K., L.D. Brodkin, R.I. Weiner, and P.K. Siiteri (1977) Aromatization and 5a-reduction of androgens in discrete hypothalamic and limbic regions of the male and female rat. Endocrinology 101:841-848.
33. 2). J. Comp. Neurol. 290:502-515.
34. Simerly, R.B., C. Chang, M. Muramatsu, and L.W. Swanson (1990) Distribution of androgen and estrogen receptor mRNA containing cells in the rat brain: An in situ hybridization study. J. Comp. Neurol. 294:76-95.
35. Simmons, D.M., J.L. Arriza, and L.W. Swanson (1989) A complete protocol for in situ hybridization of messenger RNA's in brain and other tissues with radiolabelled single-stranded RNA probes. J. Histotech. 12:169-181.
36. Stumpf, W.E., M. Sar, and D.A. Keefer (1975) Atlas of estrogen target cells in rat brain. In: Anatomical Neuroendocrinology. Basel: Karger, pp. 104-119.
37. Swanson, L.W. (1992) Brain Maps: Structure of the Rat Brain. Amsterdam: Elsevier.
38. Toran-Allerand, C.D. (1976) Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: Implications for sexual differentiation. Brain Res. 106:407-412.
39. Toran-Allerand, C.D., K. Hashimoto, W.T. Greenough, and M. Saltarelli (1983) Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: III. Effects of estrogen on dendritic differentiation. Dev. Brain Res. 7:97-101.
40. Tsuruo, Y., K. Ishimura, H. Fujita, and Y. Osawa (1994) Immunocytochemical localization of aromatase-containing neurons in the rat brain during pre- and postnatal development. Cell Tissue Res. 278:29-39.
41. Wang, J. and S. Chen (1992) Identification of a promoter and a silencer at the 3′-end of the first intron of the human aromatase gene. Molec. Endocrinol. 6:1479-1488.
42. Yamada, N.M., S. Hirata, and J. Kato (1994) Distribution and postnatal changes of aromatase mRNA in the female rat brain. J. Steroid Biochem. Molec. Biol. 45:529-533.