Direct measurements of human colon crypt stem cell niche genetic fidelity: The role of chance in non-Darwinian mutation selection

Frontiers in Oncology

Volumn 3 OCT, Issue , 2013, Pages

  Kang, Haeyoun ^a   Shibata, Darryl ^b  

^a CHA University   (South Korea)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aging; Human; Muller's ratchet; Neutral drift; Non Darwinian; Replication errors; Stem cell niche

Indexed keywords

ADOLESCENT; ADULT; AGED; AGING; ARTICLE; CELL DEATH; CELL DIVISION; CELL FATE; CELL POPULATION; CELL SURVIVAL; CHROMOSOME DELETION; CHROMOSOME NUMBER; CLINICAL ARTICLE; COLON; COLORECTAL CANCER; CONTROLLED STUDY; CRYPT CELL; CYTOARCHITECTURE; DNA MICROARRAY; FEMALE; GENE CONVERSION; GENE MUTATION; GENETIC ANALYSIS; GENETIC DRIFT; GENETIC FIDELITY; HETEROZYGOSITY LOSS; HUMAN; INTESTINE CRYPT; MALE; MIDDLE AGED; NEOPLASM; POINT MUTATION; REPRODUCTIVE FITNESS; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL NICHE; ULCERATIVE COLITIS; VERY ELDERLY;

EID: 84891047895     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00264     Document Type: Article

References (46)

1. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development (1990) 110:1001-20.
2. Humphries A, Wright NA. Colonic crypt organization and tumorigenesis. Nat Rev Cancer (2008) 8:415-24. doi: 10.1038/nrc2392
3. Cairns J. Mutation selection and the natural history of cancer. Nature (1975) 255:197-200. doi:10.1038/255197a0
4. Potten CS. Extreme sensitivity of some intestinal crypt cells to X and gamma irradiation. Nature (1977) 269:518-21. doi:10.1038/269518a0
5. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature (2007) 449:1003-7. doi:10.1038/nature06196
6. Clevers H. The intestinal crypt, a prototype stem cell compartment. Cell (2013) 154:274-84. doi:10.1016/j.cell.2013.07.004
7. Potten CS, Hume WJ, Reid P, Cairns J. The segregation of DNA in epithelial stem cells. Cell (1978) 15:899-906. doi:10.1016/0092-8674(78)90274-X
8. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci (2002) 115:2381-8.
9. Quyn AJ, Appleton PL, Carey FA, Steele RJ, Barker N, Clevers H, et al. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell (2010) 6:175-81. doi:10.1016/j.stem.2009.12.007
10. Schepers AG, Vries R, van den Born M, van de Wetering M, Clevers H. Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J (2011) 30:1104-9. doi:10.1038/emboj.2011.26
11. Escobar M, Nicolas P, Sangar F, Laurent-Chabalier S, Clair P, Joubert D, et al. Intestinal epithelial stem cells do not protect their genome by asymmetric chromosome segregation. Nat Commun (2011) 2:258. doi:10.1038/ncomms1260
12. Steinhauser ML, Bailey AP, Senyo SE, Guillermier C, Perlstein TS, Gould AP, et al. Multi-isotope imaging mass spectrometry quantifies stem cell division and metabolism. Nature (2012) 481:516-9. doi:10.1038/nature10734
13. Hsieh JC, Van Den Berg D, Kang H, Hsieh CL, Lieber MR. Large chromosome deletions, duplications, and gene conversion events accumulate with age in normal human colon crypts. Aging Cell (2013) 12:269-79. doi:10.1111/acel.12053
14. Lopez-Garcia C, Klein AM, Simons BD, Winton DJ. Intestinal stem cell replacement follows a pattern of neutral drift. Science (2010) 330:822-5. doi:10.1126/science.1196236
15. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell (2010) 143:134-44. doi:10.1016/j.cell.2010.09.016
16. Yatabe Y, Tavaré S, Shibata D. Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci U S A (2001) 98:10839-44. doi:10.1073/pnas.191225998
17. Campbell F, Williams GT, Appleton MA, Dixon MF, Harris M, Williams ED. Post-irradiation somatic mutation and clonal stabilisation time in the human colon. Gut (1996) 39:569-73. doi:10.1136/gut.39.4.569
18. O'Connor PM, Lapointe TK, Beck PL, Buret AG. Mechanisms by which inflammation may increase intestinal cancer risk in inflammatory bowel disease. Inflamm Bowel Dis (2010) 16:1411-20. doi:10.1002/ibd.21217
19. Saldivar JC, Shibata H, Huebner K. Pathology and biology associated with the fragile FHIT gene and gene product. J Cell Biochem (2010) 109:858-65.
20. Bignell GR, Greenman CD, Davies H, Butler AP, Edkins S, Andrews JM, et al. Signatures of mutation and selection in the cancer genome. Nature (2010) 463:893-8. doi:10.1038/nature08768
21. Ribas M, Masramon L, Aiza G, Capellà G, Miró R, Peinado MA. The structural nature of chromosomal instability in colon cancer cells. FASEB J (2003) 17:289-91.
22. Roschke AV, Stover K, Tonon G, Schäffer AA, Kirsch IR. Stable karyotypes in epithelial cancer cell lines despite high rates of ongoing structural and numerical chromosomal instability. Neoplasia (2002) 4:19-31. doi:10.1038/sj.neo.7900197
23. Thompson SL, Compton DA. Examining the link between chromosomal instability and aneuploidy in human cells. J Cell Biol (2008) 180:665-72. doi:10.1083/jcb.200712029
24. Lengauer C, Kinzler KW, Vogelstein B. Genetic instabilities in human cancers. Nature (1998) 396:643-9. doi:10.1038/25292
25. Lengauer C, Kinzler KW, Vogelstein B. Genetic instability in colorectal cancers. Nature (1997) 386:623-7. doi:10.1038/386623a0
26. Xie T, D'Ario G, Lamb JR, Martin E, Wang K, Tejpar S, et al. A comprehensive characterization of genome-wide copy number aberrations in colorectal cancer reveals novel oncogenes and patterns of alterations. PLoS ONE (2012) 7:e42001. doi:10.1371/journal.pone.0042001
27. Laurie CC, Laurie CA, Rice K, Doheny KF, Zelnick LR, McHugh CP, et al. Detectable clonal mosaicism from birth to old age and its relationship to cancer. Nat Genet (2012) 44:642-50. doi:10.1038/ng.2271
28. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell (2008) 132:598-611. doi:10.1016/j.cell.2008.01.038
29. Campbell F, Fuller CE, Williams GT, Williams ED. Human colonic stem cell mutation frequency with and without irradiation. J Pathol (1994) 174:175-82. doi:10.1002/path.1711740306
30. Greaves LC, Preston SL, Tadrous PJ, Taylor RW, Barron MJ, Oukrif D, et al. Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission. Proc Natl Acad Sci U S A (2006) 103:714-9. doi:10.1073/pnas.0505903103
31. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet (2007) 41:169-92. doi:10.1146/annurev.genet.41.042007.165900
32. King JL, Jukes TH. Non-Darwinian evolution. Science (1969) 16:788-98. doi:10.1126/science.164.3881.788
33. Whitlock MC, Bürger R. Fixation of new mutations in small populations. In: Ferrière R, Dieckmann U, Couvet D editors. Evolutionary Conservation Biology. Cambridge: Cambridge University Press (2004). p. 155-70.
34. Whitlock MC. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution (2000) 54:1855-61. doi:10.1111/j.0014-3820.2000.tb01232.x
35. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW. Cancer genome landscapes. Science (2013) 339:1546-58. doi:10.1126/science.1235122
36. 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. doi:10.1073/pnas.1221068110
37. Woo YJ, Siegmund KD, Tavaré S, Shibata D. Older individuals appear to acquire mitotically older colorectal cancers. J Pathol (2009) 217:483-8. doi:10.1002/path.2506
38. Wang TL, Rago C, Silliman N, Ptak J, Markowitz S, Willson JK, et al. Prevalence of somatic alterations in the colorectal cancer cell genome. Proc Natl Acad Sci U S A (2002) 99:3076-80. doi:10.1073/pnas.261714699
39. Rubin AF, Green P. Mutation patterns in cancer genomes. Proc Natl Acad Sci U S A (2009) 106:21766-70. doi:10.1073/pnas.0912499106
40. Woo YH, Li WH. DNA replication timing and selection shape the landscape of nucleotide variation in cancer genomes. Nat Commun (2012) 3:1004. doi:10.1038/ncomms1982
41. Calabrese P, Shibata D. A simple algebraic cancer equation: calculating how cancers may arise with normal mutation rates. BMC Cancer (2010) 10:3. doi:10.1186/1471-2407-10-3
42. Calabrese P, Tavaré S, Shibata D. Pre-tumor progression: clonal evolution of human stem cell populations. Am J Pathol (2004) 164:1337-46. doi:10.1016/S0002-9440(10)63220-8
43. Miller AJ, Dudley SD, Tsao JL, Shibata D, Liskay RM. Tractable Cre-lox system for stochastic alteration of genes in mice. Nat Methods (2008) 5:227-9. doi:10.1038/nmeth.1183
44. Fischer JM, Miller AJ, Shibata D, Liskay RM. Different phenotypic consequences of simultaneous versus stepwise Apc loss. Oncogene (2012) 31:2028-38. doi:10.1038/onc.2011.385
45. Tennessen JA, Bigham AW, O'Connor TD, Fu W, Kenny EE, Gravel S, et al. Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science (2012) 337:64-9. doi:10.1126/science.1219240
46. Felsenstein J. The evolutionary advantage of recombination. Genetics (1974) 78:737-56.