Tumorigenesis: It takes a village

Nature Reviews Cancer

Volumn 15, Issue 8, 2015, Pages 473-483

  Tabassum, Doris P ^a,b   Polyak, Kornelia ^b,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

CANCER CELL; CANCER PROGNOSIS; CANCER THERAPY; CARCINOGENESIS; CELL FUNCTION; CELL INTERACTION; CELL POPULATION; COOPERATION; DISEASE COURSE; DROSOPHILA MELANOGASTER; EVIDENCE BASED MEDICINE; GENETIC HETEROGENEITY; HUMAN; MATHEMATICAL MODEL; MOLECULAR BIOLOGY; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH; XENOTRANSPLANTATION; ANIMAL; BIOLOGICAL MODEL; CELL PROLIFERATION; METASTASIS; NEOPLASMS; PATHOLOGY;

ANIMALS; CARCINOGENESIS; CELL PROLIFERATION; HUMANS; MODELS, BIOLOGICAL; NEOPLASM METASTASIS; NEOPLASMS;

EID: 84937970942     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3971     Document Type: Review

References (90)

1. Aristotle Metaphysica Vol. 8, 1045a (1933)
2. Nowell, P. C. The clonal evolution of tumor cell populations. Science 194, 23-28 (1976)
3. Heppner, G. H. Tumor heterogeneity. Cancer Res. 44, 2259-2265 (1984)
4. Marusyk, A., Almendro, V. &Polyak, K. Intra-tumour heterogeneity: a looking glass for cancer? Nat. Rev. Cancer 12, 323-334 (2012)
5. Gerlinger, M. et al. Cancer: evolution within a lifetime. Annu. Rev. Genet. 48, 215-236 (2014)
6. McGranahan, N. &Swanton, C. Biological and therapeutic impact of intratumor heterogeneity in cancer evolution. Cancer Cell 27, 15-26 (2015)
7. Kreso, A. &Dick, J. E. Evolution of the cancer stem cell model. Cell Stem Cell 14, 275-291 (2014)
8. Lajara, R. et al. Dual regulation of insulin-like growth factor I expression during renal hypertrophy. Am. J. Physiol. 257, F252-F261 (1989)
9. Gillies, R. J., Verduzco, D. &Gatenby, R. A. Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat. Rev. Cancer 12, 487-493 (2012)
10. Fidler, I. J. &Kripke, M. L. Metastasis results from preexisting variant cells within a malignant tumor. Science 197, 893-895 (1977)
11. Dexter, D. L. et al. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res. 38, 3174-3181 (1978)
12. Fidler, I. J. Tumor heterogeneity and the biology of cancer invasion and metastasis. Cancer Res. 38, 2651-2660 (1978)
13. Miller, B. E., Miller, F. R., Wilburn, D. &Heppner, G. H. Dominance of a tumor subpopulation line in mixed heterogeneous mouse mammary tumors. Cancer Res. 48, 5747-5753 (1988)
14. Miller, B. E., Miller, F. R. &Heppner, G. H. Interactions between tumor subpopulations affecting their sensitivity to the antineoplastic agents cyclophosphamide and methotrexate. Cancer Res. 41, 4378-4381 (1981)
15. Miller, B. E., Machemer, T., Lehotan, M. &Heppner, G. H. Tumor subpopulation interactions affecting melphalan sensitivity in palpable mouse mammary tumors. Cancer Res. 51, 4378-4387 (1991)
16. Vogelstein, B. &Kinzler, K. W. Cancer genes and the pathways they control. Nat. Med. 10, 789-799 (2004)
17. Gatenby, R. A., Cunningham, J. J. &Brown, J. S. Evolutionary triage governs fitness in driver and passenger mutations and suggests targeting never mutations. Nat. Commun. 5, 5499 (2014)
18. Merlo, L. M., Pepper, J. W., Reid, B. J. &Maley, C. C. Cancer as an evolutionary and ecological process. Nat. Rev. Cancer 6, 924-935 (2006)
19. Egeblad, M., Nakasone, E. S. &Werb, Z. Tumors as organs: complex tissues that interface with the entire organism. Dev. Cell 18, 884-901 (2010)
20. Heppner, G. H. Tumor cell societies. J. Natl Cancer Inst. 81, 648-649 (1989)
21. Michelson, S. Facilitation of emergence of multidrug-resistant state by alteration of tumor environment: implications from competitive ecology models. Cancer Treat. Rep. 71, 1093-1094 (1987)
22. Tomlinson, I. &Bodmer, W. Selection, the mutation rate and cancer: ensuring that the tail does not wag the dog. Nat. Med. 5, 11-12 (1999)
23. Merlo, L. M., Kosoff, R. E., Gardiner, K. L. &Maley, C. C. An in vitro co-culture model of esophageal cells identifies ascorbic acid as a modulator of cell competition. BMC Cancer 11, 461 (2011)
24. Hanahan, D. &Weinberg, R. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011)
25. Axelrod, R., Axelrod, D. E. &Pienta, K. J. Evolution of cooperation among tumor cells. Proc. Natl Acad. Sci. USA 103, 13474-13479 (2006)
26. Korolev, K. S., Xavier, J. B. &Gore, J. Turning ecology and evolution against cancer. Nat. Rev. Cancer 14, 371-380 (2014)
27. Cleary, A. S., Leonard, T. L., Gestl, S. A. &Gunther, E. J. Tumour cell heterogeneity maintained by cooperating subclones in Wnt-driven mammary cancers. Nature 508, 113-117 (2014)
28. Marusyk, A. et al. Non-cell-Autonomous driving of tumour growth supports sub-clonal heterogeneity. Nature 514, 54-58 (2014)
29. Mateo, F. et al. SPARC mediates metastatic cooperation between CSC and non-CSC prostate cancer cell subpopulations. Mol. Cancer 13, 237 (2014)
30. Chapman, A. et al. Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep. 8, 688-695 (2014)
31. Hendrix, M. J., Seftor, E. A., Hess, A. R. &Seftor, R. E. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat. Rev. Cancer 3, 411-421 (2003)
32. Wagenblast, E. et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature 520, 358-362 (2015)
33. Michelson, S., Miller, B. E., Glicksman, A. S. &Leith, J. T. Tumor micro-ecology and competitive interactions. J. Theor. Biol. 128, 233-246 (1987)
34. Foster, K. R. Biomedicine. Hamiltonian medicine: why the social lives of pathogens matter. Science 308, 1269-1270 (2005)
35. Lambert, G. et al. An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat. Rev. Cancer 11, 375-382 (2011)
36. Crespi, B., Foster, K. &Ubeda, F. First principles of Hamiltonian medicine. Phil. Trans. R. Soc. B 369, 20130366 (2014)
37. Marusyk, A. &Polyak, K. Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta 1805, 105-117 (2010)
38. Archetti, M., Ferraro, D. A. &Christofori, G. Heterogeneity for IGF-II production maintained by public goods dynamics in neuroendocrine pancreatic cancer. Proc. Natl Acad. Sci. USA 112, 1833-1838 (2015)
39. Czaran, T. L., Hoekstra, R. F. &Pagie, L. Chemical warfare between microbes promotes biodiversity. Proc. Natl Acad. Sci. USA 99, 786-790 (2002)
40. Tomlinson, I. P. &Bodmer, W. F. Modelling the consequences of interactions between tumour cells. Br. J. Cancer 75, 157-160 (1997)
41. Waite, A. J. &Shou, W. Adaptation to a new environment allows cooperators to purge cheaters stochastically. Proc. Natl Acad. Sci. USA 109, 19079-19086 (2012)
42. Bondar, T. &Medzhitov, R. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6, 309-322 (2010)
43. Moreno, E. &Basler, K. dMyc transforms cells into super-competitors. Cell 117, 117-129 (2004)
44. Baker, N. E. Cell competition. Curr. Biol. 21, R11-R15 (2011)
45. Vincent, J. P., Fletcher, A. G. &Baena-Lopez, L. A. Mechanisms and mechanics of cell competition in epithelia. Nat. Rev. Mol. Cell Biol. 14, 581-591 (2013)
46. Amoyel, M. &Bach, E. A. Cell competition: how to eliminate your neighbours. Development 141, 988-1000 (2014)
47. Merino, M. M. et al. Elimination of unfit cells maintains tissue health and prolongs lifespan. Cell 160, 461-476 (2015)
48. Alcolea, M. P. &Jones, P. H. Cell competition: winning out by losing notch. Cell Cycle 14, 9-17 (2015)
49. Brumby, A. M. &Richardson, H. E. scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 22, 5769-5779 (2003)
50. Uhlirova, M., Jasper, H. &Bohmann, D. Non-cell-Autonomous induction of tissue overgrowth by JNK/Ras cooperation in a Drosophila tumor model. Proc. Natl Acad. Sci. USA 102, 13123-13128 (2005)
51. Wu, M., Pastor-Pareja, J. C. &Xu, T. Interaction between RasV12 and scribbled clones induces tumour growth and invasion. Nature 463, 545-548 (2010)
52. Ohsawa, S. et al. Mitochondrial defect drives non-Autonomous tumour progression through Hippo signalling in Drosophila. Nature 490, 547-551 (2012)
53. Calbo, J. et al. A functional role for tumor cell heterogeneity in a mouse model of small cell lung cancer. Cancer Cell 19, 244-256 (2011)
54. Zhang, M. et al. Intratumoral heterogeneity in a Trp53-null mouse model of human breast cancer. Cancer Discov. 5, 520-533 (2015)
55. Kern, S. E. &Shibata, D. The fuzzy math of solid tumor stem cells: a perspective. Cancer Res. 67, 8985-8988 (2007)
56. Duong, T. et al. VEGFD regulates blood vascular development by modulating SOX18 activity. Blood 123, 1102-1112 (2014)
57. Inda, M. M. et al. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 24, 1731-1745 (2010)
58. Eirew, P. et al. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature 518, 422-426 (2015)
59. Kreso, A. et al. Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339, 543-548 (2013)
60. Maley, C. C. et al. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat. Genet. 38, 468-473 (2006)
61. Notta, F. et al. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 469, 362-367 (2011)
62. Almendro, V. et al. Inference of tumor evolution during chemotherapy by computational modeling and in situ analysis of genetic and phenotypic cellular diversity. Cell Rep. 6, 514-527 (2014)
63. Aceto, N. et al. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell 158, 1110-1122 (2014)
64. Grant, P. R., Grant, B. R., Markert, J. A., Keller, L. F. &Petren, K. Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution 58, 1588-1599 (2004)
65. Snuderl, M. et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20, 810-817 (2011)
66. Francis, J. M. et al. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov. 4, 956-971 (2014)
67. Anderson, K. et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 469, 356-361 (2011)
68. Greaves, M. &Maley, C. C. Clonal evolution in cancer. Nature 481, 306-313 (2012)
69. Oesterreich, S. &Davidson, N. E. The search for ESR1 mutations in breast cancer. Nat. Genet. 45, 1415-1416 (2013)
70. Jeselsohn, R. et al. Emergence of constitutively active estrogen receptor-mutations in pretreated advanced estrogen receptor-positive breast cancer. Clin. Cancer Res. 20, 1757-1767 (2014)
71. Li, S. et al. Endocrine-therapy-resistant ESR1 variants revealed by genomic characterization of breast-cancer-derived xenografts. Cell Rep. 4, 1116-1130 (2013)
72. Toy, W. et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat. Genet. 45, 1439-1445 (2013)
73. Robinson, D. R. et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat. Genet. 45, 1446-1451 (2013)
74. Vogelstein, B. &Kinzler, K. W. Digital PCR. Proc. Natl Acad. Sci. USA 96, 9236-9241 (1999)
75. Hobor, S. et al. TGF? and amphiregulin paracrine network promotes resistance to EGFR blockade in colorectal cancer cells. Clin. Cancer Res. 20, 6429-6438 (2014)
76. Thliveris, A. T. et al. Transformation of epithelial cells through recruitment leads to polyclonal intestinal tumors. Proc. Natl Acad. Sci. USA 110, 11523-11528 (2013)
77. Fomchenko, E. I. et al. Recruited cells can become transformed and overtake PDGF-induced murine gliomas in vivo during tumor progression. PLoS ONE 6, e20605 (2011
78. Singh, R., Pochampally, R., Watabe, K., Lu, Z. &Mo, Y. Y. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol. Cancer 13, 256 (2014)
79. Gefen, O. &Balaban, N. Q. The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol. Rev. 33, 704-717 (2009)
80. Sharma, S. V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80 (2010)
81. Oliveira, N. M., Niehus, R. &Foster, K. R. Evolutionary limits to cooperation in microbial communities. Proc. Natl Acad. Sci. USA 111, 17941-17946 (2014)
82. Pepper, J. W., Scott Findlay, C., Kassen, R., Spencer, S. L. &Maley, C. C. Cancer research meets evolutionary biology. Evol. Appl. 2, 62-70 (2009)
83. Pepper, J. W. Defeating pathogen drug resistance: guidance from evolutionary theory. Evolution 62, 3185-3191 (2008)
84. Pienta, K. J., McGregor, N., Axelrod, R. &Axelrod, D. E. Ecological therapy for cancer: defining tumors using an ecosystem paradigm suggests new opportunities for novel cancer treatments. Transl Oncol. 1, 158-164 (2008)
85. Pepper, J. W. Drugs that target pathogen public goods are robust against evolved drug resistance. Evol. Appl. 5, 757-761 (2012)
86. Mateo, J., Gerlinger, M., Rodrigues, D. N. &de Bono, J. S. The promise of circulating tumor cell analysis in cancer management. Genome Biol. 15, 448 (2014)
87. De Mattos-Arruda, L. et al. Circulating tumour cells and cell-free DNA as tools for managing breast cancer. Nat. Rev. Clin. Oncol. 10, 377-389 (2013)
88. Haber, D. A. &Velculescu, V. E. Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. Cancer Discov. 4, 650-661 (2014)
89. Brown, R., Curry, E., Magnani, L., Wilhelm-Benartzi, C. S. &Borley, J. Poised epigenetic states and acquired drug resistance in cancer. Nat. Rev. Cancer 14, 747-753 (2014)
90. Al-Dimassi, S., Abou-Antoun, T. &El-Sibai, M. Cancer cell resistance mechanisms: a mini review. Clin. Transl Oncol. 16, 511-516 (2014