The C-terminal domain of the DNA polymerase catalytic subunit regulates the primase and polymerase activities of the human DNA polymerase α-primase complex

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22021-22034

  Zhang, Yinbo ^a,b   Baranovskiy, Andrey G ^a   Tahirov, Tahir H ^a   Pavlov, Youri I ^a,b,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEIC ACIDS; RNA;

C-TERMINAL DOMAINS; CATALYTIC SUBUNITS; DNA POLYMERASE; DNA REPLICATIONS; HUMAN DNA POLYMERASE; POLYMERASE ACTIVITIES; REPLICATIVE POLYMERASE; SYNTHESIZING COMPLEX;

POLYMERS;

DNA DIRECTED DNA POLYMERASE ALPHA; DNA PRIMASE; DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE ALPHA-PRIMASE; DNA PRIMASE P58 SUBUNIT, HUMAN; MULTIENZYME COMPLEX; PROTEIN SUBUNIT; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMPLEX FORMATION; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; RNA SYNTHESIS; CHEMISTRY; DNA REPLICATION; ENZYME ACTIVE SITE; GENETICS; METABOLISM; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE; TWO HYBRID SYSTEM;

CATALYTIC DOMAIN; DNA POLYMERASE I; DNA PRIMASE; DNA REPLICATION; HUMANS; MULTIENZYME COMPLEXES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84905867880     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570333     Document Type: Article

References (62)

1. García-Gómez, S., Reyes, A., Martínez- Jiménez, M. I., Chocrón, E. S., Mourón, S., Terrados, G., Powell, C., Salido, E., Méndez, J., Holt, I. J., and Blanco, L. (2013) PrimPol, an archaic primase/polymerase operating in human cells. Mol. Cell 52, 541-553
2. Garg, P., and Burgers, P. M. (2005) DNA polymerases that propagate the eukaryotic DNA replication fork. Crit. Rev. Biochem. Mol. Biol. 40, 115-128
3. Pavlov, Y. I., Shcherbakova, P. V., and Rogozin, I. B. (2006) Roles of DNA polymerases in replication, repair, and recombination in eukaryotes. Int. Rev. Cytol. 255, 41-132
4. Kunkel, T. A. (2009) Evolving views of DNA replication (in)fidelity. Cold Spring Harb. Symp. Quant. Biol. 74, 91-101
5. MacNeill, S. (2012) Composition and dynamics of the eukaryotic replisome: a brief overview. Subcell. Biochem. 62, 1-17
6. Waisertreiger, I. S., Liston, V. G., Menezes, M. R., Kim, H. M., Lobachev, K. S., Stepchenkova, E. I., Tahirov, T. H., Rogozin, I. B., and Pavlov, Y. I. (2012) Modulation of mutagenesis in eukaryotes by DNA replication fork dynamics and quality of nucleotide pools. Environ. Mol. Mutagen 53, 699-724
7. Tanaka, S., and Araki, H. (2013) Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb. Perspect. Biol. 5, a010371
8. Pellegrini, L. (2012) The Pol-primase complex. Subcell. Biochem. 62, 157-169
9. Tahirov, T. H. (2012) Structure and function of eukaryotic DNA polymerase. Subcell. Biochem. 62, 217-236
10. Hogg, M., and Johansson, E. (2012) DNA polymerase. Subcell. Biochem. 62, 237-257
11. Kunkel, T. A., and Burgers, P. M. (2008) Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 18, 521-527
12. Pavlov, Y. I., and Shcherbakova, P. V. (2010) DNA polymerases at the eukaryotic fork-20 years later. Mutat Res 685, 45-53
13. Johansson, E., and Dixon, N. (2013) Replicative DNA polymerases. Cold Spring Harb. Perspect. Biol. 5, a012799
14. Lawrence, C. W., and Hinkle, D. C. (1996) DNA polymerase α and the control of DNA damage induced mutagenesis in eukaryotes. Cancer Surv. 28, 21-31
15. Northam, M. R., Robinson, H. A., Kochenova, O. V., and Shcherbakova, P. V. (2010) Participation of DNA polymerase α in replication of undamaged DNA in Saccharomyces cerevisiae. Genetics 184, 27-42
16. Kuchta, R. D., and Stengel, G. (2010) Mechanism and evolution of DNA primases. Biochim Biophys Acta 1804, 1180-1189
17. Perera, R. L., Torella, R., Klinge, S., Kilkenny, M. L., Maman, J. D., and Pellegrini, L. (2013) Mechanism for primingDNAsynthesis by yeastDNA polymerase. Elife 2, e00482
18. Zerbe, L. K., and Kuchta, R. D. (2002) The p58 subunit of human DNA primase is important for primer initiation, elongation, and counting. Biochemistry 41, 4891-4900
19. Smith, D. J., and Whitehouse, I. (2012) Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483, 434-438
20. Baranovskiy, A. G., Lada, A. G., Siebler, H. M., Zhang, Y., Pavlov, Y. I., and Tahirov, T. H. (2012) DNA polymerase α and α switch by sharing accessory subunits of DNA polymerase. J. Biol. Chem. 287, 17281-17287
21. Johnson, R. E., Prakash, L., and Prakash, S. (2012) Pol31 and Pol32 subunits of yeastDNApolymerase α are also essential subunits ofDNApolymerase. Proc. Natl. Acad. Sci. U.S.A. 109, 12455-12460
22. Makarova, A. V., Stodola, J. L., and Burgers, P. M. (2012) A four-subunit DNA polymerase α complex containing Pol α accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res. 40, 11618-11626
23. Gómez-Llorente, Y., Malik, R., Jain, R., Choudhury, J. R., Johnson, R. E., Prakash, L., Prakash, S., Ubarretxena-Belandia, I., and Aggarwal, A. K. (2013) The architecture of yeast DNA polymerase. Cell Rep. 5, 79-86
24. Lee, Y. S., Gregory, M. T., and Yang, W. (2014) Human Pol α purified with accessory subunits is active in translesion DNA synthesis and complements Pol in cisplatin bypass. Proc. Natl. Acad. Sci. U.S.A. 111, 2954-2959
25. Dua, R., Levy, D. L., and Campbell, J. L. (1998) Role of the putative zinc finger domain of Saccharomyces cerevisiae DNA polymerase α in DNA replication and the S/M checkpoint pathway. J. Biol. Chem. 273, 30046-30055
26. Klinge, S., Núñez-Ramírez, R., Llorca, O., and Pellegrini, L. (2009) 3D architecture of DNA Pol α reveals the functional core of multi-subunit replicative polymerases. EMBO J. 28, 1978-1987
27. Netz, D. J., Stith, C. M., Stümpfig, M., Köpf, G., Vogel, D., Genau, H. M., Stodola, J. L., Lill, R., Burgers, P. M., and Pierik, A. J. (2012) Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nat. Chem. Biol. 8, 125-132
28. Tahirov, T. H., Makarova, K. S., Rogozin, I. B., Pavlov, Y. I., and Koonin, E. V. (2009) Evolution of DNA polymerases: an inactivated polymeraseexonuclease module in Pol α and a chimeric origin of eukaryotic polymerases from two classes of archaeal ancestors. Biol. Direct 4, 11
29. Copeland, W. C., and Wang, T. S. (1993) Enzymatic characterization of the individual mammalian primase subunits reveals a biphasic mechanism for initiation of DNA replication. J. Biol. Chem. 268, 26179-26189
30. Klinge, S., Hirst, J., Maman, J. D., Krude, T., and Pellegrini, L. (2007) An iron-sulfur domain of the eukaryotic primase is essential for RNA primer synthesis. Nat. Struct. Mol. Biol. 14, 875-877
31. Carr, A. M., Paek, A. L., and Weinert, T. (2011) DNA replication: failures and inverted fusions. Semin. Cell Dev. Biol. 22, 866-874
32. Weiner, B. E., Huang, H., Dattilo, B. M., Nilges, M. J., Fanning, E., and Chazin, W. J. (2007) An iron-sulfur cluster in the C-terminal domain of the p58 subunit of humanDNAprimase. J. Biol. Chem. 282, 33444-33451
33. Vaithiyalingam, S., Warren, E. M., Eichman, B. F., and Chazin, W. J. (2010) Insights into eukaryotic DNA priming from the structure and functional interactions of the 4Fe-4S cluster domain of human DNA primase. Proc. Natl. Acad. Sci. U.S.A. 107, 13684-13689
34. Kilkenny, M. L., De Piccoli, G., Perera, R. L., Labib, K., and Pellegrini, L. (2012) A conserved motif in the C-terminal tail of DNA polymerase tethers primase to the eukaryotic replisome. J. Biol. Chem. 287, 23740-23747
35. Mizuno, T., Yamagishi, K., Miyazawa, H., and Hanaoka, F. (1999) Molecular architecture of the mouseDNApolymerase-primase complex. Mol. Cell. Biol. 19, 7886-7896
36. Huang, H., Weiner, B. E., Zhang, H., Fuller, B. E., Gao, Y., Wile, B. M., Zhao, K., Arnett, D. R., Chazin, W. J., and Fanning, E. (2010) Structure of a DNA polymerase-primase domain that docks on the SV40 helicase and activates the viral primosome. J. Biol. Chem. 285, 17112-17122
37. Zhou, B., Arnett, D. R., Yu, X., Brewster, A., Sowd, G. A., Xie, C. L., Vila, S., Gai, D., Fanning, E., and Chen, X. S. (2012) Structural basis for the interaction of a hexameric replicative helicase with the regulatory subunit of human DNA polymerase-primase. J. Biol. Chem. 287, 26854-26866
38. Kilkenny, M. L., Longo, M. A., Perera, R. L., and Pellegrini, L. (2013) Structures of human primase reveal design of nucleotide elongation site and mode of Pol α tethering. Proc. Natl. Acad. Sci. U.S.A. 110, 15961-15966
39. Baranovskiy, A. G., Gu, J., Babayeva, N. D., Agarkar, V. B., Suwa, Y., and Tahirov, T. H. (2014) Crystallization and preliminary X-ray diffraction analysis of human DNA primase. Acta Crystallogr. F Struct. Biol. Commun. 70, 206-210
40. Simon, A. C., Zhou, J. C., Perera, R. L., van Deursen, F., Evrin, C., Ivanova, M. E., Kilkenny, M. L., Renault, L., Kjaer, S., Matak-Vinkovi, D., Labib, K., Costa, A., and Pellegrini, L. (2014) A Ctf4 trimer couples the CMG helicase to DNA polymerase α in the eukaryotic replisome. Nature 510, 293-297
41. Sheaff, R. J., Kuchta, R. D., and Ilsley, D. (1994) Calf thymus DNA polymerase-primase: "communication" and primer-template movement between the two active sites. Biochemistry 33, 2247-2254
42. Agarkar, V. B., Babayeva, N. D., Pavlov, Y. I., and Tahirov, T. H. (2011) Crystal structure of the C-terminal domain of human DNA primase large subunit: Implications for the mechanism of the primase-polymerase switch. Cell Cycle 10, 926-931
43. Sauguet, L., Klinge, S., Perera, R. L., Maman, J. D., and Pellegrini, L. (2010) Shared active site architecture between the large subunit of eukaryotic primase and DNA photolyase. PLoS ONE 5, e10083
44. Mizuno, T., Ito, N., Yokoi, M., Kobayashi, A., Tamai, K., Miyazawa, H., and Hanaoka, F. (1998) The second-largest subunit of the mouse DNA polymerase-primase complex facilitates both production and nuclear translocation of the catalytic subunit of DNA polymerase. Mol. Cell. Biol. 18, 3552-3562
45. Feng, W., and D'Urso, G. (2001) Schizosaccharomyces pombe cells lacking the amino-terminal catalytic domains of DNA polymerase α are viable but require the DNA damage checkpoint control. Mol. Cell. Biol. 21, 4495-4504
46. Mäkiniemi, M., Pospiech, H., Kilpeläinen, S., Jokela, M., Vihinen, M., and Syväoja, J. E. (1999) A novel family of DNA-polymerase-associated B subunits. Trends Biochem. Sci 24, 14-16
47. Gambus, A., van Deursen, F., Polychronopoulos, D., Foltman, M., Jones, R. C., Edmondson, R. D., Calzada, A., and Labib, K. (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase α within the eukaryotic replisome. EMBO J. 28, 2992-3004
48. Huang, S. G., Weisshart, K., Gilbert, I., and Fanning, E. (1998) Stoichiometry and mechanism of assembly of SV40 T antigen complexes with the viral origin of DNA replication and DNA polymerase-primase. Biochemistry 37, 15345-15352
49. Bohn, E. W., and Wilson, S. H. (1974) Studies on the activity of the a particle-associated DNA polymerase. Cancer Res. 34, 1977-1981
50. Lao-Sirieix, S. H., Nookala, R. K., Roversi, P., Bell, S. D., and Pellegrini, L. (2005) Structure of the heterodimeric core primase. Nat. Struct. Mol. Biol. 12, 1137-1144
51. Copeland, W. C., and Tan, X. (1995) Active site mapping of the catalytic mouse primase subunit by alanine scanning mutagenesis. J. Biol. Chem. 270, 3905-3913
52. Vaithiyalingam, S., Arnett, D. R., Aggarwal, A., Eichman, B. F., Fanning, E., and Chazin, W. J. (2014) Insights into eukaryotic primer synthesis from structures of the p48 subunit of human DNA primase. J. Mol. Biol. 426, 558-569
53. Frick, D. N., and Richardson, C. C. (2001) DNA primases. Annu. Rev. Biochem. 70, 39-80
54. 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
55. Nick McElhinny, S. A., Watts, B. E., Kumar, D., Watt, D. L., Lundström, E. B., Burgers, P. M., Johansson, E., Chabes, A., and Kunkel, T. A. (2010) Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Natl. Acad. Sci. U.S.A. 107, 4949-4954
56. Mirkin, S. M., and Frank-Kamenetskii, M. D. (1994) H-DNA and related structures. Annu. Rev. Biophys. Biomol. Struct. 23, 541-576
57. Chomilier, J., Sun, J. S., Collier, D. A., Garestier, T., Hélène, C., and Lavery, R. (1992)Acomputational and experimental study of the bending induced at a double-triple helix junction. Biophys. Chem. 45, 143-152
58. Oguey, C., Foloppe, N., and Hartmann, B. (2010) Understanding the sequence-dependence of DNA groove dimensions: implications for DNA Interactions. PLoS ONE 5, e15931
59. Hile, S. E., and Eckert, K. A. (2004) Positive correlation between DNA polymerase-primase pausing and mutagenesis within polypyrimidine/ polypurine microsatellite sequences. J. Mol. Biol. 335, 745-759
60. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a pol α family DNA polymerase. Cell 105, 657-667
61. Bebenek, A., Carver, G. T., Dressman, H. K., Kadyrov, F. A., Haseman, J. K., Petrov, V., Konigsberg, W. H., Karam, J. D., and Drake, J. W. (2002) Dissecting the fidelity of bacteriophage RB69 DNA polymerase: site-specific modulation of fidelity by polymerase accessory proteins. Genetics 162, 1003-1018
62. Aguirre, J. D., Chifotides, H. T., Angeles-Boza, A. M., Chouai, A., Turro, C., and Dunbar, K. R. (2009) Redox-regulated Inhibition of T7 RNA polymerase via establishment of disulfide linkages by substituted Dppz dirhodium(II,II) complexes. Inorg. Chem. 48, 4435-4444