First steps in experimental cancer evolution

Evolutionary Applications

Volumn 6, Issue 3, 2013, Pages 535-548

  Taylor, Tiffany B ^a   Johnson, Louise J ^a   Jackson, Robert W ^a   Brockhurst, Michael A ^b   Dash, Philip R ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Carcinogenesis; Evolutionary trade offs; Kin competition; Metastasis; Resistance; Resource competition; Social evolution

Indexed keywords

EID: 84875637563     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12041     Document Type: Article

References (114)

1. Aktipis, C. A., C. C. Maley, and J. W. Pepper 2012. Dispersal Evolution in Neoplasms: The Role of Disregulated Metabolism in the Evolution of Cell Motility. Cancer Prevention Research 5(2):266-275.
2. Alizon, S., and P. Taylor 2008. Empty sites can promote altruistic behavior. Evolution 62(6):1335-1344.
3. Anderson, A. R., A. M. Weaver, P. T. Cummings, and V. Quaranta 2006. Tumor Morphology and Phenotypic Evolution Driven by Selective Pressure from the Microenvironment. Cell 127(5):905-915.
4. Andersson, D. I. 2006. The biological cost of mutational antibiotic resistance: any practical conclusions? Current Opinion in Microbiology 9(5):461-465.
5. Andersson, D. I., and D. Hughes 2010. Antibiotic resistance and its cost: is it possible to reverse resistance? Nature Reviews Microbiology 8(4):260-271.
6. Araujo, R. P., and D. L. S. McElwain 2004. New insights into vascular collapse and growth dynamics in solid tumors. Journal of Theoretical Biology 228(3):335-346.
7. Attolini, C. S. O., and F. Michor 2009. Evolutionary Theory of Cancer. Annals of the New York Academy of Sciences 1168(1):23-51.
8. Axelrod, R., D. E. Axelrod, and K. J. Pienta 2006. Evolution of cooperation among tumor cells. Proceedings of the National Academy of Sciences 103(36):13474-13479.
9. Banfield, W. G., P. A. Woke, C. M. MacKay, and H. L. Cooper 1965. Mosquito Transmission of a Reticulum Cell Sarcoma of Hamsters. Science 148(3674):1239-1240.
10. Barrick, J. E., D. S. Yu, S. H. Yoon, H. Jeong, T. K. Oh, D. Schneider, R. E. Lenski et al. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461(7268):1243-1247.
11. Ben-Jacob, E., D. S. Coffey, and H. Levine 2012. Bacterial survival strategies suggest rethinking cancer cooperativity. Trends in microbiology 20(9):403-410.
12. Bernards, R., and R. A. Weinberg 2002. Metastasis genes: A progression puzzle. Nature 418(6900):823-823.
13. Bielas, J. H., K. R. Loeb, B. P. Rubin, L. D. True, and L. A. Loeb 2006. From the Cover: Human cancers express a mutator phenotype. Proceedings of the National Academy of Sciences 103(48):18238-18242.
14. Blagosklonny, M. V. 2002. STI-571 must select for drug-resistant cells but 'no cell breathes fire out of its nostrils like a dragon'. Leukemia 16:570-572.
15. Blount, Z. D., C. Z. Borland, and R. E. Lenski 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proceedings of the National Academy of Sciences 105(23):7899-7906.
16. Bogdan, S., and C. Klämbt 2001. Epidermal growth factor receptor signaling. Current Biology 11(8):R292-R295.
17. Boucher, Y., and R. K. Jain 1992. Microvascular Pressure Is the Principal Driving Force for Interstitial Hypertension in Solid Tumors: Implications for Vascular Collapse. Cancer Research 52(18):5110-5114.
18. Bowler, D. E., and T. G. Benton 2005. Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biological Reviews 80(02):205-225.
19. Brurberg, K. G., B. A. Graff, and E. K. Rofstad 2003. Temporal heterogeneity in oxygen tension in human melanoma xenografts. British Journal of Cancer 89(2):350-356.
20. Brurberg, K. G., H. K. Skogmo, B. A. Graff, D. R. Olsen, and E. K. Rofstad 2005. Fluctuations in pO2 in poorly and well-oxygenated spontaneous canine tumors before and during fractionated radiation therapy. Radiotherapy and Oncology 77(2):220-226.
21. Buckling, A., R. C. Maclean, M. A. Brockhurst, and N. Colegrave 2009. The Beagle in a bottle. Nature 457(7231):824-829.
22. Bull, J. J., and W. R. Harcombe 2009. Population Dynamics Constrain the Cooperative Evolution of Cross-Feeding. PLoS ONE 4(1):e4115.
23. Butler, L. M., D. B. Agus, H. I. Scher, B. Higgins, A. Rose, C. Cordon-Cardo, H. T. Thaler et al. 2000. Suberoylanilide Hydroxamic Acid, an Inhibitor of Histone Deacetylase, Suppresses the Growth of Prostate Cancer Cells in Vitro and in Vivo. Cancer Research 60(18):5165-5170.
24. Cairns, J. 1975. Mutation selection and the natural history of cancer. Nature 255(5505):197-200.
25. Cárdenas-Navia, L. I., D. Mace, R. A. Richardson, D. F. Wilson, S. Shan, and M. W. Dewhirst 2008. The Pervasive Presence of Fluctuating Oxygenation in Tumors. Cancer Research 68(14):5812-5819.
26. Chao, L., and B. R. Levin 1981. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proceedings of the National Academy of Sciences 78(10):6324-6328.
27. Chen, J., K. Sprouffske, Q. Huang, and C. C. Maley 2011. Solving the Puzzle of Metastasis: The Evolution of Cell Migration in Neoplasms. PLoS ONE 6(4):e17933.
28. Comins, H. N., W. D. Hamilton, and R. M. May 1980. Evolutionarily stable dispersal strategies. Journal of Theoretical Biology 82(2):205-230.
29. Cooper, T. F., D. E. Rozen, and R. E. Lenski 2003. Parallel changes in gene expression after 20, 000 generations of evolution in Escherichia coli. Proceedings of the National Academy of Sciences 100(3):1072-1077.
30. Coussens, L. M., B. Fingleton, and L. M. Matrisian 2002. Matrix Metalloproteinase Inhibitors and Cancer-Trials and Tribulations. Science 295(5564):2387-2392.
31. Crespi, B., and K. Summers 2005. Evolutionary biology of cancer. Trends in Ecology & Evolution 20(10):545-552.
32. Diaz Jr, L. A., R. T. Williams, J. Wu, I. Kinde, J. R. Hecht, J. Berlin, B. Allen et al. 2012. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486(7404):537-540.
33. Dingli, D., and M. A. Nowak 2006. Cancer biology: Infectious tumour cells. Nature 443(7107):35-36.
34. Egeblad, M., and Z. Werb 2002. New functions for the matrix metalloproteinases in cancer progression. Nature Reviews Cancer 2(3):161-174.
35. Elena, S. F., and R. E. Lenski 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics 4(6):457-469.
36. Fiegna, F., Y.-T. N. Yu, S. V. Kadam, and G. J. Velicer 2006. Evolution of an obligate social cheater to a superior cooperator. Nature 441(7094):310-314.
37. Frank, S. A. 2003. Repression of competition and the evolution of cooperation. Evolution 57(4):693-705.
38. Friedl, P., and K. Wolf 2003. Tumour-cell invasion and migration: diversity and escape mechanisms. Nature Reviews Cancer 3(5):362-374.
39. Frumkin, D., A. Wasserstrom, S. Itzkovitz, T. Stern, A. Harmelin, R. Eilam, G. Rechavi et al. 2008. Cell Lineage Analysis of a Mouse Tumor. Cancer Research 68(14):5924-5931.
40. Gandon, S., and Y. Michalakis 1999. Evolutionarily Stable Dispersal Rate in a Metapopulation with Extinctions and Kin Competition. Journal of Theoretical Biology 199(3):275-290.
41. Gardner, A., and A. Grafen 2009. Capturing the superorganism: a formal theory of group adaptation. Journal of Evolutionary Biology 22(4):659-671.
42. Gerlinger, M., A. J. Rowan, S. Horswell, J. Larkin, D. Endesfelder, E. Gronroos, P. Martinez et al. 2012. Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing. New England Journal of Medicine 366(10):883-892.
43. Gorre, M. E., M. Mohammed, K. Ellwood, N. Hsu, R. Paquette, P. N. Rao, and C. L. Sawyers 2001. Clinical Resistance to STI-571 Cancer Therapy Caused by BCR-ABL Gene Mutation or Amplification. Science 293(5531):876-880.
44. Greaves, M., and C. C. Maley 2012. Clonal evolution in cancer. Nature 481(7381):306-313.
45. Griffin, A. S., and S. A. West 2002. Kin selection: fact and fiction. Trends in Ecology & Evolution 17(1):15-21.
46. Hamilton, W. D. 1964. The genetical evolution of social behaviour I & II. Journal of Theoretical Biology 7:1-52.
47. Hamilton, W. D. 1996. Narrow roads of gene land. Vol 1. Evolution of social behaviour. W. H. Freeman, Oxford.
48. Hamilton, W. D., and R. M. May 1977. Dispersal in stable habitats. Nature 269(5629):578-581.
49. Hanahan, D., and L. M. Coussens 2012. Accessories to the Crime: Functions of Cells Recruited to the Tumor Microenvironment. Cancer Cell 21(3):309-322.
50. Hanahan, D., and R. A. Weinberg 2011. Hallmarks of Cancer: The Next Generation. Cell 144(5):646-674.
51. Harris, A. L. 2002. Hypoxia - a key regulatory factor in tumour growth. Nature Reviews Cancer 2(1):38-47.
52. Heckathorn, D. D. 1996. The Dynamics and Dilemmas of Collective Action. American Sociological Review 61(2):250-277.
53. Hegreness, M., N. Shoresh, D. Damian, D. Hartl, and R. Kishony 2008. Accelerated evolution of resistance in multidrug environments. Proceedings of the National Academy of Sciences 105(37):13977-13981.
54. de Jong, J. S., P. J. van Diest, P. van der Valk, and J. P. A. Baak 1998. Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. II: Correlations with proliferation and angiogenesis. The Journal of Pathology 184(1):53-57.
55. Kalas, W., J. L. Yu, C. Milsom, J. Rosenfeld, R. Benezra, P. Bornstein, and J. Rak 2005. Oncogenes and Angiogenesis: Down-regulation of Thrombospondin-1 in Normal Fibroblasts Exposed to Factors from Cancer Cells Harboring Mutant Ras. Cancer Research 65(19):8878-8886.
56. Klein, C. A. 2003. The Systemic Progression of Human Cancer: A Focus on the Individual Disseminated Cancer Cell-The Unit of Selection. Advances in Cancer Research, 89:35-67.
57. Kobayashi, S., T. J. Boggon, T. Dayaram, P. A. Jänne, O. Kocher, M. Meyerson, B. E. Johnson et al. 2005. EGFR Mutation and Resistance of Non-Small-Cell Lung Cancer to Gefitinib. New England Journal of Medicine 352(8):786-792.
58. Komarova, N. L., and D. Wodarz . 2005. Drug resistance in cancer: Principles of emergence and prevention. Proceedings of the National Academy of Sciences 102(27):9714-9719.
59. Kümmerli, R., A. Gardner, S. A. West, and A. S. Griffin 2009. Limited dispersal, budding dispersal, and cooperation: an experimental study. Evolution 63(4):939-949.
60. Kümmerli, R., P. van den Berg, A. S. Griffin, S. A. West, and A. Gardner 2010. Repression of competition favours cooperation: experimental evidence from bacteria. Journal of Evolutionary Biology 23(4):699-706.
61. Lee, V. T., and O. Schneewind 2001. Protein secretion and the pathogenesis of bacterial infections. Genes & Development 15(14):1725-1752.
62. Lehmann, L., and L. Keller 2006. The evolution of cooperation and altruism - a general framework and a classification of models. Journal of Evolutionary Biology 19(5):1365-1376.
63. Leigh, E. G. 1977. How does selection reconcile individual advantage with the good of the group? Proceedings of the National Academy of Sciences of the United States of America 74(10):4542-4546.
64. Lenski, R. E., and M. Travisano 1994. Dynamics of adaptation and diversification: a 10, 000-generation experiment with bacterial populations. Proceedings of the National Academy of Sciences 91(15):6808-6814.
65. Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler 1991. Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2, 000 Generations.. The American Naturalist 138(6):1315-1341.
66. Leroi, A. M., V. Koufopanou, and A. Burt 2003. Cancer selection. Nature Reviews Cancer 3(3):226-231.
67. Levin, B. R., V. Perrot, and N. Walker 2000. Compensatory Mutations, Antibiotic Resistance and the Population Genetics of Adaptive Evolution in Bacteria. Genetics 154(3):985-997.
68. Liotta, L. A., and E. C. Kohn 2001. The microenvironment of the tumour-host interface. Nature 411(6835):375-379.
69. Liotta, L. A., and E. C. Kohn 2003. Cancer's deadly signature. Nature Genetics 33(1):10-11.
70. Liotta, L. A., P. S. Steeg, and W. G. Stetler-Stevenson 1991. Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell 64(2):327-336.
71. Loeb, L. A. 2001. A Mutator Phenotype in Cancer. Cancer Research 61(8):3230-3239.
72. MacLean, R. C., A. R. Hall, G. G. Perron, and A. Buckling 2010. The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nature Reviews Genetics 11(6):405-414.
73. Maisnier-Patin, S., and D. I. Andersson 2004. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Research in Microbiology 155(5):360-369.
74. Maynard Smith, J., and E. Szathmáry 1995. The Major Transitions in Evolution. Freeman, Oxford.
75. Merlo, L. M. F., J. W. Pepper, B. J. Reid, and C. C. Maley 2006. Cancer as an evolutionary and ecological process. Nature Reviews Cancer 6(12):924-935.
76. Michor, F., T. P. Hughes, Y. Iwasa, S. Branford, N. P. Shah, C. L. Sawyers, and M. A. Nowak 2005. Dynamics of chronic myeloid leukaemia. Nature 435(7046):1267-1270.
77. Mueller, M. M., and N. E. Fusenig 2004. Friends or foes - bipolar effects of the tumour stroma in cancer. Nature Reviews Cancer 4(11):839-849.
78. Nadell, C. D., K. R. Foster, and J. B. Xavier 2010. Emergence of Spatial Structure in Cell Groups and the Evolution of Cooperation. PLoS Computational Biology 6(3):e1000716.
79. Novak, M., T. Pfeiffer, R. E. Lenski, U. Sauer, and S. Bonhoeffer 2006. Experimental Tests for an Evolutionary Trade-Off between Growth Rate and Yield in E. coli. The American Naturalist 168(2):242-251.
80. Nowell, P. C. 1976. The clonal evolution of tumor cell populations. Science 194(4260):23-28.
81. Nunney, L 2003. The population genetics of multistage carcinogenesis. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1520):1183-1191.
82. Poon, A., B. H. Davis, and L. Chao 2005. The Coupon Collector and the Suppressor Mutation. Genetics 170(3):1323-1332.
83. Queller, D. C. 1984. Kin selection and frequency dependence: a game theoretic approach. Biological Journal of the Linnean Society 23 (2-3):133-143.
84. Queller, D. C., E. Ponte, S. Bozzaro, and J. E. Strassmann 2003. Single-Gene Greenbeard Effects in the Social Amoeba Dictyostelium discoideum. Science 299(5603):105-106.
85. Rainey, P., and M. Travisano 1998. Adaptive radiation in a heterogeneous environment. Nature 394(6688):69-72.
86. Read, A. F., and S. Huijben 2009. PERSPECTIVE: Evolutionary biology and the avoidance of antimicrobial resistance. Evolutionary Applications 2(1):40-51.
87. Ronce, O 2007. How Does It Feel to Be Like a Rolling Stone? Ten Questions About Dispersal Evolution. Annual Review of Ecology, Evolution, and Systematics 38(1):231-253.
88. Ross-Gillespie, A., A. Gardner, S. A. West, and A. S. Griffin 2007. Frequency Dependence and Cooperation: Theory and a Test with Bacteria. The American Naturalist 170(3):331-342.
89. Royuela, M., M. Ricote, M. S. Parsons, I. García-Tuñón, R. Paniagua, and M. P. de Miguel 2004. Immunohistochemical analysis of the IL-6 family of cytokines and their receptors in benign, hyperplasic, and malignant human prostate. The Journal of Pathology 202(1):41-49.
90. Schrag, S. J., V. Perrot, and B. R. Levin 1997. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proceedings of the Royal Society of London. Series B: Biological Sciences 264(1386):1287-1291.
91. Sequist, L. V., B. A. Waltman, D. Dias-Santagata, S. Digumarthy, A.B. Turke, P. Fidias, K. Bergethon et al. 2011. Genotypic and Histological Evolution of Lung Cancers Acquiring Resistance to EGFR Inhibitors. Science Translational Medicine 3(75):75ra26.
92. Shah, N. P., B. J. Skaggs, S. Branford, T. P. Hughes, J. M. Nicoll, R. L. Paquette, and C. L. Sawyers . 2007. Sequential ABL kinase inhibitor therapy selects for compound drug-resistant BCR-ABL mutations with altered oncogenic potency. The Journal of Clinical Investigation 117(9):2562-2569.
93. Shannon, K. M. 2002. Resistance in the land of molecular cancer therapeutics. Cancer Cell 2(2):99-102.
94. Sniegowski, P. D., P. J. Gerrish, and R. E. Lenski 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387(6634):703-705.
95. Stetler-Stevenson, W. G., S. Aznavoorian, and L. A. Liotta 1993. Tumor Cell Interactions with the Extracellular Matrix During Invasion and Metastasis. Annual Review of Cell Biology 9(1):541-573.
96. Stoecklein, N. H., S. B. Hosch, M. Bezler, F. Stern, C. H. Hartmann, C. Vay, A. Siegmund et al. 2008. Direct Genetic Analysis of Single Disseminated Cancer Cells for Prediction of Outcome and Therapy Selection in Esophageal Cancer. Cancer Cell 13(5):441-453.
97. Strassman, J. E., Y. Zhu, and D. C. Queller 2000. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408(6815):965.
98. Szakacs, G., J. K. Paterson, J. A. Ludwig, C. Booth-Genthe, and M. M. Gottesman 2006. Targeting multidrug resistance in cancer. Nature Reviews Drug Discovery 5(3):219-234.
99. Taylor, P 1992. Altruism in viscous populations - an inclusive fitness model. Evolutionary Ecology 6(4):352-356.
100. Taylor, T. B., and A. Buckling 2010. Competition and Dispersal in Pseudomonas aeruginosa. The American Naturalist 176(1):83-89.
101. Taylor, P. D., and S. A. Frank 1996. How to Make a Kin Selection Model. Journal of Theoretical Biology 180(1):27-37.
102. Tlsty, T. D. 2001. Stromal cells can contribute oncogenic signals. Seminars in Cancer Biology 11(2):97-104.
103. Turke, A. B., K. Zejnullahu, Y. Wu, Y. Song, D. Dias-Santagata, E. Lifshits, L. Toschi et al. 2010. Preexistence and Clonal Selection of MET Amplification in EGFR Mutant NSCLC. Cancer Cell 17(1):77-88.
104. Turner, P. E., and L. Chao 1999. Prisoner's dilemma in an RNA virus. Nature 398(6726):441-443.
105. Vaupel, P., and L. Harrison 2004. Tumor Hypoxia: Causative Factors, Compensatory Mechanisms, and Cellular Response. The Oncologist 9(suppl 5):4-9.
106. Velicer, G. J., L. Kroos, and R. E. Lenski 2000. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404(6778):598-601.
107. Vogelstein, B., and K. W. Kinzler 1993. The multistep nature of cancer. Trends in Genetics 9(4):138-141.
108. Weaver, V. M., and P. Gilbert 2004. Watch thy neighbor: cancer is a communal affair. Journal of Cell Science 117(8):1287-1290.
109. Wei, Y., X. Wang, J. Liu, I. Nememan, A. H. Singh, H. Weiss, and B. R. Levin 2011. The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility. Proceedings of the National Academy of Sciences 108(10):4047-4052.
110. West, S. A., S. P. Diggle, A. Buckling, A. Gardner, and A. S. Griffin 2007. The Social Lives of Microbes. Annual Review of Ecology, Evolution, and Systematics 38(1):53-77.
111. Wielgoss, S., J. E. Barrick, O. Tenaillon, S. Cruveiller, B. Chane-Woon-Ming, C. Médigue, R. E. Lenski et al. 2011. Mutation Rate Inferred From Synonymous Substitutions in a Long-Term Evolution Experiment With Escherichia coli. G3: Genes, Genomes, Genetics 1(3):183-186.
112. Woods, R., D. Schneider, C. L. Winkworth, M. A. Riley, and R. E. Lenski 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences 103(24):9107-9112.
113. Yap, T., C. Swanton, and J. de Bono 2012. Personalization of prostate cancer prevention and therapy: are clinically qualified biomarkers in the horizon? The EPMA Journal 3(1):1-7.
114. Zhang, L., W. Zhou, V. E. Velculescu, S. E. Kern, R. H. Hruban, S. R. Hamilton, B. Vogelstein et al. 1997. Gene expression profiles in normal and cancer cells. Science, 276(5316):1268-1272.