Epistatic interactions and drug response

Journal of Pathology

Volumn 232, Issue 2, 2014, Pages 255-263

  Weigelt, Britta ^a   Reis Filho, Jorge S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

epistasis; genetic interaction; genotype; massively parallel sequencing; mutation; precision medicine; targeted therapy

Indexed keywords

B RAF KINASE; BCR ABL PROTEIN; BRCA1 PROTEIN; CRIZOTINIB; DASATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GEFITINIB; IMATINIB; LAPATINIB; NERATINIB; NILOTINIB; OLAPARIB; PERTUZUMAB; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; RAS PROTEIN; RUCAPARIB; SCATTER FACTOR RECEPTOR; SUNITINIB; TRASTUZUMAB; VANDETANIB; VELIPARIB; VEMURAFENIB;

BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GENETICS; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL (TOPIC); DISEASE COURSE; DRUG RESPONSE; EPISTASIS; FEEDBACK SYSTEM; GASTROINTESTINAL STROMAL TUMOR; GENE AMPLIFICATION; GENE INTERACTION; GENE MUTATION; GENETIC HETEROGENEITY; GENETIC SCREENING; GENETIC VARIABILITY; GENOTYPE; GLIOBLASTOMA; HUMAN; INDEL MUTATION; INFLAMMATORY INFILTRATE; LUNG CANCER; LUNG NON SMALL CELL CANCER; MELANOMA; MICROSATELLITE INSTABILITY; OVARY CANCER; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; THYROID CANCER; TREATMENT RESPONSE; TUMOR GENE; TUMOR MICROENVIRONMENT;

EPISTASIS; GENETIC INTERACTION; GENOTYPE; MASSIVELY PARALLEL SEQUENCING; MUTATION; PRECISION MEDICINE; TARGETED THERAPY;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; EPIGENESIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; GENOMICS; HUMANS; INDIVIDUALIZED MEDICINE; MOLECULAR TARGETED THERAPY; NEOPLASMS; PHENOTYPE; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84890282746     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4265     Document Type: Review

References (93)

1. The Cancer Genome Atlas. National Cancer Institute; National Human Genome Research Institute. [Accessed 10 September 2013]. Available from: http://cancergenome.nih.gov/
2. Hudson TJ, Anderson W, Artez A, et al., International network of cancer genome projects. Nature 2010; 464: 993-998.
3. Ledford H., Big science: the cancer genome challenge. Nature 2010; 464: 972-974.
4. Meyerson M, Gabriel S, Getz G,. Advances in understanding cancer genomes through second-generation sequencing. Nature Rev Genet 2010; 11: 685-696.
5. Haber DA, Gray NS, Baselga J,. The evolving war on cancer. Cell 2011; 145: 19-24.
6. Chin L, Andersen JN, Futreal PA,. Cancer genomics: from discovery science to personalized medicine. Nature Med 2011; 17: 297-303.
7. Garraway LA, Lander ES,. Lessons from the cancer genome. Cell 2013; 153: 17-37.
8. Basu A, Bodycombe NE, Cheah JH, et al., An interactive resource to identify cancer genetic and lineage dependencies targeted by small molecules. Cell 2013; 154: 1151-1161.
9. Vogel CL, Cobleigh MA, Tripathy D, et al., Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 2002; 20: 719-726.
10. Sordella R, Bell DW, Haber DA, et al., Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004; 305: 1163-1167.
11. Pao W, Miller V, Zakowski M, et al., EGF receptor gene mutations are common in lung cancers from 'never smokers' and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A 2004; 101: 13306-13311.
12. Lynch TJ, Bell DW, Sordella R, et al., Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-2139.
13. Weigelt B, Pusztai L, Ashworth A, et al., Challenges translating breast cancer gene signatures into the clinic. Nature Rev Clin Oncol 2012; 9: 58-64.
14. Garnett MJ, Edelman EJ, Heidorn SJ, et al., Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012; 483: 570-575.
15. Barretina J, Caponigro G, Stransky N, et al., The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483: 603-607.
16. Heravi-Moussavi A, Anglesio MS, Cheng SW, et al., Recurrent somatic DICER1 mutations in nonepithelial ovarian cancers. N Engl J Med 2012; 366: 234-242.
17. Shah SP, Roth A, Goya R, et al., The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012; 486: 395-399.
18. Wiegand KC, Shah SP, Al-Agha OM, et al., ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 2010; 363: 1532-1543.
19. Demetri GD, von Mehren M, Blanke CD, et al., Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002; 347: 472-480.
20. Duensing A, Heinrich MC, Fletcher CD, et al., Biology of gastrointestinal stromal tumors: KIT mutations and beyond. Cancer Invest 2004; 22: 106-116.
21. Bollag G, Hirth P, Tsai J, et al., Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature 2010; 467: 596-599.
22. Chapman PB, Hauschild A, Robert C, et al., Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011; 364: 2507-2516.
23. Garraway LA, Janne PA,. Circumventing cancer drug resistance in the era of personalized medicine. Cancer Discov 2012; 2: 214-226.
24. Prahallad A, Sun C, Huang S, et al., Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012; 483: 100-103.
25. The Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
26. Kandoth C, Schultz N, Cherniack AD, et al., Integrated genomic characterization of endometrial carcinoma. Nature 2013; 497: 67-73.
27. Crockford A, Jamal-Hanjani M, Hicks J, et al. Implications of intratumour heterogeneity for treatment stratification. J Pathol 2013; 232: 264-273.
28. Weinstein IB. Cancer. Addiction to oncogenes-the Achilles heal of cancer. Science 2002; 297: 63-64.
29. Geyer CE, Forster J, Lindquist D, et al., Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006; 355: 2733-2743.
30. Bose R, Kavuri SM, Searleman AC, et al., Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov 2013; 3: 224-237.
31. Montemurro F, Scaltriti M,. Biomarkers of drugs targeting HER-family signaling in cancer. J Pathol 2013; 232: 219-229.
32. Weigelt B, Reis-Filho JS,. Activating mutations in HER2: neu opportunities and neu challenges. Cancer Discov 2013; 3: 145-147.
33. Salesse S, Verfaillie CM,. BCR/ABL: from molecular mechanisms of leukemia induction to treatment of chronic myelogenous leukemia. Oncogene 2002; 21: 8547-8559.
34. Antonescu CR, Besmer P, Guo T, et al., Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 2005; 11: 4182-4190.
35. Shah NP, Nicoll JM, Nagar B, et al., Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2002; 2: 117-125.
36. Mitelman F, Johansson B, Mertens F,. The impact of translocations and gene fusions on cancer causation. Nature Rev Cancer 2007; 7: 233-245.
37. Chinnaiyan AM, Palanisamy N,. Chromosomal aberrations in solid tumors. Prog Mol Biol Transl Sci 2010; 95: 55-94.
38. Shah SP, Kobel M, Senz J, et al., Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med 2009; 360: 2719-2729.
39. Ashworth A, Lord CJ, Reis-Filho JS,. Genetic interactions in cancer progression and treatment. Cell 2011; 145: 30-38.
40. The Cancer Genome Atlas Network. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489: 519-525.
41. Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415-421.
42. Stephens PJ, McBride DJ, Lin ML, et al., Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009; 462: 1005-1010.
43. Banerji S, Cibulskis K, Rangel-Escareno C, et al., Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 2012; 486: 405-409.
44. Stephens PJ, Tarpey PS, Davies H, et al., The landscape of cancer genes and mutational processes in breast cancer. Nature 2012; 486: 400-404.
45. Parker JS, Mullins M, Cheang MC, et al., Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27: 1160-1167.
46. Perou CM, Sorlie T, Eisen MB, et al., Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
47. Weigelt B, Mackay A, A'Hern R, et al., Breast cancer molecular profiling with single sample predictors a retrospective analysis. Lancet Oncol 2010; 11: 339-349.
48. Mackay A, Weigelt B, Grigoriadis A, et al., Microarray-based class discovery for molecular classification of breast cancer: analysis of interobserver agreement. J Natl Cancer Inst 2011; 103: 662-673.
49. Reis-Filho JS, Pusztai L,. Gene expression profiling in breast cancer: classification, prognostication, and prediction. Lancet 2011; 378: 1812-1823.
50. Pao W, Girard N,. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011; 12: 175-180.
51. Pao W, Hutchinson KE,. Chipping away at the lung cancer genome. Nature Med 2012; 18: 349-351.
52. Kosaka T, Yatabe Y, Endoh H, et al., Mutations of the epidermal growth factor receptor gene in lung cancer: biological and clinical implications. Cancer Res 2004; 64: 8919-8923.
53. Riely GJ, Politi KA, Miller VA, et al., Update on epidermal growth factor receptor mutations in non-small cell lung cancer. Clin Cancer Res 2006; 12: 7232-7241.
54. Imielinski M, Berger AH, Hammerman PS, et al., Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012; 150: 1107-1120.
55. Yap TA, Gerlinger M, Futreal PA, et al., Intratumor heterogeneity: seeing the wood for the trees. Sci Transl Med 2012; 4: 127ps110.
56. Turner NC, Reis-Filho JS,. Genetic heterogeneity and cancer drug resistance. Lancet Oncol 2012; 13: e178-e185.
57. Bartlett AI, Starcyznski J, Robson T, et al., Heterogeneous HER2 gene amplification: impact on patient outcome and a clinically relevant definition. Am J Clin Pathol 2011; 136: 266-274.
58. Kim MA, Lee HJ, Yang HK, et al., Heterogeneous amplification of ERBB2 in primary lesions is responsible for the discordant ERBB2 status of primary and metastatic lesions in gastric carcinoma. Histopathology 2011; 59: 822-831.
59. Knudson AG Jr., Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci U S A 1971; 68: 820-823.
60. Gowen LC, Johnson BL, Latour AM, et al., Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nature Genet 1996; 12: 191-194.
61. 5-6 early embryonic lethality by p53 or p21 null mutation. Nature Genet 1997; 16: 298-302.
62. Martins FC, De S, Almendro V, et al., Evolutionary pathways in BRCA1-associated breast tumors. Cancer Discov 2012; 2: 503-511.
63. Jonsson G, Staaf J, Vallon-Christersson J, et al., The retinoblastoma gene undergoes rearrangements in BRCA1-deficient basal-like breast cancer. Cancer Res 2012; 72: 4028-4036.
64. Heidorn SJ, Milagre C, Whittaker S, et al., Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010; 140: 209-221.
65. Cerami E, Gao J, Dogrusoz U, et al., The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2: 401-404.
66. Gao J, Aksoy BA, Dogrusoz U, et al., Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013; 6: pl1.
67. Engelman JA, Zejnullahu K, Mitsudomi T, et al., MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-1043.
68. Pao W, Miller VA, Politi KA, et al., Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2: e73.
69. Turke AB, Zejnullahu K, Wu YL, et al., Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010; 17: 77-88.
70. Sequist LV, Waltman BA, Dias-Santagata D, et al., Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011; 3: 75ra26.
71. Janku F, Wheler JJ, Westin SN, et al., PI3K/AKT/mTOR inhibitors in patients with breast and gynecologic malignancies harboring PIK3CA mutations. J Clin Oncol 2012; 30: 777-782.
72. Janku F, Tsimberidou AM, Garrido-Laguna I, et al., PIK3CA mutations in patients with advanced cancers treated with PI3K/AKT/mTOR axis inhibitors. Mol Cancer Ther 2011; 10: 558-565.
73. Stemke-Hale K, Gonzalez-Angulo AM, Lluch A, et al., An integrative genomic and proteomic analysis of PIK3CA, PTEN, and AKT mutations in breast cancer. Cancer Res 2008; 68: 6084-6091.
74. Urick ME, Rudd ML, Godwin AK, et al., PIK3R1 (p85α) is somatically mutated at high frequency in primary endometrial cancer. Cancer Res 2011; 71: 4061-4067.
75. Futreal PA, Coin L, Marshall M, et al., A census of human cancer genes. Nature Rev Cancer 2004; 4: 177-183.
76. Oda K, Okada J, Timmerman L, et al., PIK3CA cooperates with other phosphatidylinositol 3'-kinase pathway mutations to effect oncogenic transformation. Cancer Res 2008; 68: 8127-8136.
77. Weigelt B, Warne PH, Lambros MB, et al., PI3K pathway dependencies in endometrioid endometrial cancer cell lines. Clin Cancer Res 2013; 19: 3533-3544.
78. Su KY, Chen HY, Li KC, et al., Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J Clin Oncol 2012; 30: 433-440.
79. Sakai W, Swisher EM, Karlan BY, et al., Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008; 451: 1116-1120.
80. Swisher EM, Sakai W, Karlan BY, et al., Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res 2008; 68: 2581-2586.
81. Edwards SL, Brough R, Lord CJ, et al., Resistance to therapy caused by intragenic deletion in BRCA2. Nature 2008; 451: 1111-1115.
82. Barber LJ, Sandhu S, Chen L, et al., Secondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitor. J Pathol 2013; 229: 422-429.
83. Norquist B, Wurz KA, Pennil CC, et al., Secondary somatic mutations restoring BRCA1/2 predict chemotherapy resistance in hereditary ovarian carcinomas. J Clin Oncol 2011; 29: 3008-3015.
84. Sullivan RJ, Flaherty KT,. Resistance to BRAF-targeted therapy in melanoma. Eur J Cancer 2013; 49: 1297-1304.
85. Straussman R, Morikawa T, Shee K, et al., Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012; 487: 500-504.
86. Shia J, Black D, Hummer AJ, et al., Routinely assessed morphological features correlate with microsatellite instability status in endometrial cancer. Hum Pathol 2008; 39: 116-125.
87. Shia J, Ellis NA, Paty PB, et al., Value of histopathology in predicting microsatellite instability in hereditary nonpolyposis colorectal cancer and sporadic colorectal cancer. Am J Surg Pathol 2003; 27: 1407-1417.
88. Singh A, Settleman J,. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741-4751.
89. Baselga J., Bringing precision medicine to the clinic: from genomic profiling to the power of clinical observation. Ann Oncol 2013; 24: 1956-1957.
90. Sleijfer S, Bogaerts J, Siu LL,. Designing transformative clinical trials in the cancer genome era. J Clin Oncol 2013; 31: 1834-1841.
91. Iyer G, Hanrahan AJ, Milowsky MI, et al., Genome sequencing identifies a basis for everolimus sensitivity. Science 2012; 338: 221.
92. Wang H, Yang H, Shivalila CS, et al., One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013; 153: 910-918.
93. Hwang WY, Fu Y, Reyon D, et al., Efficient genome editing in zebrafish using a CRISPR-Cas system. Nature Biotechnol 2013; 31: 227-229.