ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers

Cancer Research

Volumn 71, Issue 21, 2011, Pages 6718-6727

  Guan, Bin ^a   Wang, Tian Li ^a   Shih, Ie Ming ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRG1 PROTEIN; PROTEIN ARID1A; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARID1A GENE; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CARCINOGENICITY; CDKN1A GENE; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GYNECOLOGIC CANCER; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; SMAD3 GENE; TP53 GENE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; WILD TYPE;

ADENOCARCINOMA, CLEAR CELL; ANIMALS; CELL LINE, TUMOR; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA HELICASES; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC COMPLEMENTATION TEST; HUMANS; MICE; MICE, NUDE; MULTIPROTEIN COMPLEXES; MUTATION; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; OVARIAN NEOPLASMS; P21-ACTIVATED KINASES; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; SMAD3 PROTEIN; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 80155131218     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-1562     Document Type: Article

References (52)

1. Liu H, Mulholland N, Fu H, Zhao K. Cooperative activity of BRG1 and Z-DNA formation in chromatin remodeling. Mol Cell Biol 2006;26:2550-9.
2. Nie Z, Xue Y, Yang D, Zhou S, Deroo BJ, Archer TK, et al. A specificity and targeting subunit of a human SWI/SNF family-related chromatinremodeling complex. Mol Cell Biol 2000;20:8879-88. (Pubitemid 32248734)
3. Wang W, Cote J, Xue Y, Zhou S, Khavari PA, Biggar SR, et al. Purification and biochemical heterogeneity of the mammalian SWISNF complex. EMBO J 1996;15:5370-82. (Pubitemid 26336219)
4. Shih Ie M, Sheu JJ, Santillan A, Nakayama K, Yen MJ, Bristow RE, et al. Amplification of a chromatin remodeling gene, Rsf-1/HBXAP, in ovarian carcinoma. Proc Natl Acad Sci U S A 2005;102:14004-9. (Pubitemid 41377693)
5. Choi JH, Sheu JJ, Guan B, Jinawath N, Markowski P, Wang TL, et al. Functional analysis of 11q13.5 amplicon identifies Rsf-1 (HBXAP) as a gene involved in paclitaxel resistance in ovarian cancer. Cancer Res 2009;69:1407-15.
6. Sheu JJ, Choi JH, Yildiz I, Tsai FJ, Shaul Y, Wang TL, et al. The roles of human sucrose nonfermenting protein 2 homologue in the tumorpromoting functions of Rsf-1. Cancer Res 2008;68:4050-7.
7. Sheu JJ, Guan B, Choi JH, Lin A, Lee CH, Hsiao YT, et al. Rsf-1, a chromatin remodeling protein, induces DNA damage and promotes genomic instability. J Biol Chem 2010;285:38260-9.
8. Fang FM, Li CF, Huang HY, Lai MT, Chen CM, Chiu IW, et al. Overexpression of a chromatin remodeling factor, Rsf-1/HBXAP, correlates with aggressive oral squamous cell carcinoma. Am J Pathol 2011;178:2407-15.
9. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011;469:539-42.
10. Medina PP, Romero OA, Kohno T, Montuenga LM, Pio R, Yokota J, et al. Frequent BRG1/SMARCA4-inactivating mutations in human lung cancer cell lines. Hum Mutat 2008;29:617-22. (Pubitemid 351614585)
11. Rodriguez-Nieto S, Cañada A, Pros E, Pinto AI, Torres-Lanzas J, Lopez-Rios F, et al. Massive parallel DNA pyrosequencing analysis of the tumor suppressor BRG1/SMARCA4 in lung primary tumors. Hum Mutat 2010;32:E1999-2017
12. Jones S, Wang TL, Shih IM, Mao TL, Nakayama K, Roden R, et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 2010;330:228-31.
13. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T, et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 2010;363:1532-43.
14. Guan B, Mao TL, Panuganti PK, Kuhn E, Kurman RJ, Maeda D, et al. Mutation and loss of expression of ARID1A in uterine low-grade endometrioid carcinoma. Am J Surg Pathol 2011;35:625-32.
15. Hurlstone AF, Olave IA, Barker N, van Noort M, Clevers H. Cloning and characterization of hELD/OSA1, a novel BRG1 interacting protein. Biochem J 2002;364:255-64. (Pubitemid 34538969)
16. Van Rechem C, Boulay G, Leprince D. HIC1 interacts with a specific subunit of SWI/SNF complexes, ARID1A/BAF250A. Biochem Biophys Res Commun 2009;385:586-90.
17. Ho L, Crabtree GR. Chromatin remodelling during development. Nature 2010;463:474-84.
18. Reisman D, Glaros S, Thompson EA. The SWI/SNF complex and cancer. Oncogene 2009;28:1653-68.
19. Gao X, Tate P, Hu P, Tjian R, Skarnes WC, Wang Z. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci U S A 2008;105:6656-61. (Pubitemid 351754562)
20. Krosl J, Mamo A, Chagraoui J, Wilhelm BT, Girard S, Louis I, et al. A mutant allele of the Swi/Snf member BAF250a determines the pool size of fetal liver hemopoietic stem cell populations. Blood 2010;116:1678-84.
21. Alessio N, Squillaro T, Cipollaro M, Bagella L, Giordano A, Galderisi U. The BRG1 ATPase of chromatin remodeling complexes is involved in modulation of mesenchymal stem cell senescence through RB-P53 pathways. Oncogene 2010;29:5452-63.
22. Dallas PB, Pacchione S, Wilsker D, Bowrin V, Kobayashi R, Moran E. The human SWI-SNF complex protein p270 is an ARID family member with non-sequence-specific DNA binding activity. Mol Cell Biol 2000;20:3137-46. (Pubitemid 30215026)
23. Wilsker D, Patsialou A, Zumbrun SD, Kim S, Chen Y, Dallas PB, et al. The DNA-binding properties of the ARID-containing subunits of yeast and mammalian SWI/SNF complexes. Nucleic Acids Res 2004; 32:1345-53. (Pubitemid 38864679)
24. Wang X, Nagl NG, Wilsker D, Van Scoy M, Pacchione S, Yaciuk P, et al. Two related ARID family proteins are alternative subunits of human SWI/SNF complexes. Biochem J 2004;383:319-25. (Pubitemid 39446693)
25. Inoue H, Furukawa T, Giannakopoulos S, Zhou S, King DS, Tanese N. Largest subunits of the human SWI/SNF chromatin-remodeling complex promote transcriptional activation by steroid hormone receptors. J Biol Chem 2002;277:41674-85. (Pubitemid 35257474)
26. Sastry L, Johnson T, Hobson MJ, Smucker B, Cornetta K. Titering lentiviral vectors: comparison of DNA, RNA and marker expression methods. Gene Ther 2002;9:1155-62. (Pubitemid 34993938)
27. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993;75:817-25. (Pubitemid 23346378)
28. Lee HJ, Lee JK, Miyake S, Kim SJ. A novel E1A-like inhibitor of differentiation (EID) family member, EID-2, suppresses transforming growth factor (TGF)-beta signaling by blocking TGF-beta-induced formation of Smad3-Smad4 complexes. J Biol Chem 2004;279: 2666-72. (Pubitemid 38114254)
29. Nitta M, Katabuchi H, Ohtake H, Tashiro H, Yamaizumi M, Okamura H. Characterization and tumorigenicity of human ovarian surface epithelial cells immortalized by SV40 large T antigen. Gynecol Oncol 2001;81:10-7. (Pubitemid 32368071)
30. Choi JH, Choi KC, Auersperg N, Leung PC. Overexpression of folliclestimulating hormone receptor activates oncogenic pathways in preneoplastic ovarian surface epithelial cells. J Clin Endocrinol Metab 2004;89:5508-16. (Pubitemid 39518434)
31. Gorai I, Nakazawa T, Miyagi E, Hirahara F, Nagashima Y, Minaguchi H. Establishment and characterization of two human ovarian clear cell adenocarcinoma lines from metastatic lesions with different properties. Gynecol Oncol 1995;57:33-46.
32. Maeda D, Mao TL, Fukayama M, Nakagawa S, Yano T, Taketani Y, et al. Clinicopathological significance of loss of ARID1A Immunoreactivity in ovarian clear cell carcinoma. Int J Mol Sci 2010;11:5120-8.
33. Wu R, Hendrix-Lucas N, Kuick R, Zhai Y, Schwartz DR, Akyol A, et al. Mouse model of human ovarian endometrioid adenocarcinoma based on somatic defects in the Wnt/beta-catenin and PI3K/Pten signaling pathways. Cancer Cell 2007;11:321-33. (Pubitemid 46518315)
34. Oh J, Sohn DH, Ko M, Chung H, Jeon SH, Seong RH. BAF60a interacts with p53 to recruit the SWI/SNF complex. J Biol Chem 2008;283:11924-34.
35. Lee D, Kim JW, Seo T, Hwang SG, Choi EJ, Choe J. SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J Biol Chem 2002;277:22330-7. (Pubitemid 34967200)
36. Naidu SR, Love IM, Imbalzano AN, Grossman SR, Androphy EJ. The SWI/SNF chromatin remodeling subunit BRG1 is a critical regulator of p53 necessary for proliferation of malignant cells. Oncogene 2009; 28:2492-501.
37. Wang X, Nagl NG Jr, Flowers S, Zweitzig D, Dallas PB, Moran E. Expression of p270 (ARID1A), a component of human SWI/SNF complexes, in human tumors. Int J Cancer 2004;112:636.
38. Huang J, Zhao YL, Li Y, Fletcher JA, Xiao S. Genomic and functional evidence for an ARID1A tumor suppressor role. Genes Chromosomes Cancer 2007;46:745-50. (Pubitemid 46912345)
39. Birnbaum DJ, Adélaïde J, Mamessier E, Finetti P, Lagarde A, Monges G, et al. Genome profiling of pancreatic adenocarcinoma. Genes Chromosomes Cancer 2011;50:456-65.
40. Inoue H, Giannakopoulos S, Parkhurst CN, Matsumura T, Kono EA, Furukawa T, et al. Target genes of the largest human SWI/SNF complex subunit control cell growth. Biochem J 2011;434:83-92.
41. Nagl NG Jr, Patsialou A, Haines DS, Dallas PB, Beck GR Jr, Moran E. The p270 (ARID1A/SMARCF1) subunit of mammalian SWI/SNF-related complexes is essential for normal cell cycle arrest. Cancer Res 2005;65:9236-44. (Pubitemid 41507989)
42. Nagl NG Jr, Zweitzig DR, Thimmapaya B, Beck GR Jr, Moran E. The cmyc gene is a direct target of mammalian SWI/SNF-related complexes during differentiation-associated cell cycle arrest. Cancer Res 2006;66:1289-93. (Pubitemid 43259906)
43. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009;9:400-14.
44. Sodir NM, Chen X, Park R, Nickel AE, Conti PS, Moats R, et al. Smad3 deficiency promotes tumorigenesis in the distal colon of ApcMin/+ mice. Cancer Res 2006;66:8430-8. (Pubitemid 44449154)
45. Baker SJ, Markowitz S, Fearon ER, Willson JK, Vogelstein B. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 1990;249:912-5.
46. Willis A, Jung EJ, Wakefield T, Chen X. Mutant p53 exerts a dominant negative effect by preventing wild-type p53 from binding to the promoter of its target genes. Oncogene 2004;23:2330-8. (Pubitemid 38496788)
47. Yan W, Chen X. Identification of GRO1 as a critical determinant for mutant p53 gain of function. J Biol Chem 2009;284:12178-87.
48. Choi JH, Lee KT, Leung PC. Estrogen receptor alpha pathway is involved in leptin-induced ovarian cancer cell growth. Carcinogenesis 2011;32:589-96.
49. Ali SH, DeCaprio JA. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin Cancer Biol 2001;11:15-23.
50. Sheppard HM, Corneillie SI, Espiritu C, Gatti A, Liu X. New insights into the mechanism of inhibition of p53 by simian virus 40 large T antigen. Mol Cell Biol 1999;19:2746-53. (Pubitemid 29144518)
51. Bocchetta M, Eliasz S, De Marco MA, Rudzinski J, Zhang L, Carbone M. The SV40 large T antigen-p53 complexes bind and activate the insulin-like growth factor-I promoter stimulating cell growth. Cancer Res 2008;68:1022-9. (Pubitemid 351272219)
52. Di Cristofano A, Ellenson LH. Endometrial carcinoma. Annu Rev Pathol 2007;2:57-85. (Pubitemid 46448060)