GATA4 is a critical regulator of gonadectomy-induced adrenocortical tumorigenesis in mice

Endocrinology

Volumn 153, Issue 6, 2012, Pages 2599-2611

  Krachulec, Justyna ^a,b   Vetter, Melanie ^a,b   Schrade, Anja ^a,b   Löbs, Ann Kathrin ^a,b   Bielinska, Malgorzata ^a   Cochran, Rebecca ^a   Kyrönlahti, Antti ^a,c   Pihlajoki, Marjut ^a,c   Parviainen, Helka ^c   Jay, Patrick Y ^a   Heikinheimo, Markku ^a,c   Wilson, David B ^a  

^a ST LOUIS CHILDREN S HOSPITAL   (United States)

^b MANNHEIM UNIVERSITY OF APPLIED SCIENCES   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; TRANSCRIPTION FACTOR GATA 4;

ADRENAL CORTEX TUMOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ESTROGEN SYNTHESIS; FEMALE; GENE EXPRESSION PROFILING; GONADECTOMY; HAPLOINSUFFICIENCY; MALE; MOUSE; NONHUMAN; OBESITY; OVARIECTOMY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TUMOR GROWTH;

EID: 84861324100     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-2135     Document Type: Article

References (85)

1. Thompson GB, Young Jr WF 2003 Adrenal incidentaloma. Curr Opin Oncol 15:84-90 (Pubitemid 36135653)
2. Bertherat J, Mosnier-Pudar H, Bertagna X 2002 Adrenal incidentalomas. Curr Opin Oncol 14:58-63 (Pubitemid 34072965)
3. Barlaskar FM, Hammer GD 2007 The molecular genetics of adrenocortical carcinoma. Rev Endocr Metab Disord 8:343-348
4. Volante M, Buttigliero C, Greco E, Berruti A, Papotti M 2008 Pathological and molecular features of adrenocortical carcinoma: an update. J Clin Pathol 61:787-793 (Pubitemid 351969722)
5. Cavlan D, Bharwani N, Grossman A 2010 Androgen- and estrogen-secreting adrenal cancers. Semin Oncol 37:638-648
6. Beuschlein F, Galac S, Wilson DB 2012 Animal models of adrenocortical tumorigenesis. Mol Cell Endocrinol 351:78-86
7. Bielinska M, Kiiveri S, Parviainen H, Mannisto S, Heikinheimo M, Wilson DB 2006 Gonadectomy-induced adrenocortical neoplasia in the domestic ferret (Mustela putorius furo) and laboratory mouse. Vet Pathol 43:97-117
8. Johnsen IK, Slawik M, Shapiro I, Hartmann MF, Wudy SA, Looyenga BD, Hammer GD, Reincke M, Beuschlein F 2006 Gonadectomy in mice of the inbred strain CE/J induces proliferation of subcapsular adrenal cells expressing gonadal marker genes. J Endocrinol 190:47-57 (Pubitemid 44161061)
9. Bernichtein S, Alevizaki M, Huhtaniemi I 2008 Is the adrenal cortex a target for gonadotropins? Trends Endocrinol Metab 19:231-238
10. Bernichtein S, Peltoketo H, Huhtaniemi I 2009 Adrenal hyperplasia and tumours in mice in connection with aberrant pituitary-gonadal function. Mol Cell Endocrinol 300:164-168
11. Bernichtein S, Petretto E, Jamieson S, Goel A, Aitman TJ, Mangion JM, Huhtaniemi IT 2008 Adrenal gland tumorigenesis after gonadectomy in mice is a complex genetic trait driven by epistatic loci. Endocrinology 149:651-661 (Pubitemid 351159319)
12. Bielinska M, Genova E, Boime I, Parviainen H, Kiiveri S, Leppäluoto J, Rahman N, Heikinheimo M, Wilson DB 2005 Gonadotropin- induced adrenocortical neoplasia in NU/J nude mice. Endocrinology 146:3975-3984 (Pubitemid 41175769)
13. Bielinska M, Parviainen H, Porter-Tinge SB, Kiiveri S, Genova E, Rahman N, Huhtaniemi IT, Muglia LJ, Heikinheimo M, Wilson DB 2003 Mouse strain susceptibility to gonadectomy-induced adrenocortical tumor formation correlates with the expression of GATA-4 and luteinizing hormone receptor. Endocrinology 144:4123-4133 (Pubitemid 37088768)
14. Viger RS, Guittot SM, Anttonen M, Wilson DB, Heikinheimo M 2008 Role of the GATA family of transcription factors in endocrine development, function, and disease. Mol Endocrinol 22:781-798 (Pubitemid 351485626)
15. Manuylov NL, Fujiwara Y, Adameyko II, Poulat F, Tevosian SG 2007 The regulation of Sox9 gene expression by the GATA4/FOG2 transcriptional complex in dominant XX sex reversal mouse models. Dev Biol 307:356-367 (Pubitemid 47008917)
16. Manuylov NL, Smagulova FO, Leach L, Tevosian SG 2008 Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 135:3731-3743
17. Tevosian SG, Albrecht KH, Crispino JD, Fujiwara Y, Eicher EM, Orkin SH 2002 Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 129:4627-4634 (Pubitemid 35203743)
18. Bielinska M, Seehra A, Toppari J, Heikinheimo M, Wilson DB 2007 GATA-4 is required for sex steroidogenic cell development in the fetal mouse. Dev Dyn 236:203-213 (Pubitemid 46095092)
19. Bouma GJ, Washburn LL, Albrecht KH, Eicher EM 2007 Correct dosage of Fog2 and Gata4 transcription factors is critical for fetal testis development in mice. Proc Natl Acad Sci USA 104:14994-14999 (Pubitemid 47619581)
20. Kyrönlahti A, Euler R, Bielinska M, Schoeller EL, Moley KH, Toppari J, Heikinheimo M, Wilson DB 2011 GATA4 regulates Sertoli cell function and fertility in adult male mice. Mol Cell Endocrinol 333:85-95
21. Kyrönlahti A, Vetter M, Euler R, Bielinska M, Jay PY, Anttonen M, Heikinheimo M, Wilson DB 2011 GATA4 deficiency impairs ovarian function in adult mice. Biol Reprod 84:1033-1044
22. Manuylov NL, Zhou B, Ma Q, Fox SC, Pu WT, Tevosian SG 2011 Conditional ablation of Gata4 and Fog2 genes in mice reveals their distinct roles in mammalian sexual differentiation. Dev Biol 353:229-241
23. Parviainen H, Kiiveri S, Bielinska M, Rahman N, Huhtaniemi IT, Wilson DB, Heikinheimo M 2007 GATA transcription factors in adrenal development and tumors. Mol Cell Endocrinol 265-266:17-22 (Pubitemid 46273979)
24. Molkentin JD, Lin Q, Duncan SA, Olson EN 1997 Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11:1061-1072 (Pubitemid 27199884)
25. Kuo CT, Morrisey EE, Anadappa R, Sigrist K, Lu MM, Parmacek MS, Soudais C, Leiden JM 1997 GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 11:1048-1060 (Pubitemid 27199883)
26. Narita N, Bielinska M, Wilson D 1997 Cardiomyocyte differentiation by GATA-4-deficient embryonic stem cells. Development 122:3755-3764 (Pubitemid 27482972)
27. Narita N, Bielinska M, Wilson DB 1997 Wild type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev Biol 189:270-274 (Pubitemid 27428368)
28. Watt AJ, Battle MA, Li J, Duncan SA 2004 GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc Natl Acad Sci USA 101:12573-12578 (Pubitemid 39122065)
29. Pu WT, Ishiwata T, Juraszek AL, Ma Q, Izumo S 2004 GATA4 is a dosage-sensitive regulator of cardiac morphogenesis. Dev Biol 275:235-244 (Pubitemid 39298188)
30. Zeisberg EM, Ma Q, Juraszek AL, Moses K, Schwartz RJ, Izumo S, Pu WT 2005 Morphogenesis of the right ventricle requires myocardial expression of Gata4. J Clin Invest 115:1522-1531 (Pubitemid 40814660)
31. Oka T, Maillet M, Watt AJ, Schwartz RJ, Aronow BJ, Duncan SA, Molkentin JD 2006 Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 98:837-845
32. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR 2002 Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat Genet 32:408-410 (Pubitemid 35266116)
33. Jeyasuria P, Ikeda Y, Jamin SP, Zhao L, De Rooij DG, Themmen AP, Behringer RR, Parker KL 2004 Cell-specific knockout of steroidogenic factor 1 reveals its essential roles in gonadal function. Mol Endocrinol 18:1610-1619 (Pubitemid 38859570)
34. Soriano P 1999 Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71 (Pubitemid 29036285)
35. Alexander BM, Van Kirk EA, Naughton LM, Murdoch WJ 2007 Ovarian morphometrics in TP53-deficient mice. Anat Rec (Hoboken) 290:59-64 (Pubitemid 46328084)
36. Beuschlein F, Mutch C, Bavers DL, Ulrich-Lai YM, Engeland WC, Keegan C, Hammer GD 2002 Steroidogenic factor-1 is essential for compensatory adrenal growth following unilateral adrenalectomy. Endocrinology 143:3122-3135 (Pubitemid 34809885)
37. Anttonen M, Ketola I, Parviainen H, Pusa AK, Heikinheimo M 2003 FOG-2 and GATA-4 are coexpressed in the mouse ovary and can modulate Müllerian- inhibiting substance expression. Biol Reprod 68:1333-1340 (Pubitemid 36359122)
38. Fahle M, Palm G 1983 Calculation of surface areas from serial sections. J Neurosci Methods 9:75-85 (Pubitemid 13002634)
39. Woolley GW 1949 The adrenal cortex and its tumors. Ann NY Acad Sci 50:616-626
40. Jay PY, Bielinska M, Erlich JM, Mannisto S, Pu WT, Heikinheimo M, Wilson DB 2007 Impaired mesenchymal cell funciton in Gata4 mutant mice leads to diaphragmatic hernias and primary lung defects. Dev Biol 301:602-614 (Pubitemid 46073982)
41. Pangas SA, Jorgez CJ, Matzuk MM 2004 Growth differentiation factor 9 regulates expression of the bone morphogenetic protein antagonist gremlin. J Biol Chem 279:32281-32286 (Pubitemid 39014678)
42. Ward JM, Anver MR, Mahler JF, Devor-Henneman DE, Maronpot RR, Sundberg JP, Frederickson RM 2002 Pathology of mice commonly used in genetic engineering (C57BL/6; B6,129; and FVB/n). In: Pathology of genetically engineered mice. Ames, IA: Iowa State University Press; 161-179
43. Frith CH, Dunn TB 1994 Tumours of the adrenal gland. IARC Sci Publ 111:595-609
44. Charles MA, Saunders TL, Wood WM, Owens K, Parlow AF, Camper SA, Ridgway EC, Gordon DF 2006 Pituitary-specific Gata2 knockout: effects on gonadotrope and thyrotrope function. Mol Endocrinol 20:1366-1377 (Pubitemid 43801237)
45. Lo A, Zheng W, Gong Y, Crochet JR, Halvorson L 2011 GATA transcription factors regulate luteinizing hormone β (LHβ) gene expression. J Mol Endocrinol 47:45-58
46. Kim JS, Kubota H, Kiuchi Y, Doi K, Saegusa J 1997 Subcapsular cell hyperplasia and mast cell infiltration in the adrenal cortex of mice: comparative study in 7 inbred strains. Exp Anim 46:303-306 (Pubitemid 127446700)
47. Teng CT 2002 Lactoferrin gene expression and regulation: an overview. Biochem Cell Biol 80:7-16 (Pubitemid 34194222)
48. Rossi JA, Bruschi LC 1989 Alteration of the submandibular glands of female mice during pregnancy and lactation. A histological, histometric and histochemical study. Acta Morphol Hung 37:135-145 (Pubitemid 20352387)
49. Freeman ME, Kanyicska B, Lerant A, Nagy G 2000 Prolactin: structure, function, and regulation of secretion. Physiol Rev 80:1523-1631
50. Rulli SB, Kuorelahti A, Karaer O, Pelliniemi LJ, Poutanen M, Huhtaniemi I 2002 Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin. Endocrinology 143:4084-4095 (Pubitemid 35244387)
51. Kero J, Poutanen M, Zhang FP, Rahman N, McNicol AM, Nilson JH, Keri RA, Huhtaniemi IT 2000 Elevated luteinizing hormone induces expression of its receptor and promotes steroidogenesis in the adrenal cortex. J Clin Invest 105:633-641 (Pubitemid 30146510)
52. Kiss R, de Launoit Y, L'Hermite-Balériaux M, L'Hermite M, Paridaens RJ, Danguy AJ, Pasteels JL 1987 Effect of prolactin and estradiol on cell proliferation in the uterus and the MXT mouse mammary neoplasm. J Natl Cancer Inst 78:993-998 (Pubitemid 17093026)
53. Rogers NH, Perfield II JW, Strissel KJ, Obin MS, Greenberg AS 2009 Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 150:2161-2168
54. Kiiveri S, Liu J, Westerholm-Ormio M, Narita N, Wilson DB, Voutilainen R, Heikinheimo M 2002 Differential expression of GATA-4 and GATA-6 in fetal and adult mouse and human adrenal tissue. Endocrinology 143:3136-3143 (Pubitemid 34809886)
55. Bland ML, Jamieson CA, Akana SF, Bornstein SR, Eisenhofer G, Dallman MF, Ingraham HA 2000 Haploinsufficiency of steroidogenic factor-1 in mice disrupts adrenal development leading to an impaired stress response. Proc Natl Acad Sci USA 97:14488-14493 (Pubitemid 32016603)
56. Xu Q, Lin HY, Yeh SD, Yu IC, Wang RS, Chen YT, Zhang C, Altuwaijri S, Chen LM, Chuang KH, Chiang HS, Yeh S, Chang C 2007 Infertility with defective spermatogenesis and steroidogenesis in male mice lacking androgen receptor in Leydig cells. Endocrine 32:96-106 (Pubitemid 350242553)
57. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM 2008 Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 28:248-257
58. Boyer A, Hermo L, Paquet M, Robaire B, Boerboom D 2008 Seminiferous tubule degeneration and infertility in mice with sustained activation of WNT/CTNNB1 signaling in Sertoli cells. Biol Reprod 79:475-485
59. Archambeault DR, Yao HH 2010 Activin A, a product of fetal Leydig cells, is a unique paracrine regulator of Sertoli cell proliferation and fetal testis cord expansion. Proc Natl Acad Sci USA 107:10526-10531
60. Tanwar PS, Kaneko-Tarui T, Zhang L, Rani P, Taketo MM, Teixeira J 2010 Constitutive WNT/β-catenin signaling in murine Sertoli cells disrupts their differentiation and ability to support spermatogenesis. Biol Reprod 82:422-432
61. Ren Y, Cowan RG, Harman RM, Quirk SM 2009 Dominant activation of the hedgehog signaling pathway in the ovary alters theca development and prevents ovulation. Mol Endocrinol 23:711-723
62. Sharawy MM, Liebelt AG, Dirksen TR, Penney DP 1980 Fine structural study of postcastrational adrenocortical carcinomas in female CE-mice. Anat Rec 198:125-133 (Pubitemid 11163109)
63. Hernandez Gifford JA, Hunzicker-Dunn ME, Nilson JH 2009 Conditional deletion of β-catenin mediated by Amhr2cre in mice causes female infertility. Biol Reprod 80:1282-1292
64. Schoemaker NJ, Teerds KJ, Mol JA, Lumeij JT, Thijssen JH, Rijnberk A 2002 The role of luteinizing hormone in the pathogenesis of hyperadrenocorticism in neutered ferrets. Mol Cell Endocrinol 197:117-125 (Pubitemid 35304785)
65. Tevosian SG, Manuylov NL 2008 To β or not to β: Canonical β-catenin signaling pathway and ovarian development. Dev Dyn 237:3672-3680
66. LaVoie HA, Singh D, Hui YY 2004 Concerted regulation of the porcine steroidogenic acute regulatory protein gene promoter activity by follicle-stimulating hormone and insulin-like growth factor I in granulosa cells involves GATA-4 and CCAAT/enhancer binding protein β. Endocrinology 145:3122-3134 (Pubitemid 38829981)
67. Kwintkiewicz J, Cai Z, Stocco C 2007 Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation of Cyp19 expression in rat granulosa cells. Mol Endocrinol 21:933-947 (Pubitemid 46984733)
68. Rahman NA, Kiiveri S, Rivero-Müller A, Levallet J, Vierre S, Kero J, Wilson DB, Heikinheimo M, Huhtaniemi I 2004 Adrenocortical tumorigenesis in transgenic mice expressing the inhibin α-subunit promoter/SV40 virus T-antigen transgene: relationship between ectopic expression of luteinizing hormone receptor and transcription factor GATA-4. Mol Endocrinol 18:2553-2569 (Pubitemid 39335988)
69. Bielinska M, Parviainen H, Kiiveri S, Heikinheimo M, Wilson DB 2009 Origin and molecular pathology of adrenocortical neoplasms. Vet Pathol 46:194-210
70. Berthon A, Sahut-Barnola I, Lambert-Langlais S, de Joussineau C, Damon-Soubeyrand C, Louiset E, Taketo MM, Tissier F, Bertherat J, Lefrançois-Martinez AM, Martinez A, Val P 2010 Constitutive β-catenin activation induces adrenal hyperplasia and promotes adrenal cancer development. Hum Mol Genet 19:1561-1576
71. Zhao L, Bakke M, Hanley NA, Majdic G, Stallings NR, Jeyasuria P, Parker KL 2004 Tissue-specific knockouts of steroidogenic factor 1. Mol Cell Endocrinol 215:89-94 (Pubitemid 38333246)
72. Zubair M, Oka S, Parker KL, Morohashi K 2009 Transgenic expression of Ad4BP/SF-1 in fetal adrenal progenitor cells leads to ectopic adrenal formation. Mol Endocrinol 23:1657-1667
73. Doghman M, Cazareth J, Lalli E 2008 The Tcf/β-catenin antagonist PKF115-584 inhibits proliferation of adrenocortical carcinoma cells. J Clin Endocrinol Metab 93:3222-3225
74. Doghman M, Karpova T, Rodrigues GA, Arhatte M, De Moura J, Cavalli LR, Virolle V, Barbry P, Zambetti GP, Figueiredo BC, Heckert LL, Lalli E 2007 Increased steroidogenic factor-1 dosage triggers adrenocortical cell proliferation and cancer. Mol Endocrinol 21:2968-2987 (Pubitemid 350223508)
75. Tremblay JJ, Viger RS 2003 A mutated form of steroidogenic factor 1 (SF-1 G35E) that causes sex reversal in humans fails to synergize with transcription factor GATA-4. J Biol Chem 278:42637-42642 (Pubitemid 37310537)
76. Pelusi C, Zhao L, Stallings NR, Parker KL 2007 Combined haploinsufficiency of SF-1 and GATA4 does not reveal a genetic interaction in mouse gonadal development. Sex Dev 1:152-160 (Pubitemid 47236997)
77. Meler EN, Scott-Moncrieff JC, Peter AT, Bennett S, Ramos-Vara J, Salisbury SK, Naughton JF 2011 Cyclic estrous-like behavior in a spayed cat associated with excessive sex-hormone production by an adrenocortical carcinoma. J Feline Med Surg 13:473-478
78. Wagner S, Kiupel M, Peterson II RA, Heikinheimo M, Wilson DB 2008 Cytochrome b5 expression in gonadectomy-induced adrenocortical neoplasms of the domestic ferret (Mustela putorius furo). Vet Pathol 45:439-442
79. Peterson II RA, Kiupel M, Bielinska M, Kiiveri S, Heikinheimo M, Capen CC, Wilson DB 2004 Transcription factor GATA-4 is a marker of anaplasia in adrenocortical neoplasms of the domestic ferret (Mustela putorius furo). Vet Pathol 41:446-449 (Pubitemid 39091040)
80. Fidler WJ 1977 Ovarian thecal metaplasia in adrenal glands. Am J Clin Pathol 67:318-323 (Pubitemid 8082643)
81. Wont TW, Warner NE 1971 Ovarian thecal metaplasia in the adrenal gland. Arch Pathol 92:319-328
82. Romberger CF, Wong TW 1989 Thecal metaplasia in the adrenal gland of a man with acquired bilateral testicular atrophy. Arch Pathol Lab Med 113:1071-1075 (Pubitemid 19228106)
83. Kim AC, Barlaskar FM, Heaton JH, Else T, Kelly VR, Krill KT, Scheys JO, Simon DP, Trovato A, Yang WH, Hammer GD 2009 In search of adrenocortical stem and progenitor cells. Endocr Rev 30:241-263
84. Zubair M, Parker KL, Morohashi K 2008 Developmental links between the fetal and adult zones of the adrenal cortex revealed by lineage tracing. Mol Cell Biol 28:7030-7040
85. Val P, Jeays-Ward K, Swain A 2006 Identification of a novel population of adrenal-like cells in the mammalian testis. Dev Biol 299:250-25