Genome-wide analysis of the specificity and mechanisms of replication infidelity driven by imbalanced dNTP pools

Nucleic Acids Research

Volumn 44, Issue 4, 2015, Pages 1669-1680

  Watt, Danielle L ^a,b   Buckland, Robert J ^a   Lujan, Scott A ^b   Kunkel, Thomas A ^b   Chabes, Andrei ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYCYTIDINE TRIPHOSPHATE; DEOXYRIBONUCLEOSIDE TRIPHOSPHATE; THYMIDINE TRIPHOSPHATE; DEOXYRIBONUCLEOTIDE;

ARTICLE; CONTROLLED STUDY; DNA REPLICATION; DNA SEQUENCE; GENE DELETION; GENE INSERTION; GENOME ANALYSIS; MISMATCH REPAIR; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; CELL CYCLE; FUNGAL GENOME; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MUTAGENESIS; MUTATION; MUTATION RATE; NUCLEOTIDE SEQUENCE; SACCHAROMYCES CEREVISIAE;

BASE SEQUENCE; CELL CYCLE; DEOXYRIBONUCLEOTIDES; DNA MISMATCH REPAIR; DNA REPLICATION; GENOME, FUNGAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MUTAGENESIS; MUTATION; MUTATION RATE; SACCHAROMYCES CEREVISIAE;

EID: 84960479505     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1298     Document Type: Article

References (46)

1. Yao, N.Y., Schroeder, J.W., Yurieva, O., Simmons, L.A. and O'Donnell, M.E. (2013) Cost of rNTP/dNTP pool imbalance at the replication fork. Proc. Natl. Acad. Sci. U.S.A., 110, 12942-12947.
2. Kunz, B.A., Kohalmi, S.E., Kunkel, T.A., Mathews, C.K., McIntosh, E.M. and Reidy, J.A. (1994) International commission for protection against environmental mutagens and carcinogens. Deoxyribonucleoside triphosphate levels: a critical factor in the maintenance of genetic stability. Mutat. Res., 318, 1-64.
3. Mathews, C.K. (2006) DNA precursor metabolism and genomic stability. FASEB, 20, 1300-1314.
4. Mathews, C.K. (2014) Deoxyribonucleotides as genetic and metabolic regulators. FASEB J., 28, 3832-3840.
5. Jiricny, J. (2013) Postreplicative mismatch repair. Cold Spring Harb. Perspect. Biol., 5, 1-23.
6. Kumar, D., Abdulovic, A.L., Viberg, J., Nilsson, A.K., Kunkel, T.A. and Chabes, A. (2011) Mechanisms of mutagenesis in vivo due to imbalanced dNTP pools. Nucleic Acids Res., 39, 1360-1371.
7. Kumar, D., Viberg, J., Nilsson, A.K. and Chabes, A. (2010) Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res., 38, 3975-3983.
8. Buckland, R.J., Watt, D.L., Chittoor, B., Nilsson, A.K., Kunkel, T.A. and Chabes, A. (2014) Increased and imbalanced dNTP pools symmetrically promote both leading and lagging strand replication infidelity. PLoS Genet., 10, e1004846.
9. Lujan, S.A., Clausen, A.R., Clark, A.B., MacAlpine, H.K., MacAlpine, D.M., Malc, E.P., Mieczkowski, P.A., Burkholder, A.B., Fargo, D.C., Gordenin, D.A. et al. (2014) Heterogeneous polymerase fidelity and mismatch repair bias genome variation and composition. Genome Res., 24, 1751-1764.
10. Jia, S., Marjavaara, L., Buckland, R., Sharma, S. and Chabes, A. (2015) Determination of deoxyribonucleoside triphosphate concentrations in yeast cells by strong anion-exchange high-performance liquid chromatography coupled with ultraviolet detection. Methods Mol. Biol., 1300, 113-121.
11. Sabouri, N., Viberg, J., Goyal, D.K., Johansson, E. and Chabes, A. (2008) Evidence for lesion bypass by yeast replicative DNA polymerases during DNA damage. Nucleic Acids Res., 36, 5660-5667.
12. Larrea, A.A., Lujan, S.A., McElhinny, S.A.N., Mieczkowski, P.A., Resnick, M.A., Gordenin, D.A. and Kunkel, T.A. (2010) Genome-wide model for the normal eukaryotic DNA replication fork. Proc. Natl. Acad. Sci. U.S.A., 107, 17674-17679.
13. Schneider, T.D. and Stephens, R.M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100.
14. Johnson, R.E., Klassen, R., Prakash, L. and Prakash, S. (2015) A major role of DNA polymerase delta in replication of both the leading and lagging DNA strands. Mol. Cell, 59, 163-175.
15. Clausen, A.R., Lujan, S.A., Burkholder, A.B., Orebaugh, C.D., Williams, J.S., Clausen, M.F., Malc, E.P., Mieczkowski, P.A., Fargo, D.C., Smith, D.J. et al. (2015) Tracking replication enzymology in vivo by genome-wide mapping of ribonucleotide incorporation. Nat. Struct. Mol. Biol., 22, 185-191.
16. Daigaku, Y., Keszthelyi, A., Müller, C.A., Miyabe, I., Brooks, T., Retkute, R., Hubank, M., Nieduszynski, C.A. and Carr, A.M. (2015) A global profile of replicative polymerase usage. Nat. Struct. Mol. Biol., 22, 192-198.
17. Koh, K.D., Balachander, S., Hesselberth, J.R. and Storici, F. (2015) Ribose-seq: global mapping of ribonucleotides embedded in genomic DNA. Nat. Methods, 12, 251-257.
18. Reijns, M.A., Kemp, H., Ding, J., de Proce, S.M., Jackson, A.P. and Taylor, M.S. (2015) Lagging-strand replication shapes the mutational landscape of the genome. Nature, 518, 502-506.
19. Sasaki, S., Mello, C.C., Shimada, A., Nakatani, Y., Hashimoto, S., Ogawa, M., Matsushima, K., Gu, S.G., Kasahara, M., Ahsan, B. et al. (2009) Chromatin-associated periodicity in genetic variation downstream of transcriptional start sites. Science, 323, 401-404.
20. Tolstorukov, M.Y., Volfovsky, N., Stephens, R.M. and Park, P.J. (2011) Impact of chromatin structure on sequence variability in the human genome. Nat. Struct. Mol. Biol., 18, 510-515.
21. Phear, G., Nalbantoglu, J. and Meuth, M. (1987) Next-nucleotide effects in mutations driven by DNA precursor pool imbalances at the aprt locus of Chinese hamster ovary cells. Proc. Natl. Acad. Sci. U.S.A., 84, 4450-4454.
22. Kunkel, T.A., Schaaper, R.M., Beckman, R.A. and Loeb, L.A. (1981) On the fidelity of DNA replication. Effect of the next nucleotide on proofreading. J. Biol. Chem., 256, 9883-9889.
23. Fersht, A.R. (1979) Fidelity of replication of phage phi X174 DNA by DNA polymerase III holoenzyme: spontaneous mutation by misincorporation. Proc. Natl. Acad. Sci. U.S.A., 76, 4946-4950.
24. Ninio, J. (1975) Kinetic amplification of enzyme discrimination. Biochimie, 57, 587-595.
25. Streisinger, G., Okada, Y., Emrich, J., Newton, J., Tsugita, A., Terzaghi, E. and Inouye, M. (1966) Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb. Symp. Quant. Biol., 31, 77-84.
26. Kunkel, T.A. (1990) Misalignment-mediated DNA synthesis errors. Biochemistry, 29, 8003-8011.
27. Garcia-Diaz, M. and Kunkel, T.A. (2006) Mechanism of a genetic glissando: structural biology of indel mutations. Trends Biochem. Sci., 31, 206-214.
28. Lujan, S.A., Clark, A.B. and Kunkel, T.A. (2015) Differences in genome-wide repeat sequence instability conferred by proofreading and mismatch repair defects. Nucleic Acids Res., 43, 4067-4074.
29. Bebenek, K., Roberts, J.D. and Kunkel, T.A. (1992) The effects of dNTP pool imbalances on frameshift fidelity during DNA replication. J. Biol. Chem., 267, 3589-3596.
30. Kroutil, L.C., Register, K., Bebenek, K. and Kunkel, T.A. (1996) Exonucleolytic proofreading during replication of repetitive DNA. Biochemistry, 35, 1046-1053.
31. Swan, M.K., Johnson, R.E., Prakash, L., Prakash, S. and Aggarwal, A.K. (2009) Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase delta. Nat. Struct. Mol. Biol., 16, 979-986.
32. Hogg, M., Osterman, P., Bylund, G.O., Ganai, R.A., Lundstrom, E.B., Sauer-Eriksson, A.E. and Johansson, E. (2014) Structural basis for processive DNA synthesis by yeast DNA polymerase epsilon. Nat. Struct. Mol. Biol., 21, 49-55.
33. Ganai, R.A., Bylund, G.O. and Johansson, E. (2015) Switching between polymerase and exonuclease sites in DNA polymerase epsilon. Nucleic Acids Res., 43, 932-942.
34. Kunkel, T.A. (1986) Frameshift mutagenesis by eucaryotic DNA polymerases in vitro. J. Biol. Chem., 261, 13581-13587.
35. Efrati, E., Tocco, G., Eritja, R., Wilson, S.H. and Goodman, M.F. (1997) Abasic translesion synthesis by DNA polymerase beta violates the 'A-rule'. Novel types of nucleotide incorporation by human DNA polymerase beta at an abasic lesion in different sequence contexts. J. Biol. Chem., 272, 2559-2569.
36. Hashim, M.F., Schnetz-Boutaud, N. and Marnett, L.J. (1997) Replication of template-primers containing propanodeoxyguanosine by DNA polymerase beta. Induction of base pair substitution and frameshift mutations by template slippage and deoxynucleoside triphosphate stabilization. J. Biol. Chem., 272, 20205-20212.
37. Tippin, B., Kobayashi, S., Bertram, J.G. and Goodman, M.F. (2004) To slip or skip, visualizing frameshift mutation dynamics for error-prone DNA polymerases. J. Biol. Chem., 279, 45360-45368.
38. Kunkel, T.A. and Soni, A. (1988) Mutagenesis by transient misalignment. J. Biol. Chem., 263, 14784-14789.
39. Bebenek, K. and Kunkel, T.A. (1990) Frameshift errors initiated by nucleotide misincorporation. Proc. Natl. Acad. Sci. U.S.A., 87, 4946-4950.
40. Palles, C., Cazier, J.B., Howarth, K.M., Domingo, E., Jones, A.M., Broderick, P., Kemp, Z., Spain, S.L., Guarino, E., Salguero, I. et al. (2013) Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat. Genet., 45, 136-144.
41. Church, D.N., Briggs, S.E., Palles, C., Domingo, E., Kearsey, S.J., Grimes, J.M., Gorman, M., Martin, L., Howarth, K.M., Hodgson, S.V. et al. (2013) DNA polymerase epsilon and delta exonuclease domain mutations in endometrial cancer. Hum. Mol. Genet., 22, 2820-2828.
42. Goldsby, R.E., Hays, L.E., Chen, X., Olmsted, E.A., Slayton, W.B., Spangrude, G.J. and Preston, B.D. (2002) High incidence of epithelial cancers in mice deficient for DNA polymerase delta proofreading. Proc. Natl. Acad. Sci. U.S.A., 99, 15560-15565.
43. Albertson, T.M., Ogawa, M., Bugni, J.M., Hays, L.E., Chen, Y., Wang, Y., Treuting, P.M., Heddle, J.A., Goldsby, R.E. and Preston, B.D. (2009) DNA polymerase epsilon and delta proofreading suppress discrete mutator and cancer phenotypes in mice. Proc. Natl. Acad. Sci. U.S.A., 106, 17101-17104.
44. Aye, Y., Li, M., Long, M.J. and Weiss, R.S. (2015) Ribonucleotide reductase and cancer: biological mechanisms and targeted therapies. Oncogene, 34, 2011-2021.
45. Mertz, T.M., Sharma, S., Chabes, A. and Shcherbakova, P.V. (2015) Colon cancer-associated mutator DNA polymerase delta variant causes expansion of dNTP pools increasing its own infidelity. Proc. Natl. Acad. Sci. U.S.A., 112, E2467-E2476.
46. Donley, N. and Thayer, M.J. (2013) DNA replication timing, genome stability and cancer: late and/or delayed DNA replication timing is associated with increased genomic instability. Semin. Cancer Biol., 23, 80-89.