DNA binding properties of human DNA polymerase η: Implications for fidelity and polymerase switching of translesion synthesis

Genes to Cells

Volumn 9, Issue 12, 2004, Pages 1139-1150

  Kusumoto, Rika ^a,c   Masutani, Chikahide ^a   Shimmyo, Shizu ^a   Iwai, Shigenori ^a   Hanaoka, Fumio ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b Japan Science and Technology Agency   (Japan)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; COMPLEMENTARY DNA; CYCLOBUTANE; DIMER; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DOUBLE STRANDED DNA; NUCLEOTIDE; PRIMER DNA; SINGLE STRANDED DNA; THYMINE;

3' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; CANCER SUSCEPTIBILITY; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME ASSAY; GEL MOBILITY SHIFT ASSAY; GENETIC VARIABILITY; HUMAN; MOLECULAR STABILITY; PRIORITY JOURNAL; XERODERMA PIGMENTOSUM;

BASE SEQUENCE; DNA; DNA DAMAGE; DNA POLYMERASE I; DNA POLYMERASE III; DNA PRIMERS; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; ENZYME STABILITY; HUMANS; MOLECULAR SEQUENCE DATA; PYRIMIDINE DIMERS; TEMPLATES, GENETIC;

EID: 10244237651     PISSN: 13569597     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2004.00797.x     Document Type: Article

References (50)

1. Bebenek, K., Matsuda, T., Masmani, C., Hanaoka, F. & Kunkel, T.A. (2001) Proofreading of DNA polymerase η-dependent replication errors. J. Biol. Chem. 276, 2317-2320.
2. Boudsocq, F., Ling, H., Yang, W. & Woodgate, R. (2002) Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass. DNA Repair (Amst) 1, 343-358.
3. Echols, H. & Goodman, M.F. (1991) Fidelity mechanisms in DNA replication. Annu. Rev. Biochem. 60, 477-511.
4. Eki, T., Enomoto, T., Masutani, C., et al. (1991) Mouse DNA primase plays the principal role in determination of permissiveness for polyomavirus DNA replication. J. Virol. 65, 4874-4881.
5. Fien, K. & Stillman, B. (1992) Identification of replication factor C from Saccharomyces cerevisiae: a component of the leading-strand DNA replication complex. Mol. Cell. Biol. 12, 155-163.
6. Friedberg, E.C., Wagner, R. & Radman, M. (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296, 1627-1630.
7. Goodman, M.F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71, 17-50.
8. Guo, C., Fischhaber, P.I., Luk-Paszyc, M.J., et al. (2003) Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 22, 6621-6630.
9. Guo, D., Wu, X., Rajpal, D.K., Taylor, J.S. & Wang, Z. (2001) Translesion synthesis by yeast DNA polymerase ζ from templates containing lesions of ultraviolet radiation and acetylaminofluorene. Nucl. Acids Res. 29, 2875-2883.
10. Haracska, L., Johnson, R.E., Unk, I., et al. (2001a) Physical and functional interactions of human DNA polymerase η with PCNA. Mol. Cell. Biol. 21, 7199-7206.
11. Haracska, L., Kondratick, C.M., Unk, I., Prakash, S. & Prakash, L. (2001b) Interaction with PCNA is essential for yeast DNA polymerase η function. Mol. Cell 8, 407-415.
12. Haracska, L., Unk, I., Johnson, R.E., et al. (2002) Stimulation of DNA synthesis activity of human DNA polymerase κ by PCNA. Mol. Cell. Biol. 22, 784-791.
13. Hoege, C., Pfander, B., Moldovan, G.L., Pyrowolakis, G. & Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141.
14. Johnson, R.E., Yu S.L., Prakash, S. & Prakash, L. (2003) Yeast DNA polymerase ζ (zeta) is essential for error-free replication past thymine glycol. Genes Dev. 17, 77-87.
15. Johnson, R.E., Kondratick, C.M., Prakash, S. & Prakash, L. (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285, 263-265.
16. Johnson, R.E., Washington, M.T., Prakash, S. & Prakash, L. (2000) Fidelity of human DNA polymerase η. J. Biol. Chem. 275 7447-7450.
17. Kannouche, P., Broughton, B.C., Volker, M., Hanaoka, F., Mullenders, L.H. & Lehmann, A.R. (2001) Domain structure, localization, and function of DNA polymerase η, defective in xeroderma pigmentosum variant cells. Genes Dev. 15, 158-172.
18. Kannouche, P., Fernandez de Henestrosa, A.R., Coull, B., et al. (2003) Localization of DNA polymerases η and ι to the replication machinery is tightly co-ordinated in human cells. EMBO J. 22, 1223-1233.
19. Kannouche, P.L., Wing, J. & Lehmann, A.R. (2004) Interaction of human DNA polymerase η with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491-500.
20. Kunkel, T.A., Pavlov, Y.I. & Bebenek, K. (2003) Functions of human DNA polymerases η, κ and ι suggested by their properties, including fidelity with undamaged DNA templates. DNA Repair (Amst) 2, 135-149.
21. Kunkel, T.A., Roberts, J.D. & Zakour, R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Meth. Enzymol. 154, 367-382.
22. Kusumoto, R., Masutani, C., Iwai, S. & Hanaoka, F. (2002) Translesion synthesis by human DNA polymerase ν across thymine glycol lesions. Biochemistry 41, 6090-6099.
23. Lee, S.H., Eki, T. & Hurwitz, J. (1989) Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases α and δ. Proc. Natl. Acad. Sci. USA 86, 7361-7365.
24. Lehmann, A.R., Kirk-Bell, S., Arlett, C.F., et al. (1975) Xeroderma pigmentosum cells with normal levels of excision repair have a defect in DNA synthesis after UV-irradiation. Proc. Natl. Acad. Sci. USA 72, 219 -223.
25. Ling, H., Boudsocp, F., Plosky, B.S., Woodgate, R. & Yang, W. (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature 424, 1083-1087.
26. Ling, H., Boudsocp, F., Woodgate, R. & Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell 107, 91-102.
27. Maher, V.M., Ouellette, L.M., Curren, R.D. & McCormick, J.J. (1976) Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells. Nature 261, 593-595.
28. Masuda, Y., Bennett, R.A. & Demple, B. (1998) Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium. J. Biol. Chem. 273, 30360-30365.
29. Masutani, C., Araki, M., Yamada, A., et al. (1999a) Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 18 3491-3501.
30. Masutani, C., Kusumoto, R., Iwai, S. & Hanaoka, F. (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J. 19, 3100-3109.
31. Masutani, C., Kusumoto, R., Yamada, A., et al. (1999b) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399, 700-704.
32. Matsuda, T., Bebenek, K., Masutani, C., Hanaoka, F. & Kunkel, T.A. (2000) Low fidelity DNA synthesis by human DNA polymerase η. Nature 404, 1011-1013.
33. McCulloch, S.D., Kokoska, R.J., Masutani, C., Iwai, S., Hanaoka, F. & Kunkel, T.A. (2004) Preferential cis-syn thymine dimer bypass by DNA polymerase η occurs with biased fidelity. Nature 428, 97-100.
34. Misra, R.R. & Vos, J.M. (1993) Defective replication of psoralen adducts detected at the gene-specific level in xeroderma pigmentosum variant cells. Mol. Cell. Biol. 13, 1002-1012.
35. Murata, T., Iwai, S. & Ohtsuka, E. (1990) Synthesis and characterization of a substrate for T4 endonuclease V containing a phosphorodithioate linkage at the thymine dimer site. Nuclelc Acids Res. 18, 7279-7286.
36. Nelson, J.R., Lawrence, C.W. & Hinkle, D.C. (1996) Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272, 1646-1649.
37. Ohashi, E., Murakumo, Y., Kanjo, N., et al. (2004) Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9, 523-531.
38. Raha, M., Wang, G., Seidman, M.M. & Glazer, P.M. (1996) Mutagenesis by third-strand-directed psoralen adducts in repair-deficient human cells: high frequency and altered spectrum in a xeroderma pigmentosum variant. Proc. Natl. Acad. Sci. USA 93, 2941-2946.
39. Schaffner, W & Weissmann, C. (1973) A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56, 502-514.
40. Stary, A., Kannouche, P., Lehmann, A.R. & Sarasin, A. (2003) Role of DNA polymerase η in the UV mutation spectrum in human cells. J. Biol. Chem. 278, 18767-18775.
41. Stelter, P. & Ulrich, H.D. (2003) Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188-191.
42. Trincao, J., Johnson, R.E., Escalante, C.R., Prakash, S., Prakash, L. & Aggarwal, A.K. (2001) Structure of the catalytic core of S. cerevisiae DNA polymerase η: implications for translesion synthesis. Mol. Cell 8, 417-426.
43. Wang, Y.C., Maher, V.M. & McCormick, J.J. (1991) Xeroderma pigmentosum variant cells are less likely than normal cells to incorporate dAMP opposite photoproducts during replication of UV-irradiated plasmids. Proc. Natl. Acad. Sci. USA 88, 7810-7814.
44. Wang, Y.C., Maher, V.M., Mitchell, D.L. & McCormick, J.J. (1993) Evidence from mutation spectra that the UV hypermutability of xeroderma pigmentosum variant cells reflects abnormal, error-prone replication on a template containing photoproducts. Mol. Cell. Biol. 13, 4276-4283.
45. Washington, M.T., Johnson, R.E., Prakash, S. & Prakash, L. (2000) Accuracy of thymine-thymine dimer bypass by Saccharomyces cerevisiae DNA polymerase η. Proc. Natl. Acad. Sci. USA 97, 3094-3099.
46. Washington, M.T., Prakash, L. & Prakash, S. (2001) Yeast DNA polymerase η utilizes an induced-fit mechanism of nucleotide incorporation. Cell 107, 917-927.
47. Waters, H.L., Seetharam, S., Seidman, M.M. & Kraemer, K.H. (1993) Ultraviolet hypermutability of a shuttle vector propagated in xeroderma pigmentosum variant cells. J. Invest. Dermatol. 101 744-748.
48. Xie, Z., Braithwaite, E., Guo, D., Zhao, B., Geacintov, N.E. & Wang, Z. (2003) Mutagenesis of benzo[a]pyrene diol epoxide in yeast: requirement for DNA polymerase ζ and involvement of DNA polymerase η. Biochemistry 42, 11253-11262.
49. Yamada, A., Masutani, C., Iwai, S. & Hanaoka, F. (2000) Complementation of defective translesion synthesis and UV light sensitivity in xeroderma pigmentosum variant cells by human and mouse DNA polymerase η. Nucl. Acids Res. 28, 2473-2480.
50. Zhou, B.L., Pata, J.D. & Steitz, T.A. (2001) Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain. Mol. Cell 8, 427-437.