KRAS mutation testing in clinical practice

Expert Review of Molecular Diagnostics

Volumn 15, Issue 3, 2015, Pages 375-384

  Perincheri, Sudhir ^a   Hui, Pei ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

clinical oncology; KRAS; mutation testing

Indexed keywords

DNA; K RAS PROTEIN; KRAS PROTEIN, HUMAN; ONCOPROTEIN; RAS PROTEIN;

ALLELE; BILE DUCT CANCER; CANCER PROGNOSIS; CANCER THERAPY; CARCINOGENESIS; CLINICAL PRACTICE; COLON CANCER; COLORECTAL CARCINOMA; FEMALE GENITAL TRACT TUMOR; GEL ELECTROPHORESIS; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; GENETICS; HEMATOLOGIC MALIGNANCY; HIGH RESOLUTION MELTING ANALYSIS; HUMAN; LABORATORY TEST; LUNG CANCER; MOLECULAR BIOLOGY; MOLECULAR GENETICS; MOLECULAR HYBRIDIZATION; MULTICENTER STUDY (TOPIC); NONHUMAN; PANCREAS CANCER; PHASE 3 CLINICAL TRIAL (TOPIC); POLYMERASE CHAIN REACTION; PYROSEQUENCING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SANGER SEQUENCING; SEQUENCE ANALYSIS; SINGLE STRAND CONFORMATION POLYMORPHISM; THYROID CANCER; THYROID CARCINOMA; FEMALE; GENOMICS; MALE; METABOLISM; MUTATION; MUTATION RATE; NEOPLASMS; NUCLEOTIDE SEQUENCE; PROCEDURES; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; DNA MUTATIONAL ANALYSIS; FEMALE; GENETIC TESTING; GENOMICS; HUMANS; MALE; MUTATION; MUTATION RATE; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; SIGNAL TRANSDUCTION;

EID: 84923379794     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/14737159.2015.986102     Document Type: Review

References (93)

1. Malumbres M, Barbacid M. RAS oncogenes: the first 30 years. Nature Rev Cancer 2003;3(6):459-65
2. Bamford S, Dawson E, Forbes S, et al. The COSMIC (Catalogue of Somatic Mutations in Cancer) database and website. Br J Cancer 2004;91(2):355-8
3. Jancik S, Drabek J, Radzioch D, Hajduch M. Clinical relevance of KRAS in human cancers. J Biomed Biotechnol 2010;2010:150960
4. Kirsten WH, Mayer LA. Morphologic responses to a murine erythroblastosis virus. J Natl Cancer Ins 1967;39(2):311-35
5. Ellis RW, Defeo D, Shih TY, et al. The p21 src genes of Harvey and Kirsten sarcoma viruses originate from divergent members of a family of normal vertebrate genes. Nature 1981;292(5823):506-11
6. Scolnick EM, Rands E, Williams D, Parks WP. Studies on the nucleic acid sequences of Kirsten sarcoma virus: a model for formation of a mammalian RNA-containing sarcoma virus. J Virol 1973;12(3):458-63
7. Perucho M, Goldfarb M, Shimizu K, et al. Human-tumor-derived cell lines contain common and different transforming genes. Cell 1981;27(3 Pt 2):467-76
8. Shih C, Shilo BZ, Goldfarb MP, et al. Passage of phenotypes of chemically transformed cells via transfection of DNA and chromatin. Proc Natl Acad Sci USA 1979;76(11):5714-18
9. Santos E, Martin-Zanca D, Reddy EP, et al. Malignant activation of a K-ras oncogene in lung carcinoma but not in normal tissue of the same patient. Science 1984;223(4637): 661-4
10. Rajalingam K, Schreck R, Rapp UR, Albert S. Ras oncogenes and their downstream targets. Biochim Biophys Acta 2007;1773(8):1177-95
11. Ellis CA, Clark G. The importance of being K-Ras. Cell Signal 2000;12(7):425-34
12. Barbacid M. ras genes. Ann Rev Biochem 1987;56:779-827
13. Plowman SJ, Berry RL, Bader SA, et al. K-ras 4A and 4B are co-expressed widely in human tissues, and their ratio is altered in sporadic colorectal cancer. J Exp Clin Cancer Res 2006;25(2):259-67
14. Johnson L, Greenbaum D, Cichowski K, et al. K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev 1997;11(19):2468-81
15. Khalaf WF, White H, Wenning MJ, et al. K-Ras is essential for normal fetal liver erythropoiesis. Blood 2005;105(9):3538-41
16. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nature Rev Cancer 2007;7(4): 295-308
17. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nature Rev Cancer 2011;11(11):761-74
18. Downward J. Cancer: a tumour gene's fatal flaws. Nature 2009;462(7269):44-5
19. Scheffzek K, Ahmadian MR, Kabsch W, et al. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 1997; 277(5324):333-8
20. Graham DL, Eccleston JF, Lowe PN. The conserved arginine in rho-GTPase-activating protein is essential for efficient catalysis but not for complex formation with Rho.GDP and aluminum fluoride. Biochemistry 1999; 38(3):985-91
21. Magee AI, Newman CM, Giannakouros T, et al. Lipid modifications and function of the ras superfamily of proteins. Biochem Soc Trans 1992;20(2):497-9
22. Cox AD, Der CJ. Protein prenylation: more than just glue Curr Opin Cell Biol 1992; 4(6):1008-16
23. Dudler T, Gelb MH. Palmitoylation of Ha-Ras facilitates membrane binding, activation of downstream effectors, and meiotic maturation in Xenopus oocytes. J Biol Chem 1996;271(19):11541-7
24. Milligan G, Parenti M, Magee AI. The dynamic role of palmitoylation in signal transduction. Trends Biochem Sci 1995; 20(5):181-7
25. Jackson JH, Li JW, Buss JE, et al. Polylysine domain of K-ras 4B protein is crucial for malignant transformation. Proc Natl Acad Sci USA 1994;91(26):12730-4
26. Anderson SM. Laboratory methods for KRAS mutation analysis. Expert Rev Mol Diagn 2011;11(6):635-42
27. Shackelford RE, Whitling NA, McNab P, et al. KRAS Testing: a Tool for the Implementation of Personalized Medicine. Genes Cancer 2012;3(7-8):459-66
28. Metzker ML. Emerging technologies in DNA sequencing. Genome Res 2005; 15(12):1767-76
29. Tsiatis AC, Norris-Kirby A, Rich RG, et al. Comparison of Sanger sequencing, pyrosequencing, and melting curve analysis for the detection of KRAS mutations: diagnostic and clinical implications. J Mol Diagn 2010;12(4):425-32
30. Dufort S, Richard MJ, de Fraipont F. Pyrosequencing method to detect KRAS mutation in formalin-fixed and paraffin-embedded tumor tissues. Analytical Biochem 2009;391(2):166-8
31. 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
32. Weichert W, Schewe C, Lehmann A, et al. KRAS genotyping of paraffin-embedded colorectal cancer tissue in routine diagnostics: comparison of methods and impact of histology. J Mol Diagn 2010; 12(1):35-42
33. Gao J, Li YY, Sun PN, Shen L. Comparative analysis of dideoxy sequencing, the KRAS StripAssay and pyrosequencing for detection of KRAS mutation. World J Gastroenterol 2010;16(38):4858-64
34. Krypuy M, Newnham GM, Thomas DM, et al. High resolution melting analysis for the rapid and sensitive detection of mutations in clinical samples: KRAS codon 12 and 13 mutations in non-small cell lung cancer. BMC Cancer 2006;6:295
35. Franklin WA, Haney J, Sugita M, et al. KRAS mutation: comparison of testing methods and tissue sampling techniques in colon cancer. J Mol Diagn 2010;12(1): 43-50
36. Ziai J, Hui P. BRAF mutation testing in clinical practice. Expert Rev Mol Diagn 2012;12(2):127-38
37. Emanuel JR, Damico C, Ahn S, et al. Highly sensitive nonradioactive single-strand conformational polymorphism. Detection of Ki-ras mutations. Diagn Mol Pathol B 1996;5(4):260-4
38. Dillon DA, Johnson CC, Topazian MD, et al. The utility of Ki-ras mutation analysis in the cytologic diagnosis of pancreatobiliary neoplasma. Cancer J 2000;6(5):294-301
39. Hayes VM, Westra JL, Verlind E, et al. New comprehensive denaturing-gradient-gelelectrophoresis assay for KRAS mutation detection applied to paraffin-embedded tumours. Genes Chromosomes Cancer 2000;29(4):309-14
40. Oliner K, Juan T, Suggs S, et al. A comparability study of 5 commercial KRAS tests. Diagnostic Pathol 2010;5:23
41. Pritchard CC, Akagi L, Reddy PL, et al. COLD-PCR enhanced melting curve analysis improves diagnostic accuracy for KRAS mutations in colorectal carcinoma. BMC Clin Pathol 2010;10:6
42. Kriegshauser G, Auner V, Schuster E, et al. KRAS mutation analysis in genomic DNA isolated from formalin-fixed paraffinembedded ovarian tissue: evaluation of a strip-based reverse-hybridisation assay. J Clin Pathol 2011;64(3):252-6
43. Ausch C, Buxhofer-Ausch V, Oberkanins C, et al. Sensitive detection of KRAS mutations in archived formalin-fixed paraffinembedded tissue using mutant-enriched PCR and reverse-hybridization. J Mol Diagn 2009;11(6):508-13
44. Whitehall V, Tran K, Umapathy A, et al. A multicenter blinded study to evaluate KRAS mutation testing methodologies in the clinical setting. J Mol Diagn 2009; 11(6):543-52
45. Forrester K, Almoguera C, Han K, et al. Detection of high incidence of K-ras oncogenes during human colon tumorigenesis. Nature 1987;327(6120): 298-303
46. Vogelstein B, Fearon ER, Hamilton SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988;319(9):525-32
47. Tan C, Du X. KRAS mutation testing in metastatic colorectal cancer. World J Gastroenterol 2012;18(37):5171-80
48. Andreyev HJ, Norman AR, Cunningham D, et al. Kirsten ras mutations in patients with colorectal cancer: the multicenter "RASCAL" study. J Natl Cancer Inst 1998;90(9):675-84
49. Andreyev HJ, Norman AR, Cunningham D, et al. Kirsten ras mutations in patients with colorectal cancer: the 'RASCAL II' study. Br J Cancer 2001;85(5):692-6
50. Roth AD, Tejpar S, Delorenzi M, 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(3):466-74
51. Ogino S, Meyerhardt JA, Irahara N, et al. KRAS mutation in stage III colon cancer and clinical outcome following intergroup trial CALGB 89803. Clin Cancer Res 2009; 15(23):7322-9
52. Lievre A, Bachet JB, Le Corre D, et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res 2006;66(8):3992-5
53. Khambata-Ford S, Garrett CR, Meropol NJ, et al. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol 2007;25(22): 3230-7
54. Di Fiore F, Blanchard F, Charbonnier F, et al. Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by Cetuximab plus chemotherapy. Br J Cancer 2007;96(8):1166-9
55. De Roock W, Piessevaux H, De Schutter J, et al. KRAS wild-type state predicts survival and is associated to early radiological response in metastatic colorectal cancer treated with cetuximab. Ann Oncol 2008; 19(3):508-15
56. Bibeau F, Frugier H, Boissiere-Michot F. [Responses to targeted therapies: colorectal cancer]. Ann Pathol 2009;29(Spec No 1): S74-6
57. Amado RG, Wolf M, Peeters M, et al. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol 2008;26(10):1626-34
58. Freeman DJ, Juan T, Reiner M, et al. Association of K-ras mutational status and clinical outcomes in patients with metastatic colorectal cancer receiving panitumumab alone. Clin Colorectal Cancer 2008;7(3): 184-90
59. Adelstein BA, Dobbins TA, Harris CA, et al. A systematic review and meta-analysis of KRAS status as the determinant of response to anti-EGFR antibodies and the impact of partner chemotherapy in metastatic colorectal cancer. Eur J Cancer 2011;47(9):1343-54
60. Karapetis CS, Khambata-Ford S, Jonker DJ, et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008;359(17):1757-65
61. Allegra CJ, Jessup JM, Somerfield MR, et al. American Society of Clinical Oncology provisional clinical opinion: testing for KRAS gene mutations in patients with metastatic colorectal carcinoma to predict response to anti-epidermal growth factor receptor monoclonal antibody therapy. J Clin Oncol 2009;27(12):2091-6
62. Engstrom PF, Arnoletti JP, Benson AB 3rd, et al. NCCN Clinical Practice Guidelines in Oncology: colon cancer. J Natl Compr Canc Netw 2009;7(8):778-831
63. Engstrom PF, Arnoletti JP, Benson AB 3rd, et al. NCCN Clinical Practice Guidelines in Oncology: rectal cancer. J Natl Compr Canc Netw 2009;7(8):838-81
64. Douillard JY, Siena S, Cassidy J, et al. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol 2010;28(31): 4697-705
65. Heinemann V, von Weikersthal LF, Decker T, et al. FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial. Lancet Oncol 2014;15(10):1065-75
66. Etienne-Grimaldi MC, Formento JL, Francoual M, et al. K-Ras mutations and treatment outcome in colorectal cancer patients receiving exclusive fluoropyrimidine therapy. Clin Cancer Res 2008;14(15): 4830-5
67. Douillard JY, Oliner KS, Siena S, et al. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med 2013;369(11):1023-34
68. De Roock W, Jonker DJ, Di Nicolantonio F, et al. Association of KRAS p.G13D mutation with outcome in patients with chemotherapy-refractory metastatic colorectal cancer treated with cetuximab. JAMA 2010;304(16):1812-20
69. Roberts PJ, Stinchcombe TE. KRAS mutation: should we test for it, and does it matter? J Clin Oncol 2013;31(8):1112-21
70. Zhu CQ, da Cunha Santos G, Ding K, et al. Role of KRAS and EGFR as biomarkers of response to erlotinib in National Cancer Institute of Canada Clinical Trials Group Study BR.21. J Clin Oncol 2008;26(26):4268-75
71. Brugger W, Triller N, Blasinska-Morawiec M, et al. Prospective molecular marker analyses of EGFR and KRAS from a randomized, placebo-controlled study of erlotinib maintenance therapy in advanced non-small-cell lung cancer. J Clin Oncol 2011;29(31):4113-20
72. Hirsch FR. K-ras mutations in lung cancer: the "mysterious mutation". Clin Lung Cancer 2006;8(1):11-12
73. Miglio U, Oldani A, Mezzapelle R, et al. KRAS mutational analysis in ductal adenocarcinoma of the pancreas and its clinical significance. Pathol Res Pract 2014; 210(5):307-11
74. Somoza AD, Aly FZ. Utility of molecular tests in cytopathology. CytoJournal 2014;11:5
75. Kipp BR, Fritcher EG, Clayton AC, et al. Comparison of KRAS mutation analysis and FISH for detecting pancreatobiliary tract cancer in cytology specimens collected during endoscopic retrograde cholangiopancreatography. J Mol Diagn 2010;12(6):780-6
76. Sturm PD, Rauws EA, Hruban RH, et al. Clinical value of K-ras codon 12 analysis and endobiliary brush cytology for the diagnosis of malignant extrahepatic bile duct stenosis. Clin Cancer Res 1999;5(3):629-35
77. Cai G, Mahooti S, Lipata FM, et al. Diagnostic value of K-ras mutation analysis for pancreaticobiliary cytology specimens with indeterminate diagnosis. Cancer Cytopathol 2012;120(5):313-18
78. Nikiforov YE. Molecular diagnostics of thyroid tumors. Arch Pathol Lab Med 2011;135(5):569-77
79. Garcia-Rostan G, Zhao H, Camp RL, et al. ras mutations are associated with aggressive tumor phenotypes and poor prognosis in thyroid cancer. J Clin Oncol 2003;21(17): 3226-35
80. Shih Ie M, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 2004;164(5):1511-18
81. Singer G, Oldt R 3rd, Cohen Y, et al. Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst 2003;95(6): 484-6
82. Ratner E, Lu L, Boeke M, et al. A KRAS-variant in ovarian cancer acts as a genetic marker of cancer risk. Cancer Res 2010;70(16):6509-15
83. Alomari A, Abi-Raad R, Buza N, Hui P. Frequent KRAS mutation in complex mucinous epithelial lesions of the endometrium. Mod Pathol 2014;27(5): 675-80
84. Ip PP, Irving JA, McCluggage WG, et al. Papillary proliferation of the endometrium: a clinicopathologic study of 59 cases of simple and complex papillae without cytologic atypia. Am J Surg Pathol 2013; 37(2):167-77
85. Xiong J, He M, Jackson C, et al. Endometrial carcinomas with significant mucinous differentiation associated with higher frequency of k-ras mutations: a morphologic and molecular correlation study. Int J Gynecol Cancer 2013;23(7): 1231-6
86. Birkeland E, Wik E, Mjos S, et al. KRAS gene amplification and overexpression but not mutation associates with aggressive and metastatic endometrial cancer. Br J Cancer 2012;107(12):1997-2004
87. Agarwal A, Eide CA, Harlow A, et al. An activating KRAS mutation in imatinib-resistant chronic myeloid leukemia. Leukemia 2008;22(12):2269-72
88. Holdhoff M, Schmidt K, Donehower R, Diaz LA Jr. Analysis of circulating tumor DNA to confirm somatic KRAS mutations. J Natl Cancer Inst 2009;101(18):1284-5
89. Azuara D, Ginesta MM, Gausachs M, et al. Nanofluidic digital PCR for KRAS mutation detection and quantification in gastrointestinal cancer. Clin Chem 2012; 58(9):1332-41
90. Zhou B, Irwanto A, Guo YM, et al. Exome sequencing and digital PCR analyses reveal novel mutated genes related to the metastasis of pancreatic ductal adenocarcinoma. Cancer Biol Ther 2012; 13(10):871-9
91. Arcila M, Lau C, Nafa K, Ladanyi M. Detection of KRAS and BRAF mutations in colorectal carcinoma roles for high-sensitivity locked nucleic acid-PCR sequencing and broad-spectrum mass spectrometry genotyping. J Mol Diagn 2011;13(1):64-73
92. de Biase D, Visani M, Baccarini P, et al. Next generation sequencing improves the accuracy of KRAS mutation analysis in endoscopic ultrasound fine needle aspiration pancreatic lesions. PLoS One 2014;9(2): e87651
93. Altimari A, de Biase D, De Maglio G, et al. 454 next generation-sequencing outperforms allele-specific PCR, Sanger sequencing, and pyrosequencing for routine KRAS mutation analysis of formalin-fixed, paraffin-embedded samples. OncoTargets Ther 2013;6:1057-64