Deciphering intratumor heterogeneity and temporal acquisition of driver events to refine precision medicine

The presence of multiple subclones within tumors mandates understanding of longitudinal and spatial subclonal dynamics. Resolving the spatial and temporal heterogeneity of subclones with cancer driver events may offer insight into therapy response, tumor evolutionary histories and clinical trial design.

[1]  B. Frieden,et al.  Adaptive therapy. , 2009, Cancer research.

[2]  C. Swanton,et al.  Intra-tumor heterogeneity: lessons from microbial evolution and clinical implications , 2013, Genome Medicine.

[3]  P. Phillips.  Epistasis — the essential role of gene interactions in the structure and evolution of genetic systems , 2008, Nature Reviews Genetics.

[4]  Steven A. Roberts,et al.  An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers , 2013, Nature Genetics.

[5]  M. Stratton,et al.  Clinical and biological implications of driver mutations in myelodysplastic syndromes. , 2013, Blood.

[6]  Sung-Liang Yu,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. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[7]  S. Gabriel,et al.  Discovery and saturation analysis of cancer genes across 21 tumor types , 2014, Nature.

[8]  Y. Miller,et al.  Lung cancer chemoprevention: current status and future prospects , 2013, Nature Reviews Clinical Oncology.

[9]  Jun Liu,et al.  Loss of human epidermal growth factor receptor 2 (HER2) expression in metastatic sites of HER2-overexpressing primary breast tumors. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[10]  Benjamin J. Raphael,et al.  Mutational landscape and significance across 12 major cancer types , 2013, Nature.

[11]  P. A. Futreal,et al.  Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. , 2012, The New England journal of medicine.

[12]  A. Bouchard-Côté,et al.  PyClone: statistical inference of clonal population structure in cancer , 2014, Nature Methods.

[13]  Jan Bogaerts,et al.  Designing transformative clinical trials in the cancer genome era. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[14]  T. Ørntoft,et al.  Mutational context and diverse clonal development in early and late bladder cancer. , 2014, Cell reports.

[15]  M. Nowak,et al.  Distant Metastasis Occurs Late during the Genetic Evolution of Pancreatic Cancer , 2010, Nature.

[16]  Douglas A Lauffenburger,et al.  Addressing genetic tumor heterogeneity through computationally predictive combination therapy. , 2013, Cancer discovery.

[17]  A. Iafrate,et al.  Mechanisms of Acquired Crizotinib Resistance in ALK-Rearranged Lung Cancers , 2012, Science Translational Medicine.

[18]  Ali Bashashati,et al.  Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling , 2013, The Journal of pathology.

[19]  Tracy T Batchelor,et al.  A hypermutation phenotype and somatic MSH6 mutations in recurrent human malignant gliomas after alkylator chemotherapy. , 2006, Cancer research.

[20]  E. Lander,et al.  Lessons from the Cancer Genome , 2013, Cell.

[21]  A. McKenna,et al.  Evolution and Impact of Subclonal Mutations in Chronic Lymphocytic Leukemia , 2012, Cell.

[22]  J. Shih,et al.  Comparison of epidermal growth factor receptor mutations between primary and corresponding metastatic tumors in tyrosine kinase inhibitor-naive non-small-cell lung cancer. , 2009, Annals of oncology : official journal of the European Society for Medical Oncology.

[23]  Charles Swanton,et al.  Intratumor Heterogeneity: Seeing the Wood for the Trees , 2012, Science Translational Medicine.

[24]  L. Galluzzi,et al.  Molecular mechanisms of cisplatin resistance , 2012, Oncogene.

[25]  A. Børresen-Dale,et al.  The Life History of 21 Breast Cancers , 2012, Cell.

[26]  Jian Li,et al.  Temporal dissection of tumorigenesis in primary cancers. , 2011, Cancer discovery.

[27]  N. McGranahan,et al.  The causes and consequences of genetic heterogeneity in cancer evolution , 2013, Nature.

[28]  K. Anderson,et al.  Genetic variegation of clonal architecture and propagating cells in leukaemia , 2011, Nature.

[29]  V. P. Collins,et al.  Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics , 2013, Proceedings of the National Academy of Sciences.

[30]  E. Antonarakis,et al.  Evolving standards in the treatment of docetaxel-refractory castration-resistant prostate cancer , 2011, Prostate Cancer and Prostatic Diseases.

[31]  G. Parmigiani,et al.  Heterogeneity of genomic evolution and mutational profiles in multiple myeloma , 2014, Nature Communications.

[32]  E. Felip,et al.  Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. , 2012, The Lancet. Oncology.

[33]  P. Johnston,et al.  Cancer drug resistance: an evolving paradigm , 2013, Nature Reviews Cancer.

[34]  Irmtraud M. Meyer,et al.  The clonal and mutational evolution spectrum of primary triple-negative breast cancers , 2012, Nature.

[35]  Dennis C. Friedrich,et al.  MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. , 2014, Cancer discovery.

[36]  James Hicks,et al.  Tracing the tumor lineage , 2010, Molecular oncology.

[37]  P. Jänne,et al.  The road to resistance: EGFR mutation and cetuximab , 2012, Nature Medicine.

[38]  Steven J. M. Jones,et al.  Mutational Analysis Reveals the Origin and Therapy-Driven Evolution of Recurrent Glioma , 2014, Science.

[39]  S. Swamy,et al.  PICNIC: an algorithm to predict absolute allelic copy number variation with microarray cancer data , 2009, Biostatistics.

[40]  Christophe Lemetre,et al.  Predictive Performance of Microarray Gene Signatures: Impact of Tumor Heterogeneity and Multiple Mechanisms of Drug Resistance , 2014 .

[41]  K. Schaefer,et al.  Prevalence and Heterogeneity of KRAS, BRAF, and PIK3CA Mutations in Primary Colorectal Adenocarcinomas and Their Corresponding Metastases , 2010, Clinical Cancer Research.

[42]  Yi-long Wu,et al.  Relative abundance of EGFR mutations predicts benefit from gefitinib treatment for advanced non-small-cell lung cancer. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[43]  Luca Toschi,et al.  Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. , 2010, Cancer cell.

[44]  S. Digumarthy,et al.  Genotypic and Histological Evolution of Lung Cancers Acquiring Resistance to EGFR Inhibitors , 2011, Science Translational Medicine.

[45]  A. Sivachenko,et al.  Punctuated Evolution of Prostate Cancer Genomes , 2013, Cell.

[46]  K. Kinzler,et al.  Detection and quantification of rare mutations with massively parallel sequencing , 2011, Proceedings of the National Academy of Sciences.

[47]  N. Potter,et al.  Single-cell genetic analysis reveals the composition of initiating clones and phylogenetic patterns of branching and parallel evolution in myeloma , 2014, Leukemia.

[48]  K. Lim,et al.  Clinical significance of heterogeneity in response to retreatment with epidermal growth factor receptor tyrosine kinase inhibitors in patients with lung cancer acquiring secondary resistance to the drug. , 2014, Clinical lung cancer.

[49]  J. Hicks,et al.  Assessing the order of critical alterations in prostate cancer development and progression by IHC: further evidence that PTEN loss occurs subsequent to ERG gene fusion , 2013, Prostate Cancer and Prostatic Diseases.

[50]  Johannes G. Reiter,et al.  The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers , 2012, Nature.

[51]  M. Dowsett,et al.  Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. , 2005, The New England journal of medicine.

[52]  Ken Chen,et al.  Clonal architecture of secondary acute myeloid leukemia. , 2012, The New England journal of medicine.

[53]  K. Kinzler,et al.  Cancer Genome Landscapes , 2013, Science.

[54]  P. A. Futreal,et al.  Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing , 2014, Nature Genetics.

[55]  Mark Cobbold,et al.  Tracking Genomic Cancer Evolution for Precision Medicine: The Lung TRACERx Study , 2014, PLoS biology.

[56]  C. Maley,et al.  Cancer is a disease of clonal evolution within the body1–3. This has profound clinical implications for neoplastic progression, cancer prevention and cancer therapy. Although the idea of cancer as an evolutionary problem , 2006 .

[57]  A. Børresen-Dale,et al.  Mutational Processes Molding the Genomes of 21 Breast Cancers , 2012, Cell.

[58]  Jesse J. Salk,et al.  Detection of ultra-rare mutations by next-generation sequencing , 2012, Proceedings of the National Academy of Sciences.

[59]  A. McKenna,et al.  Absolute quantification of somatic DNA alterations in human cancer , 2012, Nature Biotechnology.

[60]  Andrew Menzies,et al.  The patterns and dynamics of genomic instability in metastatic pancreatic cancer , 2010, Nature.

[61]  J. Salk.  Clonal evolution in cancer , 2010 .

[62]  Chao Zhang,et al.  RAF inhibitors transactivate RAF dimers and ERK signaling in cells with wild-type BRAF , 2010, Nature.

[63]  A. McKenna,et al.  Widespread genetic heterogeneity in multiple myeloma: implications for targeted therapy. , 2014, Cancer cell.

[64]  James R. Downing,et al.  Genomic Analysis of the Clonal Origins of Relapsed Acute Lymphoblastic Leukemia , 2008, Science.

[65]  K. Matsuo,et al.  Heterogeneous distribution of EGFR mutations is extremely rare in lung adenocarcinoma. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[66]  J. Troge,et al.  Tumour evolution inferred by single-cell sequencing , 2011, Nature.

[67]  A. Bardelli,et al.  Molecular mechanisms of resistance to cetuximab and panitumumab in colorectal cancer. , 2010, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[68]  Joshua F. McMichael,et al.  Genome Remodeling in a Basal-like Breast Cancer Metastasis and Xenograft , 2010, Nature.

[69]  Renzo Boldorini,et al.  Increased Detection Sensitivity for KRAS Mutations Enhances the Prediction of Anti-EGFR Monoclonal Antibody Resistance in Metastatic Colorectal Cancer , 2011, Clinical Cancer Research.