Expression pattern, cellular localization and promoter activity analysis of ovarian aromatase (Cyp19a1a) in protogynous hermaphrodite red-spotted grouper

Molecular and Cellular Endocrinology

Volumn 307, Issue 1-2, 2009, Pages 224-236

  Huang, Wei ^a   Zhou, Li ^a   Li, Zhi ^a   Gui, Jian Fang ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Cyp19a1a b; Grouper; Hermaphrodite; Immunofluorescene localization; Promoter activity; Sex reversal

Indexed keywords

AROMATASE; CCAAT ENHANCER BINDING PROTEIN; CIS ACTING ELEMENT; COMPLEMENTARY DNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOCHROME P450 19A1A; LUCIFERASE; PROTEIN ARE; PROTEIN SF 1; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXL1; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR SOX5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA FLANKING REGION; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; FEMALE; FISH; GENE DELETION; HERMAPHRODITISM; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MALE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MOTIF; RED SPOTTED GROUPER; SEX DIFFERENTIATION; SEX TRANSFORMATION; TATA BOX; TESTIS; TISSUE SPECIFICITY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; AROMATASE; BASE SEQUENCE; BINDING SITES; CONSERVED SEQUENCE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HERMAPHRODITISM; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; OVARY; PERCIFORMES; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE DELETION; TRANSCRIPTION FACTORS;

EID: 67349113957     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.04.003     Document Type: Article

References (61)

1. Akatsuka N., Komatsuzaki E., Ishikawa A., Suzuki I., Yamane N., and Miyata S. Expression of the gonadal p450 aromatase gene of Xenopus and characterization of the 5′-flanking region of the aromatase gene. J. Steroid Biochem. Mol. Biol. 96 (2005) 45-50
2. 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
3. Blazquez M., González A., Papadaki M., Mylonas C., and Piferrer F. Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax). Gen. Comp. Endocrinol. 158 (2008) 95-101
4. Callard G.V., and Tchoudakova A. Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish. J. Steroid Biochem. Mol. Biol. 61 (1997) 387-392
5. Carlone D.L., and Richards J.S. Evidence that functional interactions of CREB and SF-1 mediate hormone regulated expression of the aromatase gene in granulosa cells and constitutive expression in R2C cells. J. Steroid Biochem. Mol. Biol. 61 (1997) 223-231
6. Chang X., Kobayashi T., Senthilkumaran B., Kobayashi-Kajura H., Sudhakumari C.C., and Nagahama Y. Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 141 (2005) 101-115
7. Choi J.Y., Park J.G., Jeong H.B., Lee Y.D., Takemura A., and Kim S.J. Molecular cloning of cytochrome P450 aromatases in the protogynous wrasse, Halichoeres tenuispinis. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 141 (2005) 49-59
8. Dalla Valle L., Lunardi L., and Belvedere C.P. European sea bass (Dicentratus labrax L.) cytochrome P450arom: cDNA cloning, expression and genomic organization. J. Steroid Biochem. Mol. Biol. 80 (2002) 25-34
9. Devlin H., and Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208 (2002) 191-364
10. Fenske M., and Segner H. Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat. Toxicol. 67 (2004) 105-126
11. Galay-Burgos M., Gealy C., Navarro-Martín L., Piferrer F., Zanuy S., and Sweeney G.E. Cloning of the promoter from the gonadal aromatase gene of the European sea bass and identification of single nucleotide polymorphisms. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 145 (2006) 47-53
12. Gardner L., Anderson T., Place A.R., Dixon B., and Elizur A. Sex change strategy and the aromatase genes. J. Steroid Biochem. Mol. Biol. 94 (2005) 395-404
13. Gelinas D., Pitoc G.A., and Callard G.V. Isolation of a goldfish brain cytochrome P450 aromatase cDNA: mRNA expression during the seasonal cycle and after steroid treatment. Mol. Cell. Endocrinol. 16 (1998) 81-93
14. 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
15. Guiguen Y., Fostier A., Piferrer F., and Chang C.F. Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen. Comp. Endocrinol. (2009) 10.1016/j.ygcen.2009.03.002
16. Hinshelwood M.M., Smith M.E., Murry B.A., and Mendelson C.R. A 278 bp region just upstream of the human CYP19 (aromatase) gene mediates ovary-specific expression in transgenic mice. Endocrinology 141 (2000) 2050-2053
17. Ijiri S., Kazeto Y., Lokman P.M., Adachi S., and Yamauchi K. Characterization of a cDNA encoding P-450 aromatase (CYP19) from Japanese eel ovary and its expression in ovarian follicles during induced ovarian development. Gen. Comp. Endocrinol. 130 (2003) 193-203
18. Kato T., Matsui K., Takase M., Kobayashi M., and Nakamura M. Expression of P450 aromatase protein in developing and in sex-reversed gonads of the XX/XY type of the frog Rana rugosa. Gen. Comp. Endocrinol. 137 (2004) 227-236
19. Kazeto Y., Ijiri S., Place A.R., Zohar Y., and Trant J.M. The 5′-flanking regions of CYP19A1A1 and CYP19A1A2 in zebrafish. Biochem. Biophys. Res. Commun. 288 (2001) 503-508
20. Kitano T., Takamune K., Nagahama Y., and Abe S.I. Aromatase inhibitor and 17alpha-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol. Reprod. Dev. 56 (2000) 1-5
21. Kobayashi Y., Sunobe T., Kobayashi T., Nakamura M., Suzuki N., and Nagahama Y. Molecular cloning and expression of Ad4BP/SF-1 in the serial sex changing gobiid fish, Trimma okinawae. Biochem. Biophys. Res. Commun. 332 (2005) 1073-1080
22. Kroon F.J., and Liley N.R. The role of steroid hormones in protogynous sex change in the Blackeye goby, Coryphopterus nicholsii (Teleostei: Gobiidae). Gen. Comp. Endocrinol. 118 (2000) 273-283
23. Kwon J.Y., Haghpanah V., Kogson-Hurtado L.M., McAndrew B.J., and Penman D.J. Masculinization of genetic female nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287 (2000) 46-53
24. Kwon J.Y., Mc Andrew 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
25. Li C.J., Zhou L., Wang Y., Hong Y.H., and Gui J.F. Molecular and expression characterization of three gonadotropin subunits common α, FSHβ and LHβ in groupers. Mol. Cell. Endocrinol. 233 (2005) 33-46
26. Li F.B., and Gui J.F. Clonal diversity and genealogical relationships of gibel carp in four hatcheries. Anim. Genet. 39 (2008) 28-33
27. Li G.L., Liu X.C., Zhang Y., Bei J.X., and Lin H.R. Cloning and expression of two cytochrome P450 aromatase genes in red-spotted grouper Epinephelus akaara. Acta Zoolog. Sin. 50 (2004) 791-799
28. Li G.L., Liu X.C., and Lin H.R. Aromatase inhibitor letrozole induces sex inversion in the protogynous red spotted grouper (Epinephelus akaara). Acta Physiol. Sin. 57 (2005) 473-479
29. Li G.L., Liu X.C., and Lin H.R. Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara). Anim. Reprod. Sci. 99 (2007) 156-166
30. 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
31. Mei J., Chen B., Yue H.M., and Gui J.F. Identification of a C1q family member associated with cortical granules and follicular cell apoptosis in Carassius auratus gibelio. Mol. Cell. Endocrinol. 289 (2008) 67-76
32. Mei J., Zhang Q.Y., Li Z., Lin S., and Gui J.F. C1q-like inhibits p53-mediated apoptosis and controls normal hematopoiesis during zebrafish embryogenesis. Dev. Biol. 319 (2008) 273-284
33. Morales V., Gonzalez-Robayna I., Hernandez I., Quintana J., Santana P., Ruiz de Galarreta C.M., and Fanjul L.F. The inducible isoform of CREM (inducible cAMP early repressor, ICER) is a repressor of CYP19 rat ovarian promoter. J. Endocrinol. 179 (2003) 417-425
34. Nocillado J.N., Elizur A., Avitan A., Carrick F., and Levavi-Sivan B. Cytochrome P450 aromatase in grey mullet: cDNA and promoter isolation; brain, pituitary and ovarian expression during puberty. Mol. Cell. Endocrinol. 263 (2006) 65-78
35. Oshima Y., Kato T., Wang D., Murakami T., Matsuda Y., Nagahama Y., and Nakamura M. Promoter activity and chromosomal location of the Rana rugosa P450 aromatase (CYP19) gene. Zoolog. Sci. 23 (2006) 79-85
36. Piferrer F., Zanuy S., Carrillo M., Solar I.I., Devlin R.M., and Donaldson E.M. Brief treatment with an aromatase inhibitor during sex differentiation causes chromosomally female salmon to develop as normal, functional males. J. Exp. Zool. 270 (1994) 255-262
37. Sampath K.R., Ijiri S., and Trant J.M. Changes in the expression of genes encoding steroidogenic enzymes in the channel catfish (Ictalurus punctatus) ovary throughout a reproductive cycle. Biol. Reprod. 63 (2000) 1676-1682
38. Simpson E.R., Mahendroo M.S., Means G.D., Kilgore M.W., Hinshelwood M.M., Graham-Lorence S., Amarneh B., Ito Y., Fisher C.R., Michael M.D., et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocrinol. Rev. 15 (1994) 342-355
39. Stocco C. Aromatase expression in the ovary: hormonal and molecular regulation. Steroids 73 (2008) 473-487
40. Sunobe T., Nakamura M., Kobayashi Y., Kobayashi T., and Nagahama Y. Aromatase immunoreactivity and the role of enzymes in steroid pathways for inducing sex change in the hermaphrodite gobiid fish Trimma okinawae. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 141 (2005) 54-59
41. Tanaka M., Fukada S., Matsuyama M., and Nagahama Y. Structure and promoter analysis of the cytochrome P450 aromatase gene of the teleost fish, Medaka, Oriyzias latipes. J. Biochem. 117 (1995) 719-725
42. 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 in the ovary. J. Mol. Endocrinol. 8 (1992) 53-61
43. 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
44. 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
45. Tong S.K., and Chung B.C. Analysis of zebrafish cyp19 promoters. J. Steroid Biochem. Mol. Biol. 86 (2003) 381-386
46. Trant J.M., Gavasso S., Ackers J., Chung B.C., and Place A.R. Developmental expression of cytochrome P450 aromatase genes (Cyp19a1a and Cyp19a1b) in zebrafish fry (Danio rerio). J. Exp. Zool. 290 (2001) 475-483
47. 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
48. Uchida D., Yamashita M., Kitano T., and Iguchi T. An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 137 (2004) 11-20
49. Van Seuningen I., Perrais M., Pigny P., Porchet N., and Aubert J.P. Sequence of the 5′-flanking region and promoter activity of the human mucin gene MUC5B in different phenotypes of colon cancer cells. Biochem. J. 348 (2000) 675-686
50. Wang Y., Zhou L., Yao B., Li C.J., and Gui J.F. Differential expression of thyroid-stimulating hormone beta subunit in gonads during sex reversal of orange-spotted and red-spotted grouper. Mol. Cell. Endocrinol. 220 (2004) 77-88
51. Xia W., Zhou L., Yao B., Li C.J., and Gui J.F. Differential and spermatogenic cell-specific expression of DMRT1 during sex reversal in protogynous hermaphroditic groupers. Mol. Cell. Endocrinol. 263 (2007) 156-172
52. Yao B., Zhou L., Wang Y., Xia W., and Gui J.F. Differential expression and dynamic changes of SOX3 during gametogenesis and sex reversal in protogynous hermaphroditic fish. J. Exp. Zool. Part A: Ecol. Genet. Physiol. 307 (2007) 207-219
53. Yoshiura Y., Senthilkumaran B., Watanabe M., Oba Y., Kobayashi T., and Nagahama Y. Synergistic expression of Ad4BP/SF-1 and cytochrome P-450 aromatase (ovarian type) in the ovary of Nile tilapia, Oreochromis niloticus, during vitellogenesis suggests transcriptional interaction. Biol. Reprod. 68 (2003) 1545-1553
54. Zhang W.M., Zhang Y., Zhang L.H., Zhao H.H., Li X., Huang H., and Lin H.R. The mRNA expression of P450 aromatase, gonadotropin β-subunits and FTZ-F1 in the orange-spotted grouper (Epinephelus Coioides) during 17α-methyltestosterone-induced precocious sex change. Mol. Reprod. Dev. 74 (2007) 665-673
55. 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
56. Zhang Y.B., Jiang J., Chen Y.D., Zhu R., Shi Y., Zhang Q.Y., and Gui J.F. The innate immune response to grass carp hemorrhagic virus (GCHV) in cultured Carassius auratus blastulae (CAB) cells. Dev. Comp. Immunol. 31 (2007) 232-243
57. Zhao J.G., Zhou L., Jin J.Y., Zhao Z., Lan J., Zhang Y.B., Zhang Q.Y., and Gui J.F. Antimicrobial activity-specific to Gram-negative bacteria and immune modulation-mediated-NF-κB and Sp1 of a medaka β-defensin. Dev. Comp. Immunol. 33 (2009) 624-637
58. Zhou L., and Gui J.F. Molecular mechanisms underlying sex change in hermaphroditic groupers. Fish Physiol. Biochem. (2009) (available online)
59. Zhou L., Li C.J., Wang Y., Xia W., Yao B., Jin J.Y., and Gui J.F. Identification and characterization of a MBP isoform specific to hypothalamus in orange-spotted grouper (Epinephelus coioides). J. Chem. Neuroanat. 34 (2007) 47-59
60. Zhou L., Yao B., Xia W., Li C.J., Wang Y., Shi Y.H., and Gui J.F. EST-based identification of genes expressed in the hypothalamus of male orange-spotted grouper (Epinephelus coioides). Aquaculture 256 (2006) 129-139
61. Zhu R., Zhang Y.B., Zhang Q.Y., and Gui J.F. Functional domains and the antiviral effect of the dsRNA-dependent protein kinase PKR from Paralichthys olivaceu. J. Virol. 82 (2008) 6889-6901