Measuring cancer evolution from the genome

Journal of Pathology

Volumn 241, Issue 2, 2017, Pages 183-191

  Graham, Trevor A ^a   Sottoriva, Andrea ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

clonal evolution of cancer; gradualism; hopeful monsters; intratumour heterogeneity; neutral evolution; next generation sequencing; punctuated equilibrium; saltation; selection; subclones

Indexed keywords

CANCER GROWTH; CARCINOGENESIS; DYNAMICS; EVOLUTION; GENE MUTATION; GENOME; GENOTYPE; MALIGNANT NEOPLASM; PHENOTYPE; PRIORITY JOURNAL; REVIEW; ANIMAL; GENETIC PREDISPOSITION; GENETIC SCREENING; GENETICS; HUMAN; NEOPLASMS; PATHOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; GENOTYPE; HUMANS; NEOPLASMS; PHENOTYPE;

EID: 85003794681     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4821     Document Type: Review

References (80)

1. Alexandrov LB, Jones PH, Wedge DC, et al. Clock-like mutational processes in human somatic cells. Nat Genet 2015; 47: 1402–1407.
2. Xue Y, Wang Q, Long Q, et al. Human Y chromosome base-substitution mutation rate measured by direct sequencing in a deep-rooting pedigree. Curr Biol 2009; 19: 1453–1457.
3. 1000Genomes Project Consortium, Abecasis GR, Altshuler D, et al. A map of human genome variation from population-scale sequencing. Nature 2010; 467: 1061–1073.
4. Laird CD, Pleasant ND, Clark AD, et al. Hairpin-bisulfite PCR: assessing epigenetic methylation patterns on complementary strands of individual DNA molecules. Proc Natl Acad Sci USA 2004; 101: 204–209.
5. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature 1998; 396: 643–649.
6. Rajagopalan H, Lengauer C. Aneuploidy and cancer. Nature 2004; 432: 338–341.
7. Schwarz RF, Trinh A, Sipos B, et al. Phylogenetic quantification of intra-tumour heterogeneity. PLoS Comput Biol 2014; 10: e1003535.
8. Shibata D, Tavare S. Counting divisions in a human somatic cell tree: how, what and why? Cell Cycle 2006; 5: 610–614.
9. de Bruin EC, McGranahan N, Mitter R, et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 2014; 346: 251–256.
10. Gerlinger M, Horswell S, Larkin J, et al. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat Genet 2014; 46: 225–233.
11. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012; 366: 883–892.
12. Thirlwell C, Will OCC, Domingo E, et al. Clonality assessment and clonal ordering of individual neoplastic crypts shows polyclonality of colorectal adenomas. Gastroenterology 2010; 138: 1441–1454.
13. Siegmund K, Marjoram P, Woo Y, et al. Inferring clonal expansion and cancer stem cell dynamics from DNA methylation patterns in colorectal cancers. Proc Natl Acad Sci USA 2009; 106: 4828–4833.
14. Sottoriva A, Kang H, Ma Z, et al. A Big Bang model of human colorectal tumor growth. Nat Genet 2015; 47: 209–216.
15. Jones S, Chen W-D, Parmigiani G, et al. Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci USA 2008; 105: 4283–4288.
16. Yachida S, Jones S, Bozic I, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010; 467: 1114–1117.
17. Schwarz RF, Ng CK, Cooke SL, et al. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: a phylogenetic analysis. PLoS Med 2015; 12: e1001789.
18. Sottoriva A, Spiteri I, Piccirillo SG, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 2013; 110: 4009–4014.
19. Sottoriva A, Spiteri I, Shibata D, et al. Single-molecule genomic data delineate patient-specific tumor profiles and cancer stem cell organization. Cancer Res 2013; 73: 41–49.
20. Zhang J, Fujimoto J, Zhang J, et al. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science 2014; 346: 256–259.
21. Okosun J, Bodor C, Wang J, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet 2014; 46: 176–181.
22. Nik-Zainal S, Van Loo P, Wedge DC, et al. The life history of 21 breast cancers. Cell 2012; 149: 994–1007.
23. Yates LR, Gerstung M, Knappskog S, et al. Subclonal diversification of primary breast cancer revealed by multiregion sequencing. Nat Med 2015; 21: 751–759.
24. Gundem G, Van Loo P, Kremeyer B, et al. The evolutionary history of lethal metastatic prostate cancer. Nature 2015; 520: 353–357.
25. Li X, Galipeau PC, Paulson TG, et al. Temporal and spatial evolution of somatic chromosomal alterations: a case-cohort study of Barrett's esophagus. Cancer Prev Res (Phila) 2014; 7: 114–127.
26. Diaz LA, Jr, Williams RT, Wu J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012; 486: 537–540.
27. Sieber OM, Tomlinson SR, Tomlinson IPM. Tissue, cell and stage specificity of (epi)mutations in cancers. Nat Rev Cancer 2005; 5: 649–655.
28. Lipinski KA, Barber LJ, Davies MN, et al. Cancer evolution and the limits of predictability in precision cancer medicine. Trends Cancer 2016; 2: 49–63.
29. Vermeulen L, Morrissey E, van der Heijden M, et al. Defining stem cell dynamics in models of intestinal tumor initiation. Science 2013; 342: 995–998.
30. Lamlum H, Papadopoulou A, Ilyas M, et al. APC mutations are sufficient for the growth of early colorectal adenomas. Proc Natl Acad Sci USA 2000; 97: 2225–2228.
31. Sansom OJ, Reed KR, Hayes AJ, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004; 18: 1385–1390.
32. Aktipis CA, Boddy AM, Gatenby RA, et al. Life history trade-offs in cancer evolution. Nat Rev Cancer 2013; 13: 883–892.
33. Humphries A, Wright NA. Colonic crypt organization and tumorigenesis. Nat Rev Cancer 2008; 8: 415–424.
34. Pepper JW, Sprouffske K, Maley CC. Animal cell differentiation patterns suppress somatic evolution. PLoS Comput Biol 2007; 3: e250.
35. Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 2009; 458: 719–724.
36. Vogelstein B, Papadopoulos N, Velculescu VE, et al. Cancer genome landscapes. Science 2013; 339: 1546–1558.
37. Roth A, Khattra J, Yap D, et al. PyClone: statistical inference of clonal population structure in cancer. Nat Methods 2014; 11: 396–398.
38. Andor N, Harness JV, Muller S, et al. EXPANDS: expanding ploidy and allele frequency on nested subpopulations. Bioinformatics 2014; 30: 50–60.
39. Fischer A, Vazquez-Garcia I, Illingworth CJ, et al. High-definition reconstruction of clonal composition in cancer. Cell Rep 2014; 7: 1740–1752.
40. Stratton MR, Campbell PJ, Futreal PA. The cancer genome. Nature 2009; 458: 719–724.
41. Marusyk A, Tabassum DP, Altrock PM, et al. Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity. Nature 2014; 514: 54–58.
42. Williams MJ, Werner B, Barnes CP, et al. Identification of neutral tumor evolution across cancer types. Nat Genet 2016; 48: 238–244.
43. Bozic I, Gerold JM, Nowak MA. Quantifying clonal and subclonal passenger mutations in cancer evolution. PLoS Comput Biol 2016; 12: e1004731.
44. Durrett R. Population genetics of neutral mutations in exponentially growing cancer cell populations. Ann Appl Probab 2013; 23: 230–250.
45. Ostrow SL, Barshir R, DeGregori J, et al. Cancer evolution is associated with pervasive positive selection on globally expressed genes. PLoS Genet 2014; 10: e1004239.
46. Martincorena I, Roshan A, Gerstung M, et al. Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science 2015; 348: 880–886.
47. Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415–421.
48. Greenman C, Stephens P, Smith R, et al. Patterns of somatic mutation in human cancer genomes. Nature 2007; 446: 153–158.
49. Driessens G, Beck B, Caauwe A, et al. Defining the mode of tumour growth by clonal analysis. Nature 2012; 488: 527–530.
50. Merlo LMF, Pepper JW, Reid BJ, et al. Cancer as an evolutionary and ecological process. Nat Rev Cancer 2006; 6: 924–935.
51. Beerenwinkel N, Antal T, Dingli D, et al. Genetic progression and the waiting time to cancer. PLoS Comput Biol 2007; 3: e225.
52. Bozic I, Antal T, Ohtsuki H, et al. Accumulation of driver and passenger mutations during tumor progression. Proc Natl Acad Sci USA 2010; 107: 18545–18550.
53. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487: 330–337.
54. Castro-Giner F, Ratcliffe P, Tomlinson I. The mini-driver model of polygenic cancer evolution. Nat Rev Cancer 2015; 15: 680–685.
55. Andor N, Graham TA, Jansen M, et al. Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nat Med 2016; 22: 105–113.
56. Morris LG, Riaz N, Desrichard A, et al. Pan-cancer analysis of intratumor heterogeneity as a prognostic determinant of survival. Oncotarget 2016; 7: 10051–10063.
57. Eldredge N, Gould SJ. Punctuated equilibria: an alternative to phyletic gradualism. In Models in Paleobiology, Schopf T (ed.), Freeman, Cooper & Co., San Francisco, 1972; 82–115.
58. Goldschmidt R. The Material Basis of Evolution. Yale University Press: New Haven, 1940.
59. Rowan AJ, Lamlum H, Ilyas M, et al. APC mutations in sporadic colorectal tumors: a mutational ‘hotspot’ and interdependence of the ‘two hits’. Proc Natl Acad Sci USA 2000; 97: 3352–3357.
60. Jones A, Thirlwell C, Howarth K, et al. Analysis of copy number changes suggests chromosomal instability in a minority of large colorectal adenomas. J Pathol 2007; 213: 249–256.
61. Campbell PJ, Pleasance ED, Stephens PJ, et al. Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc Natl Acad Sci USA 2008; 105: 13081–13086.
62. Kim TM, Jung SH, An CH, et al. Subclonal genomic architectures of primary and metastatic colorectal cancer based on intratumoral genetic heterogeneity. Clin Cancer Res 2015; 21: 4461–4472.
63. Jesinghaus M, Wolf T, Pfarr N, et al. Distinctive spatiotemporal stability of somatic mutations in metastasized microsatellite-stable colorectal cancer. Am J Surg Pathol 2015; 39: 1140–1147.
64. Stephens PJ, Greenman CD, Fu B, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 2011; 144: 27–40.
65. Kloosterman WP, Hoogstraat M, Paling O, et al. Chromothripsis is a common mechanism driving genomic rearrangements in primary and metastatic colorectal cancer. Genome Biol 2011; 12: R103.
66. Molenaar JJ, Koster J, Zwijnenburg DA, et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012; 483: 589–593.
67. Zhang CZ, Spektor A, Cornils H, et al. Chromothripsis from DNA damage in micronuclei. Nature 2015; 522: 179–184.
68. Baca SC, Prandi D, Lawrence MS, et al. Punctuated evolution of prostate cancer genomes. Cell 2013; 153: 666–677.
69. Carter SL, Cibulskis K, Helman E, et al. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol 2012; 30: 413–421.
70. Dewhurst SM, McGranahan N, Burrell RA, et al. Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov 2014; 4: 175–185.
71. Wang Y, Waters J, Leung ML, et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 2014; 512: 155–160.
72. Gao R, Davis A, McDonald TO, et al. Punctuated copy number evolution and clonal stasis in triple-negative breast cancer. Nat Genet 2016; 48: 1119–1130.
73. Stachler MD, Taylor-Weiner A, Peng S, et al. Paired exome analysis of Barrett's esophagus and adenocarcinoma. Nat Genet 2015; 47: 1047–1055.
74. Gordon DJ, Resio B, Pellman D. Causes and consequences of aneuploidy in cancer. Nat Rev Genet 2012; 13: 189–203.
75. Tsao JL, Yatabe Y, Salovaara R, et al. Genetic reconstruction of individual colorectal tumor histories. Proc Natl Acad Sci USA 2000; 97: 1236–1241.
76. Armitage P, Doll R. The age distribution of cancer and a multi-stage theory of carcinogenesis. Br J Cancer 1954; 8: 1–12.
77. Ding L, Ley TJ, Larson DE, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012; 481: 506–510.
78. Anderson K, Lutz C, van Delft FW, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 2011; 469: 356–361.
79. Findlay JM, Castro-Giner F, Makino S, et al. Differential clonal evolution in oesophageal cancers in response to neo-adjuvant chemotherapy. Nat Commun 2016; 7: 11111.
80. Siravegna G, Mussolin B, Buscarino M, et al. Clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nat Med 2015; 21: 795–801.