Tissue- and sex-specific regulation of CYP19A1 expression in the Atlantic croaker (Micropogonias undulatus)

General and Comparative Endocrinology

Volumn 149, Issue 2, 2006, Pages 205-216

  Nunez, B Scott ^a   Applebaum, Scott L ^a  

^a The University of Texas at Austin   (United States)

Author keywords

Aromatase; Brain; CYP19A1; Gonadotropin; Ovary; Sex steroids; Teleost; Testis

Indexed keywords

17,20BETA,21 TRIHYDROXY 4 PREGNEN 3 ONE; AROMATASE; CHORIONIC GONADOTROPIN; COMPLEMENTARY DNA; CYTOCHROME P450 19A1; ESTRADIOL; RNA 18S; SEX HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; ATLANTIC CROAKER; BRAIN; BRAIN LEVEL; DNA SEQUENCE; ENZYME ISOLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE ISOLATION; GONAD; GONAD DEVELOPMENT; IN VITRO STUDY; MALE; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; OVARY DEVELOPMENT; OVARY FOLLICLE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPAWNING; STATISTICAL SIGNIFICANCE; TELEOST; TESTIS; UNINDEXED SEQUENCE;

EID: 33749249546     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2006.06.005     Document Type: Article

References (91)

1. Abney T.O. The potential roles of estrogens in regulating Leydig cell development and function: a review. Steroids 64 (1999) 610-617
2. Amarneh B., Corbin C.J., Peterson J.A., Simpson E.R., and Graham-Lorence S. Functional domains of human aromatase cytochrome P450 characterized by linear alignment and site-directed mutagenesis. Mol. Endocrinol. 7 (1993) 1617-1624
3. Andreassen T.K., Skjoedt K., Anglade I., Kah O., and Korsgaard B. Molecular cloning, characterisation, and tissue distribution of oestrogen receptor alpha in eelpout (Zoarces viviparus). Gen. Comp. Endocrinol. 132 (2003) 356-368
4. Balthazart J., and Ball G.F. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci. 21 (1998) 243-249
5. Barbieri L.R., Chittenden M.E., and Lowerrebarbieri S.K. Maturity, spawning, and ovarian cycle of Atlantic croaker, Micropogonias undulatus, in the Chesapeake Bay and adjacent coastal waters. Fish. B-NOAA 92 (1994) 671-685
6. Belvedere P., Dalla Valle L., Lucchetti A., Ramina A., Vianello S., and Colombo L. Extraglandular expression of genes encoding steroidogenic cytochromes in rainbow trout (Oncorhynchus mykiss Walbaum). Ann. N.Y. Acad. Sci. 839 (1998) 589-591
7. Blazquez M., and Piferrer F. Cloning, sequence analysis, tissue distribution, and sex-specific expression of the neural form of P450 aromatase in juvenile sea bass (Dicentrarchus labrax). Mol. Cell Endocrinol. 219 (2004) 83-94
8. Borg B., Andersson E., Mayer I., and Lambert J.G. Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. III. Effects of castration under different conditions and of replacement with different androgens. Exp. Biol. 48 (1989) 149-152
9. Bouma J., and Nagler J.J. Estrogen receptor-alpha protein localization in the testis of the rainbow trout (Oncorhynchus mykiss) during different stages of the reproductive cycle. Biol. Reprod. 65 (2001) 60-65
10. Bourguiba S., Genissel C., Lambard S., Bouraima H., and Carreau S. Regulation of aromatase gene expression in Leydig cells and germ cells. J. Steroid Biochem. Mol. Biol. 86 (2003) 335-343
11. Braun A.M., and Thomas P. Androgens inhibit estradiol-17beta synthesis in Atlantic croaker (Micropogonias undulatus) ovaries by a nongenomic mechanism initiated at the cell surface. Biol. Reprod. 69 (2003) 1642-1650
12. Brinkmann A.O., Leemborg F.G., Roodnat E.M., De Jong F.H., and Van der Molen H.J. A specific action of estradiol on enzymes involved in testicular steroidogenesis. Biol. Reprod. 23 (1980) 801-809
13. Callard G.V., Petro Z., and Ryan K.J. Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103 (1978) 2283-2290
14. Callard G., Schlinger B., and Pasmanik M. Nonmammalian vertebrate models in studies of brain-steroid interactions. J. Exp. Zool. Suppl. 4 (1990) 6-16
15. Callard G.V., Tchoudakova A.V., Kishida M., and Wood E. Differential tissue distribution, developmental programming, estrogen regulation and promoter characteristics of cyp19 genes in teleost fish. J. Steroid Biochem. Mol. Biol. 79 (2001) 305-314
16. Chang X.T., Kobayashi T., Kajiura H., Nakamura M., and Nagahama Y. Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): changes in P450arom mRNA, protein and enzyme activity in ovarian follicles during oogenesis. J. Mol. Endocrinol. 18 (1997) 57-66
17. Chiang E.F., Yan Y.L., Guiguen Y., Postlethwait J., and Chung B. Two Cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain. Mol. Biol. Evol. 18 (2001) 542-550
18. Choi C.Y., and Habibi H.R. Molecular cloning of estrogen receptor alpha and expression pattern of estrogen receptor subtypes in male and female goldfish. Mol. Cell Endocrinol. 204 (2003) 169-177
19. Corbin C.J., Khalil M.W., and Conley A.J. Functional ovarian and placental isoforms of porcine aromatase. Mol. Cell Endocrinol. 113 (1995) 29-37
20. Dalla Valle L., Lunardi L., Colombo L., and Belvedere P. European sea bass (Dicentrarchus labrax L.) cytochrome P450arom: cDNA cloning, expression and genomic organization. J. Steroid Biochem. Mol. Biol. 80 (2002) 25-34
21. Dorrington J.H., Fritz I.B., and Armstrong D.T. Control of testicular estrogen synthesis. Biol. Reprod. 18 (1978) 55-64
22. Fink L., Seeger W., Ermert L., Hanze J., Stahl U., Grimminger F., Kummer W., and Bohle R.M. Real-time quantitative RT-PCR after laser-assisted cell picking. Nat. Med. 4 (1998) 1329-1333
23. Fisher C.R., Graves K.H., Parlow A.F., and Simpson E.R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. USA 95 (1998) 6965-6970
24. Fitzpatrick S.L., and Richards J.S. Regulation of cytochrome P450 aromatase messenger ribonucleic acid and activity by steroids and gonadotropins in rat granulosa cells. Endocrinology 129 (1991) 1452-1462
25. Fitzpatrick S.L., Carlone D.L., Robker R.L., and Richards J.S. Expression of aromatase in the ovary: down-regulation of mRNA by the ovulatory luteinizing hormone surge. Steroids 62 (1997) 197-206
26. Fukada S., Tanaka M., Matsuyama M., Kobayashi D., and Nagahama Y. Isolation, characterization, and expression of cDNAs encoding the medaka (Oryzias latipes) ovarian follicle cytochrome P-450 aromatase. Mol. Reprod. Dev. 45 (1996) 285-290
27. Gen K., Okuzawa K., Senthilkumaran B., Tanaka H., Moriyama S., and Kagawa H. Unique expression of gonadotropin-I and -II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biol. Reprod. 63 (2000) 308-319
28. Gen K., Okuzawa K., Kumakura N., Yamaguchi S., and Kagawa H. Correlation between messenger RNA expression of cytochrome P450 aromatase and its enzyme activity during oocyte development in the red seabream (Pagrus major). Biol. Reprod. 65 (2001) 1186-1194
29. Genissel C., Levallet J., and Carreau S. Regulation of cytochrome P450 aromatase gene expression in adult rat Leydig cells: comparison with estradiol production. J. Endocrinol. 168 (2001) 95-105
30. Gonzalez A., and Piferrer F. Characterization of aromatase activity in the sea bass: effects of temperature and different catalytic properties of brain and ovarian homogenates and microsomes. J. Exp. Zool. 293 (2002) 500-510
31. Gonzalez A., and Piferrer F. Aromatase activity in the European sea bass (Dicentrarchus labrax L.) brain. Distribution and changes in relation to age, sex, and the annual reproductive cycle. Gen. Comp. Endocrinol. 132 (2003) 223-230
32. Goto-Kazeto R., Kight K.E., Zohar Y., Place A.R., and Trant J.M. Localization and expression of aromatase mRNA in adult zebrafish. Gen. Comp. Endocrinol. 139 (2004) 72-84
33. Greytak S.R., Champlin D., and Callard G.V. Isolation and characterization of two cytochrome P450 aromatase forms in killifish (Fundulus heteroclitus): Differential expression in fish from polluted and unpolluted environments. Aquat. Toxicol. 71 (2005) 371-389
34. Guiguen Y., Baroiller J.F., Ricordel M.J., Iseki K., McMeel O.M., Martin S.A., and Fostier A. Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol. Reprod. Dev. 54 (1999) 154-162
35. Halm S., Martinez-Rodriguez G., Rodriguez L., Prat F., Mylonas C.C., Carrillo M., and Zanuy S. Cloning, characterisation, and expression of three oestrogen receptors (ERalpha, ERbeta1 and ERbeta2) in the European sea bass, Dicentrarchus labrax. Mol. Cell Endocrinol. 223 (2004) 63-75
36. Hawkins M.B., Thornton J.W., Crews D., Skipper J.K., Dotte A., and Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl. Acad. Sci. USA 97 (2000) 10751-10756
37. Hess R.A. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1 (2003) 52
38. Kagawa H., Young G., and Nagahama Y. Relationship between seasonal plasma estradiol-17 beta and testosterone levels and in vitro production by ovarian follicles of amago salmon (Oncorhynchus rhodurus). Biol. Reprod. 29 (1983) 301-309
39. Kagawa H., Gen K., Okuzawa K., and Tanaka H. Effects of luteinizing hormone and follicle-stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicles of red seabream, Pagrus major. Biol. Reprod. 68 (2003) 1562-1568
40. Kanamori A., Adachi S., and Nagahama Y. Developmental changes in steroidogenic responses of ovarian follicles of amago salmon (Oncorhynchus rhodurus) to chum salmon gonadotropin during oogenesis. Gen. Comp. Endocrinol. 72 (1988) 13-24
41. Kazeto Y., Ijiri S., Place A.R., Zohar Y., and Trant J.M. The 5′-flanking regions of CYP19A1 and CYP19A2 in zebrafish. Biochem. Biophys. Res. Commun. 288 (2001) 503-508
42. Kazeto Y., Place A.R., and Trant J.M. Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat. Toxicol. 69 (2004) 25-34
43. Khan I.A., Hawkins M.B., and Thomas P. Gonadal stage-dependent effects of gonadal steroids on gonadotropin II secretion in the Atlantic croaker (Micropogonias undulatus). Biol. Reprod. 61 (1999) 834-841
44. Kishida M., and Callard G.V. Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 142 (2001) 740-750
45. Kishida M., McLellan M., Miranda J.A., and Callard G.V. Estrogen and xenoestrogens upregulate the brain aromatase isoform (P450aromB) and perturb markers of early development in zebrafish (Danio rerio). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129 (2001) 261-268
46. Kumar S., Tamura K., and Nei M. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5 (2004) 150-163
47. Kwon J.Y., McAndrew B.J., and Penman D.J. Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus. Mol. Reprod. Dev. 59 (2001) 359-370
48. Labrie F. Extragonadal synthesis of sex steroids: intracrinology. Ann. Endocrinol. -Paris 64 (2003) 95-107
49. Larsson D.G., Mayer I., Hyllner S.J., and Forlin L. Seasonal variations of vitelline envelope proteins, vitellogenin, and sex steroids in male and female eelpout (Zoarces viviparus). Gen. Comp. Endocrinol. 125 (2002) 184-196
50. Liu X., Liang B., and Zhang S. Sequence and expression of cytochrome P450 aromatase and FTZ-F1 genes in the protandrous black porgy (Acanthopagrus schlegeli). Gen. Comp. Endocrinol. 138 (2004) 247-254
51. Loomis A.K., and Thomas P. Binding characteristics of estrogen receptor (ER) in Atlantic croaker (Micropogonias undulatus) testis: different affinity for estrogens and xenobiotics from that of hepatic ER. Biol. Reprod. 61 (1999) 51-60
52. Loomis A.K., and Thomas P. Effects of estrogens and xenoestrogens on androgen production by Atlantic croaker testes in vitro: evidence for a nongenomic action mediated by an estrogen membrane receptor. Biol. Reprod. 62 (2000) 995-1004
53. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., and Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA 90 (1993) 11162-11166
54. Luckenbach J.A., Early L.W., Rowe A.H., Borski R.J., Daniels H.V., and Godwin J. Aromatase cytochrome P450: cloning, intron variation, and ontogeny of gene expression in southern flounder (Paralichthys lethostigma). J. Exp. Zoolog. A Comp. Exp. Biol. 303 (2005) 643-656
55. Maestro M.A., Planas J.V., Moriyama S., Gutierrez J., Planas J., and Swanson P. Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. Gen. Comp. Endocrinol. 106 (1997) 189-201
56. Mayer I., Borg B., Berglund I., and Lambert J.G. Effects of castration and androgen treatment on aromatase activity in the brain of mature male Atlantic salmon (Salmo salar L.) parr. Gen. Comp. Endocrinol. 82 (1991) 86-92
57. Menuet A., Anglade I., Le Guevel R., Pellegrini E., Pakdel F., and Kah O. Distribution of aromatase mRNA and protein in the brain and pituitary of female rainbow trout: comparison with estrogen receptor alpha. J. Comp. Neurol. 462 (2003) 180-193
58. Menuet A., Pellegrini E., Brion F., Gueguen M.M., Anglade I., Pakdel F., and Kah O. Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene. J. Comp. Neurol. 485 (2005) 304-320
59. Montserrat N., Gonzalez A., Mendez E., Piferrer F., and Planas J.V. Effects of follicle stimulating hormone on estradiol-17 beta production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro. Gen. Comp. Endocrinol. 137 (2004) 123-131
60. Nagahama Y., Yoshikuni M., Yamashita M., Tokumoto T., and Katsu Y. Regulation of oocyte growth and maturation in fish. Curr. Top. Dev. Biol. 30 (1995) 103-145
61. Onoda M., and Hall P.F. Inhibition of testicular microsomal cytochrome P-450 (17 alpha-hydroxylase/C-17,20-lyase) by estrogens. Endocrinology 109 (1981) 763-767
62. Ozols J., Heinemann F., and Johnson E. Amino acid sequence of an analogous peptide from two forms of cytochrome P-450. J. Biol. Chem. 256 (1981) 11405-11408
63. Pace M.C., and Thomas P. Steroid-induced oocyte maturation in Atlantic croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Biol. Reprod. 73 (2005) 988-996
64. Pasmanik M., and Callard G.V. Changes in brain aromatase and 5 alpha-reductase activities correlate significantly with seasonal reproductive cycles in goldfish (Carassius auratus). Endocrinology 122 (1988) 1349-1356
65. Patino R., and Thomas P. Induction of maturation of Atlantic croaker oocytes by 17 alpha,20 beta,21-trihydroxy-4-pregnen-3-one in vitro: consideration of some biological and experimental variables. J. Exp. Zool. 255 (1990) 97-109
66. Pomerantz D.K. Effects of in vivo gonadotropin treatment on estrogen levels in the testis of the immature rat. Biol. Reprod. 21 (1979) 1247-1255
67. Prat F., Sumpter J.P., and Tyler C.R. Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductivecycle in male and female rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 54 (1996) 1375-1382
68. Saitou N., and Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 (1987) 406-425
69. Scott, A.P., Stewart, C. and Allen, Y. (2000). 17b-Oestradiol in male flatfish. In: 6th International Symposium on Reproductive Physiology of Fish, Bergen, Norway.
70. Senthilkumaran B., Yoshikuni M., and Nagahama Y. A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol. Cell Endocrinol. 215 (2004) 11-18
71. Simpson E.R. Aromatase: biologic relevance of tissue-specific expression. Semin. Reprod. Med. 22 (2004) 11-23
72. Simpson E.R., Misso M., Hewitt K.N., Hill R.A., Boon W.C., Jones M.E., Kovacic A., Zhou J., and Clyne C.D. Estrogen-the good, the bad, and the unexpected. Endocr. Rev. 26 (2005) 322-330
73. Socorro S., Power D.M., Olsson P.E., and Canario A.V. Two estrogen receptors expressed in the teleost fish, Sparus aurata: cDNA cloning, characterization and tissue distribution. J. Endocrinol. 166 (2000) 293-306
74. Sumpter J.P. Xenoendorine disrupters-environmental impacts. Toxicol. Lett. 102-103 (1998) 337-342
75. Tanaka M., Telecky T.M., Fukada S., Adachi S., Chen S., and Nagahama Y. Cloning and sequence analysis of the cDNA encoding P-450 aromatase (P450arom) from a rainbow trout (Oncorhynchus mykiss) ovary; relationship between the amount of P450arom mRNA and the production of oestradiol-17 beta in the ovary. J. Mol. Endocrinol. 8 (1992) 53-61
76. Tcholakian R.K., and Steinberger A. In vitro metabolism of testosterone by cultured Sertoli cells and the effect of FSH. Steroids 33 (1979) 495-526
77. Tchoudakova A., and Callard G.V. Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology 139 (1998) 2179-2189
78. Tchoudakova A., Pathak S., and Callard G.V. Molecular cloning of an estrogen receptor beta subtype from the goldfish, Carassius auratus. Gen. Comp. Endocrinol. 113 (1999) 388-400
79. Tchoudakova A., Kishida M., Wood E., and Callard G.V. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. Mol. Biol. 78 (2001) 427-439
80. Teves A.C., Granneman J.C., van Dijk W., and Bogerd J. Cloning and expression of a functional estrogen receptor-alpha from African catfish (Clarias gariepinus) pituitary. J. Mol. Endocrinol. 30 (2003) 173-185
81. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
82. Tong S.K., and Chung B.C. Analysis of zebrafish cyp19 promoters. J. Steroid. Biochem. Mol. Biol. 86 (2003) 381-386
83. Trant J.M., and Thomas P. Changes in ovarian steroidogenesis in vitro associated with final maturation of Atlantic croaker oocytes. Gen. Comp. Endocrinol. 75 (1989) 405-412
84. Trant J.M., and Thomas P. Isolation of a novel maturation-inducing steroid produced in vitro by ovaries of Atlantic croaker. Gen. Comp. Endocrinol. 75 (1989) 397-404
85. Trant J.M., Lehrter J., Gregory T., Nunez S., and Wunder J. Expression of cytochrome P450 aromatase in the channel catfish, Ictalurus punctatus. J. Steroid Biochem. Mol. Biol. 61 (1997) 393-397
86. Trudeau V.L., Sloley B.D., Wong A.O., and Peter R.E. Interactions of gonadal steroids with brain dopamine and gonadotropin-releasing hormone in the control of gonadotropin-II secretion in the goldfish. Gen. Comp. Endocrinol. 89 (1993) 39-50
87. Tzchori I., Degani G., Hurvitz A., and Moav B. Cloning and developmental expression of the cytochrome P450 aromatase gene (CYP19) in the European eel (Anguilla anguilla). Gen. Comp. Endocrinol. 138 (2004) 271-280
88. Valladares L.E., and Payne A.H. Acute stimulation of aromatization in Leydig cells by human chorionic gonadotropin in vitro. Proc. Natl. Acad. Sci. USA 76 (1979) 4460-4463
89. Valle L.D., Ramina A., Vianello S., Belvedere P., and Colombo L. Cloning of two mRNA variants of brain aromatase cytochrome P450 in rainbow trout (Oncorhynchus mykiss Walbaum). J. Steroid Biochem. Mol. Biol. 82 (2002) 19-32
90. Wu C., Patino R., Davis K.B., and Chang X. Localization of estrogen receptor alpha and beta RNA in germinal and nongerminal epithelia of the channel catfish testis. Gen. Comp. Endocrinol. 124 (2001) 12-20
91. Zhang Y., Zhang W., Zhang L., Zhu T., Tian J., Li X., and Lin H. Two distinct cytochrome P450 aromatases in the orange-spotted grouper (Epinephelus coioides): cDNA cloning and differential mRNA expression. J. Steroid Biochem. Mol. Biol. 92 (2004) 39-50