Loss of IGFBP7 expression and persistent AKT activation contribute to SMARCB1/Snf5-mediated tumorigenesis

Oncogene

Volumn 33, Issue 23, 2014, Pages 3024-3032

  Darr, J ^a   Klochendler, A ^a   Isaac, S ^a   Eden, A ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

malignant rhabdoid tumors; SMARCB1 Snf5; Swi Snf

Indexed keywords

INSULIN LIKE GROWTH FACTOR BINDING PROTEIN 7; PROTEIN KINASE B; SMARCB1 PROTEIN; SOMATOMEDIN BINDING PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL ADHESION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

MUS;

ANIMALS; CARCINOGENESIS; CELL ADHESION; CELL LINE, TUMOR; CHROMOSOMAL PROTEINS, NON-HISTONE; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; MALE; MICE; MICE, KNOCKOUT; MICE, SCID; PROTO-ONCOGENE PROTEINS C-AKT; RHABDOID TUMOR; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84902202543     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.261     Document Type: Article

References (63)

1. Klochendler-Yeivin A, Fiette L, Barra J, Muchardt C, Babinet C, Yaniv M. The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep 2000; 1: 500-506.
2. Roberts CW, Leroux MM, Fleming MD, Orkin SH. Highly penetrant, rapid tumorigenesis through conditional inversion of the tumor suppressor gene Snf5. Cancer Cell 2002; 2: 415-425. (Pubitemid 41039107)
3. Versteege I, Sevenet N, Lange J, Rousseau-Merck MF, Ambros P, Handgretinger R et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature 1998; 394: 203-206. (Pubitemid 28325977)
4. Wilson BG, Roberts CW. SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 2011; 11: 481-492.
5. Phelan ML, Sif S, Narlikar GJ, Kingston RE. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell 1999; 3: 247-253. (Pubitemid 29292625)
6. 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: 539-542.
7. Reisman DN, Sciarrotta J, Wang W, Funkhouser WK, Weissman BE. Loss of BRG1/ BRM in human lung cancer cell lines and primary lung cancers: correlation with poor prognosis. Cancer Res 2003; 63: 560-566. (Pubitemid 36158131)
8. Medjkane S, Novikov E, Versteege I, Delattre O. The tumor suppressor hSNF5/INI1 modulates cell growth and actin cytoskeleton organization. Cancer Res 2004; 64: 3406-3413. (Pubitemid 38657912)
9. Oruetxebarria I, Venturini F, Kekarainen T, Houweling A, Zuijderduijn LM, Mohd-Sarip A et al. P16INK4a is required for hSNF5 chromatin remodeler-induced cellular senescence in malignant rhabdoid tumor cells. J Biol Chem 2004; 279: 3807-3816. (Pubitemid 38140626)
10. Zhang ZK, Davies KP, Allen J, Zhu L, Pestell RG, Zagzag D et al. Cell cycle arrest and repression of cyclin D1 transcription by INI1/hSNF5. Mol Cell Biol 2002; 22: 5975-5988. (Pubitemid 34815844)
11. Tsikitis M, Zhang Z, Edelman W, Zagzag D, Kalpana GV. Genetic ablation of Cyclin D1 abrogates genesis of rhabdoid tumors resulting from Ini1 loss. Proc Natl Acad Sci USA 2005; 102: 12129-12134. (Pubitemid 41291140)
12. Versteege I, Medjkane S, Rouillard D, Delattre O. A key role of the hSNF5/INI1 tumour suppressor in the control of the G1-S transition of the cell cycle. Oncogene 2002; 21: 6403-6412. (Pubitemid 35155445)
13. Isakoff MS, Sansam CG, Tamayo P, Subramanian A, Evans JA, Fillmore CM et al. Inactivation of the Snf5 tumor suppressor stimulates cell cycle progression and cooperates with p53 loss in oncogenic transformation. Proc Natl Acad Sci USA 2005; 102: 17745-17750. (Pubitemid 41803568)
14. Cheng SW, Davies KP, Yung E, Beltran RJ, Yu J, Kalpana GV. c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function. Nat Genet 1999; 22: 102-105. (Pubitemid 29214815)
15. Jagani Z, Mora-Blanco EL, Sansam CG, McKenna ES, Wilson B, Chen D et al. Loss of the tumor suppressor Snf5 leads to aberrant activation of the Hedgehog-Gli pathway. Nat Med 2010; 16: 1429-1433.
16. Klochendler-Yeivin A, Picarsky E, Yaniv M. Increased DNA damage sensitivity and apoptosis in cells lacking the Snf5/Ini1 subunit of the SWI/SNF chromatin remodeling complex. Mol Cell Biol 2006; 26: 2661-2674.
17. Smith MJ, Walker JA, Shen Y, Stemmer-Rachamimov A, Gusella JF, Plotkin SR. Expression of SMARCB1 (INI1) mutations in familial schwannomatosis. Hum Mol Genet 2012; 21: 5239-5245.
18. Ae K, Kobayashi N, Sakuma R, Ogata T, Kuroda H, Kawaguchi N et al. Chromatin remodeling factor encoded by ini1 induces G1 arrest and apoptosis in ini1-deficient cells. Oncogene 2002; 21: 3112-3120. (Pubitemid 34548082)
19. Reincke BS, Rosson GB, Oswald BW, Wright CF. INI1 expression induces cell cycle arrest and markers of senescence in malignant rhabdoid tumor cells. J Cell Physiol 2003; 194: 303-313. (Pubitemid 36176892)
20. Betz BL, Strobeck MW, Reisman DN, Knudsen ES, Weissman BE. Re-expression of hSNF5/INI1/BAF47 in pediatric tumor cells leads to G1 arrest associated with induction of p16ink4a and activation of RB. Oncogene 2002; 21: 5193-5203. (Pubitemid 34948131)
21. Charboneau A, Chai J, Jordan J, Funkhouser W, Judkins A, Biegel J et al. P-Akt expression distinguishes two types of malignant rhabdoid tumors. J Cell Physiol 2006; 209: 422-427. (Pubitemid 44484633)
22. Jozwiak J, Bikowska B, Grajkowska W, Sontowska I, Roszkowski M, Galus R. Activation of Akt/mTOR pathway in a patient with atypical teratoid/rhabdoid tumor. Folia Neuropathol 2010; 48: 185-189.
23. Foster K, Wang Y, Zhou D, Wright C. Dependence on PI3K/Akt signaling for malignant rhabdoid tumor cell survival. Cancer Chemother Pharmacol 2009; 63: 783-791.
24. Nicholson KM, Anderson NG. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 2002; 14: 381-395. (Pubitemid 34214843)
25. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13: 2905-2927.
26. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96: 857-868. (Pubitemid 29165088)
27. Burgering BM, Coffer PJ. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995; 376: 599-602.
28. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T et al. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 2005; 19: 2199-2211. (Pubitemid 41330321)
29. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 2001; 411: 355-365. (Pubitemid 32467045)
30. Lee RS, Stewart C, Carter SL, Ambrogio L, Cibulskis K, Sougnez C et al. A remarkably simple genome underlies highly malignant pediatric rhabdoid cancers. J Clin Invest 2012; 122: 2983-2988.
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-15550. (Pubitemid 41528093)
32. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34: 267-273. (Pubitemid 36792858)
33. Wang L, Baiocchi RA, Pal S, Mosialos G, Caligiuri M, Sif S. The BRG1- and hBRMassociated factor BAF57 induces apoptosis by stimulating expression of the cylindromatosis tumor suppressor gene. Mol Cell Biol 2005; 25: 7953-7965. (Pubitemid 41262990)
34. Hendricks KB, Shanahan F, Lees E. Role for BRG1 in cell cycle control and tumor suppression. Mol Cell Biol 2004; 24: 362-376. (Pubitemid 38010061)
35. Wang X, Sansam CG, Thom CS, Metzger D, Evans JA, Nguyen PT et al. Oncogenesis caused by loss of the SNF5 tumor suppressor is dependent on activity of BRG1, the ATPase of the SWI/SNF chromatin remodeling complex. Cancer Res 2009; 69: 8094-8101.
36. Aguilar RC, Wendland B. Endocytosis of membrane receptors: two pathways are better than one. Proc Natl Acad Sci USA 2005; 102: 2679-2680. (Pubitemid 40299850)
37. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6: 112-126. (Pubitemid 40215807)
38. Oh Y, Nagalla SR, Yamanaka Y, Kim HS, Wilson E, Rosenfeld RG. Synthesis and characterization of insulin-like growth factor-binding protein (IGFBP)-7. Recombinant human mac25 protein specifically binds IGF-I and -II. J Biol Chem 1996; 271: 30322-30325.
39. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 2008; 132: 363-374. (Pubitemid 351191995)
40. Figueroa JA, Sharma J, Jackson JG, McDermott MJ, Hilsenbeck SG, Yee D. Recombinant insulin-like growth factor binding protein-1 inhibits IGF-I, serum, and estrogen-dependent growth of MCF-7 human breast cancer cells. J Cell Physiol 1993; 157: 229-236. (Pubitemid 23332765)
41. Evdokimova V, Tognon CE, Benatar T, Yang W, Krutikov K, Pollak M et al. IGFBP7 binds to the IGF-1 receptor and blocks its activation by insulin-like growth factors. Sci Signal 2012; 5: ra92.
42. Hooper AT, Shmelkov SV, Gupta S, Milde T, Bambino K, Gillen K et al. Angiomodulin is a specific marker of vasculature and regulates vascular endothelial growth factor-A-dependent neoangiogenesis. Circ Res 2009; 105: 201-208.
43. Pen A, Durocher Y, Slinn J, M Rukhlova, Charlebois C, DB Stanimirovic et al. Insulin-like growth factor binding protein 7 exhibits tumor suppressive and vessel stabilization properties in U87MG and T98G glioblastoma cell lines. Cancer Biol Ther 2011; 12: 634-646.
44. Chen D, Yoo BK, Santhekadur PK, Gredler R, Bhutia SK, Das SK et al. Insulin-like growth factor-binding protein-7 functions as a potential tumor suppressor in hepatocellular carcinoma. Clin Cancer Res 2011; 17: 6693-6701.
45. Tamura K, Hashimoto K, Suzuki K, Yoshie M, Kutsukake M, Sakurai T. Insulin-like growth factor binding protein-7 (IGFBP7) blocks vascular endothelial cell growth factor (VEGF)-induced angiogenesis in human vascular endothelial cells. Eur J Pharmacol 2009; 610: 61-67.
46. Drobic B, Perez-Cadahia B, Yu J, Kung SK, Davie JR. Promoter chromatin remodeling of immediate-early genes is mediated through H3 phosphorylation at either serine 28 or 10 by the MSK1 multi-protein complex. Nucleic Acids Res 2010; 38: 3196-3208.
47. Zhang M, Fang H, Zhou J, Herring BP. A novel role of Brg1 in the regulation of SRF/MRTFA-dependent smooth muscle-specific gene expression. J Biol Chem 2007; 282: 25708-25716. (Pubitemid 47372829)
48. Xi Q, He W, Zhang XH, Le HV, Massague J. Genome-wide impact of the BRG1 SWI/ SNF chromatin remodeler on the transforming growth factor beta transcriptional program. J Biol Chem 2008; 283: 1146-1155.
49. Nocentini S. Apoptotic response of malignant rhabdoid tumor cells. Cancer Cell Int 2003; 3: 11.
50. Arcaro A, Doepfner KT, Boller D, Guerreiro AS, Shalaby T, Jackson SP et al. Novel role for insulin as an autocrine growth factor for malignant brain tumour cells. Biochem J 2007; 406: 57-66. (Pubitemid 47264735)
51. Vizioli MG, Sensi M, Miranda C, Cleris L, Formelli F, Anania MC et al. IGFBP7: an oncosuppressor gene in thyroid carcinogenesis. Oncogene 2010; 29: 3835-3844.
52. Sato Y, Chen Z, Miyazaki K. Strong suppression of tumor growth by insulin-like growth factor-binding protein-related protein 1/tumor-derived cell adhesion factor/mac25. Cancer Sci 2007; 98: 1055-1063. (Pubitemid 46865391)
53. Benatar T, Yang W, Amemiya Y, Evdokimova V, Kahn H, Holloway C et al. IGFBP7 reduces breast tumor growth by induction of senescence and apoptosis pathways. Breast Cancer Res Treat 2012; 133: 563-573.
54. Burger AM, Leyland-Jones B, Banerjee K, Spyropoulos DD, Seth AK. Essential roles of IGFBP-3 and IGFBP-rP1 in breast cancer. Eur J Cancer 2005; 41: 1515-1527. (Pubitemid 40981832)
55. Yamanaka Y, Wilson EM, Rosenfeld RG, Oh Y. Inhibition of insulin receptor activation by insulin-like growth factor binding proteins. J Biol Chem 1997; 272: 30729-30734. (Pubitemid 27527507)
56. Ahmed S, Yamamoto K, Sato Y, Ogawa T, Herrmann A, Higashi S et al. Proteolytic processing of IGFBP-related protein-1 (TAF/angiomodulin/mac25) modulates its biological activity. Biochem Biophys Res Commun 2003; 310: 612-618. (Pubitemid 37163708)
57. Beattie J, Kreiner M, Allan GJ, Flint DJ, Domingues D, van der Walle CF. IGFBP-3and IGFBP-5 associate with the cell binding domain (CBD) of fibronectin. Biochem Biophys Res Commun 2009; 381: 572-576.
58. Collett-Solberg PF, Cohen P. The role of the insulin-like growth factor binding proteins and the IGFBP proteases in modulating IGF action. Endocrinol Metab Clin North Am 1996; 25: 591-614. (Pubitemid 26304475)
59. Hollmann TJ, Hornick JL. INI1-deficient tumors: diagnostic features and molecular genetics. Am J Surg Pathol 2011; 35: e47-e63.
60. Euhus DM, Hudd C, LaRegina MC, Johnson FE. Tumor measurement in the nude mouse. J Surg Oncol 1986; 31: 229-234. (Pubitemid 16104025)
61. Naviaux RK, Costanzi E, Haas M, Verma IM. The pCL vector system: rapid production of helper-free, high-Titer, recombinant retroviruses. J Virol 1996; 70: 5701-5705. (Pubitemid 26240755)
62. Muchardt C, Sardet C, Bourachot B, Onufryk C, Yaniv M. A human protein with homology to Saccharomyces cerevisiae SNF5 interacts with the potential helicase hbrm. Nucleic Acids Res 1995; 23: 1127-1132.
63. Barzily-Rokni M, Friedman N, Ron-Bigger S, Isaac S, Michlin D, Eden A. Synergism between DNA methylation and macroH2A1 occupancy in epigenetic silencing of the tumor suppressor gene p16 (CDKN2A). Nucleic Acids Res 2011; 39: 1326-1335.