Survival Benefit of Exercise Differs by Tumor IRS1 Expression Status in Colorectal Cancer

Annals of Surgical Oncology

Volumn 23, Issue 3, 2016, Pages 908-917

  Hanyuda, Akiko ^a   Kim, Sun A ^b   Martinez Fernandez, Alejandro ^b   Qian, Zhi Rong ^b   Yamauchi, Mai ^b   Nishihara, Reiko ^a,b   Morikawa, Teppei ^b,c   Liao, Xiaoyun ^b   Inamura, Kentaro ^b,d   Mima, Kosuke ^b   Cao, Yin ^a,e   Zhang, Xuehong ^b,f   Wu, Kana ^a   Chan, Andrew T ^b,e,f   Giovannucci, Edward L ^a   Meyerhardt, Jeffrey A ^b   Fuchs, Charles S ^b,f   Shivdasani, Ramesh A ^b   Ogino, Shuji ^a,b,f  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIVERSITY OF TOKYO HOSPITAL   (Japan)

^d CANCER INSTITUTE   (Japan)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; K RAS PROTEIN; PIK3CA PROTEIN; SOMATOMEDIN; TUMOR MARKER; UNCLASSIFIED DRUG; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; COLORECTAL CANCER; CPG ISLAND; EXERCISE; FEMALE; FOLLOW UP; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LONG INTERSPERSED NUCLEOTIDE ELEMENT 1; LONG INTERSPERSED REPEAT; MAJOR CLINICAL STUDY; MALE; MICROSATELLITE INSTABILITY; PHENOTYPE; PHYSICAL ACTIVITY; PROTEIN EXPRESSION; PROTEIN METHYLATION; CANCER GRADING; COLORECTAL NEOPLASMS; DNA METHYLATION; ENZYME IMMUNOASSAY; GENETICS; KINESIOTHERAPY; METABOLISM; MORTALITY; MUTATION; PROGNOSIS; PROSPECTIVE STUDY; SURVIVAL RATE; TISSUE MICROARRAY;

AGED; BIOMARKERS, TUMOR; COLORECTAL NEOPLASMS; DNA METHYLATION; EXERCISE THERAPY; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOENZYME TECHNIQUES; INSULIN RECEPTOR SUBSTRATE PROTEINS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICROSATELLITE INSTABILITY; MUTATION; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; PROSPECTIVE STUDIES; SURVIVAL RATE; TISSUE ARRAY ANALYSIS;

EID: 84957842982     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-015-4967-4     Document Type: Article

References (75)

1. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr. 2001;131(11 Suppl):3109S–20S.
2. Giovannucci E. Modifiable risk factors for colon cancer. Gastroenterol Clin North Am. 2002;31(4):925–43.
3. Chang CK, Ulrich CM. Hyperinsulinaemia and hyperglycaemia: possible risk factors of colorectal cancer among diabetic patients. Diabetologia. 2003;46(5):595–607.
4. Komninou D, Ayonote A, Richie JP Jr, Rigas B. Insulin resistance and its contribution to colon carcinogenesis. Exp Biol Med (Maywood). 2003;228(4):396–405.
5. Limburg PJ, Stolzenberg-Solomon RZ, Vierkant RA, et al. Insulin, glucose, insulin resistance, and incident colorectal cancer in male smokers. Clin Gastroenterol Hepatol. 2006;4(12):1514–21.
6. Giovannucci E. Metabolic syndrome, hyperinsulinemia, and colon cancer: a review. Am J Clin Nutr. 2007;86(3):s836–s842.
7. Giovannucci E, Harlan DM, Archer MC, et al. Diabetes and cancer: a consensus report. Diabetes Care. 2010;33(7):1674–85.
8. Kasuga M, Ueki K, Tajima N, et al. Report of the Japan Diabetes Society/Japanese Cancer Association Joint Committee on Diabetes and Cancer. Cancer Sci. 2013;104(7):965–76.
9. Cohen DH, LeRoith D. Obesity, type 2 diabetes, and cancer: the insulin and IGF connection. Endocr Relat Cancer. 2012;19(5):F27–F45.
10. Sciacca L, Vigneri R, Tumminia A, et al. Clinical and molecular mechanisms favoring cancer initiation and progression in diabetic patients. Nutr Metab Cardiovasc Dis. 2013;23(9):808–15.
11. Platz EA, Willett WC, Colditz GA, Rimm EB, Spiegelman D, Giovannucci E. Proportion of colon cancer risk that might be preventable in a cohort of middle-aged US men. Cancer Causes Control. 2000;11(7):579–88.
12. International Agency for Research on Cancer. Weight control and physical activity. Lyon: IARC Press, 2002. p. 6.
13. Samad AK, Taylor RS, Marshall T, Chapman MA. A meta-analysis of the association of physical activity with reduced risk of colorectal cancer. Color Dis. 2005;7(3):204–13.
14. World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: American Institute for Cancer Research; 2007. p. 2.
15. Wiseman M. The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc. 2008;67(3):253–56.
16. Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M. The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer. 2009;125(1):171–80.
17. Wolin KY, Yan Y, Colditz GA, Lee IM. Physical activity and colon cancer prevention: a meta-analysis. Br J Cancer. 2009;100(4):611–16.
18. Schmitz KH, Holtzman J, Courneya KS, Masse LC, Duval S, Kane R. Controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev. 2005;14(7):1588–95.
19. Meyerhardt JA, Giovannucci EL, Holmes MD, et al. Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol. 2006;24(22):3527–34.
20. Meyerhardt JA, Giovannucci EL, Ogino S, et al. Physical activity and male colorectal cancer survival. Arch Intern Med. 2009;169(22):2102–08.
21. Ballard-Barbash R, Friedenreich CM, Courneya KS, Siddiqi SM, McTiernan A, Alfano CM. Physical activity, biomarkers, and disease outcomes in cancer survivors: a systematic review. J Natl Cancer Inst. 2012;104(11):815–40.
22. Je Y, Jeon JY, Giovannucci EL, Meyerhardt JA. Association between physical activity and mortality in colorectal cancer: a meta-analysis of prospective cohort studies. Int J Cancer. 2013;133(8):1905–13.
23. Campbell PT, Patel A V, Newton CC, Jacobs EJ, Gapstur SM. Associations of recreational physical activity and leisure time spent sitting with colorectal cancer survival. J Clin Oncol. 2013;31(7):876–85.
24. Haydon AM, Macinnis RJ, English DR, Giles GG. Effect of physical activity and body size on survival after diagnosis with colorectal cancer. Gut. 2006;55(1):62–67.
25. Boyle T, Fritschi L, Platell C, Heyworth J. Lifestyle factors associated with survival after colorectal cancer diagnosis. Br J Cancer. 2013;109(3):814–22.
26. Bommer GT, Feng Y, Iura A, et al. IRS1 regulation by Wnt/beta-catenin signaling and varied contribution of IRS1 to the neoplastic phenotype. J Biol Chem. 2010;285(3):1928–38.
27. Esposito DL, Aru F, Lattanzio R, et al. The insulin receptor substrate 1 (IRS1) in intestinal epithelial differentiation and in colorectal cancer. PLoS One. 2012;7(4):e36190.
28. Slattery ML, Samowitz W, Curtin K, et al. Associations among IRS1, IRS2, IGF1, and IGFBP3 genetic polymorphisms and colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2004;13(7):1206–14.
29. Wang Y, Nishina PM, Naggert JK. Degradation of IRS1 leads to impaired glucose uptake in adipose tissue of the type 2 diabetes mouse model TALLYHO/Jng. J Endocrinol. 2009;203(1):65–74.
30. Wainszelbaum MJ, Liu J, Kong C, et al. TBC1D3, a hominoid-specific gene, delays IRS-1 degradation and promotes insulin signaling by modulating p70 S6 kinase activity. PLoS One. 2012;7(2):e31225.
31. Dearth RK, Cui X, Kim HJ, Hadsell DL, Lee A V. Oncogenic transformation by the signaling adaptor proteins insulin receptor substrate (IRS)-1 and IRS-2. Cell Cycle. 2007;6(6):705–13.
32. Guo YS, Narayan S, Yallampalli C, Singh P. Characterization of insulinlike growth factor I receptors in human colon cancer. Gastroenterology. 1992;102(4 Pt 1):1101–8.
33. Chang Q, Li Y, White MF, Fletcher JA, Xiao S. Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: therapeutic implications. Cancer Res. 2002;62(21):6035–8.
34. Sandhu MS, Dunger DB, Giovannucci EL. Insulin, insulin-like growth factor-I (IGF-I), IGF binding proteins, their biologic interactions, and colorectal cancer. J Natl Cancer Inst. 2002;94(13):972–80.
35. Durai R, Yang W, Gupta S, Seifalian AM, Winslet MC. The role of the insulin-like growth factor system in colorectal cancer: review of current knowledge. Int J Colorectal Dis. 2005;20(3):203–20.
36. Pollak M. Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer. 2008;8(12):915–28.
37. Porter HA, Perry A, Kingsley C, Tran NL, Keegan AD. IRS1 is highly expressed in localized breast tumors and regulates the sensitivity of breast cancer cells to chemotherapy, while IRS2 is highly expressed in invasive breast tumors. Cancer Lett. 2013;338(2):239–48.
38. Chan AT, Ogino S, Fuchs CS. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N Engl J Med. 2007;356(21):2131–42.
39. Liao X, Lochhead P, Nishihara R, et al. Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N Engl J Med. 2012;367(17):1596–606.
40. Meyerhardt JA, Ogino S, Kirkner GJ, et al. Interaction of molecular markers and physical activity on mortality in patients with colon cancer. Clin Cancer Res. 2009;15(18):5931–6.
41. Morikawa T, Kuchiba A, Lochhead P, et al. Prospective analysis of body mass index, physical activity, and colorectal cancer risk associated with beta-catenin (CTNNB1) status. Cancer Res. 2013;73(5):1600–10.
42. Yamauchi M, Lochhead P, Imamura Y, et al. Physical activity, tumor PTGS2 expression, and survival in patients with colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(6):1142–52.
43. Ogino S, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. CpG island methylator phenotype-low (CIMP-low) in colorectal cancer: possible associations with male sex and KRAS mutations. J Mol Diagnostics. 2006;8(5):582–8.
44. Imamura Y, Morikawa T, Liao X, et al. Specific mutations in KRAS codons 12 and 13, and patient prognosis in 1075 BRAF wild-type colorectal cancers. Clin Cancer Res. 2012;18(17):4753–63.
45. Ogino S, Kawasaki T, Brahmandam M, et al. Sensitive sequencing method for KRAS mutation detection by Pyrosequencing. J Mol Diagn. 2005;7(3):413–21.
46. Nosho K, Kawasaki T, Ohnishi M, et al. PIK3CA mutation in colorectal cancer: relationship with genetic and epigenetic alterations. Neoplasia. 2008;10(6):534–41.
47. Liao X, Morikawa T, Lochhead P, et al. Prognostic role of PIK3CA mutation in colorectal cancer: cohort study and literature review. Clin Cancer Res. 2012;18(8):2257–68.
48. Ogino S, Kawasaki T, Brahmandam M, et al. Precision and performance characteristics of bisulfite conversion and real-time PCR (MethyLight) for quantitative DNA methylation analysis. J Mol Diagnostics. 2006;8(2):209–17.
49. Nosho K, Irahara N, Shima K, et al. Comprehensive biostatistical analysis of CpG island methylator phenotype in colorectal cancer using a large population-based sample. PLoS One. 2008;3(11):e3698.
50. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009;58(1):90–6.
51. Ogino S, Kawasaki T, Nosho K, et al. LINE-1 hypomethylation is inversely associated with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Int J Cancer. 2008;122(12):2767–73.
52. Irahara N, Nosho K, Baba Y, et al. Precision of pyrosequencing assay to measure LINE-1 methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J Mol Diagn. 2010;12(2):177–83.
53. Kawasaki T, Nosho K, Ohnishi M, et al. Correlation of beta-catenin localization with cyclooxygenase-2 expression and CpG island methylator phenotype (CIMP) in colorectal cancer. Neoplasia. 2007;9(7):569–77.
54. Morikawa T, Kuchiba A, Liao X, et al. Tumor TP53 expression status, body mass index and prognosis in colorectal cancer. Int J Cancer. 2012;131(5):1169–78.
55. Ogino S, Brahmandam M, Kawasaki T, Kirkner GJ, Loda M, Fuchs CS. Combined analysis of COX-2 and p53 expressions reveals synergistic inverse correlations with microsatellite instability and CpG island methylator phenotype in colorectal cancer. Neoplasia. 2006;8(6):458–64.
56. Morikawa T, Kuchiba A, Yamauchi M, et al. Association of CTNNB1 (beta-catenin) alterations, body mass index, and physical activity with survival in patients with colorectal cancer. JAMA. 2011;305(16):1685–94.
57. Lee DH, Kim JY, Lee MK, et al. Effects of a 12-week home-based exercise program on the level of physical activity, insulin, and cytokines in colorectal cancer survivors: a pilot study. Support Care Cancer. 2013;21(9):2537–45.
58. Chia WK, Ali R, Toh HC. Aspirin as adjuvant therapy for colorectal cancer–reinterpreting paradigms. Nat Rev Clin Oncol. 2012;9(10):561–70.
59. Galon J, Pages F, Marincola FM, et al. Cancer classification using the Immunoscore: a worldwide task force. J Transl Med. 2012;10:205.
60. Bardhan K, Liu K. Epigenetics and colorectal cancer pathogenesis. Cancers (Basel). 2013;5(2):676–713.
61. Colussi D, Brandi G, Bazzoli F, Ricciardiello L. Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci. 2013;14(8):16365–85.
62. Bishehsari F, Mahdavinia M, Vacca M, Malekzadeh R, Mariani-Costantini R. Epidemiological transition of colorectal cancer in developing countries: environmental factors, molecular pathways, and opportunities for prevention. World J Gastroenterol. 2014;20(20):6055–72.
63. Okugawa Y, Grady WM, Goel A. Epigenetic alterations in colorectal cancer: emerging biomarkers. Gastroenterology. 2015;149(5):1204–25.
64. Weisenberger DJ, Levine AJ, Long TI, et al. Association of the colorectal CpG island methylator phenotype with molecular features, risk factors, and family history. Cancer Epidemiol Biomarkers Prev. 2015;24(3):512–9.
65. Ogino S, Fuchs CS, Giovannucci E. How many molecular subtypes? Implications of the unique tumor principle in personalized medicine. Expert Rev Mol Diagn. 2012;12(6):621-628.
66. Ogino S, Lochhead P, Chan AT, et al. Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod Pathol. 2013;26(4):465–84.
67. Kido Y, Burks DJ, Withers D, et al. Tissue-specific insulin resistance in mice with mutations in the insulin receptor, IRS-1, and IRS-2. J Clin Invest. 2000;105(2):199–205.
68. Huang C, Thirone AC, Huang X, Klip A. Differential contribution of insulin receptor substrates 1 versus 2 to insulin signaling and glucose uptake in l6 myotubes. J Biol Chem. 2005;280(19):19426–35.
69. Karlsson HK, Zierath JR. Insulin signaling and glucose transport in insulin resistant human skeletal muscle. Cell Biochem Biophys. 2007;48(2–3):103–13.
70. Ogino S, Stampfer M. Lifestyle factors and microsatellite instability in colorectal cancer: the evolving field of molecular pathological epidemiology. J Natl Cancer Inst. 2010;102(6):365–7.
71. Ogino S, Chan AT, Fuchs CS, Giovannucci E. Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field. Gut. 2011;60(3):397–411.
72. Ogino S, Galon J, Fuchs CS, Dranoff G. Cancer immunology: analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol. 2011;8(12):711–9.
73. Ogino S, King EE, Beck AH, Sherman ME, Milner DA, Giovannucci E. Interdisciplinary education to integrate pathology and epidemiology: towards molecular and population-level health science. Am J Epidemiol. 2012;176(8):659–67.
74. Ogino S, Lochhead P, Giovannucci E, Meyerhardt JA, Fuchs CS, Chan AT. Discovery of colorectal cancer PIK3CA mutation as potential predictive biomarker: power and promise of molecular pathological epidemiology. Oncogene. 2014;33(23):2949–55.
75. Ogino S, Campbell PT, Nishihara R, et al. Proceedings of the second international molecular pathological epidemiology (MPE) meeting. Cancer Causes Control. 2015;26(7):959–72.