Multiple forms of human DNA polymerase delta sub-assembling in cellular DNA transactions

Current Protein and Peptide Science

Volumn 17, Issue 8, 2016, Pages 746-755

  Zhang, Qian ^a   Chen, Huiqing ^a   Chen, Yan ^a   Zhou, Yajing ^a  

^a JIANGSU UNIVERSITY   (China)

Author keywords

Apoptosis; DNA damage and repair; DNA polymerase ; DNA replication; Heterotrimer Pol 3; P12 degradation

Indexed keywords

BACMID; CELL DNA; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE EPSILON; ISOENZYME; OKAZAKI FRAGMENT; POLYHEDRIN; PRIMER RNA; PROTEASOME; PROTEIN P50; PROTEIN P68; SMALL INTERFERING RNA; DNA; DNA DIRECTED DNA POLYMERASE GAMMA; PROTEIN SUBUNIT;

APOPTOSIS; ARTICLE; BACULOVIRIDAE; BACULOVIRUS EXPRESSION SYSTEM; BOMBYX MORI; CELL CYCLE PROGRESSION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE CHECKPOINT; DNA REPAIR; DNA REPLICATION; ENZYME SUBUNIT; ESCHERICHIA COLI; EXCISION REPAIR; GENE; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; IMMUNOAFFINITY CHROMATOGRAPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHYLOGENY; POLD4 GENE; POLYMERIZATION; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; ULTRAVIOLET IRRADIATION; BIOLOGICAL MODEL; CLASSIFICATION; DNA DAMAGE; GENETICS; METABOLISM; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION;

DNA; DNA DAMAGE; DNA POLYMERASE III; DNA REPAIR; DNA REPLICATION; HUMANS; MODELS, GENETIC; PHYLOGENY; PROTEIN SUBUNITS; SIGNAL TRANSDUCTION;

EID: 85007579493     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/1389203717666160226145006     Document Type: Article

References (78)

1. Nick McElhinny, S.A.; Gordenin, D.A.; Stith, C.M.; Burgers, P.M.; Kunkel, T.A. Division of labor at the eukaryotic replication fork. Mol. Cell, 2008, 30(2), 137-144.
2. Burgers, P.M. Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem., 2009, 284(7), 4041-4045.
3. Kunkel, T.A.; Burgers, P.M. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol., 2008, 75(11), 521-527.
4. Waga, S.; Stillman, B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature, 1994, 369(6411), 207-212.
5. Bambara, R.A.; Murante, R.S.; Henricksen, L.A. Enzymes and reactions at the eukaryotic DNA replication fork. J. Biol. Chem., 1997, 272(8), 4641-4650.
6. Miyabe, I.; Kunkel, T.A.; Carr, A.M. The major roles of DNA polymerases epsilon and delta at the eukaryotic replication fork are evolutionarily conserved. PLoS Genet., 2011, 7(12), e1002401.
7. Zheng, L.; Shen, B. Okazaki fragment maturation: nucleases take centre stage. J. Mol. Cell Biol., 2011, 3(1), 23-30.
8. Pavlov, Y.I.; Frahm, C.; Nick McElhinny, S.A.; Niimi, A.; Suzuki, M.; Kunkel, T.A. Evidence that errors made by DNA polymerase alpha are corrected by DNA polymerase delta. Curr. Biol., 2006, 76(2), 202-201.
9. Balakrishnan, L.; Bambara, R.A. Flap endonuclease 1. Annu. Rev. Biochem., 2013, 82, 119-138.
10. Pavlov, Y.I.; Shcherbakova, P.V. DNA polymerases at the eukaryotic fork-20 years later. Mutat. Res., 2010, 685(1-2), 45-53.
11. Branzei, D.; Foiani, M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol., 2008, 9(4), 291-308.
12. Sancar, A.; Lindsey-Boltz, L.A.; Unsal-Kacmaz, K.; Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem., 2004, 73, 39-85.
13. Prindle, M.J.; Loeb, L.A. DNA polymerase delta in DNA replication and genome maintenance. Environ. Mol. Mutagen, 2012, 53(9), 666-682.
14. MacNeill, S.A.; Baldacci, G.; Burgers, P.M.; Hubscher, U. A unified nomenclature for the subunits of eukaryotic DNA polymerase delta. Trends Biochem. Sci., 2001, 26(1), 16-11.
15. Bermudez, V.P.; MacNeill, S.A.; Tappin, I.; Hurwitz, J. The influence of the Cdc21 subunit on the properties of the Schizosac-charomyces pombe DNA polymerase delta. J. Biol. Chem., 2002, 277(39), 36853-36862.
16. Zuo, S.; Bermudez, V.; Zhang, G.; Kelman, Z.; Hurwitz, J. Structure and activity associated with multiple forms of Schizosac-charomyces pombe DNA polymerase delta. J. Biol. Chem., 2000, 275(1), 5153-5162.
17. Reynolds, N.; Watt, A.; Fantes, P.A.; MacNeill, S.A. Cdm1, the smallest subunit of DNA polymerase d in the fission yeast Schizosaccharomyces pombe, is non-essential for growth and division. Curr. Genet., 1998, 34(4), 250-258.
18. Burgers, P.M.; Gerik, K.J. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase delta. J. Biol. Chem., 1998, 273(31), 19156-19162.
19. 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(31), 19141-19155.
20. Garg, P.; Burgers, P.M. DNA polymerases that propagate the eukaryotic DNA replication fork. Crit. Rev. Biochem. Mol. Biol., 2005, 40(2), 115-128.
21. Podust, V.N.; Chang, L.S.; Ott, R.; Dianov, G.L.; Fanning, E. Reconstitution of human DNA polymerase delta using recombinant baculoviruses: the p12 subunit potentiates DNA polymerizing activity of the four-subunit enzyme. J. Biol. Chem., 2002, 277(6), 3894-3901.
22. Xie, B.; Mazloum, N.; Liu, L.; Rahmeh, A.; Li, H.; Lee, M.Y. Reconstitution and characterization of the human DNA polymerase delta four-subunit holoenzyme. Biochemistry, 2002, 47(44), 13133-13142.
23. Li, H.; Xie, B.; Zhou, Y.; Rahmeh, A.; Trusa, S.; Zhang, S.; Gao, Y.; Lee, E.Y.; Lee, M.Y. Functional roles of p12, the fourth subunit of human DNA polymerase delta. J. Biol. Chem., 2006, 287(21), 14148-14155.
24. Lee, M.Y.; Zhang, S.; Lin, S.H.; Chea, J.; Wang, X.; LeRoy, C.; Wong, A.; Zhang, Z.; Lee, E.Y. Regulation of human DNA polymerase delta in the cellular responses to DNA damage. Environ. Mol. Mutagen, 2012, 53(9), 683-698.
25. Lee, M.Y.; Zhang, S.; Lin, S.H.; Wang, X.; Darzynkiewicz, Z.; Zhang, Z.; Lee, E.Y. The tail that wags the dog: p12, the smallest subunit of DNA polymerase delta, is degraded by ubiquitin ligases in response to DNA damage and during cell cycle progression. Cell Cycle, 2014, 73(1), 23-31.
26. Byrnes, J.J.; Downey, K.M.; Black, V.L.; So, A.G. A new mammalian DNA polymerase with 3’ to 5’ exonuclease activity: DNA polymerase delta. Biochemistry, 1976, 75(13), 2811-2823.
27. Morrison, A.; Johnson, A. L.; Johnston, L. H.; Sugino, A. Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J.,. 1993, 72(4),. 1461-1413.
28. Morrison, A.; Sugino, A. The 3’—>5’ exonucleases. of both DNA polymerases delta and epsilon participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol. Gen. Genet., 1994, 242(3), 289-296.
29. Simon, M.; Giot, L.; Faye, G. The 3’ to 5’ exonuclease activity located in the DNA polymerase delta subunit of Saccharomyces cerevisiae is required for accurate replication. EMBO J., 1991, 70(8), 2165-2110.
30. Lee, M.Y.; Tan, C.K.; So, A.G.; Downey, K.M. Purification of deoxyribonucleic acid polymerase delta from calf thymus: partial characterization of physical properties. Biochemistry, 1980, 79(10), 2096-2101.
31. Lee, M.Y.; Tan, C.K.; Downey, K.M.; So, A.G. Structural and functional properties of calf thymus DNA polymerase delta. Prog. Nucleic Acid Res. Mol. Biol., 1981, 26, 83-96.
32. Lee, M.Y.; Tan, C.K.; Downey, K.M.; So, A.G. Further studies on calf thymus DNA polymerase delta purified to homogeneity by a new procedure. Biochemistry, 1984, 23(9), 1906-1913.
33. Lee, M.Y.; Alejandro, R.; Toomey, N.L. Immunochemical studies of DNA polymerase delta: relationships with DNA polymerase alpha. Arch. Biochem. Biophys., 1989, 272(1), 1-9.
34. Lee, M.Y.; Jiang, Y.Q.; Zhang, S.J.; Toomey, N.L. Characterization of human DNA polymerase delta and its immunochemical relationships with DNA polymerase alpha and epsilon. J. Biol. Chem., 1991, 266(4), 2423-2429.
35. Hughes, P.; Tratner, I.; Ducoux, M.; Piard, K.; Baldacci, G. Isolation and identification of the third subunit of mammalian DNA polymerase delta by PCNA-affinity chromatography of mouse FM3A cell extracts. Nucleic Acids Res., 1999, 27(10), 2108-2114.
36. Mo, J.; Liu, L.; Leon, A.; Mazloum, N.; Lee, M.Y. Evidence that DNA polymerase delta isolated by immunoaffinity chromatography exhibits high-molecular weight characteristics and is associated with the KIAA0039 protein and RPA. Biochemistry, 2000, 39(24), 1245-1254.
37. Liu, L.; Mo, J.; Rodriguez-Belmonte, E.M.; Lee, M.Y. Identification of a fourth subunit of mammalian DNA polymerase delta. J. Biol. Chem., 2000, 275(25), 18139-18144.
38. Jiang, Y.; Zhang, S.J.; Wu, S.M.; Lee, M.Y. Immunoaffinity purification of DNA polymerase delta. Arch. Biochem. Biophys., 1995, 320(2), 291-304.
39. Trowitzsch, S.; Bieniossek, C.; Nie, Y.; Garzoni, F.; Berger, I. New baculovirus expression tools for recombinant protein complex production. J. Struct. Biol., 2010, 772(1), 45-54.
40. Vijayachandran, L.S.; Viola, C.; Garzoni, F.; Trowitzsch, S.; Bien-iossek, C.; Chaillet, M.; Schaffitzel, C.; Busso, D.; Romier, C.; Poterszman, A.; Richmond, T.J.; Berger, I. Robots, pipelines, polyproteins: enabling multiprotein expression in prokaryotic and eukaryotic cells. J. Struct. Biol., 2011, 775(2), 198-208.
41. Bieniossek, C.; Imasaki, T.; Takagi, Y.; Berger, I. MultiBac: expanding the research toolbox for multiprotein complexes. Trends Biochem. Sci., 2012, 37(2), 49-51.
42. Zhou, Y.; Chen, H.; Li, X.; Wang, Y.; Chen, K.; Zhang, S.; Meng, X.; Lee, E.Y.; Lee, M.Y. Production of recombinant human DNA polymerase delta in a Bombyx mori bioreactor. PLoS One, 2011, 6(1), e22224.
43. Zhou, Y.; Meng, X.; Zhang, S.; Lee, E.Y.; Lee, M.Y. Characterization of human DNA polymerase delta and its subassemblies reconstituted by expression in the MultiBac system. PLoS One, 2012, 7(6), e39156.
44. Berger, I.; Fitzgerald, D. J.; Richmond, T.J. Baculovirus expression system for heterologous multiprotein complexes. Nat. Biotechnol., 2004, 22(12), 1583-1581.
45. Liu, S.; Lu, G.; Ali, S.; Liu, W.; Zheng, L.; Dai, H.; Li, H.; Xu, H.; Hua, Y.; Zhou, Y.; Ortega, J.; Li, G.M.; Kunkel, T.A.; Shen, B. Okazaki fragment maturation involves alpha-segment error editing by the mammalian FEN1/MutSalpha functional complex. EMBO J., 2015, 34(13), 1829-1843.
46. Bravo, R.; Frank, R.; Blundell, P.A.; Macdonald-Bravo, H. Cy-clin/PCNA is the auxiliary protein of DNA polymerase-delta. Nature, 1987, 326(6112), 515-511.
47. Prelich, G.; Tan, C.K.; Kostura, M.; Mathews, M.B.; So, A.G.; Downey, K.M.; Stillman, B. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature, 1987, 326(6112), 511-520.
48. Zhang, S.J.; Zeng, X.R.; Zhang, P.; Toomey, N.L.; Chuang, R.Y.; Chang, L.S.; Lee, M.Y. A conserved region in the amino terminus of DNA polymerase delta is involved in proliferating cell nuclear antigen binding. J. Biol. Chem., 1995, 270(14), 1988-1992.
49. Zhang, P.; Mo, J.Y.; Perez, A.; Leon, A.; Liu, L.; Mazloum, N.; Xu, H.; Lee, M.Y. Direct interaction of proliferating cell nuclear antigen with the p125 catalytic subunit of mammalian DNA polymerase delta. J. Biol. Chem., 1999, 274(38), 26641-26653.
50. Lu, X.; Tan, C.K.; Zhou, J.Q.; You, M.; Carastro, L.M.; Downey, K.M.; So, A.G. Direct interaction of proliferating cell nuclear antigen with the small subunit of DNA polymerase delta. J. Biol. Chem., 2002, 277(21), 24340-24345.
51. Wang, Y.; Zhang, Q.; Chen, H.; Li, X.; Mai, W.; Chen, K.; Zhang, S.; Lee, E.Y.; Lee, M.Y.; Zhou, Y. P50, the small subunit of DNA polymerase delta, is required for mediation of the interaction of polymerase delta subassemblies with PCNA. PLoS One, 2011, 6(11), e21092.
52. Xie, S.; Xie, B.; Lee, M.Y.; Dai, W. Regulation of cell cycle checkpoints by polo-like kinases. Oncogene, 2005, 24(2), 211-286.
53. Park, C.J.; Lee, J.H.; Choi, B.S. Solution structure of the DNA-binding domain of RPA from Saccharomyces cerevisiae and its interaction with single-stranded DNA and SV40 T antigen. Nucleic Acids Res., 2005, 33(13), 4112-4181.
54. Zhang, S.; Zhou, Y.; Trusa, S.; Meng, X.; Lee, E. Y.; Lee, M.Y. A novel DNA damage response: rapid degradation of the p12 subunit of dna polymerase delta. J. Biol. Chem., 2007, 282(21), 15330-15340.
55. Meng, X.; Zhou, Y.; Zhang, S.; Lee, E.Y.; Frick, D.N.; Lee, M.Y. DNA damage alters DNA polymerase delta to a form that exhibits increased discrimination against modified template bases and mismatched primers. Nucleic Acids Res., 2009, 37(2), 641-651.
56. Goodman, M.F.; Fygenson, K.D. DNA polymerase fidelity: from genetics toward a biochemical understanding. Genetics, 1998, 748(4), 1415-1482.
57. Reha-Krantz, L.J. Regulation of DNA polymerase exonucleolytic proofreading activity: studies of bacteriophage T4 “antimutator” DNA polymerases. Genetics, 1998, 748(4), 1551-1551.
58. Meng, X.; Zhou, Y.; Lee, E.Y.; Lee, M.Y.; Frick, D.N. The p12 subunit of human polymerase delta modulates the rate and fidelity of DNA synthesis. Biochemistry, 2010, 49(11), 3545-3554.
59. Lin, S.H.; Wang, X.; Zhang, S.; Zhang, Z.; Lee, E.Y.; Lee, M.Y. Dynamics of enzymatic interactions during short flap human Okazaki fragment processing by two forms of human DNA polymerase delta. DNA Repair (Amst), 2013, 72(11), 922-935.
60. Wilson, S.H.; Sobol, R.W.; Beard, W.A.; Horton, J.K.; Prasad, R.; Vande Berg, B.J. DNA polymerase beta and mammalian base excision repair. Cold Spring Harb. Symp. Quant. Biol., 2000, 65, 143-155.
61. Parikh, S.S.; Mol, C.D.; Hosfield, D.J.; Tainer, J.A. Envisioning the molecular choreography of DNA base excision repair. Curr. Opin. Struct. Biol., 1999, 9(1), 31-41.
62. Dianov, G.; Price, A.; Lindahl, T. Generation of single-nucleotide repair patches following excision of uracil residues from DNA. Mol. Cell Biol., 1992, 72(4), 1605-1612.
63. Matsumoto, Y.; Bogenhagen, D.F. Repair of a synthetic abasic site involves concerted reactions of DNA synthesis followed by excision and ligation. Mol. Cell Biol., 1991, 77(9), 4441-4441.
64. Sobol, R.W.; Prasad, R.; Evenski, A.; Baker, A.; Yang, X.P.; Horton, J.K.; Wilson, S.H. The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity. Nature, 2000, 405(6188), 801-810.
65. Yoshimura, M.; Kohzaki, M.; Nakamura, J.; Asagoshi, K.; Sonoda, E.; Hou, E.; Prasad, R.; Wilson, S. H.; Tano, K.; Yasui, A.; Lan, L.; Seki, M.; Wood, R.D.; Arakawa, H.; Buerstedde, J.M.; Hochegger, H.; Okada, T.; Hiraoka, M.; Takeda, S. Vertebrate POLQ and POLbeta cooperate in base excision repair of oxidative DNA damage. Mol. Cell, 2006, 24(1), 115-125.
66. Sobol, R.W.; Horton, J.K.; Kuhn, R.; Gu, H.; Singhal, R.K.; Prasad, R.; Rajewsky, K.; Wilson, S.H. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature, 1996, 379(6561), 183-186.
67. Blank, A.; Kim, B.; Loeb, L.A. DNA polymerase delta is required for base excision repair of DNA methylation damage in Saccharo-myces cerevisiae. Proc. Natl. Acad. Sci. U. S. A., 1994, 97(19), 9041-9051.
68. Parsons, J.L.; Preston, B.D.; O’Connor, T.R.; Dianov, G.L. DNA polymerase delta-dependent repair of DNA single strand breaks containing 3’-end proximal lesions. Nucleic Acids Res., 2007, 35(4), 1054-1063.
69. Chea, J.; Zhang, S.; Zhao, H.; Zhang, Z.; Lee, E.Y.; Darzynkiewicz, Z.; Lee, M.Y. Spatiotemporal recruitment of human DNA polymerase delta to sites of UV damage. Cell Cycle, 2012, 77(15), 2885-2895.
70. Zhang, S.; Zhou, Y.; Sarkeshik, A.; Yates, J.R., 3rd; Thomson, T.M.; Zhang, Z.; Lee, E.Y.; Lee, M.Y. Identification of RNF8 as a ubiquitin ligase involved in targeting the p12 subunit of DNA polymerase delta for degradation in response to DNA damage. J. Biol. Chem., 2013, 288(5), 2941-2950.
71. Huang, Q.M.; Akashi, T.; Masuda, Y.; Kamiya, K.; Takahashi, T.; Suzuki, M. Roles of POLD4, smallest. subunit of DNA polymerase delta, in nuclear structures and genomic stability of human cells. Biochem. Biophys. Res. Commun., 2010, 397(1), 542-546.
72. Huang, Q.M.; Tomida, S.; Masuda, Y.; Arima, C.; Cao, K.; Kasa-hara, T.A.; Osada, H.; Yatabe, Y.; Akashi, T.; Kamiya, K.; Takaha-shi, T.; Suzuki, M. Regulation of DNA polymerase POLD4 influences genomic instability in lung cancer. Cancer Res., 2010, 70(21), 8401-8416.
73. Fan, X.; Zhang, Q.; You, C.; Qian, Y.; Gao, J.; Liu, P.; Chen, H.; Song, H.; Chen, Y.; Chen, K.; Zhou, Y. Proteolysis of the human DNA polymerase delta smallest subunit p12 by mu-calpain in calcium-triggered apoptotic HeLa cells. PLoS One, 2014, 9(4), e93642.
74. Johnson, D.E. Noncaspase proteases in apoptosis. Leukemia, 2000, 74(9), 1695-1103.
75. Nakagawa, T.; Yuan, J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol., 2000, 750(4), 881-894.
76. Song, H.F.; Chen, H.Q.; Wang, Y.; Zhou, Y.J. Genome-wide survey and phylogenetic analysis on subunit sequences of eukaryotic DNA polymerase delta. Genet. Mol. Res., 2014, 73(4), 9558-9568.
77. Herniou, E.A.; Luque, T.; Chen, X.; Vlak, J.M.; Winstanley, D.; Cory, J.S.; O’Reilly, D.R. Use of whole genome sequence data to infer baculovirus phylogeny. J. Virol., 2001, 75(11), 8111-8126.
78. Tahirov, T.H. Structure and function of eukaryotic DNA polym-erase delta. Subcell. Biochem., 2012, 62, 211-236.