A novel variant of DNA polymerase ζ, Rev3δC, highlights differential regulation of Pol32 as a subunit of polymerase δ versus ζ in Saccharomyces cerevisiae

DNA Repair

Volumn 24, Issue , 2014, Pages 138-149

  Siebler, Hollie M ^a   Lada, Artem G ^a   Baranovskiy, Andrey G ^a   Tahirov, Tahir H ^a   Pavlov, Youri I ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Mgs1; Pol32; Polymerase switch; Polymerase ; Translesion DNA synthesis; UV mutagenesis

Indexed keywords

DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE ZETA; UNCLASSIFIED DRUG; CYCLINE; DNA DIRECTED DNA POLYMERASE GAMMA; DNA HELICASE; DNA POLYMERASE ZETA; MGS1 PROTEIN, S CEREVISIAE; NUCLEOTIDYLTRANSFERASE; POL31 PROTEIN, S CEREVISIAE; POL32 PROTEIN, S CEREVISIAE; REV1 PROTEIN, S CEREVISIAE; REV3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; FUNGAL STRAIN; FUNGUS MUTANT; INDUCED MUTATION; METAL BINDING; MUTAGENESIS; NONHUMAN; PHENOTYPE; PLASMID; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SURVIVAL; ULTRAVIOLET RADIATION; WESTERN BLOTTING; ZINC FINGER MOTIF; GENETICS; GENOMIC INSTABILITY; METABOLISM; MUTATION; RADIATION RESPONSE; UBIQUITINATION;

SACCHAROMYCES CEREVISIAE;

DNA HELICASES; DNA POLYMERASE III; DNA-DIRECTED DNA POLYMERASE; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENOMIC INSTABILITY; MUTAGENESIS; MUTATION; NUCLEOTIDYLTRANSFERASES; PROLIFERATING CELL NUCLEAR ANTIGEN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION; ULTRAVIOLET RAYS;

EID: 84919777165     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2014.04.013     Document Type: Article

References (64)

1. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press. 2nd ed.
2. Boiteux S., Jinks-Robertson S. DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics 2013, 193:1025-1064.
3. Friedberg E.C. Suffering in silence: the tolerance of DNA damage. Nat. Rev. Mol. Cell Biol. 2005, 6:943-953.
4. Waters L.S., Minesinger B.K., Wiltrout M.E., D'Souza S., Woodruff R.V., Walker G.C. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 2009, 73:134-154.
5. Sale J.E. Translesion DNA synthesis and mutagenesis in eukaryotes. Cold Spring Harb. Perspect. Biol. 2013, 5:a012708.
6. Lehmann A.R., Fuchs R.P. Gaps and forks in DNA replication: rediscovering old models. DNA Repair (Amst.) 2006, 5:1495-1498.
7. Ohmori H., Friedberg E.C., Fuchs R.P.P., Goodman M.F., Hanaoka F., Hinkle D., Kunkel T.A., Lawrence C.W., Livneh Z., Nohmi T., Prakash L., Prakash S., Todo T., Walker G.C., Wang Z., Woodgate R. The Y-family of DNA polymerases. Mol. Cell 2001, 8:7-8.
8. Pages V., Fuchs R.P. How DNA lesions are turned into mutations within cells?. Oncogene 2002, 21:8957-8966.
9. Pavlov Y.I., Shcherbakova P.V., Rogozin I.B. Roles of DNA polymerases in replication, repair, and recombination. Int. Rev. Cytol. 2006, 255:41-132.
10. Yang W. Portraits of a Y-family DNA polymerase. FEBS Lett. 2005, 579:868-872.
11. Prakash S., Johnson R.E., Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74:317-353.
12. Livneh Z., Ziv O., Shachar S. Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 2010, 9:729-735.
13. Gan G.N., Wittschieben J.P., Wittschieben B.O., Wood R.D. DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res. 2008, 18:174-183.
14. Stone J.E., Kumar D., Binz S.K., Inase A., Iwai S., Chabes A., Burgers P.M., Kunkel T.A. Lesion bypass by S. cerevisiae Pol zeta alone. DNA Repair (Amst.) 2011, 10:826-834.
15. Ulrich H.D. How to activate a damage-tolerant polymerase: consequences of PCNA modifications by ubiquitin and SUMO. Cell Cycle 2004, 3:15-18.
16. Pages V., Bresson A., Acharya N., Prakash S., Fuchs R.P., Prakash L. Requirement of Rad5 for DNA polymerase zeta-dependent translesion synthesis in Saccharomyces cerevisiae. Genetics 2008, 180:73-82.
17. Prakash S., Prakash L. Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 2002, 16:1872-1883.
18. Stelter P., Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 2003, 425:188-191.
19. Ulrich H.D. Deubiquitinating PCNA: a downside to DNA damage tolerance. Nat. Cell Biol. 2006, 8:303-305.
20. Huang T.T., D'Andrea A.D. Regulation of DNA repair by ubiquitylation. Nat. Rev. Mol. Cell Biol. 2006, 7:323-334.
21. Lawrence C.W., Maher V.M. Mutagenesis in eukaryotes dependent on DNA polymerase zeta and Rev1p. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2001, 356:41-46.
22. Zhong X., Garg P., Stith C.M., Nick McElhinny S.A., Kissling G.E., Burgers P.M., Kunkel T.A. The fidelity of DNA synthesis by yeast DNA polymerase zeta alone and with accessory proteins. Nucleic Acids Res. 2006, 34:4731-4742.
23. Northam M.R., Garg P., Baitin D.M., Burgers P.M.J., Shcherbakova P.V. A novel function of DNA polymerase ζ regulated by PCNA. EMBO J. 2006, 25:4316-4325.
24. Northam M.R., Robinson H.A., Kochenova O.V., Shcherbakova P.V. Participation of DNA polymerase zeta in replication of undamaged DNA in Saccharomyces cerevisiae. Genetics 2010, 184:27-42.
25. Northam M.R., Moore E.A., Mertz T.M., Binz S.K., Stith C.M., Stepchenkova E.I., Wendt K.L., Burgers P.M., Shcherbakova P.V. DNA polymerases zeta and Rev1 mediate error-prone bypass of non-B DNA structures. Nucleic Acids Res. 2014, 42:290-306.
26. Auerbach P.A., Demple B. Roles of Rev1, Pol zeta, Pol32 and Pol eta in the bypass of chromosomal abasic sites in Saccharomyces cerevisiae. Mutagenesis 2010, 25:63-69.
27. Wittschieben J.P., Reshmi S.C., Gollin S.M., Wood R.D. Loss of DNA polymerase zeta causes chromosomal instability in mammalian cells. Cancer Res. 2006, 66:134-142.
28. Loeb L.A., Monnat R.J. DNA polymerases and human disease. Nat. Rev. Genet. 2008, 9:594-604.
29. Stallons L.J., McGregor W.G. Translesion synthesis polymerases in the prevention and promotion of carcinogenesis. J. Nucleic Acids 2010, 2010. pii: 643857.
30. Lin X., Trang J., Okuda T., Howell S.B. DNA polymerase zeta accounts for the reduced cytotoxicity and enhanced mutagenicity of cisplatin in human colon carcinoma cells that have lost DNA mismatch repair. Clin. Cancer Res. 2006, 12:563-568.
31. Nelson J.R., Lawrence C.W., Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 1996, 272:1646-1649.
32. Baranovskiy A.G., Lada A.G., Siebler H.M., Zhang Y., Pavlov Y.I., Tahirov T.H. DNA polymerase δ and ζ switch by sharing accessory subunits of DNA polymerase δ. J. Biol. Chem. 2012, 287:17281-17287.
33. Lee Y.S., Gregory M.T., Yang W. Human Pol zeta purified with accessory subunits is active in translesion DNA synthesis and complements Pol eta in cisplatin bypass. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:2954-2959.
34. Johnson R.E., Prakash L., Prakash S. Pol31 and Pol32 subunits of yeast DNA polymerase delta are also essential subunits of DNA polymerase zeta. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12455-12460.
35. Makarova A.V., Stodola J.L., Burgers P.M. A four-subunit DNA polymerase zeta complex containing Pol delta accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res. 2012, 1-9.
36. Langston L.D., O'Donnell M. Subunit sharing among high- and low-fidelity DNA polymerases. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12268-12269.
37. Baranovskiy A.G., Babayeva N.D., Liston V.G., Rogozin I.B., Koonin E.V., Pavlov Y.I., Vassylyev D.G., Tahirov T.H. X-ray structure of the complex of regulatory subunits of human DNA polymerase delta. Cell Cycle 2008, 7:3026-3036.
38. Tahirov T.H. Structure and structure and function of eukaryotic DNA polymerase δ. Subcell. Biochem. 2012, 62:217-236.
39. Gomez-Llorente Y., Malik R., Jain R., Choudhury J.R., Johnson R.E., Prakash L., Prakash S., Ubarretxena-Belandia I., Aggarwal A.K. The architecture of yeast DNA polymerase zeta. Cell Rep. 2013, 5:79-86.
40. Daraba A., Gali V.K., Halmai M., Haracska L., Unk I. Def1 promotes the degradation of Pol3 for polymerase exchange to occur during DNA-damage-induced mutagenesis in Saccharomyces cerevisiae. PLoS Biol. 2014, 12:e1001771.
41. Klinge S., Nunez-Ramirez R., Llorca O., Pellegrini L. 3D architecture of DNA Pol alpha reveals the functional core of multi-subunit replicative polymerases. EMBO J. 2009, 28:1978-1987.
42. Netz D.J., Stith C.M., Stumpfig M., Kopf G., Vogel D., Genau H.M., Stodola J.L., Lill R., Burgers P.M., Pierik A.J. Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat. Chem. Biol. 2012, 8:125-132.
43. Waisertreiger I.S., Liston V.G., Menezes M.R., Kim H.M., Lobachev K.S., Stepchenkova E.I., Tahirov T.H., Rogozin I.B., Pavlov Y.I. Modulation of mutagenesis in eukaryotes by DNA replication fork dynamics and quality of nucleotide pools. Environ. Mol. Mutagen. 2012, 53:699-724.
44. Saugar I., Parker J.L., Zhao S., Ulrich H.D. The genome maintenance factor Mgs1 is targeted to sites of replication stress by ubiquitylated PCNA. Nucleic Acids Res. 2012, 40:245-257.
45. Pavlov Y.I., Shcherbakova P.V., Kunkel T.A. In vivo consequences of putative active site mutations in yeast DNA polymerases α, δ, and ζ. Genetics 2001, 159:47-64.
46. Burgers P.M. Overexpression of multisubunit replication factors in yeast. Methods 1999, 18:349-355.
47. Garg P., Stith C.M., Majka J., Burgers P.M. Proliferating cell nuclear antigen promotes translesion synthesis by DNA polymerase zeta. J. Biol. Chem. 2005, 280:23446-23450.
48. Kozmin S.G., Pavlov Y.I., Kunkel T.A., Sage E. Roles of Saccharomyces cerevisiae DNA polymerases Polη and Polζ in response to irradiation by simulated sunlight. Nucleic Acids Res. 2003, 31:4541-4552.
49. Tahirov T.H., Makarova K.S., Rogozin I.B., Pavlov Y.I., Koonin E.V. Evolution of DNA polymerases: an inactivated polymerase-exonuclease module in Pol epsilon and a chimeric origin of eukaryotic polymerases from two classes of archaeal ancestors. Biol. Direct 2009, 4:10.
50. Whelan W.L., Gocke E., Manney T.R. The CAN1 locus of Saccharomyces cerevisiae: fine-structure analysis and forward mutation rates. Genetics 1979, 91:35-51.
51. Gerik K.J., Li X., Pautz A., Burgers P.M. Characterization of the two small subunits of Saccharomyces cerevisiae DNA polymerase delta. J. Biol. Chem. 1998, 273:19747-19755.
52. Huang M.E., de Calignon A., Nicolas A., Galibert F. POL32, a subunit of the Saccharomyces cerevisiae DNA polymerase delta, defines a link between DNA replication and the mutagenic bypass repair pathway. Curr. Genet. 2000, 38:178-187.
53. Acharya N., Haracska L., Johnson R.E., Unk I., Prakash S., Prakash L. Complex formation of yeast Rev1 and Rev7 proteins: a novel role for the polymerase-associated domain. Mol. Cell. Biol. 2005, 25:9734-9740.
54. Hishida T., Ohya T., Kubota Y., Kamada Y., Shinagawa H. Functional and physical interaction of yeast Mgs1 with PCNA: impact on RAD6-dependent DNA damage tolerance. Mol. Cell. Biol. 2006, 26:5509-5517.
55. Giot L., Chanet R., Simon M., Facca C., Faye G. Involvement of the yeast DNA polymerase δ in DNA repair in vivo. Genetics 1997, 146:1239-1251.
56. Kunkel T.A., Burgers P.M. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 2008, 18:521-527.
57. Pages V., Johnson R.E., Prakash L., Prakash S. Mutational specificity and genetic control of replicative bypass of an abasic site in yeast. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:1170-1175.
58. Pavlov Y.I., Shcherbakova P.V. DNA polymerases at the eukaryotic fork-20 years later. Mutat. Res. 2010, 685:45-53.
59. Kikuchi S., Hara K., Shimizu T., Sato M., Hashimoto H. Structural basis of recruitment of DNA polymerase zeta by interaction between REV1 and REV7 proteins. J. Biol. Chem. 2012, 287:33847-33852.
60. Acharya N., Johnson R.E., Pages V., Prakash L., Prakash S. Yeast Rev1 protein promotes complex formation of DNA polymerase zeta with Pol32 subunit of DNA polymerase delta. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:9631-9636.
61. Hishida T., Iwasaki H., Ohno T., Morishita T., Shinagawa H. A yeast gene, MGS1, encoding a DNA-dependent AAA(+) ATPase is required to maintain genome stability. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8283-8289.
62. Nomura H., Yoshimura A., Edo T., Kanno S., Tada S., Seki M., Yasui A., Enomoto T. WRNIP1 accumulates at laser light irradiated sites rapidly via its ubiquitin-binding zinc finger domain and independently from its ATPase domain. Biochem. Biophys. Res. Commun. 2012, 417:1145-1150.
63. Tsurimoto T., Shinozaki A., Yano M., Seki M., Enomoto T. Human Werner helicase interacting protein 1 (Wrnip1) functions as a novel modulator for DNA polymerase δ. Genes Cells 2005, 10:13-22.
64. Branzei D., Seki M., Onoda F., Enomoto T. The product of Saccharomyces cerevisiae WHIP/MGS1, a gene related to replication factor C genes, interacts functionally with DNA polymerase delta. Mol. Genet. Genomics 2002, 268:371-386.