Beyond translesion synthesis: Polymerase κ fidelity as a potential determinant of microsatellite stability

Nucleic Acids Research

Volumn 40, Issue 4, 2012, Pages 1636-1647

  Hile, Suzanne E ^a   Wang, Xiaoxiao ^b   Lee, Marietta Y W T ^b   Eckert, Kristin A ^a  

^a PENN STATE CANCER INSTITUTE   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE ETA; DNA POLYMERASE; DNA POLYMERASE DELTA4; DNA POLYMERASE KAPPA; GUANINE; HOLOENZYME; MICROSATELLITE DNA; REPETITIVE DNA; THYMIDINE KINASE; THYMINE; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DNA REPLICATION; DNA SYNTHESIS; HERPES SIMPLEX VIRUS; HUMAN; IN VITRO STUDY; INDEL MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN STABILITY;

ALLELES; DNA; DNA DAMAGE; DNA POLYMERASE III; DNA-DIRECTED DNA POLYMERASE; HUMANS; INDEL MUTATION; MICROSATELLITE INSTABILITY; MICROSATELLITE REPEATS;

SIMPLEXVIRUS;

EID: 84863280866     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr889     Document Type: Article

References (60)

1. Richard, G. F., Kerrest, A. and Dujon, B. (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol. Mol. Biol. Rev., 72, 686-727.
2. Subramanian, S., Mishra, R. K. and Singh, L. (2003) Genome-wide analysis of microsatellite repeats in humans: their abundance and density in specific genomic regions. Genome biol., 4, R13.
3. Gemayel, R., Vinces, M. D., Legendre, M. and Verstrepen, K. J. (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu. Rev. Genet., 44, 445-477.
4. Hefferon, T. W., Groman, J. D., Yurk, C. E. and Cutting, G. R. (2004) A variable dinucleotide repeat in the CFTR gene contributes to phenotype diversity by forming RNA secondary structures that alter splicing. Proc. Natl Acad. Sci. USA, 101, 3504-3509. (Pubitemid 38338225)
5. Gangwal, K., Sankar, S., Hollenhorst, P. C., Kinsey, M., Haroldsen, S. C., Shah, A. A., Boucher, K. M., Watkins, W. S., Jorde, L. B., Graves, B. J. et al. (2008) Microsatellites as EWS/FLI response elements in Ewing's sarcoma. Proc. Natl Acad. Sci. USA, 105, 10149-10154.
6. Mirkin, S. M. (2007) Expandable DNA repeats and human disease. Nature, 447, 932-940. (Pubitemid 46975760)
7. Waters, L. S., Minesinger, B. K., Wiltrout, M. E., D'Souza, S., Woodruff, R. V. and Walker, G. C. (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev., 73, 134-154.
8. Sweasy, J. B., Lauper, J. M. and Eckert, K. A. (2006) DNA polymerases and human diseases. Radiat. Res., 166, 693-714. (Pubitemid 44706607)
9. Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T. et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8. (Pubitemid 32772900)
10. Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K. and Hanaoka, F. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature, 399, 700-704. (Pubitemid 29289067)
11. Johnson, R. E., Washington, M. T., Prakash, S. and Prakash, L. (2000) Fidelity of human DNA polymerase eta. J. Biol. Chem., 275, 7447-7450. (Pubitemid 30159635)
12. Masutani, C., Kusumoto, R., Iwai, S. and Hanaoka, F. (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase eta. Embo. J., 19, 3100-3109. (Pubitemid 30386780)
13. Avkin, S., Goldsmith, M., Velasco-Miguel, S., Geacintov, N., Friedberg, E. C. and Livneh, Z. (2004) Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells: the role of DNA polymerase kappa. J. Biol. Chem., 279, 53298-53305. (Pubitemid 40051834)
14. Jarosz, D. F., Godoy, V. G., Delaney, J. C., Essigmann, J. M. and Walker, G. C. (2006) A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature, 439, 225-228. (Pubitemid 43083146)
15. Rey, L., Sidorova, J. M., Puget, N., Boudsocq, F., Biard, D. S., Monnat, R. J. Jr, Cazaux, C. and Hoffmann, J. S. (2009) Human DNA polymerase eta is required for common fragile site stability during unperturbed DNA replication. Mol. Cell. Biol., 29, 3344-3354.
16. Betous, R., Rey, L., Wang, G., Pillaire, M. J., Puget, N., Selves, J., Biard, D. S., Shin-ya, K., Vasquez, K. M., Cazaux, C. et al. (2009) Role of TLS DNA polymerases eta and kappa in processing naturally occurring structured DNA in human cells. Mol. Carcinog., 48, 369-378.
17. Ogi, T., Limsirichaikul, S., Overmeer, R. M., Volker, M., Takenaka, K., Cloney, R., Nakazawa, Y., Niimi, A., Miki, Y., Jaspers, N. G. et al. (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Mol. Cell, 37, 714-727.
18. Burr, K. L., Velasco-Miguel, S., Duvvuri, V. S., McDaniel, L. D., Friedberg, E. C. and Dubrova, Y. E. (2006) Elevated mutation rates in the germline of Polkappa mutant male mice. DNA Repair, 5, 860-862. (Pubitemid 43928884)
19. Bebenek, K. and Kunkel, T. A. (2004) Functions of DNA polymerases. Adv. Protein Chem., 69, 137-165. (Pubitemid 39600959)
20. Fortune, J. M., Pavlov, Y. I., Welch, C. M., Johansson, E., Burgers, P. M. and Kunkel, T. A. (2005) Saccharomyces cerevisiae DNA polymerase delta: high fidelity for base substitutions but lower fidelity for single-and multi-base deletions. J. Biol. Chem., 280, 29980-29987. (Pubitemid 41177077)
21. Korona, D. A., Lecompte, K. G. and Pursell, Z. F. (2010) The high fidelity and unique error signature of human DNA polymerase epsilon. Nucleic Acids Res., 39, 1763-1773.
22. Abdulovic, A. L., Hile, S. E., Kunkel, T. A. and Eckert, K. A. (2011) The in vitro fidelity of yeast DNA polymerase delta and polymerase varepsilon holoenzymes during dinucleotide microsatellite DNA synthesis. DNA Repair, 10, 497-505.
23. Xie, B., Mazloum, N., Liu, L., Rahmeh, A., Li, H. and Lee, M. Y. (2002) Reconstitution and characterization of the human DNA polymerase delta four-subunit holoenzyme. Biochemistry, 41, 13133-13142. (Pubitemid 35244702)
24. Eckert, K. A., Mowery, A. and Hile, S. E. (2002) Misalignment-mediated DNA polymerase beta mutations: comparison of microsatellite and frame-shift error rates using a forward mutation assay. Biochemistry, 41, 10490-10498.
25. Hile, S. E. and Eckert, K. A. (2008) DNA polymerase kappa produces interrupted mutations and displays polar pausing within mononucleotide microsatellite sequences. Nucleic Acids Res., 36, 688-696. (Pubitemid 351250458)
26. Eckert, K. A., Hile, S. E. and Vargo, P. L. (1997) Development and use of an in vitro HSV-tk forward mutation assay to study eukaryotic DNA polymerase processing of DNA alkyl lesions. Nucleic Acids Res., 25, 1450-1457. (Pubitemid 27303676)
27. Opresko, P. L., Sweasy, J. B. and Eckert, K. A. (1998) The mutator form of polymerase beta with amino acid substitution at tyrosine 265 in the hinge region displays an increase in both base substitution and frame shift errors. Biochemistry, 37, 2111-2119. (Pubitemid 28119285)
28. Hile, S. E. and Eckert, K. A. (2004) Positive correlation between DNA polymerase alpha-primase pausing and mutagenesis within polypyrimidine/ polypurine microsatellite sequences. J. Mol. Biol., 335, 745-759. (Pubitemid 38352817)
29. Hashimoto, K., Shimizu, K., Nakashima, N. and Sugino, A. (2003) Fidelity of DNA polymerase delta holoenzyme from Saccharomyces cerevisiae: the sliding clamp proliferating cell nuclear antigen decreases its fidelity. Biochemistry, 42, 14207-14213. (Pubitemid 37499417)
30. Matsuda, T., Bebenek, K., Masutani, C., Rogozin, I. B., Hanaoka, F. and Kunkel, T. A. (2001) Error rate and specificity of human and murine DNA polymerase eta. J. Mol. Biol., 312, 335-346. (Pubitemid 32928129)
31. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W. J., Gerlach, V. L., Friedberg, E. C., Ohmori, H. and Kunkel, T. A. (2000) Fidelity and processivity of DNA synthesis by DNA polymerase kappa, the product of the human DINB1 gene. J. Biol. Chem., 275, 39678-39684. (Pubitemid 32058996)
32. Schmitt, M. W., Matsumoto, Y. and Loeb, L. A. (2009) High fidelity and lesion bypass capability of human DNA polymerase delta. Biochimie, 91, 1163-1172.
33. Eckert, K. A. and Hile, S. E. (2009) Every microsatellite is different: Intrinsic DNA features dictate mutagenesis of common microsatellites present in the human genome. Mol. Carcinog., 48, 379-388.
34. Kelkar, Y. D., Strubczewski, N., Hile, S. E., Chiaromonte, F., Eckert, K. A. and Makova, K. D. (2010) What is a microsatellite: a computational and experimental definition based upon repeat mutational behavior at A/T and GT/AC repeats. Genome Biol. Evol., 2, 620-635.
35. Indiani, C., Langston, L. D., Yurieva, O., Goodman, M. F. and O'Donnell, M. (2009) Translesion DNA polymerases remodel the replisome and alter the speed of the replicative helicase. Proc. Natl Acad. Sci. USA, 106, 6031-6038.
36. Zhuang, Z., Johnson, R. E., Haracska, L., Prakash, L., Prakash, S. and Benkovic, S. J. (2008) Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc. Natl Acad. Sci. USA, 105, 5361-5366. (Pubitemid 351753868)
37. Guo, C., Kosarek-Stancel, J. N., Tang, T. S. and Friedberg, E. C. (2009) Y-family DNA polymerases in mammalian cells. Cell. Mol. Life Sci., 66, 2363-2381.
38. Friedberg, E. C., Wagner, R. and Radman, M. (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science, 296, 1627-1630. (Pubitemid 34579143)
39. Takata, K. and Wood, R. D. (2009) Bypass specialists operate together. EMBO J., 28, 313-314.
40. Ogi, T., Shinkai, Y., Tanaka, K. and Ohmori, H. (2002) Pol kappa protects mammalian cells against the lethal and mutagenic effects of benzo[a]pyrene. Proc. Natl Acad. Sci. USA, 99, 15548-15553. (Pubitemid 35403971)
41. Perera, F., Hemminki, K., Jedrychowski, W., Whyatt, R., Campbell, U., Hsu, Y., Santella, R., Albertini, R. and O'Neill, J. P. (2002) In utero DNA damage from environmental pollution is associated with somatic gene mutation in newborns. Cancer Epidemiol. Biomarkers Prev., 11, 1134-1137. (Pubitemid 35192673)
42. Phillips, D. H., Hewer, A., Martin, C. N., Garner, R. C. and King, M. M. (1988) Correlation of DNA adduct levels in human lung with cigarette smoking. Nature, 336, 790-792. (Pubitemid 19014441)
43. Acharya, N., Johnson, R. E., Pages, V., Prakash, L. and Prakash, S. (2009) Yeast Rev1 protein promotes complex formation of DNA polymerase zeta with Pol32 subunit of DNA polymerase delta. Proc. Natl Acad. Sci. USA, 106, 9631-9636.
44. Ohashi, E., Hanafusa, T., Kamei, K., Song, I., Tomida, J., Hashimoto, H., Vaziri, C. and Ohmori, H. (2009) Identification of a novel REV1-interacting motif necessary for DNA polymerase kappa function. Genes Cells, 14, 101-111.
45. Bergoglio, V., Bavoux, C., Verbiest, V., Hoffmann, J. S. and Cazaux, C. (2002) Localisation of human DNA polymerase kappa to replication foci. J. Cell Sci., 115, 4413-4418. (Pubitemid 36004403)
46. Reyes-Lamothe, R., Sherratt, D. J. and Leake, M. C. (2010) Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science, 328, 498-501.
47. Langston, L. D., Indiani, C. and O'Donnell, M. (2009) Whither the replisome: emerging perspectives on the dynamic nature of the DNA replication machinery. Cell Cycle, 8, 2686-2691.
48. Yang, J., Zhuang, Z., Roccasecca, R. M., Trakselis, M. A. and Benkovic, S. J. (2004) The dynamic processivity of the T4 DNA polymerase during replication. Proc. Natl Acad. Sci. USA, 101, 8289-8294. (Pubitemid 38736568)
49. 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.
50. Lone, S., Townson, S. A., Uljon, S. N., Johnson, R. E., Brahma, A., Nair, D. T., Prakash, S., Prakash, L. and Aggarwal, A. K. (2007) Human DNA polymerase kappa encircles DNA: implications for mismatch extension and lesion bypass. Mol. Cell, 25, 601-614.
51. Wilson, R. C. and Pata, J. D. (2008) Structural insights into the generation of single-base deletions by the Y family DNA polymerase dbh. Mol. Cell, 29, 767-779. (Pubitemid 351400923)
52. Wu, Y., Wilson, R. C. and Pata, J. D. (2011) The Y-family DNA polymerase Dpo4 uses a template slippage mechanism to create single-base deletions. J. Bacteriol., 193, 2630-2636.
53. Imai, K. and Yamamoto, H. (2008) Carcinogenesis and microsatellite instability: the interrelationship between genetics and epigenetics. Carcinogenesis, 29, 673-680. (Pubitemid 351494153)
54. Halford, S., Sasieni, P., Rowan, A., Wasan, H., Bodmer, W., Talbot, I., Hawkins, N., Ward, R. and Tomlinson, I. (2002) Low-level microsatellite instability occurs in most colorectal cancers and is a nonrandomly distributed quantitative trait. Cancer Res., 62, 53-57. (Pubitemid 34073985)
55. Jass, J., Whitehall, V., Young, J., Leggett, B., Meltzer, S. J., Matsubara, N. and Fishel, R. (2002) Correspondance re: Laiho et al., Low level microsatellite instability in most colorectal carcinomas. Cancer Res., 62, 1166-1170, 5988-5990.
56. Laiho, P., Launonen, V., Lahermo, P., Esteller, M., Guo, M., Herman, J. G., Mecklin, J. P., Jarvinen, H., Sistonen, P., Kim, K. M. et al. (2002) Low-level microsatellite instability in most colorectal carcinomas. Cancer Res., 62, 1166-1170. (Pubitemid 34160304)
57. Hofseth, L. J., Khan, M. A., Ambrose, M., Nikolayeva, O., Xu-Welliver, M., Kartalou, M., Hussain, S. P., Roth, R. B., Zhou, X., Mechanic, L. E. et al. (2003) The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation. J. Clin. Invest., 112, 1887-1894. (Pubitemid 38063712)
58. Whitehall, V. L., Walsh, M. D., Young, J., Leggett, B. A. and Jass, J. R. (2001) Methylation of O-6-methylguanine DNA methyltransferase characterizes a subset of colorectal cancer with low-level DNA microsatellite instability. Cancer Res., 61, 827-830. (Pubitemid 32174386)
59. Lemee, F., Bavoux, C., Pillaire, M. J., Bieth, A., Machado, C. R., Pena, S. D., Guimbaud, R., Selves, J., Hoffmann, J. S. and Cazaux, C. (2007) Characterization of promoter regulatory elements involved in downexpression of the DNA polymerase kappa in colorectal cancer. Oncogene, 26, 3387-3394. (Pubitemid 46788878)
60. Pillaire, M. J., Selves, J., Gordien, K., Gourraud, P. A., Gentil, C., Danjoux, M., Do, C., Negre, V., Bieth, A., Guimbaud, R. et al. (2010) A 'DNA replication' signature of progression and negative outcome in colorectal cancer. Oncogene, 29, 876-887.