Subtle but variable conformational rearrangements in the replication cycle of Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4) may accommodate lesion bypass

Protein Science

Volumn 15, Issue 1, 2006, Pages 135-151

  Wang, Yanli ^a   Arora, Karunesh ^a   Schlick, Tamar ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Catalytic metal ion; Conformational changes; Dpo4; Dynamics simulations; Nucleotide binding metal ion; Replication mechanism

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE IV; METAL ION; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CONFORMATIONAL TRANSITION; CORRELATION ANALYSIS; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME DEGRADATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SULFOLOBUS SOLFATARICUS;

ARGININE; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; DNA DAMAGE; DNA POLYMERASE BETA; DNA REPAIR; DNA REPLICATION; DNA, ARCHAEAL; GUANOSINE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SULFOLOBUS SOLFATARICUS; THERMODYNAMICS;

SULFOLOBUS SOLFATARICUS;

EID: 29344432100     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.051726906     Document Type: Article

References (57)

1. Abashkin, Y.G., Erickson, J.W., and Burt, S.K. 2001. Quantum chemical investigation of enzymatic activity in DNA polymerase β. A mechanistic study. J. Phys. Chem. B 105: 287-292.
2. Altona, C. and Sundaraligam, M. 1972. Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation. J. Am. Chem. Soc. 94: 8205-8212.
3. Ames, B.N. and Gold, L.S. 1991. Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250: 3-16.
4. Arora, K. and Schlick, T. 2003. Deoxyadenosine sugar puckering pathway simulated by the stochastic difference equation algorithm. Chem. Phys. Lett. 378: 1-8.
5. _. 2004. In silico evidence for DNA polymerase-beta's substrateinduced conformational change. Biophys. J. 87: 3088-3099.
6. Arora, K., Beard, W.A., Wilson, S.H., and Schlick, T. 2005. Mismatchinduced conformational distortions in polymerase β/DNA complex support an induced-fit mechanism for fidelity. Biochemistry 44: 13328-13341.
7. Barth, E. and Schlick, T. 1998a. Extrapolation versus impulse in multipletimestepping schemes. II. Linear analysis and applications to Newtonian and Langevin dynamics. J. Chem. Phys. 109: 1633-1642.
8. _. 1998b. Overcoming stability limitations in biomolecular dynamics. I. Combining force splitting via extrapolation with Langevin dynamics in LN. J. Chem. Phys. 109: 1617-1632.
9. Boudsocq, F., Iwai, S., Hanaoka, F., and Woodgate, R. 2001. Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): An archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic pol eta. Nucleic Acids Res. 29: 4607-4616.
10. Boudsocq, F., Kokoska, R.J., Plosky, B.S., Vaisman, A., Ling, H., Kunkel, T.A., Yang, W., and Woodgate, R. 2004. Investigating the role of the little finger domain of Y-family DNA polymerases in low fidelity synthesis and translesion replication. J. Biol. Chem. 279: 32932-32940.
11. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S., and Karplus, M. 1983. Charmm-Aprogramfor macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4: 187-217.
12. Brun̈ger, A.T. and Karplus, M. 1988. Polar hydrogen positions in proteins - Empirical energy placement and neutron-diffraction comparison. Proteins 4: 148-156.
13. Bunting, K.A., Roe, S.M., and Pearl, L.H. 2003. Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the β-clamp. EMBO J. 22: 5883-5892.
14. Cheng, K.C., Cahill, D.S., Kasai, H., Nishimura, S., and Loeb, L.A. 1992. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 267: 166-172.
15. Darden, T., York, D., and Pedersen, L. 1993. Particle mesh ewald-An N.Log(N) nethod for Ewald sums in large systems. J. Chem. Phys. 98: 10089-10092.
16. Feller, S.E., Zhang, Y.H., Pastor, R.W., and Brooks, B.R. 1995. Constantpressure molecular-dynamics simulation-The Langevin piston method. J. Chem. Phys. 103: 4613-4621.
17. Fiala, K.A. and Suo, Z. 2004a. Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43: 2116-2125.
18. _. 2004b. Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43: 2106-2115.
19. Fleck, O. and Schär, P. 2004. Translesion DNA synthesis: Little fingers teach tolerance. Curr. Biol. 14: R389-R391.
20. Foloppe, N. and MacKerell, A.D. 2000. All-atom empirical force field for nucleic acids. I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J. Comput. Chem. 21: 86-104.
21. Friedberg, E.C., Wagner, R., and Radman, M. 2002. Molecular biology - Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296: 1627-1630.
22. Gilson, M.K., Sharp, K.A., and Honig, B.H. 1988. Calculating the electrostatic potential of molecules in solution-Method and error assessment. J. Comput. Chem. 9: 327-335.
23. Humphrey, W., Dalke, A., and Schulten, K. 1996. VMD: Visual molecular dynamics. J. Mol. Graph. 14: 33-38.
24. Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., Phillips, J., Shinozaki, A., Varadarajan, K., and Schulten, K. 1999. NAMD2: Greater scalability for parallel molecular dynamics. J. Comput. Phys. 151: 283-312.
25. Klapper, I., Hagstrom, R., Fine, R., Sharp, K., and Honig, B. 1986. Focusing of electric fields in the active site of Cu-Zn superoxide dismutase: Effects of ionic strength and amino-acid modification. Proteins 1: 47-59.
26. Krahn, J.M., Beard, W.A., and Wilson, S.H. 2004. Structural insights into DNA polymerase b deterrents for misincorporation support an induced-fit mechanism for fidelity. Structure 12: 1823-1832.
27. Lahiri, S.D., Zhang, G.F., Dunaway-Mariano, D., and Allen, K.N. 2003. The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 299: 2067-2071.
28. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. 2001. Crystal structure of a Y-family DNA polymerase in action: A mechanism for errorprone and lesion-bypass replication. Cell 107: 91-102.
29. Ling, H., Boudsocq, F., Plosky, B.S., Woodgate, R., and Yang, W. 2003. Replication of a cis-syn thymine dimer at atomic resolution. Nature 424: 1083-1087.
30. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. 2004a. Snapshots of replication through an abasic lesion: Structural basis for base substitutions and frameshifts. Mol. Cell 13: 751-762.
31. Ling, H., Sayer, J.M., Plosky, B.S., Yagi, H., Boudsocq, F., Woodgate, R., Jerina, M., and Yang, W. 2004b. Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase. Proc. Natl. Acad. Sci. 101: 2265-2269.
32. MacKerell, A.D., Bashford, D., Bellott, M., Dunbrack Jr., R.L., Evanseck, J.D., Field, M.J., Fischer, S., Gao, J., Ha, S., Joseph-McCarthy, D., et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102: 3586-3616.
33. Marquez, V.E., Ben-Kasus, T., Barchi Jr., J.J., Green, K.M., Nicklaus, M.C., and Riald, A. 2004. Experimental and structural evidence that herpes 1 kinase and cellular DNA polymerase(s) discriminate on the basis of sugar pucker. J. Am. Chem. Soc. 126: 543-549.
34. Mezei, M. 1997. Optimal position of solute for simulations. J. Comput. Chem. 18: 812-815.
35. Mildvan, A.S. 1997. Mechanisms of signaling and related enzymes. Proteins 29: 401-416.
36. Moriya, M. 1993. Single-stranded shuttle phagemid for mutagenesis studies in mammalian-cells-8-oxoguanine in DNA induces targeted G·C→ T·A transversions in simian kidney-cells. Proc. Natl. Acad. Sci. 90: 1122-1126.
37. Perlow-Poehnelt, R.A., Likhterov, I., Scicchitano, D.A., Geacintov, N.E., and Broyde, S. 2004. The spacious active site of a Y-family DNA polymerase facilitates promiscuous nucleotide incorporation opposite a bulky carcinogen-DNA adduct - Elucidating the structure-function relationship through experimental and computational approaches. J. Biol. Chem. 279: 36951-36961.
38. Qian, X.L., Strahs, D., and Schlick, T. 2001. A new program for optimizing periodic boundary models of solvated biomolecules (PBCAID). J. Comput. Chem. 22: 1843-1850.
39. Radhakrishnan, R. and Schlick, T. 2004. Orchestration of cooperative events in DNA synthesis and repair mechanism unraveled by transition path sampling of DNA polymerase β's closing. Proc. Natl Acad. Sci. 101: 5970-5975.
40. _. 2005. Fidelity discrimination in DNA polymerase β: Differing closing profiles for a mismatched G:A versus matched G:C basepair. J. Am. Chem. Soc. 127: 13245-13252.
41. Rothwell, P.J., Mitaksov, V., and Waksman, G. 2005. Motions of the fingers subdomain of klentaq1 are fast and not rate limiting: Implications for the molecular basis of fidelity in DNA polymerases. Mol. Cell 19: 345-355.
42. Ryckaert, J.P., Ciccotti, G., and Berendsen, H.J.C. 1977. Numerical-integration of cartesian equations of motion of a system with constraints - Molecular-dynamics of n-alkanes. J. Comput. Phys. 23: 327-341.
43. Sali, A., Potterton, L., Yuan, F., Vanvlijmen, H., and Karplus, M. 1995. Evaluation of comparative protein modeling by modeler. Proteins 23: 318-326.
44. Sawaya, M.R., Prasad, R., Wilson, S.H., Kraut, J., and Pelletier, H. 1997. Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: Evidence for an induced fit mechanism. Biochemistry 36: 11205-11215.
45. Schlick, T. 1999. Computational molecular biophysics today: A confluence of methodological advances and complex biomolecular applications. J. Comput. Phys. 151: 1-8.
46. _. 2001. Time-trimming tricks for dynamic simulations: Splitting force updates to reduce computational work. Structure 9: R45-R53.
47. Schlick, T., Barth, E., and Mandziuk, M. 1997. Biomolecular dynamics at long timesteps: Bridging the timescale gap between simulation and experimentation. Annu. Rev. Biophys. Biomol. Struct. 26: 181-222.
48. Shibutani, S. and Grollman, A.P. 1994. Miscoding during DNA-synthesis on damaged DNA templates catalyzed by mammalian-cell extracts. Cancer Lett. 83: 315-322.
49. Silvian, L.F., Toth, E.A., Pham, P., Goodman, M.F., and Ellenberger, T. 2001. Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat. Struct. Biol. 8: 984-989.
50. Steitz, T.A. 1993. DNA-dependent and RNA-dependent DNA-polymerases. Curr. Opin. Struc. Biol. 3: 31-38.
51. Vaisman, A., Ling, H., Woodgate, R., and Yang, W. 2005. Fidelity of Dpo4: Effect of metal ions, nucleotide selection and pyrophosphorolysis. EMBO J. 24: 2957-2967.
52. Wang, L.H., Wu, M., Yan, S.F., Patel, D.J., Geacintov, N.E., and Broyde, S. 2005. Accommodation of a 1S-(-)-Benzo[c]phenanthrenyl-N-6-dA adduct in the Y-family dpo4 DNA polymerase active site: Structural insights through molecular dynamics simulations. Chem. Res. Toxicol. 18: 441-456.
53. Yang, W. 2003. Damage repair DNA polymerases Y. Curr. Opin. Struct. Biol. 13: 23-30.
54. Yang, L.J., Beard, W.A., Wilson, S.H., Broyde, S., and Schlick, T. 2002a. Polymerase β simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se. J. Mol. Biol. 317: 651-671.
55. Yang, L.J., Beard, W.A., Wilson, S.H., Roux, B., Broyde, S., and Schlick, T., 2002b. Local deformations revealed by dynamics simulations of DNA Polymerase β with DNA mismatches at the primer terminus. J. Mol. Biol. 321: 459-478.
56. Yang, L.J., Arora, K., Beard, W.A., Wilson, S.H., and Schlick, T. 2004. Critical role of magnesium ions in DNA polymerase β's closing and active site assembly. J. Am. Chem. Soc. 126: 8441-8453.
57. Yeiser, B., Pepper, E.D., Goodman, M.F., and Finkel, S.E. 2002. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. Proc. Natl Acad. Sci. 99: 8737-8741.