Global expression profiling of sex cord stromal tumors from men1 heterozygous mice identifies altered TGF-ß signaling, decreased Gata6 and increased Csf1r expression

International Journal of Cancer

Volumn 124, Issue 5, 2009, Pages 1122-1132

  Mould, Arne W ^a   Duncan, Russell ^a   Serewko Auret, Magdalena ^a   Loffler, Kelly A ^a   Biondi, Christine ^a   Gartside, Michael ^a   Kay, Graham F ^a   Hayward, Nicholas K ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Csf1r; Gata6; Knockout mice; Microarray; Multiple endocrine neoplasia type; Regulation of transcription; TGF

Indexed keywords

COLONY STIMULATING FACTOR RECEPTOR; TRANSCRIPTION FACTOR GATA 6; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN; GATA6 PROTEIN, MOUSE; MEN1 PROTEIN, MOUSE; ONCOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; FEMALE; GENE; GENE EXPRESSION; HETEROZYGOSITY; HYPOPHYSIS TUMOR; MALE; MEN1 GENE; MOUSE; NONHUMAN; OVARY CANCER; PANCREAS TUMOR; PRIORITY JOURNAL; SEX CORD TUMOR; TESTIS CANCER; ANIMAL; C57BL MOUSE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENETICS; IMMUNOHISTOCHEMISTRY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CLUSTER ANALYSIS; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; SEX CORD-GONADAL STROMAL TUMORS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 58749108837     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24057     Document Type: Article

References (75)

1. Chandrasekharappa SC, Guru SC, Manickam P, Olufemi SE, Collins FS, Emmert-Buck MR, Debelenko LV, Zhuang Z, Lubensky IA, Liotta LA, Crabtree JS, Wang Y, et al. Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 1997;276: 404 - 7.
2. Lemmens I, Van de Ven WJ, Kas K, Zhang CX, Giraud S, Wautot V, Buisson N, De Witte K, Salandre J, Lenoir G, Pugeat M, Calender A, et al. Identification of the multiple endocrine neoplasia type 1 (MEN1) gene. The European Consortium on MEN1. Hum Mol Genet 1997;6:1177 - 83.
3. Yang Y, Hua X. In search of tumor suppressing functions of menin. Mol Cell Endocrinol 2007.
4. Ikeo Y, Sakurai A, Hashizume K. Characterization of the MEN1 gene product, menin, by site-specific polyclonal antibodies. Jpn J Cancer Res 1999;90:1088 - 95.
5. Ikeo Y, Sakurai A, Suzuki R, Zhang MX, Koizumi S, Takeuchi Y, Yumita W, Nakayama J, Hashizume K. Proliferation-associated expression of the MEN1 gene as revealed by in situ hybridization: possible role of the menin as a negative regulator of cell proliferation under DNA damage. Lab Invest 2000;80:797 - 804.
6. Kaji H, Canaff L, Goltzman D, Hendy GN. Cell cycle regulation of menin expression. Cancer Res 1999;59:5097 - 101.
7. Ratineau C, Bernard C, Poncet G, Blanc M, Josso C, Fontaniere S, Calender A, Chayvialle JA, Zhang CX, Roche C. Reduction of menin expression enhances cell proliferation and is tumorigenic in intestinal epithelial cells. J Biol Chem 2004;279:24477 - 84.
8. Mould AW, Duncan R, Serewko-Auret M, Loffler KA, Biondi C, Gartside M, Kay GF, Hayward NK. Global expression profiling of murine MEN1-associated tumors reveals a regulatory role for menin in transcription, cell cycle and chromatin remodelling. Int J Cancer 2007;121:776 - 83.
9. Hussein N, Casse H, Fontaniere S, Morera AM, Asensio MJ, Bakeli S, Lu JL, Coste I, Di Clemente N, Bertolino P, Zhang CX. Reconstituted expression of menin in Men1-deficient mouse Leydig tumour cells induces cell cycle arrest and apoptosis. Eur J Cancer 2007; 43:402 - 14.
10. Schnepp RW, Chen YX, Wang H, Cash T, Silva A, Diehl JA, Brown E, Hua X. Mutatin of tumor suppressor gene Men1 acutely enhances proliferation of pancreatic islet cells. Cancer Res 2006;66:5707 - 15.
11. Scacheri PC, Davis S, Odom DT, Crawford GE, Perkins S, Halawi MJ, Agarwal SK, Marx SJ, Spiegel AM, Meltzer PS, Collins FS. Genome- wide analysis of menin binding provides insights into MEN1 tumorigenesis. PLoS Genet 2006;2:e51.
12. Karnik SK, Hughes CM, Gu X, Rozenblatt-Rosen O, McLean GW, Xiong Y, Meyerson M, Kim SK. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Proc Natl Acad Sci USA 2005; 102:14659 - 64.
13. Milne TA, Hughes CM, Lloyd R, Yang Z, Rozenblatt-Rosen O, Dou Y, Schnepp RW, Krankel C, Livolsi VA, Gibbs D, Hua X, Roeder RG, et al. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc Natl Acad Sci USA 2005;102:749 - 54.
14. La P, Schnepp RW, D Petersen C, C Silva A, Hua X. Tumor suppressor menin regulates expression of insulin-like growth factor binding protein 2. Endocrinology 2004;145:3443 - 50.
15. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, Kay GF, Hayward NK, et al. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 2004;13:587 - 97.
16. La P, Yang Y, Karnik SK, Silva AC, Schnepp RW, Kim SK, Hua X. Menin-mediated caspase 8 expression in suppressing multiple endocrine neoplasia type 1. J Biol Chem 2007;282:31332 - 40.
17. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Auferio DJ, Kitabayashi I, Herr W, Cleary ML. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 2004;24:5639 - 49.
18. Bertolino P, Tong WM, Galendo D, Wang ZQ, Zhang CX. Heterozygous Men1 mutant mice develop a range of endocrine tumors mimicking multiple endocrine neoplasia type 1. Mol Endocrinol 2003;17: 1880 - 92.
19. Loffler KA, Biondi CA, Gartside M, Waring P, Stark M, Serewko- Auret MM, Muller HK, Hayward NK, Kay GF. Broad tumor spectrum in a mouse model of multiple endocrine neoplasia type 1. Int J Cancer 2007;120:259 - 67.
20. Hussein N, Lu J, Casse H, Fontaniere S, Morera AM, Guittot SM, Calender A, Di Clemente N, Zhang CX. Deregulation of anti-Mullerian hormone/BMP and transforming growth factor-{beta} pathways in Leydig cell lesions developed in male heterozygous multiple endocrine neoplasia type 1 mutant mice. Endocr Relat Cancer 2008; 15:217 - 27.
21. Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM. Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 2008;28:248 - 57.
22. Sowa H, Kaji H, Kitazawa S, Tsukamoto T, Yano S, Tsukada T, Canaff L, Hendy GN, Sugimoto T, Chihara K. Menin inactivation leads to loss of transforming growth factor beta inhibition of parathyroid cell proliferation and parathyroid hormone secretion. Cancer Res 2004;64:2222 - 8.
23. Biondi C, Gartside M, Tonks I, Paterson C, Hayward NK, Kay GF. Targeting and conditional inactivation of the murine Men1 locus using the Cre recombinase: loxP system. Genesis 2002;32:150 - 1.
24. Imbeaud S, Graudens E, Boulanger V, Barlet X, Zaborski P, Eveno E, Mueller O, Schroeder A, Auffray C. Towards standardization of RNA quality assessment using user-independent classifiers of microcapillary electrophoresis traces. Nucleic Acids Res 2005;33:e56.
25. Bonifer C, Hume DA. The transcriptional regulation of the Colony- Stimulating Factor 1 Receptor (csf1r) gene during hematopoiesis. Front Biosci 2008;13:549 - 60.
26. Mould AW, Greco SA, Cahill MM, Tonks ID, Bellomo D, Patterson C, Zournazi A, Nash A, Scotney P, Hayward NK, Kay GF. Transgenic overexpression of vascular endothelial growth factor-b isoforms by endothelial cells potentiates postnatal vessel growth in vivo and in vitro. Circ Res 2005;97:e60 - e70.
27. Sowa H, Kaji H, Hendy GN, Canaff L, Komori T, Sugimoto T, Chihara K. Menin is required for BMP-2-and TGF-beta -regulated osteoblastic differentiation through interaction with Smads and Runx2. J Biol Chem 2004;279:40267 - 75.
28. Shibanuma M, Mashimo J, Kuroki T, Nose K. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J Biol Chem 1994;269:26767 - 74.
29. Ji Y, Prasad NB, Novotny EA, Kaur S, Elkahloun A, Chen Y, Zhang RZ, Chu ML, Agarwal SK, Marx SJ, Collins FS, Chandrasekharappa SC. Mouse embryo fibroblasts lacking the tumor suppressor menin show altered expression of extracellular matrix protein genes. Mol Cancer Res 2007;5:1041 - 51.
30. Chen YX, Yan J, Keeshan K, Tubbs AT, Wang H, Silva A, Brown EJ, Hess JL, Pear WS, Hua X. The tumor suppressor menin regulates hematopoiesis and myeloid transformation by influencing Hox gene expression. Proc Natl Acad Sci USA 2006;103:1018 - 23.
31. Nikolopoulos SN, Spengler BA, Kisselbach K, Evans AE, Biedler JL, Ross RA. The human non-muscle alpha-actinin protein encoded by the ACTN4 gene suppresses tumorigenicity of human neuroblastoma cells. Oncogene 2000;19:380 - 6.
32. Bai F, Pei XH, Godfrey VL, Xiong Y. Haploinsufficiency of p18(INK4c) sensitizes mice to carcinogen-induced tumorigenesis. Mol Cell Biol 2003;23:1269 - 77.
33. Seoane J, Le HV, Shen L, Anderson SA, Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004;117:211 - 23.
34. Banham AH, Beasley N, Campo E, Fernandez PL, Fidler C, Gatter K, Jones M, Mason DY, Prime JE, Trougouboff P, Wood K, Cordell JL. The FOXP1 winged helix transcription factor is a novel candidate tumorsuppressor gene on chromosome 3p. Cancer Res 2001;61:8820 - 9.
35. Caslini C, Capo-chichi CD, Roland IH, Nicolas E, Yeung AT, Xu XX. Histone modifications silence the GATA transcription factor genes in ovarian cancer. Oncogene 2006;25:5446 - 61.
36. Kamnasaran D, Qian B, Hawkins C, Stanford WL, Guha A. GATA6 is an astrocytoma tumor suppressor gene identified by gene trapping of mouse glioma model. Proc Natl Acad Sci USA 2007;104:8053 - 8.
37. Park K, Kim K, Rho SB, Choi K, Kim D, Oh SH, Park J, Lee SH, Lee JH. Homeobox Msx1 interacts with p53 tumor suppressor and inhibits tumor growth by inducing apoptosis. Cancer Res 2005;65: 749 - 57.
38. Xu LL, Shi Y, Petrovics G, Sun C, Makarem M, Zhang W, Sesterhenn IA, McLeod DG, Sun L, Moul JW, Srivastava S. PMEPA1, an androgen- regulated NEDD4-binding protein, exhibits cell growth inhibitory function and decreased expression during prostate cancer progression. Cancer Res 2003;63:4299 - 304.
39. Wu G, Guo Z, Chang X, Kim MS, Nagpal JK, Liu J, Maki JM, Kivirikko KI, Ethier SP, Trink B, Sidransky D. LOXL1 and LOXL4 are epigenetically silenced and can inhibit ras/extracellular signal-regulated kinase signaling pathway in human bladder cancer. Cancer Res 2007;67:4123 - 9.
40. Yao K, Cho YY, Bergen HR, III, Madden BJ, Choi BY, Ma WY, Bode AM, Dong Z. Nuclear factor of activated T3 is a negative regulator of Ras-JNK1/2-AP-1 induced cell transformation. Cancer Res 2007;67:8725 - 35.
41. Fujiwara Y, Ohata H, Kuroki T, Koyama K, Tsuchiya E, Monden M, Nakamura Y. Isolation of a candidate tumor suppressor gene on chromosome 8p21.3-p22 that is homologous to an extracellular domain of the PDGF receptor beta gene. Oncogene 1995;10:891 - 5.
42. Silverman RH, Halloum A, Zhou A, Dong B, Al-Zoghaibi F, Kushner D, Zhou Q, Zhao J, Wiedmer T, Sims PJ. Suppression of ovarian carcinoma cell growth in vivo by the interferon-inducible plasma membrane protein, phospholipid scramblase 1. Cancer Res 2002;62:397 - 402.
43. Flavell JR, Baumforth KR, Wood VH, Davies GL, Wei W, Reynolds GM, Morgan S, Boyce A, Kelly GL, Young LS, Murray PG. Downregulation of the TGF-beta target gene, PTPRK, by the Epstein-Barr virus encoded EBNA1 contributes to the growth and survival of Hodgkin lymphoma cells. Blood 2008;111:292 - 301.
44. Doumont G, Martoriati A, Beekman C, Bogaerts S, Mee PJ, Bureau F, Colombo E, Alcalay M, Bellefroid E, Marchesi F, Scanziani E, Pelicci PG, et al. G1 checkpoint failure and increased tumor susceptibility in mice lacking the novel p53 target Ptprv. EMBO J 2005; 24:3093 - 103.
45. Liang H, Samanta S, Nagarajan L. SSBP2, a candidate tumor suppressor gene, induces growth arrest and differentiation of myeloid leukemia cells. Oncogene 2005;24:2625 - 34.
46. Ullmannova V, Popescu NC. Expression profile of the tumor suppressor genes DLC-1 and DLC-2 in solid tumors. Int J Oncol 2006;29: 1127 - 32.
47. Ren B, Yee KO, Lawler J, Khosravi-Far R. Regulation of tumor angiogenesis by thrombospondin-1. Biochim Biophys Acta 2006; 1765:178 - 88.
48. Reuter S, Bartelmann M, Vogt M, Geisen C, Napierski I, Kahn T, Delius H, Lichter P, Weitz S, Korn B, Schwarz E. APM-1, a novel human gene, identified by aberrant co-transcription with papillomavirus oncogenes in a cervical carcinoma cell line, encodes a BTB/POZzinc finger protein with growth inhibitory activity. EMBO J 1998; 17:215 - 22.
49. 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 - 98.
50. Cristiano BE, Chan JC, Hannan KM, Lundie NA, Marmy-Conus NJ, Campbell IG, Phillips WA, Robbie M, Hannan RD, Pearson RB. A specific role for AKT3 in the genesis of ovarian cancer through modulation of G(2)-M phase transition. Cancer Res 2006; 66:11718 - 25.
51. Keshava N, Gubba S, Tekmal RR. Overexpression of macrophage colony-stimulating factor (CSF-1) and its receptor, c-fms, in normal ovarian granulosa cells leads to cell proliferation and tumorigenesis. J Soc Gynecol Investig 1999;6:41 - 9.
52. Kawakami T, Kawakami Y, Aaronson SA, Robbins KC. Acquisition of transforming properties by FYN, a normal SRC-related human gene. Proc Natl Acad Sci USA 1988;85:3870 - 4.
53. Rockman SP, Currie SA, Ciavarella M, Vincan E, Dow C, Thomas RJ, Phillips WA. Id2 is a target of the beta-catenin/T cell factor pathway in colon carcinoma. J Biol Chem 2001;276:45113 - 19.
54. Shi LH, Zhu XQ, Zhao GH, Xia YB, Zhang YS. Expression of insulin- like growth factor binding protein-2 in gastric carcinoma and its relationship with cell proliferation. World J Gastroenterol 2006; 12:6285 - 9.
55. ErdoganM, Pozzi A, Bhowmick N, MosesHL, Zent R. Signaling pathways regulating TC21-induced tumorigenesis. J Biol Chem 2007;282:27713 - 20.
56. Wu Y, Denhardt DT, Rittling SR. Osteopontin is required for full expression of the transformed phenotype by the ras oncogene. Br J Cancer 2000;83:156 - 63.
57. Kirma N, Luthra R, Jones J, Liu YG, Nair HB, Mandava U, Tekmal RR. Overexpression of the colony-stimulating factor (CSF-1) and/or its receptor c-fms in mammary glands of transgenic mice results in hyperplasia and tumor formation. Cancer Res 2004;64:4162 - 70.
58. Franklin DS, Godfrey VL, Lee H, Kovalev GI, Schoonhoven R, Chen-Kiang S, Su L, Xiong Y. CDK inhibitors p18INK4c and p27Kip1 mediate two separate pathways to collaboratively suppress pituitary tumorigenesis. Genes Dev 1998;12:2899 - 911.
59. Bai F, Pei XH, Nishikawa T, Smith MD, Xiong Y. p18Ink4c, but not p27Kip1, collaborates with Men1 to suppress neuroendocrine organ tumors. Mol Cell Biol 2007;27:1495 - 504.
60. Kaji H, Canaff L, Lebrun JJ, Goltzman D, Hendy GN. Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type beta signaling. Proc Natl Acad Sci USA 2001;98:3837 - 42.
61. Burns KH, Agno JE, Sicinski P, Matzuk MM. Cyclin D2 and p27 are tissue-specific regulators of tumorigenesis in inhibin alpha knockout mice. Mol Endocrinol 2003;17:2053 - 69.
62. Mali M, Elenius K, Miettinen HM, Jalkanen M. Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J Biol Chem 1993;268:24215 - 22.
63. Abeysinghe HR, Cao Q, Xu J, Pollock S, Veyberman Y, Guckert NL, Keng P, Wang N. THY1 expression is associated with tumor suppression of human ovarian cancer. Cancer Genet Cytogenet 2003;143:125 - 32.
64. Dallas SL, Sivakumar P, Jones CJ, Chen Q, Peters DM, Mosher DF, Humphries MJ, Kielty CM. Fibronectin regulates latent transforming growth factor-beta (TGF beta) by controlling matrix assembly of latent TGF beta-binding protein-1. J Biol Chem 2005;280:18871 - 80.
65. Lee Y, Kawagoe R, Sasai K, Li Y, Russell HR, Curran T, McKinnon PJ. Loss of suppressor-of-fused function promotes tumorigenesis. Oncogene 2007;26:6442 - 7.
66. Xiang Y, Lin G, Zhang Q, Tan Y, Lu G. Knocking down Wnt9a mRNA levels increases cellular proliferation. Mol Biol Rep 2008;35: 73 - 9.
67. Willnow TE, Hammes A, Eaton S. Lipoproteins and their receptors in embryonic development: more than cholesterol clearance. Development 2007;134:3239 - 49.
68. Afouda BA, Ciau-Uitz A, Patient R. GATA4, 5 and 6 mediate TGFbeta maintenance of endodermal gene expression in Xenopus embryos. Development 2005;132:763 - 74.
69. Peterkin T, Gibson A, Patient R. GATA-6 maintains BMP-4 and Nkx2 expression during cardiomyocyte precursor maturation. EMBO J 2003;22:4260 - 73.
70. Katoh M, Katoh M. Conserved POU/OCT- and GATA-binding sites in 5′-flanking promoter region of mammalian WNT8B orthologs. Int J Oncol 2007;30:1273 - 7.
71. Khan SA, Mirsafian M, Howdeshell K, Dorrington JH. Transforming growth factor-beta inhibits DNA synthesis in immature rat Leydig cells in vitro. Mol Cell Endocrinol 1999;148:21 - 8.
72. Lee JS, Yun BY, Kim SS, Cho C, Yoon YD, Cho BN. Changes in reproductive function and white blood cell proliferation induced in mice by injection of a prolactin-expressing plasmid into muscle. Mol Cells 2006;22:189 - 97.
73. Perks CM, Newcomb PV, Grohmann M, Wright RJ, Mason HD, Holly JM. Prolactin acts as a potent survival factor against C2-ceramide- induced apoptosis in human granulosa cells. Hum Reprod 2003;18:2672 - 7.
74. Biondi CA, Gartside MG, Waring P, Loffler KA, Stark MS, Magnuson MA, Kay GF, Hayward NK. Conditional inactivation of the MEN1 gene leads to pancreatic and pituitary tumorigenesis but does not affect normal development of these tissues. Mol Cell Biol 2004; 24:3125 - 31.
75. Sapi E, Flick MB, Rodov S, Carter D, Kacinski BM. Expression of CSF-I and CSF-I receptor by normal lactating mammary epithelial cells. J Soc Gynecol Investig 1998;5:94 - 101.