DNA synthesis across an abasic lesion by yeast Rev1 DNA polymerase

Journal of Molecular Biology

Volumn 406, Issue 1, 2011, Pages 18-28

  Nair, Deepak T ^a,b   Johnson, Robert E ^c   Prakash, Louise ^c   Prakash, Satya ^c   Aggarwal, Aneel K ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF AGRICULTURAL SCIENCES   (India)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Abasic lesion; DNA polymerase; Rev1; translesion DNA synthesis; Y family polymerase

Indexed keywords

ARGININE; DNA POLYMERASE REV1; NUCLEOTIDE;

ARTICLE; CHEMICAL BOND; DNA DAMAGE; DNA SYNTHESIS; ENZYME STRUCTURE; HYDROLYSIS; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STRUCTURE ANALYSIS; YEAST;

EID: 79151470586     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.12.016     Document Type: Article

References (49)

1. Lindahl T. DNA repair enzymes Annu. Rev. Biochem. 51 1982 61 87
2. Lindahl T., and Nyberg B. Rate of depurination of native deoxyribonucleic acid Biochemistry 11 1972 3610 3618
3. Nakamura J., and Swenberg J.A. Endogenous apurinic/apyrimidinic sites in genomic DNA of mammalian tissues Cancer Res. 59 1999 2522 2526
4. Seeberg E., Eide L., and Bjoras M. The base excision repair pathway Trends Biochem. Sci. 20 1995 391 397
5. Wallace S.S. Oxidative damage to DNA and its repair J. Scandalios, Oxidative Stress and the Molecular Biology of Antioxidant Defences 1997 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
6. Avkin S., Adar S., Blander G., and Livneh Z. Quantitative measurement of translesion replication in human cells: evidence for bypass of abasic sites by a replicative DNA polymerase Proc. Natl Acad. Sci. USA 99 2002 3764 3769
7. Boiteux S., and Laval J. Coding properties of poly(deoxycytidylic acid) templates containing uracil or apyrimidinic sites: in vitro modulation of mutagenesis by deoxyribonucleic acid repair enzymes Biochemistry 21 1982 6746 6751
8. Lawrence C.W., Borden A., Banerjee S.K., and LeClerc J.E. Mutation frequency and spectrum resulting from a single abasic site in a single-stranded vector Nucleic Acids Res. 18 1990 2153 2157
9. Loeb L.A., and Preston B.D. Mutagenesis by apurinic/apyrimidinic sites Annu. Rev. Genet. 20 1986 201 230
10. Mozzherin D.J., Shibutani S., Tan C.K., Downey K.M., and Fisher P.A. Proliferating cell nuclear antigen promotes DNA synthesis past template lesions by mammalian DNA polymerase delta Proc. Natl Acad. Sci. USA 94 1997 6126 6131
11. Pages V., Johnson R.E., Prakash L., and Prakash S. Mutational specificity and genetic control of replicative bypass of an abasic site in yeast Proc. Natl Acad. Sci. USA 105 2008 1170 1175
12. Sagher D., and Strauss B. Insertion of nucleotides opposite apurinic/apyrimidinic sites in deoxyribonucleic acid during in vitro synthesis: uniqueness of adenine nucleotides Biochemistry 22 1983 4518 4526
13. Shibutani S., Takeshita M., and Grollman A.P. Translesional synthesis on DNA templates containing a single abasic site. A mechanistic study of the "A rule" J. Biol. Chem. 272 1997 13916 13922
14. Strauss B.S. The "A" rule revisited: polymerases as determinants of mutational specificity DNA Repair (Amsterdam) 1 2002 125 135
15. Chen J., Dupradeau F.Y., Case D.A., Turner C.J., and Stubbe J. DNA oligonucleotides with A, T, G or C opposite an abasic site: structure and dynamics Nucleic Acids Res. 36 2008 253 262
16. Cuniasse P., Fazakerley G.V., Guschlbauer W., Kaplan B.E., and Sowers L.C. The abasic site as a challenge to DNA polymerase. A nuclear magnetic resonance study of G, C and T opposite a model abasic site J. Mol. Biol. 213 1990 303 314
17. Cuniasse P., Sowers L.C., Eritja R., Kaplan B., Goodman M.F., and Cognet J.A. An abasic site in DNA. Solution conformation determined by proton NMR and molecular mechanics calculations Nucleic Acids Res. 15 1987 8003 8022
18. Fiala K.A., Hypes C.D., and Suo Z. Mechanism of abasic lesion bypass catalyzed by a Y-family DNA polymerase J. Biol. Chem. 282 2007 8188 8198
19. Gelfand C.A., Plum G.E., Grollman A.P., Johnson F., and Breslauer K.J. Thermodynamic consequences of an abasic lesion in duplex DNA are strongly dependent on base sequence Biochemistry 37 1998 7321 7327
20. Hogg M., Wallace S.S., and Doublie S. Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site EMBO J. 23 2004 1483 1493
21. Ling H., Boudsocq F., Woodgate R., and Yang W. Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts Mol. Cell 13 2004 751 762
22. Matray T.J., and Kool E.T. A specific partner for abasic damage in DNA Nature 399 1999 704 708
23. Nair D.T., Johnson R.E., Prakash L., Prakash S., and Aggarwal A.K. DNA synthesis across an abasic lesion by human DNA polymerase iota Structure 17 2009 530 537
24. Nusslein-Volhard C., and Wieschaus E. Mutations affecting segment number and polarity in Drosophila Nature 287 1980 795 801
25. Obeid S., Blatter N., Kranaster R., Schnur A., Diederichs K., Welte W., and Marx A. Replication through an abasic DNA lesion: structural basis for adenine selectivity EMBO J. 29 2010 1738 1747
26. Randall S.K., Eritja R., Kaplan B.E., Petruska J., and Goodman M.F. Nucleotide insertion kinetics opposite abasic lesions in DNA J. Biol. Chem. 262 1987 6864 6870
27. Reineks E.Z., and Berdis A.J. Evaluating the contribution of base stacking during translesion DNA replication Biochemistry 43 2004 393 404
28. Zahn K.E., Belrhali H., Wallace S.S., and Doublie S. Caught bending the A-rule: crystal structures of translesion DNA synthesis with a non-natural nucleotide Biochemistry 46 2007 10551 10561
29. Beard W.A., Shock D.D., Batra V.K., Pedersen L.C., and Wilson S.H. DNA polymerase beta substrate specificity: side chain modulation of the "A-rule" J. Biol. Chem. 284 2009 31680 31689
30. Nelson J.R., Lawrence C.W., and Hinkle D.C. Deoxycytidyl transferase activity of yeast REV1 protein Nature 382 1996 729 731
31. Haracska L., Prakash S., and Prakash L. Yeast Rev1 protein is a G template-specific DNA polymerase J. Biol. Chem. 277 2002 15546 15551
32. Prakash S., Johnson R.E., and Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function Annu. Rev. Biochem. 74 2005 317 353
33. Swan M.K., Johnson R.E., Prakash L., Prakash S., and Aggarwal A.K. Structure of the human Rev1-DNA-dNTP ternary complex J. Mol. Biol. 390 2009 699 709
34. Nair D.T., Johnson R.E., Prakash L., Prakash S., and Aggarwal A.K. Rev1 employs a novel mechanism of DNA synthesis using a protein template Science 309 2005 2219 2222
35. Doublie S., Tabor S., Long A.M., Richardson C.C., and Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution Nature 391 1998 251 258
36. Li Y., Korolev S., and Waksman G. 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 1998 7514 7525
37. Steitz T.A. DNA polymerases: structural diversity and common mechanisms J. Biol. Chem. 274 1999 17395 17398
38. Johnson R.E., Washington M.T., Haracska L., Prakash S., and Prakash L. Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions Nature 406 2000 1015 1019
39. Nair D.T., Johnson R.E., Prakash S., Prakash L., and Aggarwal A.K. Replication by human DNA polymerase-iota occurs by Hoogsteen base-pairing Nature 430 2004 377 380
40. Nair D.T., Johnson R.E., Prakash L., Prakash S., and Aggarwal A.K. Human DNA polymerase iota incorporates dCTP opposite template G via a GC + Hoogsteen base pair Structure (Cambridge) 13 2005 1569 1577
41. Suzuki T., Ohsumi S., and Makino K. Mechanistic studies on depurination and apurinic site chain breakage in oligodeoxyribonucleotides Nucleic Acids Res. 22 1994 4997 5003
42. Amosova O., Coulter R., and Fresco J.R. Self-catalyzed site-specific depurination of guanine residues within gene sequences Proc. Natl Acad. Sci. USA 103 2006 4392 4397
43. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
44. Navaza J. AMoRe: an automated package for molecular replacement Acta Crystallogr. 50 1994 157 163
45. Brunger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., and Grosse-Kunstleve R. Crystallography & NMR system: a software suite for macromolecular structure determination Acta Crystallogr. Sect. D. 54 1998 905
46. Jones A.T., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. Sect. A 47 1991 110 119
47. Lovell S.C., Davis I.W., Arendall W.B. III, de Bakker P.I., Word J.M., and Prisant M.G. Structure validation by Calpha geometry: phi,psi and Cbeta deviation Proteins 50 2003 437 450
48. Collaborative Computing Project No. 4 (CCP4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. Sect. D 50 1994 760 763
49. Altona C., and Sundaralingam M. Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation J. Am. Chem. Soc. 94 1972 8205 8212