FOG-2 and GATA-4 are coexpressed in the mouse ovary and can modulate Müllerian-inhibiting substance expression

Biology of Reproduction

Volumn 68, Issue 4, 2003, Pages 1333-1340

  Anttonen, Mikko ^a   Ketola, Ilkka ^a   Parviainen, Helka ^a   Pusa, Anna Kaisa ^a   Heikinheimo, Markku ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Developmental biology; Early development; Female reproductive tract; Gene regulation; Ovary

Indexed keywords

MUELLERIAN INHIBITING FACTOR; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOG 2; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FETUS; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GRANULOSA CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; NEWBORN; NONHUMAN; NORTHERN BLOTTING; OVARY; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SERTOLI CELL; TESTIS; TRANSACTIVATION;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DNA-BINDING PROTEINS; DOWN-REGULATION; FEMALE; FETUS; GATA4 TRANSCRIPTION FACTOR; GENITALIA; GLYCOPROTEINS; MALE; MICE; OVARY; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; TESTICULAR HORMONES; TESTIS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 0037377936     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.008599     Document Type: Article

References (50)

1. Swain A, Lovell-Badge R. Mammalian sex determination: a molecular drama. Genes Dev 1999; 13:755-767.
2. Capel B. The battle of the sexes. Mech Dev 2000; 92:89-103.
3. Koopman P, Munsterberg A, Capel B, Vivian N, Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 1990; 348:450-452.
4. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991; 351:117-121.
5. Richards JS. Perspective: the ovarian follicle - a perspective in 2001. Endocrinology 2001; 142:2184-2193.
6. Orkin SH. GATA-binding transcription factors in hematopoietic cells. Blood 1992; 80:575-581.
7. Molkentin JD. The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-spesific gene expression. J Biol Chem 2000; 275:38949-38952.
8. Molkentin JD, Lin Q, Duncan SA, Olson EN. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 1997; 11:1061-1072.
9. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, Parmacek MS, Soudais C, Leiden JM. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 1997; 11:1048-1060.
10. Ito E, Toki T, Ishihara H, Ohtani H, Gu L, Yokoyama M, Engel JD, Yamamoto M. Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis. Nature 1993; 362:466-468.
11. Siggers P, Smith L, Greenfield A. Sexually dimorphic expression of GATA-2 during mouse gonad development. Mech Dev 2002; 111: 159-162.
12. Heikinheimo M, Ermolaeva M, Bielinska M, Rahman NA, Narita N, Huhtaniemi IT, Tapanainen JS, Wilson DB. Expression and hormonal regulation of transcription factors GATA-4 and GATA-6 in the mouse ovary. Endocrinology 1997; 138:3505-3514.
13. Laitinen MP, Anttonen M, Ketola I, Wilson DB, Ritvos O, Butzow R, Heikinheimo M. Transcription factors GATA-4 and GATA-6 and a GATA family cofactor, FOG-2, are expressed in human ovary and sex cord-derived ovarian tumors. J Clin Endocrinol Metab 2000; 85:3476-3483.
14. Ketola I, Rahman N, Toppari J, Bielinska M, Porter-Tinge SB, Tapanainen JS, Huhtaniemi IT, Wilson DB, Heikinheimo M. Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 1999; 140:1470-1480.
15. Ketola I, Pentikainen V, Vaskivuo T, Ilvesmaki V, Herva R, Dunkel L, Tapanainen JS, Toppari J, Heikinheimo M. Expression of transcription factor GATA-4 during human testicular development and disease. J Clin Endocrinol Metab 2000; 85:3925-3931.
16. Viger RS, Mertineit C, Trasler JM, Nemer M. Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Mullerian inhibiting substance promoter. Development 1998; 125:2665-2675.
17. Tremblay JJ, Viger RS. Transcription factor GATA-4 enhances Mullerian inhibiting substance gene transcription through a direct interaction with the nuclear receptor SF-1. Mol Endocrinol 1999; 13:1388-1401.
18. Watanabe K, Clarke TR, Lane AH, Wang X, Donahoe PK. Endogenous expression of Mullerian inhibiting substance in early postnatal rat Sertoli cells requires multiple steroidogenic factor-1 and GATA-4-binding sites. Proc Natl Acad Sci U S A 2000; 97:1624-1629.
19. Feng ZM, Wu AZ, Zhang Z, Chen CL. GATA-1 and GATA-4 transactivate inhibin/activin beta-B-subunit gene transcription in testicular cells. Mol Endocrinol 2000; 14:1820-1835.
20. Tremblay JJ, Viger RS. GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 2001; 142:977-986.
21. Silverman E, Eimerl S, Orly J. CCAAT enhancer-binding protein beta and GATA-4 binding regions within the promoter of the steroidogenic acute regulatory protein (StAR) gene are required for transcription in rat ovarian cells. J Biol Chem 1999; 274:17987-17996.
22. Jin T, Zhang X, Li H, Goss PE. Characterization of a novel silencer element in the human aromatase gene PII promoter. Breast Cancer Res Treat 2000; 62:151-159.
23. Tsang AP, Visvader JE, Turner CA, Fujiwara Y, Yu C, Weiss MJ, Crossley M, Orkin SH. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 1997; 90:109-119.
24. Tevosian SG, Deconinck AE, Cantor AB, Rieff HI, Fujiwara Y, Corfas G, Orkin SH. FOG-2: a novel GATA-family cofactor related to multitype zinc-finger proteins Friend of GATA-1 and U-shaped. Proc Natl Acad Sci U S A 1999; 96:950-955.
25. Svensson EC, Tufts RL, Polk CE, Leiden JM. Molecular cloning of FOG-2: a modulator of transcription factor GATA-4 in cardiomyocytes. Proc Natl Acad Sci U S A 1999; 96:956-961.
26. Lu JR, McKinsey TA, Xu H, Wang DZ, Richardson JA, Olson EN. FOG-2, a heart- and brain-enriched cofactor for GATA transcription factors. Mol Cell Biol 1999; 19:4495-4502.
27. Svensson EC, Huggins GS, Dardik FB, Polk CE, Leiden JM. A functionally conserved N-terminal domain of the Friend of GATA-2 (FOG-2) protein represses GATA-4-dependent transcription. J Biol Chem 2000; 275:20762-20769.
28. Svensson EC, Huggins GS, Lin H, Clendenin C, Jiang F, Tufts R, Dardik FB, Leiden JM. A syndrome of tricuspid atresia in mice with a targeted mutation of the gene encoding FOG-2. Nat Genet 2000; 25:353-356.
29. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell 2000; 101:729-739.
30. Crispino JD, Lodish MB, Thurberg BL, Litovsky SH, Collins T, Molkentin JD, Orkin SH. Proper coronary vascular development and heart morphogenesis depend on interaction of GATA-4 with FOG cofactors. Genes Dev 2001; 15:839-844.
31. Vaskivuo TE, Anttonen M, Herva R, Billig H, Dorland M, te Velde ER, Stenback F, Heikinheimo M, Tapanainen JS. Survival of human ovarian follicles from fetal to adult life: apoptosis, apoptosis-related proteins, and transcription factor GATA-4. J Clin Endocrinol Metab 2001; 86:3421-3429.
32. McCoard SA, Wise TH, Fahrenkrug SC, Ford JJ. Temporal and spatial localization patterns of GATA4 during porcine gonadogenesis. Biol Reprod 2001; 65:366-374.
33. Tremblay JJ, Robert NM, Viger RS. Modulation of endogenous GATA-4 activity reveals its dual contribution to Mullerian inhibiting substance gene transcription in Sertoli cells. Mol Endocrinol 2001; 15:1636-1650.
34. Ketola I, Anttonen M, Vaskivuo T, Tapanainen JS, Toppari J, Heikinheimo M. Developmental expression and spermatogenic stage specificity of transcription factors GATA-1 and GATA-4 and their cofactors FOG-1 and FOG-2 in the mouse testis. Eur J Endocrinol 2002; 147: 397-406.
35. Cormand B, Avela K, Pihko H, Santavuori P, Talim B, Topaloglu H, de la Chapelle A, Lehesjoki AE. Assignment of the muscle-eye-brain disease gene to 1p32-p34 by linkage analysis and homozygosity mapping. Am J Hum Genet 1999; 64:126-135.
36. Ikeda Y, Swain A, Weber TJ, Hentges KE, Zanaria E, Lalli E, Tamai KT, Sassone-Corsi P, Lovell-Badge R, Camerino G, Parker KL. Steroidogenic factor 1 and Dax-1 colocalize in multiple cell lineages: potential links in endocrine development. Mol Endocrinol 1996; 10: 1261-1272.
37. Arceci RJ, King AA, Simon MC, Orkin SH, Wilson DB. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol 1993; 13:2235-2246.
38. Martelin E, Palvimo JJ, Lapatto R, Raivio KO. Nuclear factor Y activates the human xanthine oxidoreductase gene promoter. FEBS Lett 2000; 480:84-88.
39. Kananen K, Markkula M, Rainio E, Su JG, Hsueh AJ, Huhtaniemi IT. Gonadal tumorigenesis in transgenic mice bearing the mouse inhibin alpha-subunit promoter/simian virus T-antigen fusion gene: characterization of ovarian tumors and establishment of gonadotropin-responsive granulosa cell lines. Mol Endocrinol 1995; 9:616-627.
40. Levallet J, Koskimies P, Rahman N, Huhtaniemi I. The promoter of murine follicle-stimulating hormone receptor: functional characterization and regulation by transcription factor steroidogenic factor 1. Mol Endocrinol 2001; 15:80-92.
41. Giuili G, Shen WH, Ingraham HA. The nuclear receptor SF-1 mediates sexually dimorphic expression of Mullerian inhibiting substance, in vivo. Development 1997; 124:1799-1807.
42. Clarkson MJ, Harley VR. Sex with two SOX on: SRY and SOX9 in testis development. Trends Endocrinol Metab 2002;13:106-111.
43. Arango NA, Lovell-Badge R, Behringer RR. Targeted mutagenesis of the endogenous mouse MIS gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 1999; 99:409-419.
44. Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. SOX9 induces testis development in XX transgenic mice. Nat Genet 2001; 28:215-217.
45. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 1998; 18: 6653-6665.
46. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R. SOX9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 1996; 14:62-68.
47. Ikeda Y. Shen WH, Ingraham HA, Parker KL. Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 1994; 8:654-662.
48. Munsterberg A, Lovell-Badge R. Expression of the mouse anti-Mullerian hormone gene suggests a role in both male and female sexual differentiation. Development 1991; 113:613-624.
49. Zhang Z, Wu AZ, Feng ZM, Mruk D, Cheng CY, Chen CL. Gonadotropins, via cAMP, negatively regulate GATA-1 gene expression in testicular cells. Endocrinology 2002; 143:829-836.
50. Tevosian SG, Albrecht KH, Crispino JD, Fujiwara Y, Eicher EM, Drkin SH. Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 2002; 129:4627-4634.