Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes

Gastroenterology

Volumn 148, Issue 1, 2015, Pages 88-99

  Sinicrope, Frank A ^a   Shi, Qian ^a   Smyrk, Thomas C ^a   Thibodeau, Stephen N ^a   Dienstmann, Rodrigo ^b   Guinney, Justin ^b   Bot, Brian M ^b   Tejpar, Sabine ^c   Delorenzi, Mauro ^d   Goldberg, Richard M ^e   Mahoney, Michelle ^a   Sargent, Daniel J ^a   Alberts, Steven R ^a  

^a MAYO CLINIC   (United States)

^b SAGE BIONETWORKS   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

Colorectal Cancer; Genetics; Oncogene; Prognostic Factor

Indexed keywords

CETUXIMAB; FLUOROURACIL; FOLINIC ACID; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; TUMOR MARKER; B RAF KINASE; BRAF PROTEIN, HUMAN; DNA BINDING PROTEIN; G-T MISMATCH-BINDING PROTEIN; KRAS PROTEIN, HUMAN; MLH1 PROTEIN, HUMAN; MSH2 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; RAS PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADULT; ARTICLE; CANCER ADJUVANT THERAPY; CANCER PATIENT; CANCER STAGING; CLINICAL FEATURE; COHORT ANALYSIS; COLON CANCER; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; GENE MUTATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MISMATCH REPAIR; ONCOGENE K RAS; OUTCOME ASSESSMENT; PHASE 3 CLINICAL TRIAL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; PROTEIN METHYLATION; RANDOMIZED CONTROLLED TRIAL; SURVIVAL RATE; VALIDATION STUDY; ADENOCARCINOMA; AGED; CLASSIFICATION; CLINICAL TRIAL; COLONIC NEOPLASMS; DNA METHYLATION; DNA MUTATIONAL ANALYSIS; GENETIC PREDISPOSITION; GENETICS; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; MUTATION; PATHOLOGY; PHENOTYPE; PREDICTIVE VALUE; PROCEDURES; PROMOTER REGION; PROPORTIONAL HAZARDS MODEL; REPRODUCIBILITY; RISK FACTOR; TIME FACTOR; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; COLONIC NEOPLASMS; DISEASE-FREE SURVIVAL; DNA METHYLATION; DNA MISMATCH REPAIR; DNA MUTATIONAL ANALYSIS; DNA-BINDING PROTEINS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MUTATION; MUTS HOMOLOG 2 PROTEIN; NEOPLASM STAGING; NUCLEAR PROTEINS; PHENOTYPE; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE OF TESTS; PROMOTER REGIONS, GENETIC; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS; REPRODUCIBILITY OF RESULTS; RISK FACTORS; TIME FACTORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84922949171     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.09.041     Document Type: Article

References (52)

1. W.M. Grady, and J.M. Carethers Genomic and epigenetic instability in colorectal cancer pathogenesis Gastroenterology 135 2008 1079 1099
2. J.R. Jass Classification of colorectal cancer based on correlation of clinical, morphological and molecular features Histopathology 50 2007 113 130
3. F.A. Sinicrope, and D.J. Sargent Molecular pathways: microsatellite instability in colorectal cancer: prognostic, predictive, and therapeutic implications Clin Cancer Res 18 2012 1506 1512
4. S. Ogino, K. Nosho, and G.J. Kirkner CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer Gut 58 2009 90 96
5. T. Hinoue, D.J. Weisenberger, and F. Pan Analysis of the association between CIMP and BRAF in colorectal cancer by DNA methylation profiling PLoS One 4 2009 e8357
6. E. Domingo, R.C. Niessen, and C. Oliveira BRAF-V600E is not involved in the colorectal tumorigenesis of HNPCC in patients with functional MLH1 and MSH2 genes Oncogene 24 2005 3995 3998
7. H. Davies, G.R. Bignell, and C. Cox Mutations of the BRAF gene in human cancer Nature 417 2002 949 954
8. H. Rajagopalan, A. Bardelli, and C. Lengauer Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status Nature 418 2002 934
9. S. Ogino, J.A. Meyerhardt, and N. Irahara KRAS mutation in stage III colon cancer and clinical outcome following intergroup trial CALGB 89803 Clin Cancer Res 15 2009 7322 7329
10. J.R. Jass, K.A. Do, and L.A. Simms Morphology of sporadic colorectal cancer with DNA replication errors Gut 42 1998 673 679
11. C.M. Ribic, D.J. Sargent, and M.J. Moore Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer N Engl J Med 349 2003 247 257
12. F.A. Sinicrope, M.R. Mahoney, and T.C. Smyrk Prognostic impact of deficient DNA mismatch repair in patients with stage III colon cancer from a randomized trial of FOLFOX-based adjuvant chemotherapy J Clin Oncol 31 2013 3664 3672
13. F.A. Sinicrope, N.R. Foster, and S.N. Thibodeau DNA mismatch repair status and colon cancer recurrence and survival in clinical trials of 5-fluorouracil-based adjuvant therapy J Natl Cancer Inst 103 2011 863 875
14. A.D. Roth, S. Tejpar, and M. Delorenzi Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study on the PETACC-3, EORTC 40993, SAKK 60-00 trial J Clin Oncol 28 2010 466 474
15. A.I. Phipps, D.D. Buchanan, and K.W. Makar BRAF mutation status and survival after colorectal cancer diagnosis according to patient and tumor characteristics Cancer Epidemiol Biomarkers Prev 21 2012 1792 1798
16. A.I. Phipps, D.D. Buchanan, and K.W. Makar KRAS-mutation status in relation to colorectal cancer survival: the joint impact of correlated tumour markers Br J Cancer 108 2013 1757 1764
17. W.S. Samowitz, K. Curtin, and D. Schaffer Relationship of Ki-ras mutations in colon cancers to tumor location, stage, and survival: a population-based study Cancer Epidemiol Biomarkers Prev 9 2000 1193 1197
18. W.S. Samowitz, C. Sweeney, and J. Herrick Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers Cancer Res 65 2005 6063 6069
19. P.G. Gavin, L.H. Colangelo, and D. Fumagalli Mutation profiling and microsatellite instability in stage II and III colon cancer: an assessment of their prognostic and oxaliplatin predictive value Clin Cancer Res 18 2012 6531 6541
20. N.J. Samadder, R.A. Vierkant, and L.S. Tillmans Associations between colorectal cancer molecular markers and pathways with clinicopathologic features in older women Gastroenterology 145 2013 348 356 e1-2
21. B. Leggett, and V. Whitehall Role of the serrated pathway in colorectal cancer pathogenesis Gastroenterology 138 2010 2088 2100
22. C.E. Bond, A. Umapathy, and R.L. Buttenshaw Chromosomal instability in BRAF mutant, microsatellite stable colorectal cancers PLoS One 7 2012 e47483
23. A.I. Phipps, P.J. Limburg, and J.A. Baron Association between molecular subtypes of colorectal cancer and patient survival Gastroenterology 148 2015 77 87
24. F.L. Greene, D.L. Page, and I.D. Fleming AJCC cancer staging manual 6th ed. 2002 Lippincott Raven Publishers Philadelphia, PA 200
25. T. Andre, C. Boni, and L. Mounedji-Boudiaf Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer N Engl J Med 350 2004 2343 2351
26. S.R. Alberts, D.J. Sargent, and S. Nair Effect of oxaliplatin, fluorouracil, and leucovorin with or without cetuximab on survival among patients with resected stage III colon cancer: a randomized trial JAMA 307 2012 1383 1393
27. E. Domingo, P. Laiho, and M. Ollikainen BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing J Med Genet 41 2004 664 668
28. B. Angulo, E. Garcia-Garcia, and R. Martinez A commercial real-time PCR kit provides greater sensitivity than direct sequencing to detect KRAS mutations: a morphology-based approach in colorectal carcinoma J Mol Diagn 12 2010 292 299
29. W.M. Grady, A. Rajput, and J.D. Lutterbaugh Detection of aberrantly methylated hMLH1 promoter DNA in the serum of patients with microsatellite unstable colon cancer Cancer Res 61 2001 900 902
30. E.L. Kaplan, and P. Meier Nonparametric estimation from incomplete observations J Am Stat Assn 53 1958 457 481
31. D.R. Cox Regression models and life-tables J R Stat Soc 34 1972 187 220
32. R Development Core Team: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing, 2011. Available at: http://www.R-project.org/. Accessed September, 2014.
33. C.R. Boland, and A. Goel Microsatellite instability in colorectal cancer Gastroenterology 138 2010 2073 2087. e3
34. Y.H. Kim, S. Kakar, and L. Cun Distinct CpG island methylation profiles and BRAF mutation status in serrated and adenomatous colorectal polyps Intl J Cancer 123 2008 2587 2593
35. S. Popat, R. Hubner, and R.S. Houlston Systematic review of microsatellite instability and colorectal cancer prognosis J Clin Oncol 23 2005 609 618
36. A.N. Burnett-Hartman, P.A. Newcomb, and J.D. Potter Genomic aberrations occurring in subsets of serrated colorectal lesions but not conventional adenomas Cancer Res 73 2013 2863 2872
37. F. De Sousa, E. Melo, and X. Wang Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions Nat Med 19 2013 614 618
38. L.A. Carragher, K.R. Snell, and S.M. Giblett V600EBraf induces gastrointestinal crypt senescence and promotes tumour progression through enhanced CpG methylation of p16INK4a EMBO Mol Med 2 2010 458 471
39. R. Rad, J. Cadinanos, and L. Rad A genetic progression model of Braf(V600E)-induced intestinal tumorigenesis reveals targets for therapeutic intervention Cancer Cell 24 2013 15 29
40. T. Andre, C. Boni, and M. Navarro Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial J Clin Oncol 27 2009 3109 3116
41. G. Yothers, M.J. O'Connell, and C.J. Allegra Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses J Clin Oncol 29 2011 3768 3774
42. J.P. Kuebler, H.S. Wieand, and M.J. O'Connell Oxaliplatin combined with weekly bolus fluorouracil and leucovorin as surgical adjuvant chemotherapy for stage II and III colon cancer: results from NSABP C-07 J Clin Oncol 25 2007 2198 2204
43. D.J. Sargent, S. Marsoni, and G. Monges Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer J Clin Oncol 28 2010 3219 3226
44. M. Kang, X.J. Shen, and S. Kim Somatic gene mutations in African Americans may predict worse outcomes in colorectal cancer Cancer Biomark 13 2013 359 366
45. B.E. Sylvester, D. Huo, and A. Khramtsov Molecular analysis of colorectal tumors within a diverse patient cohort at a single institution Clin Cancer Res 18 2012 350 359
46. H.J. Andreyev, A.R. Norman, and D. Cunningham Kirsten ras mutations in patients with colorectal cancer: the 'RASCAL II' study Br J Cancer 85 2001 692 696
47. W. De Roock, B. Claes, and D. Bernasconi Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemotherapy-refractory metastatic colorectal cancer: a retrospective consortium analysis Lancet Oncol 11 2010 753 762
48. Y. Imamura, T. Morikawa, and X. Liao Specific mutations in KRAS codons 12 and 13, and patient prognosis in 1075 BRAF wild-type colorectal cancers Clin Cancer Res 18 2012 4753 4763
49. A. Farina-Sarasqueta, G. van Lijnschoten, and E. Moerland The BRAF V600E mutation is an independent prognostic factor for survival in stage II and stage III colon cancer patients Ann Oncol 21 2010 2396 2402
50. S. Ogino, K. Shima, and J.A. Meyerhardt Predictive and prognostic roles of BRAF mutation in stage III colon cancer: results from intergroup trial CALGB 89803 Clin Cancer Res 18 2012 890 900
51. A. Prahallad, C. Sun, and S. Huang Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR Nature 483 2012 100 103
52. R.B. Corcoran, H. Ebi, and A.B. Turke EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib Cancer Discov 2 2012 227 235