In silico studies of the African swine fever virus DNA polymerase X support an induced-fit mechanism

Biophysical Journal

Volumn 90, Issue 1, 2006, Pages 42-56

  Sampoli Benítez, Benedetta A ^a   Arora, Karunesh ^b   Schlick, Tamar ^b  

^a MARYMOUNT MANHATTAN COLLEGE   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE; DOUBLE STRANDED DNA; VIRUS DNA;

AFRICAN SWINE FEVER VIRUS; ANALYTIC METHOD; ARTICLE; CATALYSIS; CATALYST; COMPUTER MODEL; COMPUTER SIMULATION; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; DNA STRUCTURE; EXCISION REPAIR; KINETICS; MOLECULAR DYNAMICS; MOLECULAR STABILITY; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE BINDING SITE; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; STRUCTURE ANALYSIS; VIRUS MUTATION;

AFRICAN SWINE FEVER VIRUS; DNA VIRUSES;

EID: 33646127783     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.071944     Document Type: Article

References (82)

1. Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature. 362:709-715.
2. Beckman, K. B., and B. N. Ames. 1997. Oxidative decay of DNA. J. Biol. Chem. 272:19633-19636.
3. Cadet, J., M. Berger, T. Douki, B. Morin, S. Raoul, J. L. Ravanat, and S. Spinelli. 1997. Effects of UV and visible radiation on DNA-final base damage. Biol. Chem. 378:1275-1286.
4. Seeberg, E., L. Eide, and M. Bjoras. 1995. The base excision pathway. Trends Biochem. Sci. 20:391-397.
5. Mol, C. D., S. S. Parikh, C. D. Putnam, T. P. Lo, and J. A. Tainer. 1999. DNA repair mechanisms for the recognition and removal of damaged DNA bases. Annu. Rev. Biophys. Biomol. Struct. 28:101-128.
6. Beard, W. A., D. D. Shock, B. J. Vande Berg, and S. H. Wilson. 2002. Efficiency of correct nucleotide insertion governs DNA polymerase fidelity. J. Biol. Chem. 277:47393-47398.
7. Wilson, S. H. 1998. Mammalian base excision repair and DNA polymerase β. Mutat. Res. 407:203-215.
8. Kunkel, T. A., and K. Bebenek. 1988. Recent studies of the fidelity of DNA synthesis. Biochim. Biophys. Acta. 951:1-15.
9. Zhang, Y., F. Yuan, X. Wu, and Z. Wang. 2000. Preferential incorporation of G opposite template T by the low-fidelity DNA polymerase β. Mol. Cell. Biol. 20:7099-7108.
10. Showalter, A. K., and M.-D. Tsai. 2001. A DNA polymerase with specificity for five base pairs. J. Am. Chem. Soc. 123:1776-1777.
11. Beard, W. A., and S. H. Wilson. 2003. Structural insights into the origins of DNA polymerase fidelity. Structure. 11:489-496.
12. Lehmann, A. R. 2002. Replication of damaged DNA in mammalian cells: new solutions to an old problem. Mutat. Res. 509:23-34.
13. Friedberg, E. C., R. Wagner, and M. Radman. 2002. Specialized DNA polymerases, cellular survival and the genesis of mutations. Science. 296:1627-1630.
14. Yang, W. 2005. Portraits of a Y-family DNA polymerase. FEBS Lett. 579:868-872.
15. Delarue, M., O. Poch, N. Tordo, D. Moras, and P. Argos. 1990. An attempt to unify the structure of polymerases. Protein Eng. 3:461-467.
16. Beese, L. S., and T. A. Steitz. 1991. Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 9:25-33.
17. Steitz, T. A., S. J. Smerdon, J. Jäger, and C. M. Joyce. 1994. A unified polymerase mechanism for non-homologous DNA and RNA polymerases. Science. 266:2022-2025.
18. Bolton, E. C., A. S. Mildvan, and J. D. Boeke. 2002. Inhibition of reverse transcription in vivo by elevated manganese ion concentration. Mol. Cell. 9:879-889.
19. Yang, L., K. Arora, W. A. Beard, S. H. Wilson, and T. Schlick. 2004. Critical role of magnesium ions in DNA polymerase β's closing and active site assembly. J. Am. Chem. Soc. 126:8441-8453.
20. Beard, W. A., D. D. Shock, and S. H. Wilson. 2004. Influence of DNA structure of DNA polymerase β active site function: extension of mutagenic DNA intermediates. J. Biol. Chem. 279:31921-31929.
21. Kuchta, R. D., P. Benkovic, and S. J. Benkovic. 1988. Kinetic mechanism whereby DNA polymerase I Klenow replicates DNA with high fidelity. Biochemistry. 27:6716-6725.
22. Dahlberg, M. E., and S. J. Benkovic. 1991. Kinetics mechanism of DNA polymerase I Klenow fragment. Identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry. 30:4835-4843.
23. Patel, S. S., I. Wong, and K. A. Johnson. 1991. Pre-steady state kinetic analysis of processive DNA replication inducing complete characterization of an exonuclease-deficient mutant. Biochemistry. 30:511-525.
24. Frey, M. W., L. C. Sowers, D. P. Millar, and S. J. Benkovic. 1995. The nucleotide analog 2-aminopurine as a spectroscopic probe of nucleotide incorporation by the Klenow fragment of Escherichia coli polymerase I and bacteriophage T4 DNA polymerase. Biochemistry. 34:9185-9192.
25. Vande Berg, B. J., W. A. Beard, and S. H. Wilson. 2001. DNA structure and Aspartate 276 influence nucleotide binding to human DNA polymerase β. J. Biol. Chem. 276:3408-3416.
26. Ahn, J., B. G. Werneburg, and M.-D. Tsai. 1997. DNA polymerase β: structure-fidelity relationship from pre-steady-state kinetic analyses of all possible correct and incorrect base pairs for wild type and R283A mutant. Biochemistry. 36:1100-1107.
27. Ahn, J., V. S. Kraynov, X. Zhong, B. G. Werneburg, and M.-D. Tsai. 1998. DNA polymerase β: effects of gapped DNA substrates on dNTP specificity, fidelity, processivity and conformational changes. Biochem. J. 331:79-87.
28. Kati, W. M., K. A. Johnson, L. F. Jerva, and K. S. Anderson. 1992. Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267:25988-25997.
29. Sawaya, M. R., P. Prasad, S. H. Wilson, J. Kraut, and H. Pelletier. 1997. Crystal structure of human DNA polymerase b complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry. 36:11205-11215.
30. García-Díaz, M., K. Bebenek, J. M. Krahn, L. Blanco, T. A. Kunkel, and L. C. Pedersen. 2004. A structural solution for the DNA polymerase λ-dependent repair of DNA gaps with minimal homology. Mol. Cell. 13:561-572.
31. Li, Y., S. Korolev, and G. Waksman. 1998. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J. 17:7514-7525.
32. Ollis, D. L., P. Brick, R. Hamlin, N. G. Xuong, and T. A. Steitz. 1985. Structure of a large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature. 313:762-766.
33. Steitz, T. A. 1999. DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274:17395-17398.
34. Beard, W. A., and S. H. Wilson. 2000. Structural design of a eukaryotic DNA repair polymerase: DNA polymerase beta. Mutat. Res. 460:231-244.
35. Sobol, R. W., J. K. Horton, R. Kuhn, H. Gu, R. K. Singhal, R. Prasad, K. Rajewski, and S. H. Wilson. 1996. Requirement of mammalian DNA polymerase β in base excision repair. Nature. 379:183-186.
36. Lindahl, T. 2000. Suppression of spontaneous mutagenesis in human cells by DNA base excision-repair. Mutat. Res. 462:129-135.
37. Oliveros, M., R. J. Yañez, M. L. Salas, J. Salas, E. Viñuela, and L. Blanco. 1997. Characterization of an African swine fever virus 20 kDa DNA polymerase involved in DNA repair. J. Biol. Chem. 272:30899-30910.
38. Yañez, R. J., J. M. Rodríguez, M. L. Nogal, L. Yuste, C. Enríquez, J. F. Rodíguez, and E. Vuñuela. 1995. Analysis of the complete sequence of African swine fever virus. Virology. 208:249-278.
39. García-Escudero, R., M. García-Díaz, M. L. Salas, L. Blanco, and J. Salas. 2003. DNA polymerase X of African swine fever virus: insertion fidelity on gapped DNA substrates and AP lyase activity supports a role in base excision repair of viral DNA. J. Mol. Biol. 326:1403-1412.
40. Forman, H. J., and M. Torres. 2001. Redox signaling in macrophages. Mol. Aspects Med. 22:189-216.
41. Maciejewski, M. W., R. Shin, R. Pan, A. Marintchev, A. Denninger, M. A. Mullen, K. Chen, M. R. Gryk, and G. P. Mullen. 2001. Solution structure of viral DNA repair polymerase. Nat. Struct. Biol. 8:936-941.
42. Showalter, A. K., I. Byeon, M. Su, and M.-D. Tsai. 2001. Solution structure of a viral DNA polymerase and evidence for a mutagenic function. Nat. Struct. Biol. 8:942-946.
43. Beard, W. A., and S. H. Wilson. 2001. DNA polymerases lose their grip. Nat. Struct. Biol. 8:915-917.
44. Schlick, T. 2002. Molecular Modeling and Simulation: An Interdisciplinary Guide. Springer-Verlag, New York.
45. Koshland, D. E. 1994. The key-lock theory and the induced-fit theory. Angew. Chem. Int. Ed. Engl. 33:2375-2378.
46. Post, C. B., and W. J. Ray Jr. 1995. Reexamination of induced fit as a determinant of substrate specificity in enzymatic reactions. Biochemistry. 34:15881-15885.
47. McCammon, J. A., and S. C. Harvey. 1987. Dynamics of Proteins and Nucleic Acids. Cambridge University Press, Cambridge, UK.
48. Karplus, M., and J. A. McCammon. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:646-652.
49. Qian, X., D. Strahs, and T. Schlick. 2001. A new program for optimizing periodic boundary models of solvated biomolecules PBCAID. J. Comput. Chem. 22:1843-1850.
50. Klapper, I., R. Hadstrom, R. Fine, K. Sharp, and B. Honig. 1986. Focusing of electric fields in the active site of Cu-Zn superoxide dismutase: effects of ion strength and amino acid modification. Proteins. 1:47-59.
51. Brooks, B. R., R. E. Bruccoleri, B. D. Olafson, D. J. States, S. Swaminathan, and M. Karplus. 1983. CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4:187-217.
52. MacKerell, A. D. Jr., B. R. Brooks, C. L. Brooks III, L. Nilsson, B. Roux, Y. Won, and M. Karplus. 1998. CHARMM: the energy function and its parameterization. In Encyclopedia of Computational Chemistry. P. von Ragué Schleyer, editor. John Wiley and Sons, New York. 271-277.
53. Schlick, T. 1992. Optimization methods in computational chemistry. In Reviews in Computational Chemistry, Vol. 3. K. B. Lipkowitz and D. B. Boyd, editors. VCH Publishers, New York. 1-71.
54. Yang, L., W. A. Beard, S. H. Wilson, S. Broyde, and T. Schlick. 2002. Polymerase β simulations reveal that Arg258 rotation is a slow step rather than large subdomain motion per se. J. Mol. Biol. 317:651-671.
55. Ryckaert, J. P., G. Ciccotti, and H. J. C. Berendsen. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23:327-341.
56. Darden, T., D. M. York, and L. G. Pedersen. 1993. Particle mesh Ewald: an N·logN method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
57. Kalé, L., R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz, J. Phillips, A. Shinozaki, K. Varadarajan, and K. Schulten. 1999. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151:283-312.
58. MacKerell, A. D. Jr., and N. K. Banavali. 2000. All-atom empirical force-field for nucleic acids. II. Applications to molecular dynamics simulations of DNA and RNA in solution. J. Comput. Chem. 21:105-120.
59. Feller, S. E., Y. Zhang, R. W. Pastor, and B. R. Brooks. 1995. Constant pressure molecular dynamics simulation: the Langevin piston method. J. Chem. Phys. 103:4612-4621.
60. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD-visual molecular dynamics. J. Mol. Graph. 14:33-38.
61. Arora, K., and T. Schlick. 2004. In silico evidence for DNA polymerase β's substrate-induced conformational change. Biophys. J. 87:3088-3099.
62. Arora, K., W. A. Beard, S. H. Wilson, and T. Schlick. 2005. Mismatch-induced conformational distortions in polymerase beta support an induced-fit mechanism for fidelity. Biochemistry. 44:13328-13341.
63. Qian, X., D. Strahs, and T. Schlick. 2001. Dynamic simulations of 13 TATA variants refine kinetic hypotheses on sequence/activity. J. Mol. Biol. 308:681-703.
64. Qian, X., and T. Schlick. 2002. Efficient multiple-time-step integrators with distance-based force splitting for particle-mesh-Ewald molecular dynamics simulations. J. Chem. Phys. 116:5971-5983.
65. Norberg, J., and L. Nilsson. 2000. On truncation of long-range electrostatic interactions in DNA. Biophys. J. 79:1537-1553.
66. Menge, K. L., Z. Hostomsky, B. R. Nodes, G. O. Hudson, S. Rahmati, E. W. Moomaw, R. J. Almassy, and Z. Hostomska. 1995. Structure function analysis of the mammalian DNA polymerase β active site: role of aspartic acid 256, arginine 254 and arginine 258 in nucleotidyl transfer. Biochemistry. 34:15934-15942.
67. Yang, L., W. A. Beard, S. H. Wilson, B. Roux, S. Broyde, and T. Schlick. 2002. Local deformations revealed by dynamics simulations of DNA polymerase β with DNA mismatches at the primer terminus. J. Mol. Biol. 321:459-478.
68. Radhakrishnan, R., and T. Schlick. 2004. Orchestration of cooperative event in DNA synthesis and repair mechanism unraveled by transition path sampling of DNA polymerase β's closing. Proc. Natl. Acad. Sci. USA. 101:5970-5975.
69. Arora, K., and T. Schlick. 2005. The conformational transition pathway of polymerase β/DNA upon binding correct incoming substrate. J. Phys. Chem. B. 109:5358-5367.
70. Abashkin, Y. G., J. W. Erickson, and S. K. Burt. 2001. Quantum chemical investigation of enzymatic activity in DNA polymerase β. A mechanistic study. J. Phys. Chem. B. 105:287-292.
71. Rittenhouse, R. C., W. K. Apostoluk, J. H. Miller, and T. P. Straatsma. 2003. Characterization of the active site of polymerase β by molecular dynamics and quantum chemical calculation. Proteins. 53:667-682.
72. Mildvan, A. S. 1997. Mechanism of signaling and related enzymes. Proteins. 29:401-416.
73. Radhakrishnan, R., and T. Schlick. 2005. Fidelity discrimination in DNA polymerase beta: differing closing profiles for a mismatched (G:A) versus matched (G:C) base pair. J. Am. Chem. Soc. 127:13245-13252.
74. Pelletier, H., M. R. Sawaya, A. Kumar, S. H. Wilson, and J. Kraut. 1994. Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer and ddCTP. Science. 264:1891-1903.
75. Zhong, X., S. S. Patel, B. G. Werneburg, and M.-D. Tsai. 1997. DNA polymerase β: multiple conformational changes in the mechanism of catalysis. Biochemistry. 36:11891-11900.
76. Suo, Z., and K. A. Johnson. 1998. Selective inhibition of HIV-1 reverse transcriptase by an antiviral inhibitor, R-9-2-phosphonylmethoxypropyladenine. J. Biol. Chem. 273:27250-27258.
77. Doublié, S., and T. Ellenberger. 1998. The mechanism of action of T7 DNA polymerase. Curr. Opin. Struct. Biol. 8:704-712.
78. Huang, H., R. Chopra, G. L. Verdine, and S. C. Harrison. 1998. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science. 282:1669-1675.
79. Beard, W. A., and S. H. Wilson. 1998. Structural insights into the DNA polymerase β fidelity: hold it tight if you want it right. Chem. Biol. 5:R7-R13.
80. Wong, I., S. S. Patel, and K. A. Johnson. 1991. An induced-fit mechanism for DNA replication fidelity: direct measurement by single turnover kinetics. Biochemistry. 30:526-537.
81. Doublié, S., M. R. Sawaya, and T. Ellenberger. 1999. An open and closed case for all polymerases. Structure. 7:R31-R35.
82. Yang, L., W. A. Beard, S. H. Wilson, S. Broyde, and T. Schlick. 2004. Highly organized but pliant active site of DNA polymerase β: compensatory mechanisms in mutant enzymes revealed by dynamics simulations and energy analyses. Biophys. J. 86:3392-3408.