IRS2 is a candidate driver oncogene on 13q34 in colorectal cancer

International Journal of Experimental Pathology

Volumn 94, Issue 3, 2013, Pages 203-211

  Day, Elizabeth ^a   Poulogiannis, George ^b,c   Mccaughan, Frank ^a,d   Mulholland, Shani ^d   Arends, Mark J ^d   Ibrahim, Ashraf E K ^a   Dear, Paul H ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Colorectal cancer; Copy number alterations; Insulin receptor substrates; Minimal copy regions; Molecular copy number counting; Oncogene

Indexed keywords

MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE;

ARTICLE; CELL ADHESION; CHROMOSOME 13Q; CHROMOSOME 13Q34; COLORECTAL CANCER; COLORECTAL TUMOR; COMPARATIVE GENOMIC HYBRIDIZATION; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; IN VITRO STUDY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL;

ADENOCARCINOMA; CHROMOSOMES, HUMAN, PAIR 13; COLONIC POLYPS; COLORECTAL NEOPLASMS; DATABASES, GENETIC; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84877921698     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/iep.12021     Document Type: Article

References (46)

1. Beroukhim R., Mermel C.H., Porter D. et al. (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905.
2. Bertucci F., Salas S., Eysteries S. et al. (2004) Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene 23, 1377-1391.
3. Byron S.A., Horwitz K.B., Richer J.K., Lange C.A., Zhang X., Yee D. (2006) Insulin receptor substrates mediate distinct biological responses to insulin-like growth factor receptor activation in breast cancer cells. Br. J. Cancer 95, 1220-1228.
4. Chin L., Hahn W.C., Getz G., Meyerson M. (2011) Making sense of cancer genomic data. Genes Dev. 25, 534-555.
5. Csiszar A. (2006) Structural and functional diversity of adaptor proteins involved in tyrosine kinase signalling. BioEssays 28, 465-479.
6. Daser A., Thangavelu M., Pannell R. et al. (2006) Interrogation of genomes by molecular copy-number counting (MCC). Nat. Meth. 3, 447-453.
7. Dearth R.K., Cui X., Kim H.-J. et al. (2006) Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Mol. Cell. Biol. 26, 9302-9314.
8. Dearth R.K., Cui X., Kim H.J., Hadsell D.L., Lee A.V. (2007) Oncogenic transformation by the signaling adaptor proteins insulin receptor substrate (IRS)-1 and IRS-2. Cell Cycle 6, 705-713.
9. Garnis C., Buys T.P., Lam W.L. (2004) Genetic alteration and gene expression modulation during cancer progression. Mol. Cancer 3, 9.
10. Gibson S.L., Ma Z., Shaw L.M. (2007) Divergent roles for IRS-1 and IRS-2 in breast cancer metastasis. Cell Cycle 6, 631-637.
11. Hanahan D. & Weinberg R.A. (2000) The hallmarks of cancer. Cell 100, 57-70.
12. Hennige A.M., Lammers R., Arlt D. et al. (2000) Ret oncogene signal transduction via a IRS-2/PI 3-kinase/PKB and a SHC/Grb-2 dependent pathway: possible implication for transforming activity in NIH3T3 cells. Mol. Cell. Endocrinol. 167, 69-76.
13. Hewitt R.E., McMarlin A., Kleiner D. et al. (2000) Validation of a model of colon cancer progression. J. Pathol. 192, 446-454.
14. Hong Y., Downey T., Eu K.W., Koh P.K., Cheah P.Y. (2010) A 'metastasis-prone' signature for early-stage mismatch-repair proficient sporadic colorectal cancer patients and its implications for possible therapeutics. Clin. Exp. Metastasis 27, 83-90.
15. Hsieh A.C., Truitt M.L., Ruggero D. (2011) Oncogenic AKTivation of translation as a therapeutic target. Br. J. Cancer 105, 329-336.
16. Ibrahim A.E., Arends M.J., Silva A.L. et al. (2011) Sequential DNA methylation changes are associated with DNMT3B overexpression in colorectal neoplastic progression. Gut 60, 499-508.
17. Iino H., Jass J.R., Simms L.A. et al. (1999) DNA microsatellite instability in hyperplastic polyps, serrated adenomas, and mixed polyps: a mild mutator pathway for colorectal cancer? J. Clin. Pathol. 52, 5-9.
18. Jackson J.G., Zhang X., Yoneda T., Yee D. (2001) Regulation of breast cancer cell motility by insulin receptor substrate-2 (IRS-2) in metastatic variants of human breast cancer cell lines. Oncogene 20, 7318-7325.
19. Jass J.R. (2003) Hyperplastic-like polyps as precursors of microsatellite-unstable colorectal cancer. Am. J. Clin. Pathol. 119, 773-775.
20. Kaiser S., Park Y.K., Franklin J.L. et al. (2007) Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol. 8, R131.
21. Kendall J., Liu Q., Bakleh A. et al. (2007) Oncogenic cooperation and coamplification of developmental transcription factor genes in lung cancer. Proc. Natl Acad. Sci. 104, 16663-16668.
22. Leary R.J., Lin J.C., Cummins J. et al. (2008) Integrated analysis of homozygous deletions, focal amplifications, and sequence alterations in breast and colorectal cancers. Proc. Natl Acad. Sci. USA 105, 16224-16229.
23. Lengauer C., Kinzler K.W., Vogelstein B. (1998) Genetic instabilities in human cancers. Nature 396, 643-649.
24. Lips E.H., de Graaf E.J., Tollenaar R.A. et al. (2007) Single nucleotide polymorphism array analysis of chromosomal instability patterns discriminates rectal adenomas from carcinomas. J. Pathol. 212, 269-277.
25. Manning B.D. (2004) Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J. Cell Biol. 167, 399-403.
26. Mardilovich K. & Shaw L.M. (2009) Hypoxia regulates insulin receptor substrate-2 expression to promote breast carcinoma cell survival and invasion. Cancer Res. 69, 8894-8901.
27. Mardilovich K., Pankratz S.L., Shaw L.M. (2009) Expression and function of the insulin receptor substrate proteins in cancer. Cell Commun. Signal. 7, 14.
28. Martin E.S., Tonon G., Sinha R. et al. (2007) Common and distinct genomic events in sporadic colorectal cancer and diverse cancer types. Cancer Res. 67, 10736-10743.
29. McCampbell A.S., Harris H.A., Crabtree J.S., Winneker R.C., Walker C.L., Broaddus R.R. (2010) Loss of inhibitory insulin receptor substrate-1 phosphorylation is an early event in mammalian target of rapamycin, dependent endometrial hyperplasia and carcinoma. Cancer Prev. Res. 3, 290-300.
30. McCaughan F., Darai-Ramqvist E., Bankier A.T. et al. (2008) Microdissection molecular copy-number counting (microMCC)-unlocking cancer archives with digital PCR. J. Pathol. 216, 307-316.
31. McCaughan F., Pole J.C.M., Bankier A.T. et al. (2010) Progressive 3q amplification consistently targets SOX2 in preinvasive squamous lung cancer. Am. J. Respir. Crit. Care Med. 182, 83-91.
32. Nowell P.C. (1976) The clonal evolution of tumor cell populations. Science 194, 23-28.
33. Parsons D.W., Wang T., Samuels Y. et al. (2005) Colorectal cancer: mutations in a signalling pathway. Nature 436, 792.
34. Poulogiannis G., Ichimura K., Hamoudi R.A. et al. (2010a) Prognostic relevance of DNA copy number changes in colorectal cancer. J. Pathol. 220, 338-347.
35. Poulogiannis G., McIntyre R.E., Dimitriadi M. et al. (2010b) PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc. Natl Acad. Sci. USA 107, 15145-15150.
36. Schluter K., Gassmann P., Enns A. et al. (2006) Organ-specific metastatic tumor cell adhesion and extravasation of colon carcinoma cells with different metastatic potential. Am. J. Pathol. 169, 1064-1073.
37. Skrzypczak M., Goryca K., Rubel T. et al. (2010) Modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PLoS ONE 5, e13091.
38. Stratton M.R., Campbell P.J., Futreal P.A. (2009) The cancer genome. Nature 458, 719-724.
39. Szabolcs M., Keniry M., Simpson L. et al. (2009) Irs2 inactivation suppresses tumor progression in Pten+/- mice. Am. J. Pathol. 174, 276-286.
40. TCGA (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337.
41. Tonon G., Wong K.-K., Maulik G. et al. (2005) High-resolution genomic profiles of human lung cancer. Proc. Natl Acad. Sci. USA 102, 9625-9630.
42. Wood L.D., Parsons D.W., Jones S. et al. (2007) The genomic landscapes of human breast and colorectal cancers. Science 318, 1108-1113.
43. Yuan T.L. & Cantley L.C. (2008) PI3K pathway alterations in cancer: variations on a theme. Oncogene 27, 5497-5510.
44. Zha J., O'Brien C., Savage H. et al. (2009) Molecular predictors of response to a humanized anti-insulin-like growth factor-I receptor monoclonal antibody in breast and colorectal cancer. Mol. Cancer Ther. 8, 2110-2121.
45. Zhang X., Kamaraju S., Hakuno F. et al. (2004) Motility response to insulin-like growth factor-I (IGF-I) in MCF-7 cells is associated with IRS-2 activation and integrin expression. Breast Cancer Res. Treat. 83, 161-170.
46. Zhang X., Lin M., van Golen K.L., Yoshioka K., Itoh K., Yee D. (2005) Multiple signaling pathways are activated during insulin-like growth factor-I (IGF-I) stimulated breast cancer cell migration. Breast Cancer Res. Treat. 93, 159-168.