Catalytic mechanism of human DNA polymerase λ with Mg2+ and Mn2+ from ab initio quantum mechanical/molecular mechanical studies

DNA Repair

Volumn 7, Issue 11, 2008, Pages 1824-1834

  Cisneros, G Andrés ^a   Perera, Lalith ^a   García Díaz, Miguel ^a   Bebenek, Katarzyna ^a   Kunkel, Thomas A ^a   Pedersen, Lee G ^a,b  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b University of North Carolina at Chapel Hill   (United States)

Author keywords

DNA polymerase lambda; Molecular dynamics; Polymerase catalysis; QM MM; Simulations

Indexed keywords

ASPARTIC ACID; DNA POLYMERASE; DNA POLYMERASE LAMBDA; MAGNESIUM; MANGANESE; NUCLEOTIDE; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENERGY METABOLISM; MOLECULAR MECHANICS; MUTAGENESIS; PRIORITY JOURNAL; PROTON TRANSPORT;

AMINO ACID SEQUENCE; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA POLYMERASE BETA; HUMANS; MAGNESIUM; MANGANESE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 54849390600     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.07.007     Document Type: Article

References (72)

1. Iwanaga A., Ouchida M., Miyazaki K., Hori K., and Mukai T. Functional mutation of DNA polymerase β found in human gastric cancer-inability of the base excision repair in vivo. Mutat. Res. 435 (1999) 121-128
2. Starcevic D., Dalal S., and Sweasy J.B. Is there a link between DNA polymerase β and cancer?. Cell Cycle 3 (2004) 98-1001
3. Kunkel T.A. Considering the cancer consequences of altered DNA polymerase function. Cancer Cell 3 (2003) 105-110
4. Bebenek K., and Kunkel T.A. Functions of DNA polymerases. Adv. Protein Chem. 69 (2004) 137-165
5. Cowan J. Structural and catalytic chemistry of magnesium-dependent enzymes. BioMetals 15 (2002) 225-235
6. Steitz T.A. DNA- and RNA-dependent DNA polymerases. Curr. Opin. Struct. Biol. 3 (2003) 31-38
7. Abashkin Y.G., Erickson J.W., and Burt S.K. Quantum chemical investigation of enzymatic activity in DNA polymerase β. A mechanistic study. J. Phys. Chem. B 105 (2001) 287-292
8. Fiala K.A., Abdel-Gawad W., and Suo Z. Pre-steady state kinetic studies of the fidelity and mechanism of polymerization catalyzed by truncated human DNA polymerase λ. Biochemistry 43 (2004) 6751-6762
9. Radhakrishnan R., and Schlick T. Correct and incorrect nucleotide incorporation pathways in DNA polymerase β. Biochem. Biophys. Res. Commun. 350 (2006) 521-529
10. Showalter A.K., Lamarche B.J., Bakhtina M., Su M.-I., Tang K.-H., and Tsai M.-D. Mechanistic comparison of high-fidelity and error-prone DNA polymerases and ligases involved in DNA repair. Chem. Rev. 106 (2006) 340-360
11. Rungrotmongkol T., Mulholland A.J., and Hannongbua S. Active site dynamics and combined quantum mechanics/molecular mechanics (QM/MM) modelling of a hiv-1 reverse transcriptase/DNA/dttp complex. J. Mol. Graph. Model. 26 (2007) 1-13
12. Bakhtina M., Roettger M.P., Kumar S., and Tsai M.-D. A unified kinetic mechanism applicable to multiple DNA polymerases. Biochemistry 46 (2007) 5463-5472
13. Xiang Y., and Warshel A. Quantifying free energy profiles of proton transfer reactions in solution and proteins by using a diabatic FDFT mapping. J. Phys. Chem. B 112 (2008) 1007-1015
14. Bojin M.D., and Schlick T. A quantum mechanical investigation of possible mechanisms for the nucleotidyl transfer reaction catalyzed by DNA polymerase β. J. Phys. Chem. B 111 (2007) 11244-11252
15. Lin P., Pedersen L.C., Batra V.K., Beard W.A., Wilson S.H., and Pedersen L.G. Energy analysis of chemistry for correct insertion by DNA polymerase β. Proc. Natl. Acad. Sci. 36 (2006) 13294-13299
16. Florián J., Goodman M.E., and Warshel S A. Computer simulation of the chemical catalysis of DNA polymerases: discriminating between alternative nucleotide insertion mechanisms for T7 DNA polymerase. J. Am. Chem. Soc. 125 (2003) 8163-8177
17. Florián J., Goodman M.F., and Warshel A. Computer simulations of protein functions: searching for the molecular origin of the replication fidelity of DNA polymerases. Proc. Natl. Acad. Sci. 102 (2005) 6819-6824
18. Wang L., Yu X., Hu P., Broyde S., and Zhang Y. A water-mediated and substrate-assisted catalytic mechanism for Sulfobolus solfataricus DNA polymerase IV. J. Am. Chem. Soc. 129 (2007) 4731-4737
19. Alberts I.L., Wang Y., and Schlick T. DNA polymerase β catalysis: are different mechanisms possible?. J. Am. Chem. Soc. 129 (2007) 11100-11110
20. 2+ dependence: a kinetic and thermodynamic study. Biochemistry 42 (2003) 7467-7476
21. Battra V.K., Beard W.A., Shock D.D., Pedersen L.C., and Wilson S.H. Structures of DNA polymerase β with active site mismatches suggest a transient abasic site intermediate during misincorporation. Mol. Cell 30 (2008) 315-324
22. Bebenek K., García-Díaz M., Blanco L., and Kunkel T.A. The frameshift infidelity of human DNA polymerase lambda: implications for function. J. Biol. Chem. 278 (2003) 34685-34690
23. Shevelev I., Blanca G., Villani G., Ramadan K., Spadari S., Húbscher U., and Maga G. Mutagenesis on human DNA polymerase λ: essential roles of tyr505 and phe506 for both DNA polymerase and terminal transferase activities. Nucleic Acid Res. 31 (2003) 6919-6925
24. García-Díaz M., Bebenek K., Gao G., Pedersen L.C., London R.E., and Kunkel T.A. Structure-function studies of DNA polymerase λ. DNA Rep. 4 (2005) 1358-1367
25. García-Díaz M., Bebenek K., Krahn J.M., Pedersen L.C., and Kunkel T.A. Structural analysis of strand misalignment during DNA synthesis by a human DNA polymerase. Cell 124 (2006) 331-342
26. Foley M.C., and Schlick T. Simulations of DNA Pol λ R517 mutants indicate 517's crucial role in ternary complex stability and suggest DNA slippage origin. J. Am. Chem. Soc. 130 (2008) 3967-3977
27. Braithwaite E.K., Prasad R., Shock D.D., How E.W., Beard W.A., and Wilson S.H. DNA polymerase λ mediates a back-up base excision repair activity in extracts of mouse embryonic fibroblasts. J. Biol. Chem. 280 (2005) 18469-18475
28. Braithwaite E.K., Kedar P.S., Lan L., Polosina Y.Y., Asagoshi K., Poltoratsky V.P., Horton J.K., Miller H., Teebor G.W., Yasui A., and Wilson S.H. DNA polymerase λ protects mouse fibroblasts against oxidative DNA damage and is regruited to sites of DNA damage/repair. J. Biol. Chem. 280 (2005) 31641-31647
29. Tano K., Nakamura J., Asagoshi K., Arakawa H., Sonoda E., Braithwaite E.K., Prasad R., Buerstedde J.-M., Takeda S., Watanabe M., and Wilson S.H. Interplay between DNA polymerase β and λ in repair of oxidation DNA damage in chicken dt40 cells. DNA Rep. 6 (2007) 869-875
30. Moon A.E., García-Díaz M., Batra V.K., Beard W.A., Bebenek K., Kunkel T.A., Wilson S.H., and Pedersen L.C. The X family portrait: structural insights into biological functions of X family polymerases. DNA Rep. 6 (2007) 1709-1725
31. García-Díaz M., Bebenek K., Krahn J.M., Kunkel T.A., and Pedersen L.C. A closed conformation for the pol λ catalytic cycle. Nat. Struct. Mol. Biol. 12 (2005) 97-98
32. Foley M.C., Arora K., and Schlick T. Sequential side-chain residue motions transform the binary into the ternary state of DNA polymerase λ. Biophys. J. 91 (2006) 3182-3195
33. García-Díaz M., Bebenek K., Pedersen L.C., and Kunkel T.A. Role of the catalytic metals during polymerization by DNA polymerase lambda. DNA Rep. 6 (2007) 1333-1340
34. Zhang Y., Lee T., and Yang W. A pseudo-bond approach to combining quantum mechanical and molecular mechanical methods. J. Chem. Phys. 110 (1999) 46-54
35. Zhang Y., Liu H., and Yang W. Free energy calculation on enzyme reactions with an efficient iterative procedure to determine minimum energy paths on a combined ab initio QM/MM potential energy surface. J. Chem. Phys. 112 (2000) 3483-3491
36. Zhang Y., Liu H., and Yang W. Ab Initio QM/MM and free energy calculations of enzyme reactions. Computational Methods for Macromolecules-Challenges and Applications (2002), Springer Verlag, Heidelberg, Germany
37. Frouin I., Toueille M., Ferrari E., Shevelev I., and Hübscher U. Phosphorylation of human DNA polymerase λ by the cyclin-dependent kinase cdk2/cyclin a complex is modulated by its association with proliferating cell nuclear antigen. Nucleic Acid Res. 33 (2005) 5354-5361
38. McCammon J.A., Gelin B.R., and Karplus M. Dynamics of folded proteins. Nature 267 (1977) 585-590
39. MacKerrell Jr. A.D., Brooks B., Brooks III C.L., Roux N.B., Won Y., and Karplus M. CHARMM: the energy function and its parametrization with an overview of the program. Encyclopedia of Computational Chemistry (1998), John Wiley & Sons Ltd., New York, NY
40. Leach A.R. Molecular modelling; principles and applications. 2nd ed. (2001), Prentice Hall, Harlow, UK
41. Warshel A., and Levitt M. Theoretical studies of enzymatic reactions: dielectric electrostatic and steric stabilization of the carbonium ion in the reaction of lyzozyme. J. Mol. Biol. 103 (1977) 227
42. Kollman P., Kuhn B., Donini O., Perakyla M., Stanton R., and B.D. Elucidating the nature of enzyme catalysis utilizing a new twist on an old methodology: quantum mechanical-free energy calculations on chemical reactions in enzymes and in aqueous solution. Acc. Chem. Res. 34 (2001) 72-79
43. Náray-Szabó G., and Berente I. Computer modelling of enzyme reactions. J. Mol. Struct. 666/667 (2003) 637-644
44. Woodcock H., Hodošcek M., Sherwood P., Lee Y., Schaefer H.I., and BR B. Exploring the quantum mechanical/molecular mechanical replica path method: a pathway optimization of the chorismate to prephenate claisen rearrangement catalyzed by chorismate mutase. Theor. Chem. Acc. 109 (2003) 140-148
45. Warshel A., Sharma P.K., Kato M., Xiang Y., Liu H., and Olsson M.H.M. Electrostatic basis for enzyme catalysis. Chem. Rev. 106 (2006) 3210-3235
46. Senn H., and Thiel W. QM/MM methods for biological systems. Atomistic approaches in modern biology. Topics in Current Chemistry (2007), Springer Berlin/Heidelberg, Berlin, Germany
47. Case D.A., Cheatham III T.E., Darden T.A., Gohlke H., Luo R., Merz Jr. K.M., Onufirev A., Simmerling C., Wang B., and Woods R.J. The amber biomolecular simulation programs. J. Comp. Chem. 26 (2005) 1668-1688
48. Frisch M.J., Trucks G.W., Schlegel H.B., Scuseria G.E., Robb M.A., Cheeseman J.R., Montgomery Jr. J.A., Vreven T., Kudin K.N., Burant J.C., Millam J.M., Iyengar S.S., Tomasi J., Barone V., Mennucci B., Cossi M., Scalmani G., Rega N., Petersson G.A., Nakatsuji H., Hada M., Ehara M., Toyota K., Fukuda R., Hasegawa J., Ishida M., Nakajima T., Honda Y., Kitao O., Nakai H., Klene M., Li X., Knox J.E., Hratchian H.P., Cross J.B., Bakken V., Adamo C., Jaramillo J., Gomperts R., Stratmann R.E., Yazyev O., Austin A.J., Cammi R., Pomelli C., Ochterski J.W., Ayala P.Y., Morokuma K., Voth G.A., Salvador P., Dannenberg J.J., Zakrzewski V.G., Dapprich S., Daniels A.D., Strain M.C., Farkas O., Malick D.K., Rabuck A.D., Raghavachari K., Foresman J.B., Ortiz J.V., Cui Q., Baboul A.G., Clifford S., Cioslowski J., Stefanov B.B., Liu G., Liashenko A., Piskorz P., Komaromi I., Martin R.L., Fox D.J., Keith T., Al-Laham M.A., Peng C.Y., Nanayakkara A., Challacombe M., Gill P.M.W., Johnson B., Chen W., Wong M.W., Gonzalez C., and Pople J.A. Gaussian 03, Revision D.02 (2004), Gaussian, Inc., Wallingford, CT
49. J. Ponder, TINKER, Software Tools for Molecular Design, Version 3.6: the most updated version for the TINKER program can be obtained from J.W. Ponder's WWW site at http://dasher.wustl.edu/tinker, St. Louis: Washington University, 1998.
50. Zhang Y. Improved pseudobonds for combined ab initio quantum mechanical/molecular mechanical (QM/MM) methods. J. Chem. Phys. 122 (2005) 24224
51. Burger S.K., and Yang W. Quadratic string method for determining the minimum-energy path based on multiobjective optimization. J. Chem. Phys. 124 (2006) 054109
52. Williams I., and Maggiora G. Use and abuse of the distinguished-coordinate method for transition state structure searching. J. Mol. Struct. 89 (1982) 365-378
53. Gonzalez C., and Schlegel H. Reaction path following in mass-weighted internal coordintes. J. Phys. Chem. 94 (1990) 5523
54. Schlegel H. Exploring potential energy surfaces for chemical reactions: an overview of some practical methods. J. Comp. Chem. 24 (2003) 1514-1527
55. Siegbahn P.E.M. A quantum chemical study of the mechanism of manganese catalase. Theor. Chem. Acc. 105 (2001) 197-206
56. Ivanov I., and Klein M.L. Dynamical flexibility and proton transfer in the arginase active site probed by ab initio molecular dynamics. J. Am. Chem. Soc. 127 (2005) 4010-4020
57. Liu S., Perera L., and Pedersen L.G. Binuclear manganese(II) complexes in biological systems. Mol. Phys. 105 (2007) 2893-2898
58. Becke A.D. Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98 (1993) 5648-5652
59. Lee C., Yang W., and Parr R.G. Development of the Colle-Salvetti correlation energy formula into a functional of the electron density. Phys. Rev. B 37 (1988) 785
60. Elber R., and Karplus M. A method for determining reaction paths in large molecules: application to myoglobin. Chem. Phys. Lett. 139 (1987) 375-380
61. Maragakis P., Stefan A., Brumer Y., Reichman D., and Kaxiras E. Adaptive nudged elastic band approach for transition state calculation. J. Chem. Phys. 117 (2002) 4651-4658
62. Liu H., Lu Z., Cisneros G.A., and Yang W. Parallel iterative reaction path optimization in ab initio quantum mechanical/molecular mechanical modeling of enzyme reactions. J. Chem. Phys. 121 (2004) 697-706
63. Cisneros G.A., Liu H., Lu Z., and Yang W. Reaction path determination for quantum mechanical/molecular mechanical modeling of enzyme reactions by combining first order and second order "chain-of-replicas" methods. J. Chem. Phys. 122 (2005) 114502-1-114502-9
64. Jhih-Wei C., Trout B., and Brooks B. A super-linear minimization scheme for the nudged elastic band method. J. Chem. Phys. 119 (2003) 12708-12717
65. Xie L., Liu H., and Yang W. Adapting the nudged elastic band method for determining minimum energy paths of chemical reactions in enzymes. J. Chem. Phys. 120 (2004) 8039-8052
66. Castro C., Smidansky E., Maksimchuk K.R., Arnold J.J., Korneeva V.S., Götte M., Konigsberg W., and Cameron C.E. Two proton transfers in the transition state for nucleotidyl transfer catalyzed by RNA- and DNA-dependent RNA and DNA polymerases. Proc. Natl. Acad. Sci. 104 (2007) 4267-4272
67. Hu H., and Yang W. Free energies of chemical reactions in solution and in enzymes with ab initio quantum mechanics/molecular mechanics methods. Ann. Rev. Phys. Chem. 59 (2008) 573-601
68. Liu H., Zhang Y., and Yang W. How is the active-site of enolase organized to achieve overall efficiency in catalyzing a two step reaction. J. Am. Chem. Soc. 122 (2000) 6560
69. Cisneros G.A., Liu H., Zhang Y., and Yang W. Ab-initio QM/MM study shows there is no general acid in the reaction catalyzed by 4-oxalocrotonate tautomerase. J. Am. Chem. Soc. 134 (2003) 10348-10393
70. Date T., Yamamoto S., Tanihara K., Nishimoto Y., Liu N., and Matsuk-age A. Site-directed mutagenesis of recombinant rat DNA polymerase β: involvement of arginine-183 in primer recognition. Biochemistry 29 (1990) 5027-5034
71. Menge K.L., Hostomsky Z., Nodes B.R., Hudson G.O., Rahmati S., Moomaw E.W., Almassy R.J., and Hostomska Z. Structure-function analysis of the mamailan DNA polymerase β active site: role of aspartic acid 256, arginine 254 and arginine 258 in nucleotidyl transfer. Biochemistry 34 (1995) 15934-15942
72. Notredame C., Higgins D.G., and Heringa J. T-coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302 (2000) 205-217