Conformational dynamics of a Y-family DNA polymerase during substrate binding and catalysis as revealed by interdomain förster resonance energy transfer

Biochemistry

Volumn 53, Issue 11, 2014, Pages 1768-1778

  Maxwell, Brian A ^a   Xu, Cuiling ^a   Suo, Zucai ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ENERGY TRANSFER; ENZYMES; NUCLEOTIDES; POLYMERS; PROTEINS; SUBSTRATES;

ACTIVE SITE RESIDUES; CONFORMATIONAL CHANGE; CONFORMATIONAL DYNAMICS; CONFORMATIONAL TRANSITIONS; INCORPORATION RATES; RESONANCE ENERGY TRANSFER; STRUCTURAL STUDIES; SULFOLOBUS SOLFATARICUS;

DNA;

DNA POLYMERASE; NUCLEOTIDE;

ARTICLE; CATALYSIS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA BINDING; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SITE DIRECTED MUTAGENESIS; STEADY STATE; SULFOLOBUS SOLFATARICUS;

APOPROTEINS; DNA POLYMERASE BETA; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; SULFOLOBUS SOLFATARICUS;

EID: 84897043136     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5000146     Document Type: Article

References (53)

1. Yang, W. and Woodgate, R. (2007) What a difference a decade makes: Insights into translesion DNA synthesis Proc. Natl. Acad. Sci. U.S.A. 104, 15591-15598
2. Matsuda, T., Bebenek, K., Masutani, C., Hanaoka, F., and Kunkel, T. A. (2000) Low fidelity DNA synthesis by human DNA polymerase-Ε Nature 404, 1011-1013
3. Johnson, R. E., Washington, M. T., Haracska, L., Prakash, S., and Prakash, L. (2000) Eukaryotic polymerases Î and ζ act sequentially to bypass DNA lesions Nature 406, 1015-1019
4. Zhang, Y., Yuan, F., Xin, H., Wu, X., Rajpal, D. K., Yang, D., and Wang, Z. (2000) Human DNA polymerase κ synthesizes DNA with extraordinarily low fidelity Nucleic Acids Res. 28, 4147-4156
5. Wang, Z. (2001) Translesion synthesis by the UmuC family of DNA polymerases Mutat. Res. 486, 59-70
6. Fiala, K. A., Abdel-Gawad, W., and Suo, Z. (2004) Pre-Steady-State Kinetic Studies of the Fidelity and Mechanism of Polymerization Catalyzed by Truncated Human DNA Polymerase Î Biochemistry 43, 6751-6762
7. Fiala, K. A. and Suo, Z. (2004) Mechanism of DNA Polymerization Catalyzed by Sulfolobus solfataricus P2 DNA Polymerase IV Biochemistry 43, 2116-2125
8. Wong, J. H., Fiala, K. A., Suo, Z., and Ling, H. (2008) Snapshots of a Y-family DNA polymerase in replication: Substrate-induced conformational transitions and implications for fidelity of Dpo4 J. Mol. Biol. 379, 317-330
9. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication Cell 107, 91-102
10. Xing, G., Kirouac, K., Shin, Y. J., Bell, S. D., and Ling, H. (2009) Structural insight into recruitment of translesion DNA polymerase Dpo4 to sliding clamp PCNA Mol. Microbiol. 71, 678-691
11. Rechkoblit, O., Malinina, L., Cheng, Y., Kuryavyi, V., Broyde, S., Geacintov, N. E., and Patel, D. J. (2006) Stepwise translocation of Dpo4 polymerase during error-free bypass of an oxoG lesion PLoS Biol. 4, e11
12. Eoff, R. L., Irimia, A., Angel, K. C., Egli, M., and Guengerich, F. P. (2007) Hydrogen bonding of 7,8-dihydro-8-oxodeoxyguanosine with a charged residue in the little finger domain determines miscoding events in Sulfolobus solfataricus DNA polymerase Dpo4 J. Biol. Chem. 282, 19831-19843
13. Trincao, J., Johnson, R. E., Wolfle, W. T., Escalante, C. R., Prakash, S., Prakash, L., and Aggarwal, A. K. (2004) Dpo4 is hindered in extending a G.T mismatch by a reverse wobble Nat. Struct. Mol. Biol. 11, 457-462
14. Fiala, K. A. and Suo, Z. (2004) Pre-Steady-State Kinetic Studies of the Fidelity of Sulfolobus solfataricus P2 DNA Polymerase IV Biochemistry 43, 2106-2115
15. Sherrer, S. M., Brown, J. A., Pack, L. R., Jasti, V. P., Fowler, J. D., Basu, A. K., and Suo, Z. (2009) Mechanistic Studies of the Bypass of a Bulky Single-base Lesion Catalyzed by a Y-family DNA Polymerase J. Biol. Chem. 284, 6379-6388
16. 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 polΕ Nucleic Acids Res. 29, 4607-4616
17. Fiala, K. A., Hypes, C. D., and Suo, Z. (2007) Mechanism of abasic lesion bypass catalyzed by a Y-family DNA polymerase J. Biol. Chem. 282, 8188-8198
18. Frauenfelder, H., Sligar, S. G., and Wolynes, P. G. (1991) The energy landscapes and motions of proteins Science 254, 1598-1603
19. Hammes-Schiffer, S. and Benkovic, S. J. (2006) Relating protein motion to catalysis Annu. Rev. Biochem. 75, 519-541
20. Herbst, K. J., Ni, Q., and Zhang, J. (2009) Dynamic visualization of signal transduction in living cells: From second messengers to kinases IUBMB Life 61, 902-908
21. Hammes, G. G. (2002) Multiple conformational changes in enzyme catalysis Biochemistry 41, 8221-8228
22. Panke, S. and Wubbolts, M. G. (2002) Enzyme technology and bioprocess engineering Curr. Opin. Biotechnol. 13, 111-116
23. 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
24. 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
25. Trincao, J., Johnson, R. E., Escalante, C. R., Prakash, S., Prakash, L., and Aggarwal, A. K. (2001) Structure of the catalytic core of S. cerevisiae DNA polymerase Ε: Implications for translesion DNA synthesis Mol. Cell 8, 417-426
26. Doublie, S., Sawaya, M. R., and Ellenberger, T. (1999) An open and closed case for all polymerases Structure 7, R31-R35
27. Beckman, J. W., Wang, Q., and Guengerich, F. P. (2008) Kinetic analysis of correct nucleotide insertion by a Y-family DNA polymerase reveals conformational changes both prior to and following phosphodiester bond formation as detected by tryptophan fluorescence J. Biol. Chem. 283, 36711-36723
28. Xu, C., Maxwell, B. A., Brown, J. A., Zhang, L., and Suo, Z. (2009) Global conformational dynamics of a Y-family DNA polymerase during catalysis PLoS Biol. 7, e1000225
29. Eoff, R. L., Sanchez-Ponce, R., and Guengerich, F. P. (2009) Conformational changes during nucleotide selection by Sulfolobus solfataricus DNA polymerase Dpo4 J. Biol. Chem. 284, 21090-21099
30. Maxwell, B. A., Xu, C., and Suo, Z. (2012) DNA Lesion Alters Global Conformational Dynamics of Y-family DNA Polymerase during Catalysis J. Biol. Chem. 287, 13040-13047
31. Zhang, H. and Guengerich, F. P. (2010) Effect of N2-guanyl modifications on early steps in catalysis of polymerization by Sulfolobus solfataricus P2 DNA polymerase Dpo4 T239W J. Mol. Biol. 395, 1007-1018
32. Sherrer, S. M., Maxwell, B. A., Pack, L. R., Fiala, K. A., Fowler, J. D., Zhang, J., and Suo, Z. (2012) Identification of an unfolding intermediate for a DNA lesion bypass polymerase Chem. Res. Toxicol. 25, 1531-1540
33. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global Kinetic Explorer: A new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
34. Chakraborty, S., Ittah, V., Bai, P., Luo, L., Haas, E., and Peng, Z. (2001) Structure and dynamics of the α-lactalbumin molten globule: Fluorescence studies using proteins containing a single tryptophan residue Biochemistry 40, 7228-7238
35. Lakowicz, J. R. (1999) Principles of fluorescence spectroscopy, 2 nd ed., Kluwer Academic/Plenum, New York.
36. Rothwell, P. J. and Waksman, G. (2007) A pre-equilibrium before nucleotide binding limits fingers subdomain closure by Klentaq1 J. Biol. Chem. 282, 28884-28892
37. Brenlla, A., Markiewicz, R. P., Rueda, D., and Romano, L. J. (2014) Nucleotide selection by the Y-family DNA polymerase Dpo4 involves template translocation and misalignment Nucleic Acids Res. 42, 2555-2563
38. DeLucia, A. M., Grindley, N. D., and Joyce, C. M. (2007) Conformational changes during normal and error-prone incorporation of nucleotides by a Y-family DNA polymerase detected by 2-aminopurine fluorescence Biochemistry 46, 10790-10803
39. Uljon, S. N., Johnson, R. E., Edwards, T. A., Prakash, S., Prakash, L., and Aggarwal, A. K. (2004) Crystal structure of the catalytic core of human DNA polymerase κ Structure 12, 1395-1404
40. Lone, S., Townson, S. A., Uljon, S. N., Johnson, R. E., Brahma, A., Nair, D. T., Prakash, S., Prakash, L., and Aggarwal, A. K. (2007) Human DNA polymerase κ encircles DNA: Implications for mismatch extension and lesion bypass Mol. Cell 25, 601-614
41. Alt, A., Lammens, K., Chiocchini, C., Lammens, A., Pieck, J. C., Kuch, D., Hopfner, K. P., and Carell, T. (2007) Bypass of DNA lesions generated during anticancer treatment with cisplatin by DNA polymerase Ε Science 318, 967-970
42. Silverstein, T. D., Johnson, R. E., Jain, R., Prakash, L., Prakash, S., and Aggarwal, A. K. (2010) Structural basis for the suppression of skin cancers by DNA polymerase Ε Nature 465, 1039-1043
43. 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
44. Berezhna, S. Y., Gill, J. P., Lamichhane, R., and Millar, D. P. (2012) Single-molecule Forster resonance energy transfer reveals an innate fidelity checkpoint in DNA polymerase I J. Am. Chem. Soc. 134, 11261-11268
45. Christian, T. D., Romano, L. J., and Rueda, D. (2009) Single-molecule measurements of synthesis by DNA polymerase with base-pair resolution Proc. Natl. Acad. Sci. U.S.A. 106, 21109-21114
46. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A., and Benkovic, S. J. (1987) Kinetic mechanism of DNA polymerase I (Klenow) Biochemistry 26, 8410-8417
47. Brown, J. A. and Suo, Z. (2009) Elucidating the kinetic mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase B1 Biochemistry 48, 7502-7511
48. Maxwell, B. A. and Suo, Z. (2013) Single-molecule Investigation of Substrate Binding Kinetics and Protein Conformational Dynamics of a B-family Replicative DNA Polymerase J. Biol. Chem. 288, 11590-11600
49. Li, Y., Korolev, S., and Waksman, G. (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
50. Joyce, C. M., Potapova, O., Delucia, A. M., Huang, X., Basu, V. P., and Grindley, N. D. (2008) Fingers-closing and other rapid conformational changes in DNA polymerase I (Klenow fragment) and their role in nucleotide selectivity Biochemistry 47, 6103-6116
51. Wang, Y., Arora, K., and Schlick, T. (2006) Subtle but variable conformational rearrangements in the replication cycle of Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4) may accommodate lesion bypass Protein Sci. 15, 135-151
52. Ma, D., Fowler, J. D., Yuan, C., and Suo, Z. (2010) Backbone assignment of the catalytic core of a Y-family DNA polymerase Biomol. NMR Assignments 4, 207-209
53. Ma, D., Fowler, J. D., and Suo, Z. (2011) Backbone assignment of the little finger domain of a Y-family DNA polymerase Biomol. NMR Assignments 5, 195-198