KRAS codon 12 and 13 mutations in relation to disease-free survival in BRAF-wild-type stage III colon cancers from an adjuvant chemotherapy trial (N0147 alliance)

Clinical Cancer Research

Volumn 20, Issue 11, 2014, Pages 3033-3043

  Yoon, Harry H ^b   Tougeron, David ^b   Shi, Qian ^a   Alberts, Steven R ^b   Mahoney, Michelle R ^a   Nelson, Garth D ^a   Nair, Suresh G ^c   Thibodeau, Stephen N ^b   Goldberg, Richard M ^d   Sargent, Daniel J ^a   Sinicrope, Frank A ^b  

^a Alliance Statistics and Data Center   (United States)

^b MAYO CLINIC   (United States)

^c LEHIGH VALLEY HOSPITAL   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CETUXIMAB; FLUOROURACIL; FOLINIC ACID; OXALIPLATIN; ANTINEOPLASTIC AGENT; BRAF PROTEIN, HUMAN; CODON; KRAS PROTEIN, HUMAN; MONOCLONAL ANTIBODY; ONCOPROTEIN; PLATINUM COMPLEX; RAS PROTEIN;

ADULT; AGE; AGED; ARTICLE; BRAF GENE; CANCER ADJUVANT THERAPY; CANCER GRADING; CANCER STAGING; CODON; COLON ADENOCARCINOMA; DISEASE FREE SURVIVAL; FEMALE; GENE MUTATION; HUMAN; MAJOR CLINICAL STUDY; MALE; MISMATCH REPAIR; ONCOGENE K RAS; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); VERY ELDERLY; WILD TYPE; ADENOCARCINOMA; ADJUVANT CHEMOTHERAPY; CLINICAL TRIAL; COLONIC NEOPLASMS; CONTROLLED STUDY; DNA MUTATIONAL ANALYSIS; GENETICS; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; MULTIPLEX POLYMERASE CHAIN REACTION; MUTATION; PHASE 3 CLINICAL TRIAL; PROPORTIONAL HAZARDS MODEL; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CETUXIMAB; CHEMOTHERAPY, ADJUVANT; CODON; COLONIC NEOPLASMS; DISEASE-FREE SURVIVAL; DNA MUTATIONAL ANALYSIS; FEMALE; FLUOROURACIL; HUMANS; KAPLAN-MEIER ESTIMATE; LEUCOVORIN; MALE; MIDDLE AGED; MULTIPLEX POLYMERASE CHAIN REACTION; MUTATION; NEOPLASM STAGING; ORGANOPLATINUM COMPOUNDS; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS; YOUNG ADULT;

EID: 84901813155     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-3140     Document Type: Article

References (50)

1. 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;14:16365-85.
2. Guerrero S, Casanova I, Farre L, Mazo A, Capella G, Mangues R. K-ras codon 12 mutation induces higher level of resistance to apoptosis and predisposition to anchorage-independent growth than codon 13 mutation or proto-oncogene overexpression. Cancer Res 2000;60:6750-6.
3. Smith G, Bounds R, Wolf H, Steele RJC, Carey FA, Wolf CR. Activating K-Ras mutations outwith "hotspot" codons in sporadic colorectal tumours - implications for personalised cancer medicine. Br J Cancer 2010;102:693-703.
4. Guerrero S, Figueras A, Casanova I, Farre L, Lloveras B, Capella G, et al. Codon 12 and codon 13 mutations at the K-ras gene induce different soft tissue sarcoma types in nude mice. FASEB J 2002;16:1642-4.
5. De Roock W, Jonker DJ, Di Nicolantonio F, Sartore-Bianchi A, Tu D, Siena S, et al. Association of KRAS p.G13D mutation with outcome in patients with chemotherapy-refractory metastatic colorectal cancer treated with cetuximab. JAMA 2010;304:1812-20.
6. Febbo PG, Ladanyi M, Aldape KD, De Marzo AM, Hammond ME, Hayes DF, et al. NCCN Task Force report: evaluating the clinical utility of tumor markers in oncology. J Natl Compr Canc Netw 2011;9 Suppl 5:S1-32; quiz S3.
7. Richman SD, Seymour MT, Chambers P, Elliott F, Daly CL, Meade AM, et al. KRAS and BRAF mutations in advanced colorectal cancer are associated with poor prognosis but do not preclude benefit from oxaliplatin or irinotecan: results from the MRC FOCUS trial. J Clin Oncol 2009;27:5931-7.
8. Ogino S, Meyerhardt JA, Irahara N, Niedzwiecki D, Hollis D, Saltz LB, et al. KRAS mutation in stage III colon cancer and clinical outcome following intergroup trial CALGB 89803. Clin Cancer Res 2009;15:7322-9.
9. Gavin PG, Colangelo LH, Fumagalli D, Tanaka N, Remillard MY, Yothers G, et al. Mutation profiling and microsatellite instability in stage II and III colon cancer: an assessment of their prognostic and oxaliplatin predictive value. Clin Cancer Res 2012;18:6531-41.
10. Hutchins G, Southward K, Handley K, Magill L, Beaumont C, Stahlschmidt J, et al. Value of mismatch repair, KRAS, and BRAF mutations in predicting recurrence and benefits from chemotherapy in colorectal cancer. J Clin Oncol 2011;29:1261-70.
11. Imamura Y, Morikawa T, Liao X, Lochhead P, Kuchiba A, Yamauchi M, et al. Specific mutations in KRAS codons 12 and 13, and patient prognosis in 1075 BRAF wild-type colorectal cancers. Clin Cancer Res 2012;18:4753-63.
12. Andreyev HJN, Norman AR, Cunningham D, Oates J, Dix BR, Iacopetta BJ, et al. Kirsten ras mutations in patients with colorectal cancer: the 'RASCAL II' study. Br J Cancer 2001;85:692-6. (Pubitemid 32929467)
13. Tejpar S, Celik I, Schlichting M, Sartorius U, Bokemeyer C, Van Cutsem E. Association of KRAS G13D tumor mutations with outcome in patients with metastatic colorectal cancer treated with first-line chemotherapy with or without cetuximab. J Clin Oncol 2012;30:3570-7.
14. Peeters M, Douillard JY, Van Cutsem E, Siena S, Zhang K, Williams R, et al. Mutant KRAS codon 12 and 13 alleles in patients with metastatic colorectal cancer: assessment as prognostic and predictive biomarkers of response to panitumumab. J Clin Oncol 2013;31:759-65.
15. Samowitz WS, Curtin K, Schaffer D, Robertson M, Leppert M, Slattery ML. Relationship of Ki-ras mutations in colon cancers to tumor location, stage, and survival: a population-based study. Cancer Epidemiol Biomarkers Prev 2000;9:1193-7.
16. Bazan V, Migliavacca M, Zanna I, Tubiolo C, Grassi N, Latteri MA, et al. Specific codon 13 K-ras mutations are predictive of clinical outcome in colorectal cancer patients, whereas codon 12 K-ras mutations are associated with mucinous histotype. Ann Oncol 2002;13:1438-46.
17. Yokota T, Ura T, Shibata N, Takahari D, Shitara K, Nomura M, et al. BRAF mutation is a powerful prognostic factor in advanced and recurrent colorectal cancer. Br J Cancer 2011;104:856-62.
18. Roth AD, Tejpar S, Delorenzi M, Yan P, Fiocca R, Klingbiel D, et al. 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 2010;28:466-74.
19. Zlobec I, Kovac M, Erzberger P, Molinari F, Bihl MP, Rufle A, et al. Combined analysis of specific KRAS mutation, BRAF and microsatellite instability identifies prognostic subgroups of sporadic and hereditary colorectal cancer. Int J Cancer 2010;127:2569-75.
20. Phipps AI, Buchanan DD, Makar KW, Burnett-Hartman AN, Coghill AE, Passarelli MN, et al. BRAF mutation status and survival after colorectal cancer diagnosis according to patient and tumor characteristics. Cancer Epidemiol Biomarkers Prev 2012;21:1792-8.
21. Ogino S, Shima K, Meyerhardt JA, McCleary NJ, Ng K, Hollis D, et al. Predictive and prognostic roles of BRAF mutation in stage III colon cancer: results from intergroup trial CALGB 89803. Clin Cancer Res 2012;18:890-900.
22. Samowitz WS, Sweeney C, Herrick J, Albertsen H, Levin TR, Murtaugh MA, et al. Poor survival associated with the BRAF V600E mutation in microsatellite-stable colon cancers. Cancer Res 2005;65:6063-9.
23. Van Cutsem E, Kohne CH, Lang I, Folprecht G, Nowacki MP, Cascinu S, et al. Cetuximab plus irinotecan, fluorouracil, and leucovorin as first-line treatment for metastatic colorectal cancer: updated analysis of overall survival according to tumor KRAS and BRAF mutation status. J Clin Oncol 2011;29:2011-9.
24. Price TJ, Hardingham JE, Lee CK, Weickhardt A, Townsend AR, Wrin JW, et al. Impact of KRAS and BRAF gene mutation status on outcomes from the phase III AGITG MAX trial of capecitabine alone or in combination with bevacizumab and mitomycin in advanced colorectal cancer. J Clin Oncol 2011;29:2675-82.
25. Sinicrope FA, Mahoney MR, Smyrk TC, Thibodeau SN, Warren RS, Bertagnolli MM, et al. 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 2013;31:3664-72.
26. Alberts SR, Sargent DJ, Nair S, Mahoney MR, Mooney M, Thibodeau SN, et al. Effect of oxaliplatin, fluorouracil, and leucovorin with or without cetuximab on survival among patients with resected stage III colon cancer: a randomized trial. JAMA 2012;307:1383-93.
27. Sinicrope FA, Rego RL, Garrity-Park MM, Foster NR, Sargent DJ, Goldberg RM, et al. Alterations in cell proliferation and apoptosis in colon cancers with microsatellite instability. Int J Cancer 2007;120:1232-8.
28. Chen J, Ye Y, Sun HZ, Shi GM. Association between KRAS codon 13 mutations and clinical response to anti-EGFR treatment in patients with metastatic colorectal cancer: results from a meta-analysis. Cancer Chemother Pharmacol 2013;71:265-72.
29. De Roock W, Claes B, Bernasconi D, De Schutter J, Biesmans B, Fountzilas G, et al. Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemo-therapy- refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol 2010;11:753-62.
30. Wangefjord S, Sundstrom M, Zendehrokh N, Lindquist KE, Nodin B, Jirstrom K, et al. Sex differences in the prognostic significance of KRAS codons 12 and 13, and BRAF mutations in colorectal cancer: a cohort study. Biol Sex Differ 2013;4:17.
31. Smakman N, van den Wollenberg DJ, Elias SG, Sasazuki T, Shirasawa S, Hoeben RC, et al. KRAS(D13) promotes apoptosis of human colorectal tumor cells by ReovirusT3D and oxaliplatin but not by tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res 2006;66:5403-8. (Pubitemid 43844967)
32. Basso M, Strippoli A, Orlandi A, Martini M, Calegari MA, Schinzari G, et al. KRAS mutational status affects oxaliplatin-based chemotherapy independently from basal mRNA ERCC-1 expression in metastatic colorectal cancer patients. Br J Cancer 2013;108:115-20.
33. Lin YL, Liau JY, Yu SC, Ou DL, Lin LI, Tseng LH, et al. KRAS mutation is a predictor of oxaliplatin sensitivity in colon cancer cells. PLoS ONE 2012;7:e50701.
34. Chen CC, Er TK, Liu YY, Hwang JK, Barrio MJ, Rodrigo M, et al. Computational analysis of KRAS mutations: implications for different effects on the KRAS p.G12D and p.G13D mutations. PLoS ONE 2013;8:e55793.
35. Fasano O, Aldrich T, Tamanoi F, Taparowsky E, Furth M, Wigler M. Analysis of the transforming potential of the human H-ras gene by random mutagenesis. Proc Natl Acad Sci U S A 1984;81:4008-12. (Pubitemid 14054513)
36. Cespedes MV, Sancho FJ, Guerrero S, Parreno M, Casanova I, Pavon MA, et al. K-ras Asp12 mutant neither interacts with Raf, nor signals through Erk and is less tumorigenic than K-ras Val12. Carcinogenesis 2006;27:2190-200. (Pubitemid 44644807)
37. Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD. Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature 1984;312:71-5. (Pubitemid 14010267)
38. Oliveira C, Westra JL, Arango D, Ollikainen M, Domingo E, Ferreira A, et al. Distinct patterns of KRAS mutations in colorectal carcinomas according to germline mismatch repair defects and hMLH1 methylation status. Hum Mol Genet 2004;13:2303-11. (Pubitemid 39359927)
39. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE. Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 2002;418:934. (Pubitemid 34976022)
40. Slattery ML, Curtin K, Anderson K, Ma KN, Edwards S, Leppert M, et al. Associations between dietary intake and Ki-ras mutations in colon tumors: a population-based study. Cancer Res 2000;60:6935-41. (Pubitemid 32059166)
41. Kampman E, Voskuil DW, van Kraats AA, Balder HF, van Muijen GNP, Goldbohm RA, et al. Animal products and K-ras codon 12 and 13 mutations in colon carcinomas. Carcinogenesis 2000;21:307-9. (Pubitemid 30098718)
42. Vizan P, Boros LG, Figueras A, Capella G, Mangues R, Bassilian S, et al. K-ras codon-specific mutations produce distinctive metabolic phenotypes in NIH3T3 mice [corrected] fibroblasts. Cancer Res 2005;65:5512-5. (Pubitemid 40911149)
43. Rosty C, Young JP, Walsh MD, Clendenning M, Walters RJ, Pearson S, et al. Colorectal carcinomas with KRAS mutation are associated with distinctive morphological and molecular features. Mod Pathol 2013;26:825-34.
44. Yamauchi M, Morikawa T, Kuchiba A, Imamura Y, Qian ZR, Nishihara R, et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut 2012;61:847-54.
45. Network TCGA. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487:330-7.
46. Sinicrope FA. DNA mismatch repair and adjuvant chemotherapy in sporadic colon cancer. Nat Rev Clin Oncol 2010;7:174-7.
47. Sargent DJ, Wieand HS, Haller DG, Gray R, Benedetti JK, Buyse M, et al. Disease-free survival versus overall survival as a primary end point for adjuvant colon cancer studies: individual patient data from 20,898 patients on 18 randomized trials. J Clin Oncol 2005;23:8664-70. (Pubitemid 46211509)
48. Taïeb J, Tabernero J, Mini E, Subtil F, Folprecht G, Van Laethem J-L, et al. Subgroup analyses results of the PETACC8 phase III trial comparing adjuvant FOLFOX4 with or without cetuximab (CTX) in resected stage III colon cancer (CC). J Clin Oncol 31, 2013 (suppl; abstr 3525).
49. Douillard JY, Oliner KS, Siena S, Tabernero J, Burkes R, Barugel M, et al. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med 2013;369:1023-34.
50. Peeters M, Oliner KS, Price TJ, Cervantes A, Sobrero AF, Ducreux M, et al. Analysis of KRAS/NRAS mutations in phase 3 study 20050181 of panitumumab (pmab) plus FOLFIRI versus FOLFIRI for second-line treatment (tx) of metastatic colorectal cancer (mCRC). J Clin Oncol 32, 2014 (suppl 3; abstr LBA387).