Volatility of Mutator Phenotypes at Single Cell Resolution

1. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, et al. (2006) DNA Repair and Mutagenesis. Washington, D.C.: ASM Press.

2. Preston BD, Albertson TM, Herr AJ (2010) DNA replication fidelity and cancer. Seminars in Cancer Biology 20: 281–293. doi: 10.1016/j.semcancer.2010.10.009 20951805

3. Loeb LA, Springgate CF, Battula N (1974) Errors in DNA replication as a basis of malignant changes. Cancer Res 34: 2311–2321. 4136142

4. Loeb LA (2011) Human cancers express mutator phenotypes: origin, consequences and targeting. Nat Rev Cancer 11: 450–457. doi: 10.1038/nrc3063 21593786

5. Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PMJ, Kunkel TA (2008) Division of labor at the eukaryotic replication fork. Molecular Cell 30: 137–144. doi: 10.1016/j.molcel.2008.02.022 18439893

6. Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6: 479–507. doi: 10.1146/annurev-pathol-011110-130235 21090969

7. Church DN, Briggs SEW, Palles C, Domingo E, Kearsey SJ, et al. (2013) DNA polymerase ε and δ exonuclease domain mutations in endometrial cancer. Human Molecular Genetics.

8. Yoshida R, Miyashita K, Inoue M, Shimamoto A, Yan Z, et al. (2011) Concurrent genetic alterations in DNA polymerase proofreading and mismatch repair in human colorectal cancer. European Journal of Human Genetics 19: 320–325. doi: 10.1038/ejhg.2010.216 21157497

9. Cancer Genome Atlas Network (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487: 330–337. doi: 10.1038/nature11252 22810696

10. Palles C, Cazier JB, Howarth KM, Domingo E, Jones AM, et al. (2012) Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nature Genetics 45: 136–144. doi: 10.1038/ng.2503 23263490

11. Kandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, et al. (2013) Integrated genomic characterization of endometrial carcinoma. Nature 497: 67–73. doi: 10.1038/nature12113 23636398

12. Goldsby RE, Hays LE, Chen X, Olmsted EA, Slayton WB, et al. (2002) High incidence of epithelial cancers in mice deficient for DNA polymerase δ proofreading. Proc Natl Acad Sci U S A 99: 15560–15565. 12429860

13. Goldsby RE, Lawrence NA, Hays LE, Olmsted EA, Chen X, et al. (2001) Defective DNA polymerase-δ proofreading causes cancer susceptibility in mice. Nat Med 7: 638–639. 11385474

14. Albertson TM, Ogawa M, Bugni JM, Hays LE, Chen Y, et al. (2009) DNA polymerase ε and δ proofreading suppress discrete mutator and cancer phenotypes in mice. Proc Natl Acad Sci U S A 106: 17101–17104. doi: 10.1073/pnas.0907147106 19805137

15. Shlien A, Campbell BB, de Borja R, Alexandrov LB, Merico D, et al. (2015) Combined hereditary and somatic mutations of replication error repair genes result in rapid onset of ultra-hypermutated cancers. Nature Genetics 47: 257–262. doi: 10.1038/ng.3202 25642631

16. Morrison A, Johnson AL, Johnston LH, Sugino A (1993) Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J 12: 1467–1473. 8385605

17. Tran HT, Gordenin DA, Resnick MA (1999) The 3′→5′ exonucleases of DNA polymerases δ and ε and the 5′→3′ exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol Cell Biol 19: 2000–2007. 10022887

18. Greene CN, Jinks-Robertson S (2001) Spontaneous frameshift mutations in Saccharomyces cerevisiae: accumulation during DNA replication and removal by proofreading and mismatch repair activities. Genetics 159: 65–75. 11560887

19. Sokolsky T, Alani E (2000) EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics 155: 589–599. 10835383

20. Herr AJ, Ogawa M, Lawrence NA, Williams LN, Eggington JM, et al. (2011) Mutator suppression and escape from replication error–induced extinction in yeast. PLoS Genet 7: e1002282. doi: 10.1371/journal.pgen.1002282 22022273

21. Williams LN, Herr AJ, Preston BD (2013) Emergence of DNA polymerase ε antimutators that escape error-Induced extinction in yeast. Genetics 193: 751–770. doi: 10.1534/genetics.112.146910 23307893

22. Shcherbakova PV, Pavlov YI, Chilkova O, Rogozin IB, Johansson E, et al. (2003) Unique error signature of the four-subunit yeast DNA polymerase epsilon. J Biol Chem 278: 43770–43780. 12882968

23. Pavlov YI, Noskov VN, O CY, Gordenin DA (1988) LYS2 gene mutability in diploids of Saccharomyces cerevisiae yeast. II. Frequency of mutants induced by 6-N-hydroxylaminopurine and propiolactone. Genetika 24: 1752–1760.

24. Pavlov YI, Noskov VN, Lange EK, Moiseeva EV, Pshenichnov MR, et al. (1991) The genetic activity of N6-hydroxyadenine and 2-amino-N6-hydroxyadenine in Escherichia coli, Salmonella typhimurium and Saccharomyces cerevisiae. Mutation Research/Environmental Mutagenesis and Related Subjects 253: 33–46.

25. Lada AG, Stepchenkova EI, Waisertreiger ISR, Noskov VN, Dhar A, et al. (2013) Genome-wide mutation avalanches induced in diploid yeast cells by a base analog or an APOBEC deaminase. PLoS Genet 9: e1003736. doi: 10.1371/journal.pgen.1003736 24039593

26. Tran HT, Degtyareva NP, Gordenin DA, Resnick MA (1999) Genetic factors affecting the impact of DNA polymerase δ proofreading activity on mutation avoidance in yeast. Genetics 152: 47–59. 10224242

27. Rosche WA, Foster PL (2000) Determining mutation rates in bacterial populations. Methods 20: 4–17. 10610800

28. Lynch M, Sung W, Morris K, Coffey N, Landry CR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci U S A 105: 9272–9277. doi: 10.1073/pnas.0803466105 18583475

29. Nishant KT, Wei W, Mancera E, Argueso JL, Schlattl A, et al. (2010) The baker's yeast diploid genome is remarkably stable in vegetative growth and meiosis. PLoS Genet 6: e1001109. doi: 10.1371/journal.pgen.1001109 20838597

30. Eberwine J, Sul JY, Bartfai T, Kim J (2014) The promise of single-cell sequencing. Nat Methods 11: 25–27. 24524134

31. Wang Y, Waters J, Leung ML, Unruh A, Roh W, et al. (2014) Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512: 155–160. doi: 10.1038/nature13600 25079324

32. Foster PL (2006) Methods for determining spontaneous mutation rates. Methods Enzymol 409: 195–213. 16793403

33. Zheng Q (2005) New algorithms for Luria-Delbruck fluctuation analysis. Mathematical Biosciences 196: 198–214. 15950991

34. Zheng Q (2008) A note on plating efficiency in fluctuation experiments. Mathematical Biosciences 216: 150–153. doi: 10.1016/j.mbs.2008.09.002 18822300

35. Drake JW (1991) A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci USA 88: 7160–7164. 1831267

36. Harrington JM, Kolodner RD (2007) Saccharomyces cerevisiae Msh2-Msh3 acts in repair of base-base mispairs. Mol Cell Biol 27: 6546–6554. 17636021

37. Luria SE, Delbruck M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491–511. 17247100

38. McLachlan GJ, Basford KE (1988) Mixture Models. New York: Marcel Dekker.

39. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115–121. 11588253

40. Akaike H (1976) An information criterion (AIC). Math Sci 14: 5–9.

41. Lang GI, Parsons L, Gammie AE (2013) Mutation rates, spectra, and genome-wide distribution of spontaneous mutations in mismatch repair deficient yeast. G3 (Bethesda) 3: 1453–1465. doi: 10.1534/g3.113.006429 23821616

42. Elez M, Murray AW, Bi L- J, Zhang X- E, Matic I, et al. (2010) Seeing Mutations in Living Cells. Current Biology 20: 1432–1437. doi: 10.1016/j.cub.2010.06.071 20674359

43. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, et al. (2010) A three-dimensional model of the yeast genome. Nature 465: 363–367. doi: 10.1038/nature08973 20436457

44. Meister P, Taddei A, Gasser SM (2006) In and out of the replication factory. Cell 125: 1233–1235. 16814710

45. Czajkowsky DM, Liu J, Hamlin JL, Shao Z (2008) DNA combing reveals intrinsic temporal disorder in the replication of yeast chromosome VI. Journal of Molecular Biology 375: 12–19. 17999930

46. McGuffee Sean R, Smith Duncan J, Whitehouse I (2013) Quantitative, genome-wide analysis of eukaryotic replication initiation and termination. Molecular Cell 50: 123–135. doi: 10.1016/j.molcel.2013.03.004 23562327

47. Pursell ZF, Isoz I, Lundstrom EB, Johansson E, Kunkel TA (2007) Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 317: 127–130. 17615360

48. Pavlov YI, Shcherbakova PV (2010) DNA polymerases at the eukaryotic fork-20 years later. Mutation Research 685: 45–53. doi: 10.1016/j.mrfmmm.2009.08.002 19682465

49. Garg P, Stith CM, Sabouri N, Johansson E, Burgers PM (2004) Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev 18: 2764–2773. 15520275

50. Lujan SA, Clausen AR, Clark AB, MacAlpine HK, MacAlpine DM, et al. (2014) Heterogeneous polymerase fidelity and mismatch repair bias genome variation and composition. Genome Research 24: 1751–1764. doi: 10.1101/gr.178335.114 25217194

51. Shinbrot E, Henninger EE, Weinhold N, Covington KR, Göksenin AY, et al. (2014) Exonuclease mutations In DNA polymerase epsilon reveal replication strand specific mutation patterns and human origins of replication. Genome Research 24: 2740–2750.

52. Kane DP, Shcherbakova PV (2014) A common cancer-associated DNA polymerase ε mutation causes an exceptionally strong mutator phenotype, indicating fidelity defects distinct from loss of proofreading. Cancer Research.

53. Herr AJ, Kennedy SR, Knowels GM, Schultz EM, Preston BD (2014) DNA replication error-induced extinction of diploid yeast. Genetics 196: 677–691. doi: 10.1534/genetics.113.160960 24388879

54. Sherman F (2002) Getting started with yeast. In: Guthrie C, Fink GR, editors. Part B: Guide to Yeast Genetics and Molecular and Cell Biology. Volume 350 ed. San Diego: Academic Press. pp. 3–41.

55. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. In: Fink CGaGR, editor. Part B: Guide to Yeast Genetics and Molecular and Cell Biology. Volume 350 ed: Academic Press. pp. 87–96.

56. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, et al. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115–132. 9483801

57. Zheng Q (2002) Statistical and algorithmic methods for fluctuation analysis with SALVADOR as an implementation. Mathematical Biosciences 176: 237–252. 11916511

58. Grogan DW, Carver GT, Drake JW (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci U S A 98: 7928–7933. 11427720

59. Drake JW (2009) Avoiding dangerous missense: thermophiles display especially low mutation rates. PLoS Genet 5: e1000520. doi: 10.1371/journal.pgen.1000520 19543367

60. Kaeberlein M, Powers RW 3rd, Steffen KK, Westman EA, Hu D, et al. (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310: 1193–1196. 16293764

61. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

62. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics 43: 491–498. doi: 10.1038/ng.806 21478889

63. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, et al. (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Research 22: 568–576. doi: 10.1101/gr.129684.111 22300766

64. Siow CC, Nieduszynska SR, Müller CA, Nieduszynski CA (2012) OriDB, the DNA replication origin database updated and extended. Nucleic Acids Research 40: D682–D686. doi: 10.1093/nar/gkr1091 22121216