FTZ-F1 and FOXL2 up-regulate catfish brain aromatase gene transcription by specific binding to the promoter motifs

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 1, 2012, Pages 57-66

  Sridevi, P ^a   Chaitanya, R K ^a   Dutta Gupta, Aparna ^a   Senthilkumaran, B ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

Cyp19a1b; Cytochrome P450 aromatase; FOXL2; FTZ F1; Teleosts; Transcriptional regulation

Indexed keywords

AROMATASE; CYP19A1B PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FUSHI TARAZU FACTOR 1; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CATFISH; CLARIAS GARIEPINUS; CONTROLLED STUDY; DNA BINDING MOTIF; FEMALE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REGULATORY MECHANISM; TELEOST; TRANSCRIPTION REGULATION;

ANIMALS; AROMATASE; BASE SEQUENCE; BINDING SITES; BRAIN; CATFISHES; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; STEROIDOGENIC FACTOR 1; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

CLARIAS GARIEPINUS; MAMMALIA; TELEOSTEI;

EID: 82155168601     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.10.003     Document Type: Article

References (50)

1. Simpson E.R., Clyne C., Rubin G., Boon W.C., Robertson K., Britt K., Speed C., Jones M. Aromatase-a brief overview. Ann. Rev. Physiol. 2002, 64:93-127.
2. 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., Mendelson C.R., Bulun S.E. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocrinol. Rev. 1994, 15:342-355.
3. Callard G.V., Tchoudakova A. Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish. J. Steroid Biochem. Mol. Biol. 1997, 61:387-392.
4. Tchoudakova A., Callard G.V. Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology 1998, 139:2179-2189.
5. Rasheeda M.K., Sridevi P., Senthilkumaran B. Cytochrome P450 aromatases: Impact on gonadal development, recrudescence and effect of hCG in the catfish, Clarias gariepinus. Gen. Comp. Endocrinol. 2010, 167:234-245.
6. Sudhakumari C.C., Kobayashi T., Kajiura-Kobayashi H., Wang D.S., Yoshikuni M., Nagahama Y., Senthilkumaran B. Ontogenic expression patterns of several nuclear receptors and cytochrome P450 aromatases in brain and gonads of the Nile tilapia, Oreochromis niloticus suggests their involvement in sex differentiation. Fish Physiol. Biochem. 2005, 31:129-135.
7. Conley A., Hinshelwood M. Mammalian aromatases. Reproduction 2001, 121:685-695.
8. Ijiri S., Kazeto Y., Lokman P.M., Adachi S., 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. 2003, 130:193-203.
9. Chang E.F., Yan Y.L., Guiguen Y., Postlethwait J., Chung B. Two Cyp19 (P450 aromatase) genes on duplicated zebrafish chromosomes are expressed in ovary or brain. Mol. Biol. Evol. 2001, 18:542-550.
10. Kwon J.Y., McAndrew B.J., 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. 2001, 59:359-370.
11. Chang X.T., Kobayashi T., Senthilkumaran B., Kobayashi-Kajura H., Sudhakumari C.C., Nagahama Y. Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen. Comp. Endocrinol. 2005, 141:101-115.
12. Steinke D., Hoegg S., Brinkmann H., Meyer A. Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol. 2006, 4:16.
13. Tchoudakova A., Kishida M., Wood E., Callard G.V. Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. Mol. Biol. 2001, 78:427-439.
14. Kobayashi Y., Kobayashi T., Nakamura M., Sunobe T., Morrey C.E., Suzuki N., Nagahama Y. Characterization of two types of cytochrome p450 aromatase in the serial-sex changing gobiid fish, Trimma okinawae. Zool. Sci. 2004, 21:417-425.
15. Forlano P.M., Deitcher D.L., Myers D.A., Bass A.H. Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J. Neurosci. 2001, 21:8943-8955.
16. Diotel N., Le Page Y., Mouriec K., Tong S.-K., Pellegrini E., Vaillant C., Anglade I., Brion F., Pakdel F., Chung B.-C., Kah O. Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front. Neuroendocrinol. 2010, 31:172-192.
17. Kuo M.-W., Postlethwait J., Lee W.-C., Lou S.-W., Chan W.-K., Chung B.-C. Gene duplication, gene loss and evolution of expression domains in the vertebrate nuclear receptor NR5A (Ftz-F1) family. Biochem. J. 2005, 389:19-26.
18. Nuclear receptors committee: a unified nomenclature system for the nuclear receptor superfamily. Cell 1999, 97:161-163.
19. Morohashi K., Honda S., Inomata Y., Handa H., Omura T. A common trans-acting factor, Ad4-binding protein, to the promoters of steroidogenic P-450s. J. Biol. Chem. 1992, 267:17913-17919.
20. Fayard E., Auwerx J., Schoonjans K. LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol. 2004, 14:250-260.
21. Lala D.S., Rice D.A., Parker K.L. Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I. Mol. Endocrinol. 1992, 6:1249-1258.
22. Watanabe M., Tanaka M., Kobayashi D., Yoshiura Y., Oba Y., Nagahama Y. Medaka (Oryzias latipes) FTZ-F1 potentially regulates the transcription of P-450 aromatase in ovarian follicles: cDNA cloning and functional characterization. Mol. Cell. Endocrinol. 1999, 149:221-228.
23. Kanda H., Okubo T., Omori N., Niihara H., Matsumoto N., Yamada K., Yoshimoto S., Ito M., Yamashita S., Shiba T., Takamatsu N. Transcriptional regulation of the rainbow trout CYP19a gene by FTZ-F1 homologue. J. Steroid Biochem. Mol. Biol. 2006, 99:85-92.
24. Yoshiura Y., Senthilkumaran B., Watanabe M., Oba Y., Kobayashi T., 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. 2003, 68:1545-1553.
25. Kazeto Y., Ijiri S., Place A.R., Zohar Y., Trant J.M. The 5'-flanking regions of CYP19A1 and CYP19A2 in zebrafish. Biochem. Biophys. Res. Commun. 2001, 288:503-508.
26. Pezzi V., Sirianni R., Chimento A., Maggiolini M., Bourguiba S., Delalande C., Carreau S., Ando S., Simpson E.R., Clyne C.D. Differential expression of steroidogenic factor-1/adrenal 4 binding protein and liver receptor homolog-1 (LRH-1)/fetoprotein transcription factor in the rat testis: LRH-1 as a potential regulator of testicular aromatase expression. Endocrinology 2004, 145:2186-2196.
27. Carlone D.L., Richards J.S. Functional interactions, phosphorylation, and levels of 3', 5'-cyclic adenosine monophosphate-regulatory element binding protein and steroidogenic factor-1 mediate hormone-regulated and constitutive expression of aromatase in gonadal cells. Mol. Endocrinol. 1997, 11:292-304.
28. Baron D., Cocquet J., Xia X., Fellous M., Guiguen Y., Veitia R.A. An evolutionary and functional analysis of Foxl2 in rainbow trout gonad differentiation. J. Mol. Endocrinol. 2004, 33:705-715.
29. Wang D.S., Kobayashi T., Zhou L.Y., Paul-Prasanth B., Ijiri S., Sakai F., Okubo K., Morohashi K., Nagahama Y. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1. Mol. Endocrinol. 2007, 21:712-725.
30. Park M., Shin E., Won M., Kim J.H., Go H., Kim H.L., Ko J.J., Lee K., Bae J. FoxL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1-induced CYP17 transcription in granulose cells. Mol. Endocrinol. 2010, 24:1024-1036.
31. Pannetier M., Fabre S., Batista F., Kocer A., Renault L., Jolivet G., Mandon-Pepin B., Cotinot C., Veitia R., Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J. Mol. Endocrinol. 2006, 36:399-413.
32. Fleming N.I., Knower K.C., Lazarus K.A., Fuller P.J., Simpson E.R., Clyne C.D. Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter. PLoS One 2010, 5(12):e14389.
33. Mouriec K., Lareyre J.J., Tong S.K., Le Page Y., Vaillant C., Pellegrini E., Pakdel F., Chung B.C., Kah O., Anglade I. Early regulation of brain aromatase (cyp19a1b) by estrogen receptors during zebrafish development. Dev. Dyn. 2009, 238:2641-2651.
34. Menuet A., Anglade I., Le Guevel R., Pellegrini E., Pakdel F., Kah O. Distribution of aromatase mRNA and protein in the brain and pituitary of female rainbow trout: comparison with estrogen receptor α. J. Comp. Neurol. 2003, 462:180-193.
35. Kobayashi Y., Sunobe T., Kobayashi T., Nagahama Y., Nakamura M. Promoter analysis of two aromatase genes in the serial-sex changing gobiid fish, Trimma okinawae. Fish Physiol. Biochem. 2005, 31:123-127.
36. Anglade I., Pakdel F., Bailhache T., Petit F., Salbert G., Jego P., Valotaire Y., Kah O. Distribution of estrogen receptor-immunoreactive cells in the brain of the rainbow trout (Oncorhynchus mykiss). J. Neuroendocrinol. 1994, 6:573-583.
37. Raghuveer K., Sudhakumari C.C., Senthilkumaran B., Kagawa H., Dutta-Gupta A., Nagahama Y. Gender differences in tryptophan hydroxylase-2 mRNA, serotonin, and 5-hydroxytryptophan levels in the brain of catfish, Clarias gariepinus, during sex differentiation. Gen. Comp. Endocrinol. 2011, 171:94-104.
38. P. Sridevi, B. Senthilkumaran, Cloning and differential expression of FOXL2 during the ovarian development and recrudescence in the catfish, Clarias gariepinus, Gen. Comp. Endocrinol. (2011), doi:. doi:10.1016/j.ygcen.2011.08.015.
39. T method. Nat. Protoc. 2008, 3:1101-1108.
40. Turner F.B., Cheung W.L., Cheung P. Chromatin immunoprecipitation assay for mammalian tissues. Methods in Molecular Biology, Nuclear Reprogramming: Methods and Protocols 2005, Vol. 325:261-272. Humana Press Inc., Totowa, NJ, USA. S. Pells (Ed.).
41. Kazeto Y., Trant J.M. Molecular biology of channel catfish brain cytochrome P450 aromatase (CYP19A2): cloning, preovulatory induction of gene expression, hormonal gene regulation and analysis of promoter region. J. Mol. Endocrinol. 2005, 35:571-583.
42. Parker K.L., Rice D.A., Lala D.S., Ikeda Y., Luo X., Wong M., Bakke M., Zhao L., Frigeri C., Hanley N.A., Stallings N., Schimmer B.P. Steroidogenic Factor 1: an essential mediator of endocrine development. Recent Prog. Horm. Res. 2002, 57:19-36.
43. Ohmuro-Matsuyama Y., Okubo K., Matsuda M., Ijiri S., Wang D., Guan G., Suzuki T., Matsuyama M., Morohashi K.-I., Nagahama Y. Liver receptor homologue-1 (LRH-1) activates the promoter of brain aromatase (cyp19a2) in a teleost fish, the medaka, Oryzias latipes. Mol. Reprod. Dev. 2007, 74:1065-1071.
44. Benayoun B.A., Caburet S., Dipietromaria A., Bailly-Bechet M., Batista F., Fellous M., Vaiman D., Veitia R.A. The identification and characterization of a FOXL2 response element provides insights into the pathogenesis of mutant alleles. Hum. Mol. Genet. 2008, 17:3118-3127.
45. Wang D., Kobayashi T., Zhou L., Nagahama Y. Molecular cloning and gene expression of Foxl2 in the Nile tilapia, Oreochromis niloticus. Biochem. Biophys. Res. Commun. 2004, 320:83-89.
46. Yang W.-H., Gutierrez N.M., Wang L., Ellsworth B.S., Wang C.-M. Synergistic activation of the mc2r promoter by FOXL2 and NR5A1 in mice. Biol. Reprod. 2010, 83:842-851.
47. Menuet A., Pellegrini E., Brion F., Gueguen M.-M., Anglade I., Pakdel F., Kah O. Expression and estrogen-dependent regulation of the zebrafish brain aromatase gene. J. Comp. Neurol. 2005, 485:304-320.
48. Kishida M., 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 2001, 142:740-750.
49. Le Page Y., Menuet A., Kah O., Pakdel F. Characterization of a cis-acting element involved in cell-specific expression of the zebrafish brain aromatase gene. Mol. Reprod. Dev. 2008, 75:1549-1557.
50. Vizziano-Cantonnet D., Anglade I., Pellegrini E., Gueguen M.-M., Fostier A., Guiguen Y., Kah O. Sexual dimorphism in the brain aromatase expression and activity, and in the central expression of other steroidogenic enzymes during the period of sex differentiation in monosex rainbow trout populations. Gen. Comp. Endocrinol. 2011, 170:346-355.