GATA4 deficiency impairs ovarian function in adult mice

Biology of Reproduction

Volumn 84, Issue 5, 2011, Pages 1033-1044

  Kyrönlahti, Antti ^a,d   Vetter, Melanie ^a,b   Euler, Rosemarie ^a,b   Bielinska, Malgorzata ^a   Jay, Patrick Y ^a   Anttonen, Mikko ^c   Heikinheimo, Markku ^a,d   Wilson, David B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF APPLIED SCIENCES   (Germany)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

Author keywords

Developmental biology; Fertility; Gene regulation; Granulosa cells; Ovary; Ovulation; Puberty; Transcription factor

Indexed keywords

AROMATASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CRE RECOMBINASE; GONADOTROPIN; MESSENGER RNA; PROTEIN; PROTEIN STAR; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DELAYED PUBERTY; DISEASE SEVERITY; ESTROGEN SYNTHESIS; ESTRUS CYCLE; FEMALE; FEMALE SUBFERTILITY; GENE DELETION; GENE EXPRESSION; GENETIC ENGINEERING; GENETIC RECOMBINATION; GRANULOSA CELL; HETEROZYGOTE; HORMONAL REGULATION; LITTER SIZE; LOXP SITE; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY CYST; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; PHENOTYPE; PRIORITY JOURNAL; WILD TYPE;

MUS;

EID: 79956272184     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.086850     Document Type: Article

References (66)

1. Viger RS, Guittot SM, Anttonen M, Wilson DB, Heikinheimo M. Role of the GATA family of transcription factors in endocrine development, function, and disease. Mol Endocrinol 2008; 22:781-798.
2. LaVoie HA. The role of GATA in mammalian reproduction. Exp Biol Med 2003; 228:1282-1290.
3. Tevosian SG, Manuylov NL. To beta or not to beta: canonical beta-catenin signaling pathway and ovarian development. Dev Dyn 2008; 237:3672-3680.
4. 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.
5. LaVoie HA, McCoy GL, Blake CA. Expression of the GATA-4 and GATA-6 transcription factors in the fetal rat gonad and in the ovary during postnatal development and pregnancy. Mol Cell Endocrinol 2004; 227:31-40.
6. McCoard SA, Wise TH, Fahrenkrug SC, Ford JJ. Temporal and spatial localization patterns of Gata4 during porcine gonadogenesis. Biol Reprod 2001; 65:366-374.
7. 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.
8. LaVoie HA, Singh D, Hui YY. Concerted regulation of the porcine steroidogenic acute regulatory protein gene promoter activity by folliclestimulating hormone and insulin-like growth factor I in granulosa cells involves GATA-4 and CCAAT/enhancer binding protein beta. Endocrinology 2004; 145:3122-3134.
9. Kwintkiewicz J, Cai Z, Stocco C. Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation of Cyp19 expression in rat granulosa cells. Mol Endocrinol 2007; 21:933-947.
10. Balla A, Danilovich N, Yang Y, Sairam MR. Dynamics of ovarian development in the FORKO immature mouse: structural and functional implications for ovarian reserve. Biol Reprod 2003; 69:1281-1293.
11. Vaskivuo TE, Aittomaki K, Anttonen M, Ruokonen A, Herva R, Osawa Y, Heikinheimo M, Huhtaniemi I, Tapanainen JS. Effects of folliclestimulating hormone (FSH) and human chorionic gonadotropin in individuals with an inactivating mutation of the FSH receptor. Fertil Steril 2002; 78:108-113.
12. Hiroi H, Christenson LK, Strauss JF III. Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Mol Cell Endocrinol 2004; 215:119-126.
13. Hui YY, Lavoie HA. GATA4 reduction enhances 30,50-cyclic adenosine 50-monophosphate-stimulated steroidogenic acute regulatory protein messenger ribonucleic acid and progesterone production in luteinized porcine granulosa cells. Endocrinology 2008; 149:5557-5567.
14. Sher N, Yivgi-Ohana N, Orly J. Transcriptional regulation of the cholesterol side chain cleavage cytochrome P450 gene (CYP11A1) revisited: binding of GATA, cyclic adenosine 30,50-monophosphate response element-binding protein and activating protein (AP)-1 proteins to a distal novel cluster of cis-regulatory elements potentiates AP-2 and steroidogenic factor-1-dependent gene expression in the rodent placenta and ovary. Mol Endocrinol 2007; 21:948-962.
15. Tremblay JJ, Viger RS. GATA factors differentially activate multiple gonadal promoters through conserved GATA regulatory elements. Endocrinology 2001; 142:977-986.
16. Bouchard MF, Taniguchi H, Viger RS. Protein kinase A-dependent synergism between GATA factors and the nuclear receptor, liver receptor homolog-1, regulates human aromatase (CYP19) PII promoter activity in breast cancer cells. Endocrinology 2005; 146:4905-4916.
17. Stocco C. In vivo and in vitro inhibition of cyp19 gene expression by prostaglandin F2a in murine luteal cells: implication of GATA-4. Endocrinology 2004; 145:4957-4966.
18. Stocco C, Kwintkiewicz J, Cai Z. Identification of regulatory elements in the Cyp19 proximal promoter in rat luteal cells. J Mol Endocrinol 2007; 39:211-221.
19. Manuylov NL, Smagulova FO, Leach L, Tevosian SG. Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 2008; 135:3731-3743.
20. Vainio S, Heikkila M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signaling. Nature 1999; 397:405-409.
21. Uhlenhaut NH, Treier M. Foxl2 function in ovarian development. Mol Genet Metab 2006; 88:225-234.
22. Tevosian SG, Albrecht KH, Crispino JD, Fujiwara Y, Eicher EM, Orkin 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.
23. Kuo CT, Morrisey EE, Anadappa 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.
24. 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.
25. Narita N, Bielinska M, Wilson D. Cardiomyocyte differentiation by GATA-4 deficient embryonic stem cells. Devel. 1997; 122:3755-3764.
26. Narita N, Bielinska M, Wilson DB. Wild-type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev Biol 1997; 189:270-274.
27. Watt AJ, Battle MA, Li J, Duncan SA. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc Natl Acad Sci U S A 2004; 101:12573-12578.
28. Thurisch B, Liang S, Sarioglu N, Schomburg L, Bungert J, Dame C. Transgenic mice expressing small interfering RNA against Gata4 point to a crucial role of Gata4 in the heart and gonads. J Mol Endocrinol 2009; 43: 157-169.
29. Pu WT, Ishiwata T, Juraszek AL, Ma Q, Izumo S. GATA4 is a dosagesensitive regulator of cardiac morphogenesis. Dev Biol 2004; 275:235-244.
30. Zeisberg EM, Ma Q, Juraszek AL, Moses K, Schwartz RJ, Izumo S, Pu WT. Morphogenesis of the right ventricle requires myocardial expression of Gata4. J Clin Invest 2005; 115:1522-1531.
31. Oka T, Maillet M, Watt AJ, Schwartz RJ, Aronow BJ, Duncan SA, Molkentin JD. Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 2006; 98: 837-845.
32. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. Requirement of Bmpr1a for mullerian duct regression during male sexual development. Nat Genet 2002; 32:408-410.
33. Jeyasuria P, Ikeda Y, Jamin SP, Zhao L, de Rooij DG, Themmen AP, Behringer RR, Parker KL. Cell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol 2004; 18: 1610-1619.
34. Friedrich G, Soriano P. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev 1991; 5:1513-1523.
35. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology. Biol Reprod 1982; 27:327-339.
36. Jay PY, Bielinska M, Erlich JM, Mannisto S, Pu WT, Heikinheimo M, Wilson DB. Impaired mesenchymal cell funciton in Gata4 mutant mice leads to diaphragmatic hernias and primary lung defects. Dev Biol 2007; 301:602-614.
37. Bielinska M, Jay PY, Erlich JM, Mannisto S, Urban Z, Heikinheimo M, Wilson DB. Molecular genetics of congenital diaphragmatic defects. Ann Med 2007; 39:261-274.
38. Rajagopal SK, Ma Q, Obler D, Shen J, Manichaikul A, Tomita-Mitchell A, Boardman K, Briggs C, Garg V, Srivastava D, Goldmuntz E, Broman KW, et al. Spectrum of heart disease associated with murine and human GATA4 mutation. J Mol Cell Cardiol 2007; 43:677-685.
39. Morita Y, Perez GI, Maravei DV, Tilly KI, Tilly JL. Targeted expression of Bcl-2 in mouse oocytes inhibits ovarian follicle atresia and prevents spontaneous and chemotherapy-induced oocyte apoptosis in vitro. Mol Endocrinol 1999; 13:841-850.
40. Tilly JL. Ovarian follicle counts-not as simple as 1, 2, 3. Reprod Biol Endocrinol 2003; 1:11-15.
41. Hogan B, Beddington R, Costantini F, Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press; 1994.
42. Kyronlahti A, Ramo M, Tamminen M, Unkila-Kallio L, Butzow R, Leminen A, Nemer M, Rahman N, Huhtaniemi I, Heikinheimo M, Anttonen M. GATA-4 regulates Bcl-2 expression in ovarian granulosa cell tumors. Endocrinology 2008; 149:5635-5642.
43. Kevenaar ME, Meerasahib MF, Kramer P, van de Lang-Born BM, de Jong FH, Groome NP, Themmen AP, Visser JA. Serum anti-mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology 2006; 147:3228-3234.
44. Nelson JF, Karelus K, Felicio LS, Johnson TE. Genetic influences on the timing of puberty in mice. Biol Reprod 1990; 42:649-655.
45. Pelusi C, Zhao L, Stallings NR, Parker KL. Combined haploinsufficiency of SF-1 and GATA4 does not reveal a genetic interaction in mouse gonadal development. Sex Dev 2007; 1:152-160.
46. Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci U S A 1998; 95:6965-6970.
47. Britt KL, Drummond AE, Cox VA, Dyson M, Wreford NG, Jones ME, Simpson ER, Findlay JK. An age-related ovarian phenotype in mice with targeted disruption of the Cyp19 (aromatase) gene. Endocrinology 2000; 141:2614-2623.
48. Toda K, Takeda K, Okada T, Akira S, Saibara T, Kaname T, Yamamura K, Onishi S, Shizuta Y. Targeted disruption of the aromatase P450 gene (Cyp19) in mice and their ovarian and uterine responses to 17betaestradiol. J Endocrinol 2001; 170:99-111.
49. Deutscher E, Hung-Chang Yao H. Essential roles of mesenchyme-derived beta-catenin in mouse mullerian duct morphogenesis. Dev Biol 2007; 307: 227-236.
50. Gonzalez G, Behringer RR. Dicer is required for female reproductive tract development and fertility in the mouse. Mol Reprod Dev 2009; 76:678-688.
51. Orvis GD, Jamin SP, Kwan KM, Mishina Y, Kaartinen VM, Huang S, Roberts AB, Umans L, Huylebroeck D, Zwijsen A, Wang D, Martin JF, et al. Functional redundancy of TGF-beta family type I receptors and receptor-Smads in mediating anti-mullerian hormone-induced mullerian duct regression in the mouse. Biol Reprod 2008; 78:994-1001.
52. Hernandez Gifford JA, Hunzicker-Dunn ME, Nilson JH. Conditional deletion of beta-catenin mediated by Amhr2cre in mice causes female infertility. Biol Reprod 2009; 80:1282-1292.
53. Petit FG, Jamin SP, Kurihara I, Behringer RR, DeMayo FJ, Tsai MJ, Tsai SY. Deletion of the orphan nuclear receptor COUP-TFII in uterus leads to placental deficiency. Proc Natl Acad Sci U S A 2007; 104:6293-6298.
54. Fan HY, Shimada M, Liu Z, Cahill N, Noma N, Wu Y, Gossen J, Richards JS. Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development 2008; 135:2127-2137.
55. Duggavathi R, Volle DH, Mataki C, Antal MC, Messaddeq N, Auwerx J, Murphy BD, Schoonjans K. Liver receptor homolog 1 is essential for ovulation. Genes Dev 2008; 22:1871-1876.
56. Ren Y, Cowan RG, Harman RM, Quirk SM. Dominant activation of the hedgehog signaling pathway in the ovary alters theca development and prevents ovulation. Mol Endocrinol 2009; 23:711-723.
57. Boyer A, Lapointe E, Zheng X, Cowan RG, Li H, Quirk SM, Demayo FJ, Richards JS, Boerboom D. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J 2010; 24:3010-3025.
58. Pelusi C, Ikeda Y, Zubair M, Parker KL. Impaired follicle development and infertility in female mice lacking steroidogenic factor 1 in ovarian granulosa cells. Biol Reprod 2008; 79:1074-1083.
59. Anttonen M, Ketola I, Parviainen H, Pusa AK, Heikinheimo M. FOG-2 and GATA-4 are coexpressed in the mouse ovary and can modulate mullerian-inhibiting substance expression. Biol Reprod 2003; 68:1333-1340.
60. 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.
61. van Houten EL, Themmen AP, Visser JA. Anti-mullerian hormone (AMH): regulator and marker of ovarian function. Ann Endocrinol (Paris) 2010; 71:191-197.
62. Gruijters MJ, Visser JA, Durlinger AL, Themmen AP. Anti-mullerian hormone and its role in ovarian function. Mol Cell Endocrinol 2003; 211: 85-90.
63. Weenen C, Laven JS, Von Bergh AR, Cranfield M, Groome NP, Visser JA, Kramer P, Fauser BC, Themmen AP. Anti-mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod 2004; 10:77-83.
64. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JT, Grootegoed JA, Themmen AP. Anti-mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002; 143:1076-1084.
65. Jorgez CJ, Klysik M, Jamin SP, Behringer RR, Matzuk MM. Granulosa cell-specific inactivation of follistatin causes female fertility defects. Mol Endocrinol 2004; 18:953-967.
66. Kyronlahti A, Euler R, Bielinska M, Schoeller EL, Moley KH, Toppari J, Heikinheimo M, Wilson DB. GATA4 regulates Sertoli cell function and fertility in adult male mice. Mol Cell Endocrinol 2011; 333:85-95.