Lessons in practicing cancer genomics and precision medicine

References

• Green ED, Guyer MS. National human genome research I. Charting a Course for Genomic Medicine from Base Pairs to Bedside. Nature. 2011;470(7333):204–213.
   Google Scholar
• Schnipper LE, Davidson NE, Wollins DS, et al. American society of clinical oncology statement: a conceptual framework to assess the value of cancer treatment options. J Clin Oncol. 2015;33(23):2563–2577.
   PubMed Web of Science ®Google Scholar
• de Klein A, van Kessel AG, Grosveld G, et al. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1982;300(5894):765–767.
   PubMed Web of Science ®Google Scholar
• Heinrich MC, Corless CL, Demetri GD, et al. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J Clin Oncol. 2003;21(23):4342–4349.
   PubMed Web of Science ®Google Scholar
• Chapman PB, Hauschild A, Robert C, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364(26):2507–2516.
   PubMed Web of Science ®Google Scholar
• 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(21):2129–2139.
   PubMed Web of Science ®Google Scholar
• Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med. 2010;363(18):1693–1703.
   PubMed Web of Science ®Google Scholar
• Djalalov S, Beca J, Hoch JS, et al. Cost effectiveness of EML4-ALK fusion testing and first-line crizotinib treatment for patients with advanced ALK-positive non-small-cell lung cancer. J Clin Oncol. 2014;32(10):1012–1019.
   PubMed Web of Science ®Google Scholar
• Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med. 2005;353(2):123–132.
   PubMed Web of Science ®Google Scholar
• Hancock L. The inhibition of anaplastic lymphoma kinase in non-small cell lung tumours with the ALK rearrangement may result in tumour shrinkage. Thorax. 2011;66(4):332.
   PubMedGoogle Scholar
• Janne PA, Wang X, Socinski MA, et al. Randomized phase ii trial of erlotinib alone or with carboplatin and paclitaxel in patients who were never or light former smokers with advanced lung adenocarcinoma: CALGB 30406 Trial. J Clin Oncol. 2012;30(17):2063–2069.
   PubMed Web of Science ®Google Scholar
• D’Angelo SP, Pietanza MC, Johnson ML, et al. Incidence of EGFR exon 19 deletions and L858R in tumor specimens from men and cigarette smokers with lung adenocarcinomas. J Clin Oncol. 2011;29(15):2066–2070.
   PubMed Web of Science ®Google Scholar
• Mok TS, Wu Y, Thongprasert S, et al. Gefitinib or carboplatin–paclitaxel in pulmonary adenocarcinoma. N Eng J Med. 2009;361:947–957.
   PubMed Web of Science ®Google Scholar
• Buettner R, Wolf J, Thomas RK. Lessons learned from lung cancer genomics: the emerging concept of individualized diagnostics and treatment. J Clin Oncol. 2013;31(15):1858–1865.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Kim DW, Mehra R, et al. Ceritinib in ALK-rearranged non-small-cell lung cancer. N Engl J Med. 2014;370(13):1189–1197.
   PubMed Web of Science ®Google Scholar
• Collisson EA, Cho RJ, Gray JW. What are we learning from the cancer genome? Nat Rev Clin Oncol. 2012;9(11):621–630.
   PubMed Web of Science ®Google Scholar
• Sherman RE, Li J, Shapley S, et al. Expediting drug development–the FDA’s new “breakthrough therapy” designation. N Engl J Med. 2013;369(20):1877–1880.
   PubMed Web of Science ®Google Scholar
• Sleijfer S, Bogaerts J, Siu LL. Designing transformative clinical trials in the cancer genome era. J Clin Oncol. 2013;31(15):1834–1841.
   PubMed Web of Science ®Google Scholar
• Es K, Rs H, Wistuba II, et al. The BATTLE trial: personalizing therapy for lung cancer. Cancer Discov. 2011;1(1):44–53.
   PubMed Web of Science ®Google Scholar
• Barker AD, Sigman CC, Kelloff GJ, et al. I-SPY 2: an adaptive breast cancer trial design in the setting of neoadjuvant chemotherapy. Clin Pharmacol Ther. 2009;86(1):97–100.
   PubMed Web of Science ®Google Scholar
• Dienstmann R, Rodon J, Barretina J, et al. genomic medicine frontier in human solid tumors: prospects and challenges. J Clin Oncol. 2013;31(15):1874–1884.
   PubMed Web of Science ®Google Scholar
• Steuer CE, Papadimitrakopoulou V, Herbst RS, et al. innovative clinical trials: the lung-map study. Clin Pharmacol Ther. 2015;97(5):488–491.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Gandara DR, Hirsch FR, et al. Lung master protocol (Lung-MAP)-A biomarker-driven protocol for accelerating development of therapies for squamous cell lung cancer: SWOG S1400. Clin Cancer Res. 2015;21(7):1514–1524.
   PubMed Web of Science ®Google Scholar
• R RE H, LaVange L, Abrams J, et al. Design of a disease-specific master protocol. Available from URL: http://www.focr.org/sites/default/files/CCCR12MasterProtocol.pdf [accessed 2016 May 19.
   Google Scholar
• Kazandjian D, Khozin S, Blumenthal G, et al. Benefit-risk summary of nivolumab for patients with metastatic squamous cell lung cancer after platinum-based chemotherapy: a report from the us food and drug administration. JAMA Oncol. 2016;2(1):118–122.
   PubMed Web of Science ®Google Scholar
• Lung-MAP. New Schema for Web. Available from URL: http://lung-map.org/sites/default/files/New%20Schema%20for%20Web.png [accessed 2016 May 24
   Google Scholar
• Kaplan R, Maughan T, Crook A, et al. Evaluating many treatments and biomarkers in oncology: a new design. J Clin Oncol. 2013;31(36):4562–4568.
   PubMed Web of Science ®Google Scholar
• Richman SD, Adams R, Quirke P, et al. Pre-trial inter-laboratory analytical validation of the FOCUS4 personalised therapy trial. J Clin Pathol. 2016;69(1):35–41.
   PubMed Web of Science ®Google Scholar
• Lopez-Chavez A, Thomas A, Rajan A, et al. Molecular profiling and targeted therapy for advanced thoracic malignancies: a biomarker-derived, multiarm, multihistology phase II basket trial. J Clin Oncol. 2015;33(9):1000–1007.
   PubMed Web of Science ®Google Scholar
• Massard C, Michiels S, Ferte C, et al. High-throughput genomics and clinical outcome in hard-to-treat advanced cancers: results of the MOSCATO 01 Trial. Cancer Disc. 2017;7(6):586–595.
   Web of Science ®Google Scholar
• Hainsworth JD, Meric-Bernstam F, Swanton C, et al. Targeted therapy for advanced solid tumors on the basis of molecular profiles: results from mypathway, an open-label, phase iia multiple basket study. J Clin Oncol. 2017;36(6):536–542.
   Web of Science ®Google Scholar
• Slosberg ED, Kang BP, Peguero J, et al. Signature program: a platform of basket trials. Oncotarget. 2018;9(30):21383–21395.
   PubMedGoogle Scholar
• Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science. 2013;339(6127):1546–1558.
   PubMed Web of Science ®Google Scholar
• Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature. 2009;458(7239):719–724.
   PubMed Web of Science ®Google Scholar
• Bozic I, Antal T, Ohtsuki H, et al. Accumulation of driver and passenger mutations during tumor progression. Proc Natl Acad Sci U S A. 2010;107(43):18545–18550.
   PubMed Web of Science ®Google Scholar
• Campbell PJ, Yachida S, Mudie LJ, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature. 2010;467(7319):1109–1113.
   PubMed Web of Science ®Google Scholar
• Yachida S, Jones S, Bozic I, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010;467(7319):1114–1117.
   PubMed Web of Science ®Google Scholar
• Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366(10):883–892.
   PubMed Web of Science ®Google Scholar
• Vandin F, Upfal E, Raphael BJ. De novo discovery of mutated driver pathways in cancer. Genome Res. 2012;22(2):375–385.
   PubMed Web of Science ®Google Scholar
• Miller DG. On the nature of susceptibility to cancer. The Presidential Address. Cancer. 1980;46(6):1307–1318.
   Google Scholar
• Personalizing Oncology: MJ. Perspectives and Prospects. J Clin Oncol. 2013;31(15):1904–1911.
   PubMed Web of Science ®Google Scholar
• Messersmith WA, Ahnen DJ. Targeting EGFR in colorectal cancer. N Engl J Med. 2008;359(17):1834–1836.
   PubMed Web of Science ®Google Scholar
• Macconaill LE, Van Hummelen P, Meyerson M, et al. Clinical implementation of comprehensive strategies to characterize cancer genomes: opportunities and challenges. Cancer Discov. 2011;1(4):297.
   PubMed Web of Science ®Google Scholar
• Meric-Bernstam F, Farhangfar C, Mendelsohn J, et al. Building a personalized medicine infrastructure at a major cancer center. J Clin Oncol. 2013.
   Web of Science ®Google Scholar
• Cristofanilli M, Budd GT, Ellis MJ, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 2004;351(8):781–791.
   PubMed Web of Science ®Google Scholar
• Bettegowda C, Sausen M, Leary RJ, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 2014;6(224):224ra224.
   Web of Science ®Google Scholar
• Crowley E, Di Nicolantonio F, Loupakis F, et al. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013;10(8):472–484.
   PubMed Web of Science ®Google Scholar
• Karachaliou N, Mayo-de-Las-Casas C, Molina-Vila MA, et al. Real-time liquid biopsies become a reality in cancer treatment. Ann Transl Med. 2015;3(3):36.
   PubMed Web of Science ®Google Scholar
• Oxnard GR, Thress KS, Alden RS, et al. Association between plasma genotyping and outcomes of treatment with osimertinib (AZD9291) in advanced non-small-cell lung cancer. J Clin Oncol. 2016;34(28):3375–3382.
   PubMed Web of Science ®Google Scholar
• Williams PM, Conley BA. Clinical application of liquid biopsies. JAMA Oncol. 2016;2(8):1003–1005.
   PubMed Web of Science ®Google Scholar
• Fribbens C, O’Leary B, Kilburn L, et al. Plasma ESR1 mutations and the treatment of estrogen receptor-positive advanced breast cancer. J Clin Oncol. 2016;34(25):2961–2968.
   PubMed Web of Science ®Google Scholar
• Kuderer NM, Burton KA, Blau S, et al. Comparison of 2 commercially available next-generation sequencing platforms in oncology. JAMA Oncol. 2016;3(7):996-998.
   Web of Science ®Google Scholar
• Reddy KB. Triple-negative breast cancers: an updated review on treatment options. Curr Oncol. 2011;18(4):e173–179.
   PubMed Web of Science ®Google Scholar
• Carey LA. Directed therapy of subtypes of triple-negative breast cancer. Oncologist. 2011;16(Suppl 1):71–78.
   PubMedGoogle Scholar
• Telli M, Jensen K, Abkevich V, et al. Homologous Recombination Deficiency (HRD) score predicts pathologic response following neoadjuvant platinum-based therapy in triple-negative and BRCA 1/2 mutation-associated breast cancer. Cancer Res. 2012;72(24Suppl):Abstr PD09–04.
   Google Scholar
• Duffy MJ, McGowan PM, Crown J. Targeted therapy for triple-negative breast cancer: where are we? Int J Cancer. 2012;131(11):2471–2477.
   PubMed Web of Science ®Google Scholar
• Prat A, Adamo B, Cheang MC, et al. Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist. 2013;18(2):123–133.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Baas P, Kim DW, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet. 2015;387(10027):1540–1550.
   PubMed Web of Science ®Google Scholar
• Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch repair deficiency. J Clin Oncol. 2015;33(suppl):abstr LBA100.
   Google Scholar
• Rizvi H, Sanchez-Vega F, La K, et al. Molecular determinants of response to anti-programmed cell death (PD)-1 and anti-programmed death-ligand 1 (PD-L1) blockade in patients with non-small-cell lung cancer profiled with targeted next-generation sequencing. J Clin Oncol. 2018;36(7):633–641.
   PubMed Web of Science ®Google Scholar
• Goodman AM, Kato S, Bazhenova L, et al. Tumor mutational burden as an independent predictor of response to immunotherapy in diverse cancers. Mol Cancer Ther. 2017;16(11):2598–2608.
   PubMed Web of Science ®Google Scholar
• Steuer CE, Ramalingam SS. Tumor Mutation Burden: leading Immunotherapy to the Era of Precision Medicine? J Clin Oncol. 2018;36(7):631–632.
   PubMed Web of Science ®Google Scholar
• Carbone DP, Reck M, Paz-Ares L, et al. First-line nivolumab in stage iv or recurrent non-small-cell lung cancer. N Engl J Med. 2017;376(25):2415–2426.
   PubMed Web of Science ®Google Scholar
• Deenen MJ, Cats A, Beijnen JH, et al. Part 1: background, methodology, and clinical adoption of pharmacogenetics. Oncologist. 2011;16(6):811–819.
   PubMed Web of Science ®Google Scholar
• Innocenti F, Undevia SD, Iyer L, et al. Genetic variants in the UDP-glucuronosyltransferase 1A1 gene predict the risk of severe neutropenia of irinotecan. J Clin Oncol. 2004;22(8):1382–1388.
   PubMed Web of Science ®Google Scholar
• Hoskins JM, Goldberg RM, Qu P, et al. UGT1A1*28 genotype and irinotecan-induced neutropenia: dose matters. J Natl Cancer Inst. 2007;99(17):1290–1295.
   PubMedGoogle Scholar
• Diasio RB, Johnson MR. Dihydropyrimidine dehydrogenase: its role in 5-fluorouracil clinical toxicity and tumor resistance. Clin Cancer Res. 1999;5(10):2672–2673.
   PubMed Web of Science ®Google Scholar
• Schwab M, Zanger UM, Marx C, et al. Role of genetic and nongenetic factors for fluorouracil treatment-related severe toxicity: a prospective clinical trial by the German 5-FU Toxicity Study Group. J Clin Oncol. 2008;26(13):2131–2138.
   PubMed Web of Science ®Google Scholar
• Deenen MJ, Meulendijks D, Cats A, et al. Upfront genotyping of DPYD*2A to individualize fluoropyrimidine therapy: a safety and cost analysis. J Clin Oncol. 2016;34(3):227–234.
   PubMed Web of Science ®Google Scholar
• Goetz MP, Suman VJ, Hoskin TL, et al. CYP2D6 metabolism and patient outcome in the austrian breast and colorectal cancer study group trial (ABCSG) 8. Clin Cancer Res. 2013;19(2):500–507.
   PubMed Web of Science ®Google Scholar
• Schroth W, Hamann U, Fasching PA, et al. CYP2D6 polymorphisms as predictors of outcome in breast cancer patients treated with tamoxifen: expanded polymorphism coverage improves risk stratification. Clin Cancer Res. 2010;16(17):4468–4477.
   PubMed Web of Science ®Google Scholar
• Irvin WJ Jr., Walko CM, Weck KE, et al. Genotype-guided tamoxifen dosing increases active metabolite exposure in women with reduced CYP2D6 metabolism: a multicenter study. J Clin Oncol. 2011;29(24):3232–3239.
   PubMed Web of Science ®Google Scholar
• McLeod HL, Krynetski EY, Relling MV, et al. Genetic polymorphism of thiopurine methyltransferase and its clinical relevance for childhood acute lymphoblastic leukemia. Leukemia. 2000;14(4):567–572.
   PubMed Web of Science ®Google Scholar
• Relling MV, Hancock ML, Rivera GK, et al. Mercaptopurine therapy intolerance and heterozygosity at the thiopurine S-methyltransferase gene locus. J Natl Cancer Inst. 1999;91(23):2001–2008.
   PubMedGoogle Scholar
• Stanulla M, Schaeffeler E, Flohr T, et al. Thiopurine methyltransferase (TPMT) genotype and early treatment response to mercaptopurine in childhood acute lymphoblastic leukemia. JAMA. 2005;293(12):1485–1489.
   PubMed Web of Science ®Google Scholar
• Amstutz U, Henricks LM, Offer SM, et al. Clinical Pharmacogenetics Implementation Consortium (CPIC) Guideline for Dihydropyrimidine Dehydrogenase Genotype and Fluoropyrimidine Dosing: 2017 Update. Clin Pharmacol Ther. 2018;103(2):210–216.
   PubMed Web of Science ®Google Scholar
• Goetz MP, Sangkuhl K, Guchelaar HJ, et al. Clinical Pharmacogenetics Implementation Consortium (CPIC) Guideline for CYP2D6 and Tamoxifen Therapy. Clin Pharmacol Ther. 2018;103(5):770–777.
   PubMed Web of Science ®Google Scholar
• Relling MV, Gardner EE, Sandborn WJ, et al. Clinical pharmacogenetics implementation consortium guidelines for thiopurine methyltransferase genotype and thiopurine dosing: 2013 update. Clin Pharmacol Ther. 2013;93(4):324–325.
   PubMed Web of Science ®Google Scholar
• Garraway LA. Genomics-Driven Oncology: framework for an Emerging Paradigm. J Clin Oncol. 2013;31(15):1806–1814.
   PubMed Web of Science ®Google Scholar
• McWhinney SR, McLeod HL. Using germline genotype in cancer pharmacogenetic studies. Pharmacogenomics. 2009;10(3):489–493.
   PubMed Web of Science ®Google Scholar
• Ratain MJ, Nakamura Y, Cox NJ. CYP2D6 genotype and tamoxifen activity: understanding interstudy variability in methodological quality. Clin Pharmacol Ther. 2013;94(2):185–187.
   PubMed Web of Science ®Google Scholar
• Green RC, Berg JS, Grody WW, et al. ACMG recommendations for reporting of incidental findings in clinical exome and genome sequencing. Genet Med. 2013;15(7):565–574.
   PubMed Web of Science ®Google Scholar
• ACMG. Board of Directors. ACMG policy statement: updated recommendations regarding analysis and reporting of secondary findings in clinical genome-scale sequencing. Genet Med. 2015;17:68–69.
   PubMedGoogle Scholar
• Robson ME, Bradbury AR, Arun B, et al. American Society of Clinical Oncology Policy Statement Update: genetic and Genomic Testing for Cancer Susceptibility. J Clin Oncol. 2015;33(31):3660–3667.
   PubMed Web of Science ®Google Scholar
• Hinman LM, Carl KM, Spear BB, et al. Development and regulatory strategies for drug and diagnostic co-development. Pharmacogenomics. 2010;11(12):1669–1675.
   PubMed Web of Science ®Google Scholar
• Shah A, Stewart AK, Kolacevski A, et al. Building a rapid learning health care system for oncology: why cancerlinq collects identifiable health information to achieve its vision. J Clin Oncol. 2016;34(7):756:763.
   Web of Science ®Google Scholar
• Abernethy AP, Etheredge LM, Ganz PA, et al. Rapid-learning system for cancer care. J Clin Oncol. 2010;28(27):4268–4274.
   PubMed Web of Science ®Google Scholar
• Scheuner MT, de Vries H, Kim B, et al. Are electronic health records ready for genomic medicine?. Genet Med. 2009;11(7):510–517.
   PubMed Web of Science ®Google Scholar
• Overby CL, Kohane I, Kannry JL, et al. Opportunities for genomic clinical decision support interventions. Genet Med. 2013;15(10):817–823.
   PubMed Web of Science ®Google Scholar
• Stanek EJ, Sanders CL, Taber KA, et al. Adoption of pharmacogenomic testing by US physicians: results of a nationwide survey. Clin Pharmacol Ther. 2012;91(3):450–458.
   PubMed Web of Science ®Google Scholar
• Kohane IS. Using electronic health records to drive discovery in disease genomics. Nat Rev Genet. 2011;12(6):417–428.
   PubMed Web of Science ®Google Scholar
• Hudson KL. Genomics, health care, and society. N Engl J Med. 2011;365(11):1033–1041.
   PubMed Web of Science ®Google Scholar
• Harada S, Arend R, Dai Q, et al. Implementation and utilization of the molecular tumor board to guide precision medicine. Oncotarget. 2017;8(34):57845–57854.
   PubMedGoogle Scholar
• Tafe LJ, Gorlov IP, de Abreu FB, et al. Implementation of a molecular tumor board: the impact on treatment decisions for 35 patients evaluated at dartmouth-hitchcock medical center. Oncologist. 2015;20(9):1011–1018.
   PubMed Web of Science ®Google Scholar
• Burkard ME, Deming DA, Parsons BM, et al. Implementation and clinical utility of an integrated academic-community regional molecular tumor board. JCO Precis Oncol. 2017(1):1–10
   Google Scholar
• Schwaederle M, Parker BA, Schwab RB, et al. Molecular tumor board: the university of california-san diego moores cancer center experience. Oncologist. 2014;19(6):631–636.
   PubMed Web of Science ®Google Scholar
• Knepper TC, Bell GC, Hicks JK, et al. Key lessons learned from moffitt’s molecular tumor board: the clinical genomics action committee experience. Oncologist. 2017;22(2):144–151.
   PubMed Web of Science ®Google Scholar
• Perera-Bel J, Hutter B, Heining C, et al. From somatic variants towards precision oncology: evidence-driven reporting of treatment options in molecular tumor boards. Genome Med. 2018;10(1):18.
   PubMedGoogle Scholar
• Schwaederle M, Zhao M, Jj L, et al. Association of biomarker-based treatment strategies with response rates and progression-free survival in refractory malignant neoplasms: a meta-analysis. JAMA Oncol. 2016;2(11):1452–1459.
   PubMed Web of Science ®Google Scholar
• Schwaederle M, Zhao M, Jj L, et al. Impact of precision medicine in diverse cancers: a meta-analysis of phase ii clinical trials. J Clin Oncol. 2015;33(32):3817–3825.
   PubMed Web of Science ®Google Scholar
• Micheel CM, Sweeney SM, LeNoue-Newton ML, et al. American association for cancer research project genomics evidence neoplasia information exchange: from inception to first data release and beyond—lessons learned and member institutions’ perspectives. JCO Clin Canc Inform. 2018.
   Google Scholar