New paradigms in clonal evolution: punctuated equilibrium in cancer

Journal of Pathology

Volumn 240, Issue 2, 2016, Pages 126-136

  Cross, William CH ^a   Graham, Trevor A ^a   Wright, Nicholas A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Big Bang; cancer; clonal evolution; colorectal cancer; gradualism; punctuated equilibrium

Indexed keywords

BIOINFORMATICS; CANCER GROWTH; CARCINOGENESIS; CLONAL EVOLUTION; COLORECTAL CANCER; GENOME ANALYSIS; HUMAN; MATHEMATICAL ANALYSIS; METASTASIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

EID: 84988642721     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4757     Document Type: Review

References (96)

1. Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (1st edn). John Murray: London, 1859.
2. Huxley J. Evolution: The Modern Synthesis. Harper & Brothers, New York, 1943.
3. Howell FC. Early Man (young readers edition). Life Nature Library. Time, Inc: New York, 1968.
4. Erwin DH, Anstey RL (eds). New Approaches to Speciation in the Fossil Record. Columbia University Press: New York, 1995.
5. Eldredge N, Gould SJ. Punctuated equilibria: an alternative to phyletic gradualism. In Models in Paleobiology, Schopf TJM (ed). Freeman, Cooper & Co: San Francisco, 1972; 82–115.
6. Gould SJ, Eldredge N. Punctuated equilibrium comes of age. Nature 1993; 366: 223–227.
7. Volkenstein MV. Punctualism, non-adaptationism, neutralism and evolution. Biosystems 1987; 20: 289–304.
8. Nowell PC. The clonal evolution of tumor cell populations. Science 1976; 194: 23–28.
9. Ford CE, Clarke CM. Cytogenetic evidence of clonal proliferation in primary reticular neoplasms. Proc Can Cancer Conf 1963; 5: 129–146.
10. McDonald SAC, Lavery D, Wright NA, et al. Barrett oesophagus: lessons on its origins from the lesion itself. Nature Rev Gastroenterol Hepatol 2015; 12: 50–60.
11. Choi CR, Ignjatovic-Wilson A, Askari A, et al. Low-grade dysplasia in ulcerative colitis: risk factors for developing high-grade dysplasia or colorectal cancer. Am J Gastroenterol 2015; 110: 1461–1471.
12. Smith G, Carey FA, Beattie J, et al. Mutations in APC, Kirsten-ras, and p53 – alternative genetic pathways to colorectal cancer. Proc Natl Acad Sci U S A 2002; 99: 9433–9438.
13. Maley CC. Multistage carcinogenesis in Barrett's esophagus. Cancer Lett 2007; 245: 22–32.
14. Greaves M, Maley CC. Clonal evolution in cancer. Nature 2012; 481: 306–313.
15. Baca SC, Prandi D, Lawrence MS, et al. Punctuated evolution of prostate cancer genomes. Cell 2013; 153: 666–677.
16. Eldredge N, Thompson JN, Brakefield PM, et al. The dynamics of evolutionary stasis. Paleobiology 2005; 31: 133–145.
17. Hofstad B, Vatn MH, Andersen SN, et al. Growth of colorectal polyps: redetection and evaluation of unresected polyps for a period of three years. Gut 1996; 39: 449–456.
18. Yeh AC, Ramaswamy S. Mechanisms of cancer cell dormancy – another hallmark of cancer? Cancer Res 2015; 75: 5014–5022.
19. Provine WB. Ernst Mayr: genetics and speciation. Genetics 2004; 167: 1041–1046.
20. Gupta GP, Massagué J. Cancer metastasis: building a framework. Cell 2006; 127: 679–695.
21. Nordling CO. A new theory on the cancer-inducing mechanism. Br J Cancer 1953; 7: 68.
22. Armitage P, Doll R. The age distribution of cancer and a multi-stage theory of carcinogenesis. Br J Cancer 1954; 8: 1–12.
23. Fisher JC. Multiple-mutation theory of carcinogenesis. Nature 1958; 181: 651–652.
24. Hayden EC. Technology: the $1,000 genome. Nature 2014; 507: 294–295.
25. Nik-Zainal S, Van Loo P, Wedge DC, et al. The life history of 21 breast cancers. Cell 2012; 149: 994–1007.
26. Sottoriva A, Spiteri I, Piccirillo SGM, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A 2013; 110: 4009–4014.
27. Zhang J, Fujimoto J, Zhang J, et al. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science 2014; 346: 256–259.
28. Gerlinger M, Horswell S, Larkin J, et al. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nature Genet 2014; 46: 225–233.
29. Lin D-C, Hao J-J, Nagata Y, et al. Genomic and molecular characterization of esophageal squamous cell carcinoma. Nature Genet 2014; 46: 467–473.
30. Bolli N, Avet-Loiseau H, Wedge DC, et al. Heterogeneity of genomic evolution and mutational profiles in multiple myeloma. Nature Commun 2014; 5: 2997.
31. Kim T-M, Jung S-H, 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.
32. Roche-Lestienne C, Soenen-Cornu V, Grardel-Duflos N, et al. Several types of mutations of the Abl gene can be found in chronic myeloid leukemia patients resistant to STI571, and they can pre-exist to the onset of treatment. Blood 2002; 100: 1014–1018.
33. Diaz LA, Williams RT, Wu J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012; 486: 537–540.
34. 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.
35. Greig SL. Osimertinib: first global approval. Drugs 2016; 76: 263–273.
36. Basanta D, Anderson AR. Exploiting ecological principles to better understand cancer progression and treatment. Interface Focus 2013; 3: 20130020.
37. Enriquez-Navas PM, Kam Y, Das T, et al. Exploiting evolutionary principles to prolong tumor control in preclinical models of breast cancer. Sci Transl Med 2016; 8: 327ra24.
38. Iqbal N, Iqbal N. Imatinib: a breakthrough of targeted therapy in cancer. Chemother Res Pract 2014; 2014: 1–9.
39. Cooke SL, Temple J, MacArthur S, et al. Intra-tumour genetic heterogeneity and poor chemoradiotherapy response in cervical cancer. Br J Cancer 2011; 104: 361–368.
40. Andor N, Graham TA, Jansen M, et al. Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nature Med 2015; 22: 105–113.
41. Murugaesu N, Wilson GA, Birkbak NJ, et al. Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy. Cancer Discov 2015; 5: 821–831.
42. Hainaut P, Pfeifer GP. Patterns of p53 G → T transversions in lung cancers reflect the primary mutagenic signature of DNA-damage by tobacco smoke. Carcinogenesis 2001; 22: 367–374.
43. Wang Y, Waters J, Leung ML, et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 2014; 512: 155–160.
44. Navin NE. Tumor evolution in response to chemotherapy: phenotype versus genotype. Cell Rep 2014; 6: 417–419.
45. Park SY, Gönen M, Kim HJ, et al. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J Clin Invest 2010; 120: 636–644.
46. Shibata D, Tavaré S. Counting divisions in a human somatic cell tree: how, what and why? Cell Cycle 2006; 5: 610–614.
47. Sottoriva A, Kang H, Ma Z, et al. A Big Bang model of human colorectal tumor growth. Nature Genet 2015; 47: 209–216.
48. Williams MJ, Werner B, Barnes CP, et al. Identification of neutral tumor evolution across cancer types. Nature Genet 2016; 48: 238–244.
49. Ling S, Hu Z, Yang Z, et al. Extremely high genetic diversity in a single tumor points to prevalence of non-Darwinian cell evolution. Proc Natl Acad Sci U S A 2015; 112: E6496–E6505.
50. 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.
51. Bignell GR, Greenman CD, Davies H, et al. Signatures of mutation and selection in the cancer genome. Nature 2010; 463: 893–898.
52. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759–767.
53. Lamlum H, Papadopoulou A, Ilyas M, et al. APC mutations are sufficient for the growth of early colorectal adenomas. Proc Natl Acad Sci U S A 2000; 97: 2225–2228.
54. Rabinovitch PS, Reid BJ, Haggitt RC, et al. Progression to cancer in Barrett's esophagus is associated with genomic instability. Lab Invest 1989; 60: 65–71.
55. Shivakumar BM, Rotti H, Vasudevan TG, et al. Copy number variations are progressively associated with the pathogenesis of colorectal cancer in ulcerative colitis. World J Gastroenterol 2015; 21: 616–622.
56. Soto AM, Sonnenschein C. The somatic mutation theory of cancer: growing problems with the paradigm? BioEssays. 2004; 26: 1097–1107.
57. Muzny DM, Bainbridge MN, Chang K, et al. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487: 330–337.
58. Stepanenko AA, Kavsan VM. Evolutionary karyotypic theory of cancer versus conventional cancer gene mutation theory. Biopolym Cell 2012; 28: 267–280.
59. Maher CA, Wilson RK. Chromothripsis and human disease: piecing together the shattering process. Cell 2012; 148: 29–32.
60. 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.
61. Roberts SA, Gordenin DA. Hypermutation in human cancer genomes: footprints and mechanisms. Nature Rev Cancer 2014; 14: 786–800.
62. Ionov Y, Peinado MA, Malkhosyan S, et al. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 1993; 363: 558–561.
63. Heitzer E, Tomlinson I. Replicative DNA polymerase mutations in cancer. Curr Opin Genet Dev 2014; 24: 107–113.
64. Young J, Leggett B, Gustafson C, et al. Genomic instability occurs in colorectal carcinomas but not in adenomas. Hum Mutat 1993; 2: 351–354.
65. Nik-Zainal S, Alexandrov LB, Wedge DC, et al. Mutational processes molding the genomes of 21 breast cancers. Cell 2012; 149: 979–993.
66. Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415–421.
67. Di Giulio M. Nanoarchaeum equitans is a living fossil. J Theor Biol 2006; 242: 257–260.
68. Robinson M, Amemiya CT. Coelacanths. Curr Biol 2014; 24: R62–R63.
69. Dene H, Goodman M, Walz DA, et al. The phylogenetic position of aardvark (Orycteropus afer) as suggested by its myoglobin. Hoppe-Seylers Z Physiol Chem 1983; 364: 1585–1595.
70. Hvid-Jensen F, Pedersen L, Drewes AM, et al. Incidence of adenocarcinoma among patients with Barrett's esophagus. N Engl J Med 2011; 365: 1375–1383.
71. Diamond SJ, Enestvedt BK, Jiang Z, et al. Adenoma detection rate increases with each decade of life after 50 years of age. Gastrointest Endosc 2011; 74: 135–140.
72. Aguirre-Ghiso JA. Models, mechanisms and clinical evidence for cancer dormancy. Nature Rev Cancer 2007; 7: 834–846.
73. Martincorena I, Roshan A, Gerstung M, et al. High burden and pervasive positive selection of somatic mutations in normal human skin. Science 2015; 348: 880–886.
74. Tomasetti C, Vogelstein B, Parmigiani G. Half or more of the somatic mutations in cancers of self-renewing tissues originate prior to tumor initiation. Proc Natl Acad Sci U S A 2013; 110: 1999–2004.
75. Haldane JBS. Suggestions as to quantitative measurement of rates of evolution. Evol Int J Org Evol 1949; 3: 51–56.
76. Morgan GJ. Emile Zuckerkandl, Linus Pauling, and the molecular evolutionary clock, 1959–1965. J Hist Biol 1998; 31: 155–178.
77. Lenski RE. Evolutionary rate. In Encyclopedia of Genetics 2001; 671–672.
78. Alexandrov LB, Jones PH, Wedge DC, et al. Clock-like mutational processes in human somatic cells. Nature Genet 2015; 47: 1402–1407.
79. Stec R, Semeniuk-Wojtaś A, Charkiewicz R, et al. Mutation of the PIK3CA gene as a prognostic factor in patients with colorectal cancer. Oncol Lett 2015; 10: 1423–1429.
80. Ito T, Pei J, Dulaimi E, et al. Genomic copy number alterations in renal cell carcinoma with sarcomatoid features. J Urol 2016; 195: 852–858.
81. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646–674.
82. Lavery DL, Martinez P, Gay LJ, et al. Evolution of oesophageal adenocarcinoma from metaplastic columnar epithelium without goblet cells in Barrett's oesophagus. Gut 2016; 65: 907–913.
83. 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: 1441–54.e7.
84. Kim T-M, An CH, Rhee J-K, et al. Clonal origins and parallel evolution of regionally synchronous colorectal adenoma and carcinoma. Oncotarget 2015; 6: 27725–27735.
85. Adachi Y, Yasuda K, Kakisako K, et al. Histopathologic characteristics of advanced colorectal cancer smaller than 2 cm in size. Colorectal Dis 1999; 1: 19–22.
86. Kim JH, Kang GH. Molecular and prognostic heterogeneity of microsatellite-unstable colorectal cancer. World J Gastroenterol 2014; 20: 4230–4243.
87. Gerlinger M, McGranahan N, Dewhurst SM, et al. Cancer: evolution within a lifetime. Annu Rev Genet 2014; 48: 215–236.
88. Klein CA. Parallel progression of primary tumours and metastases. Nature Rev Cancer 2009; 9: 302–312.
89. Naxerova K, Jain RK. Using tumour phylogenetics to identify the roots of metastasis in humans. Nature Rev Clin Oncol 2015; 12: 258–272.
90. Brannon A, Vakiani E, Sylvester BE, et al. Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome Biol 2014; 15: 454.
91. Gatenby RA. A change of strategy in the war on cancer. Nature 2009; 459: 508–509.
92. Beerenwinkel N, Schwarz RF, Gerstung M, et al. Cancer evolution: mathematical models and computational inference. Syst Biol 2015; 64: e1–e25.
93. Durinck S, Ho C, Wang NJ, et al. Temporal dissection of tumorigenesis in primary cancers. Cancer Discov 2011; 1: 137–143.
94. Purdom E, Ho C, Grasso CS, et al. Methods and challenges in timing chromosomal abnormalities within cancer samples. Bioinformatics 2013; 29: 3113–3120.
95. Li D, O'Reilly EM. Adjuvant and neoadjuvant therapy for pancreatic cancer. Surg Oncol Clin N Am 2016; 25: 311–326.
96. Sheldon PR. Parallel gradualistic evolution of Ordovician trilobites. Nature 1987; 330: 561–563.