Problems of somatic mutation and cancer
Corresponding Author
Steven A. Frank
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA.Search for more papers by this authorMartin A. Nowak
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA
Search for more papers by this authorCorresponding Author
Steven A. Frank
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA.Search for more papers by this authorMartin A. Nowak
Department of Ecology & Evolutionary Biology, University of California, Irvine CA 92717, USA
Search for more papers by this authorAbstract
Somatic mutation plays a key role in transforming normal cells into cancerous cells. The analysis of cancer progression therefore requires the study of how point mutations and chromosomal mutations accumulate in cellular lineages. The spread of somatic mutations depends on the mutation rate, the number of cell divisions in the history of a cellular lineage, and the nature of competition between different cellular lineages. We consider how various aspects of tissue architecture and cellular competition affect the pace of mutation accumulation. We also discuss the rise and fall of somatic mutation rates during cancer progression. BioEssays 26:291–299, 2004. © 2004 Wiley Periodicals, Inc.
References
- 1 Maynard Smith J, Szathmáry E. 1995. The Major Transitions in Evolution. San Francisco: Freeman.
- 2 Frank SA. 1996. Models of parasite virulence. Quart Rev Biol 71: 37–78.
- 3 Buss LW. 1987. The Evolution of Individuality. Princeton: Princeton Univ Press.
- 4 Outzen HC. 1980. Development of carcinogen-induced skin tumors in mice with varied states of immune capacity. Int J Cancer 26: 87–92.
- 5 Prehn RT. 1994. Stimulatory effects of immune reactions upon the growths of untransplanted tumors. Cancer Res 54: 908–914.
- 6 Prehn RT. 1999. On the prevention and therapy of prostate cancer by androgen administration. Cancer Res 59: 4161–4164.
- 7 Prehn RT. 1994. Cancers beget mutations versus mutations beget cancers. Cancer Res 54: 5296–5300.
- 8 Anderson E. 2002. The role of oestrogen and progesterone receptors in human mammary development and tumorigenesis. Breast Cancer Res 4: 197–201.
- 9 Strickland JE, Ueda M, Henings H, Yuspa SH. 1992. A model for initiated mouse skin: suppression of cells in grafts on athymic nude mice. Cancer Res 52: 1439–1444.
- 10 Hethcote HW, Knudson AG. 1978. Model for the incidence of embryonal cancers: application to retinoblastoma. Proc Natl Acad Sci USA 75: 2453–2457.
- 11 Knudson AG. 1993. Antioncogenes and human cancer. Proc Natl Acad Sci USA 90: 10914–10921.
- 12 Vogelstein B, Kinzler KW. 2002. The Genetic Basis of Human Cancer. 2nd ed. New York: McGraw-Hill.
- 13 Hutchinson JN, Muller WJ. 2000. Transgenic mouse models of human breast cancer. Oncogene 19: 6130–6137.
- 14 Nunney L. 1999. Lineage selection and the evolution of multistage carcinogenesis. Proc R Soc Lond B 266: 493–498.
- 15 Nunney L. 2003. The population genetics of multistage carcinogenesis. Proc R Soc Lond B 270: 1183–1191.
- 16 Mintz B. 1971. Clonal basis of mammalian differentiation. Symp Soc Exp Biol 25: 345–370.
- 17 Watt FM. 1998. Epidermal stem cells: markers, patterning and the control of stem cell fate. Phil Trans R Soc Lond B 353: 831–837.
- 18 Brittan M, Wright NA. 2002. Gastrointestinal stem cells. J Pathol 197: 492–509.
- 19 Janes SM, Lowell S, Hutter C. 2002. Epidermal stem cells. J Pathol 197: 479–491.
- 20 Marshman E, Booth C, Potten CS. 2002. The intestinal epithelial stem cell. BioEssays 24: 91–98.
- 21 Cairns J. 1975. Mutation selection and the natural history of cancer. Nature 255: 197–200.
- 22 Bach SP, Renehan AG, Potten CS. 2000. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 21: 469–476.
- 23 Schmidt GH, Winton DJ, Ponder BA. 1988. Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103: 785–790.
- 24 Loeffler M, Birke A, Winton D, Potten C. 1993. Somatic mutation, monoclonality and stochastic models of stem cell organization in the intestinal crypt. J Theor Biol 160: 471–491.
- 25 Yatabe Y, Tavaré S, Shibata D. 2001. Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci USA 98: 10839–10844.
- 26 Cairns J. 2002. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proc Natl Acad Sci USA 99: 10567–10570.
- 27 Merok JR, Lansita JA, Tunstead JR, Sherley JL. 2002. Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res 62: 6791–6795.
- 28 Potten CS, Owen G, Booth D. 2002. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 115: 2381–2388.
- 29 Potten CS. 1998. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Phil Trans R Soc Lond B 353: 821–830.
- 30 Michor F, Nowak MA, Frank SA, Iwasa Y. 2003. Stochastic elimination of cancer cells. Proc R Soc Lond B 270: 2017–2024.
- 31 Michor F, Iwasa Y, Komarova NL, Nowak MA. 2003. Local regulation of homeostasis favors chromosomal instability. Curr Biol 13: 581–584.
- 32 Frank SA. 2003. Somatic mutation: early steps in cancer depend on tissue architecture. Curr Biol 13: R261–R263.
- 33 Frank SA, Nowak MA. 2003. Developmental predisposition to cancer. Nature 422: 494.
- 34 Luria SE, Delbrück M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491–511.
- 35 Zheng Q. 1999. Progress of a half century in the study of the Luria-Delbr\ück distribution. Math Biosci 162: 1–32.
- 36 Nowell PC. 1976. The clonal evolution of tumor cell populations. Science 194: 23–28.
- 37 Loeb LA. 1991. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res 51: 3075–3079.
- 38 Armitage P, Doll R. 1957. A two-stage theory of carcinogenesis in relation to the age distribution of human cancer. Brit J Cancer 11: 161–169.
- 39 Fisher JC. 1958. Multiple-mutation theory of carcinogenesis. Nature 181: 651–652.
- 40 Tomlinson IPM, Novelli MR, Bodmer WF. 1996. The mutation rate and cancer. Proc Natl Acad Sci USA 93: 14800–14803.
- 41 Breivik J, Gaudernack G. 1999. Genomic instability, DNA methylation, and natural selection in colorectal carcinogenesis. Seminars in Cancer Biol 9: 245–254.
- 42 Rubin H. 2001. The role of selection in progressive neoplastic transformation. Adv Cancer Res 83: 159–207.
- 43 Cairns J. 1998. Mutation and cancer: the antecedents to our studies of adaptive mutation. Genetics 148: 1433–1440.
- 44 Lengauer C, Kinzler KW, Vogelstein B. 1997. Genetic instability in colorectal cancers. Nature 386: 623–627.
- 45 Strauss BS. 1998. Hypermutability and carcinogenesis. Genetics 148: 1619–1626.
- 46 Sniegowski PD, Gerrish PJ, Johnson T, Shaver A. 2000. The evolution of mutation rates: separating causes from consequences. BioEssays 22: 1057–1066.
- 47 Giraud A, Radman M, Matic I, Taddei F. 2001. The rise and fall of mutator bacteria. Curr Opinion Microbiol 4: 582–585.
- 48 de Visser JAGM. 2002. The fate of microbial mutators. Microbiology 148: 1247–1252.
- 49 Loeb LA. 1998. Cancer cells exhibit a mutator phenotype. Adv Cancer Res 72: 25–56.
- 50 Eigen M. 1971. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften 58: 465–523.
- 51 Eigen M, Schuster P. 1977. The hypercycle. A principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 64: 541–565.
- 52 Maynard Smith J. 1979. Hypercycles and the origin of life. Nature 280: 445–446.
- 53
Nowak MA,
May RM.
2000.
Virus Dynamics.
New York:
Oxford Univ Press.
10.1093/oso/9780198504184.001.0001 Google Scholar
- 54 Blackburn EH. 2000. Telomere states and cell fates. Nature 408: 53–56.
- 55 Artandi SE, DePinho RA. 2000. Mice without telomerase: what can they teach us about human cancer? Nature Med 6: 852–855.
- 56 Artandi SE, Alson S, Tietze JK, Sharpless NE, Ye S, Greenberg RA, Castrillon DH, Horner JW, Weiler SR, Carrasco RD, DePinho RA. 2002. Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc Natl Acad Sci USA 99: 8191–8196.
- 57 Stewart SA et al. 2002. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc Natl Acad Sci USA 99: 12606–12611.
- 58 Jones PA, Baylin SB. 2002. The fundamental role of epigenetic events in cancer. Nature Rev Genet 3: 415–428.
- 59 Graff JR, Gabrielson E, Fujii H, Baylin SB, Herman JG. 2000. Methylation patterns of the E-cadherin 5′ CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem 275: 2727–2732.
- 60 Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293: 1074–1080.
- 61 Cameron EE, Baylin SB, Herman JG. 1999. p15(INK4B) CpG island methylation in primary acute leukemia is heterogeneous and suggests density as a critical factor for transcriptional silencing. Blood 94: 2445–2451.
- 62 Okano M, Xie S, Li E. 1998. Cloning and characterization of a family of novel mammalian DNA (cytosine-5)-methyltransferases. Nature Genet 19: 219–220.
- 63 Robertson KD, Uzvolgyi E, Liang G, Talmadge C, Sumegi J, Gonzales FA, Jones PA. 1999. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res 27: 2291–2298.
- 64 Herweijer H, Wolff JA. 2003. Progress and prospects: naked DNA gene transfer and therapy. Gene Therapy 10: 453–458.