Structural and functional studies of MutS2 from Deinococcus radiodurans

DNA Repair

Volumn 21, Issue , 2014, Pages 111-119

  Zhang, Hui ^a   Xu, Qiang ^a,b   Lu, Meihua ^a   Xu, Xin ^a   Wang, Yunguang ^a   Wang, Liangyan ^a   Zhao, Ye ^a   Hua, Yuejin ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG CANCER HOSPITAL   (China)

Author keywords

Crystal soaking; Deinococcus radiodurans; Metal binding site; MutS2; Oxidative stress; Rotamer change; Smr

Indexed keywords

ALANINE; AMINO ACID; BACTERIAL PROTEIN; BUFFER; GLUTAMIC ACID; MANGANESE; MUTS2 PROTEIN; NUCLEASE; OXIDOREDUCTASE; RECA PROTEIN; UNCLASSIFIED DRUG; PROTEIN MSH2;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTALLIZATION; DEINOCOCCUS RADIODURANS; DNA DAMAGE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; RADIOSENSITIVITY; AMINO ACID SEQUENCE; CHEMISTRY; DEINOCOCCUS; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; RADIATION DOSE;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS; PROKARYOTA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CATALYTIC DOMAIN; DEINOCOCCUS; DNA DAMAGE; MOLECULAR SEQUENCE DATA; MUTS HOMOLOG 2 PROTEIN; OXIDATIVE STRESS; RADIATION TOLERANCE; REC A RECOMBINASES;

EID: 84905367838     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2014.04.012     Document Type: Article

References (61)

1. Li G.M. Mechanisms and functions of DNA mismatch repair. Cell Res. 2008, 18:85-98.
2. Kunkel T.A., Erie D.A. DNA mismatch repair. Annu. Rev. Biochem. 2005, 74:681-710.
3. Fukui K. DNA mismatch repair in eukaryotes and bacteria. J. Nucleic Acids 2010, 2010. 16 pp.
4. Bonadona V., Bonaiti B., Olschwang S., Grandjouan S., Huiart L., Longy M., Guimbaud R., Buecher B., Bignon Y.J., Caron O., Colas C., Nogues C., Lejeune-Dumoulin S., Olivier-Faivre L., Polycarpe-Osaer F., Nguyen T.D., Desseigne F., Saurin J.C., Berthet P., Leroux D., Duffour J., Manouvrier S., Frebourg T., Sobol H., Lasset C., Bonaiti-Pellie C.N. Cancer risks associated with germline mutations in MLH1, MSH2, and MSH6 genes in Lynch syndrome. JAMA: J. Am. Med. Assoc. 2011, 305:2304-2310. French Cancer Genetics.
5. Hsieh P., Yamane K. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mech. Ageing Dev. 2008, 129:391-407.
6. Sachadyn P. Conservation and diversity of MutS proteins. Mutat. Res. 2010, 694:20-30.
7. Lin Z., Nei M., Ma H. The origins and early evolution of DNA mismatch repair genes - multiple horizontal gene transfers and co-evolution. Nucleic Acids Res. 2007, 35:7591-7603.
8. Jeong E., Jo H., Kim T.G., Ban C. Characterization of multi-functional properties and conformational analysis of MutS2 from Thermotoga maritima MSB8. PLoS ONE 2012, 7:e34529.
9. Fukui K., Wakamatsu T., Agari Y., Masui R., Kuramitsu S. Inactivation of the DNA repair genes mutS, mutL or the anti-recombination gene mutS2 leads to activation of vitamin B1 biosynthesis genes. PLoS ONE 2011, 6:e19053.
10. Kang J., Huang S., Blaser M.J. Structural and functional divergence of MutS2 from bacterial MutS1 and eukaryotic MSH4-MSH5 homologs. J. Bacteriol. 2005, 187:3528-3537.
11. Vijayvargia R., Biswas I. MutS2 family protein from Pyrococcus furiosus. Curr. Microbiol. 2002, 44:224-228.
12. Fukui K., Nakagawa N., Kitamura Y., Nishida Y., Masui R., Kuramitsu S. Crystal structure of MutS2 endonuclease domain and the mechanism of homologous recombination suppression. J. Biol. Chem. 2008, 283:33417-33427.
13. Pinto A.V., Mathieu A., Marsin S., Veaute X., Ielpi L., Labigne A., Radicella J.P. Suppression of homologous and homeologous recombination by the bacterial MutS2 protein. Mol. Cell 2005, 17:113-120.
14. Wang G., Alamuri P., Humayun M.Z., Taylor D.E., Maier R.J. The Helicobacter pylori MutS protein confers protection from oxidative DNA damage. Mol. Microbiol. 2005, 58:166-176.
15. Fukui K., Kuramitsu S. Structure and function of the small MutS-related domain. Mol. Biol. Int. 2011, 691735.
16. Moreira D., Philippe H. Smr: a bacterial and eukaryotic homologue of the C-terminal region of the MutS2 family. Trends Biochem. Sci. 1999, 24:298-300.
17. Gui W.J., Qu Q.H., Chen Y.Y., Wang M., Zhang X.E., Bi L.J., Jiang T. Crystal structure of YdaL, a stand-alone small MutS-related protein from Escherichia coli. J. Struct. Biol. 2011, 174:282-289.
18. Diercks T., Ab E., Daniels M.A., de Jong R.N., Besseling R., Kaptein R., Folkers G.E. Solution structure and characterization of the DNA-binding activity of the B3BP-Smr domain. J. Mol. Biol. 2008, 383:1156-1170.
19. Krisko A., Radman M. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harbor Perspect. Biol. 2013, 5.
20. Slade D., Radman M. Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev. 2011, 75:133-191.
21. Daly M.J. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 2009, 7(3):237-245.
22. Blasius M., Sommer S., Hubscher U. Deinococcus radiodurans: what belongs to the survival kit?. Crit. Rev. Biochem. Mol. Biol. 2008, 43:221-238.
23. Cox M.M., Battista J.R. Deinococcus radiodurans - the consummate survivor. Nat. Rev. Microbiol. 2005, 3:882-892.
24. Das A.D., Misra H.S. Hypothetical proteins present during recovery phase of radiation resistant bacterium Deinococcus radiodurans are under purifying selection. J. Mol. Evol. 2013, 77:31-42.
25. Sharma A., Gaidamakova E.K., Matrosova V.Y., Bennett B., Daly M.J., Hoffman B.M. Responses of Mn2+ speciation in Deinococcus radiodurans and Escherichia coli to gamma-radiation by advanced paramagnetic resonance methods. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:5945-5950.
26. Daly M.J., Gaidamakova E.K., Matrosova V.Y., Kiang J.G., Fukumoto R., Lee D.Y., Wehr N.B., Viteri G.A., Berlett B.S., Levine R.L. Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS ONE 2010, 5:e12570.
27. Slade D., Lindner A.B., Paul G., Radman M. Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 2009, 136:1044-1055.
28. Zahradka K., Slade D., Bailone A., Sommer S., Averbeck D., Petranovic M., Lindner A.B., Radman M. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 2006, 443:569-573.
29. Mennecier S., Coste G., Servant P., Bailone A., Sommer S. Mismatch repair ensures fidelity of replication and recombination in the radioresistant organism Deinococcus radiodurans. Mol. Genet. Genom. 2004, 272:460-469.
30. Li M., Sun H., Feng Q., Lu H., Zhao Y., Zhang H., Xu X., Jiao J., Wang L., Hua Y. Extracellular dGMP enhances Deinococcus radiodurans tolerance to oxidative stress. PLoS ONE 2013, 8:e54420.
31. Jiao J., Wang L., Xia W., Li M., Sun H., Xu G., Tian B., Hua Y. Function and biochemical characterization of RecJ in Deinococcus radiodurans. DNA Repair (Amst.) 2012, 11:349-356.
32. Xu G., Wang L., Chen H., Lu H., Ying N., Tian B., Hua Y. RecO is essential for DNA damage repair in Deinococcus radiodurans. J. Bacteriol. 2008, 190:2624-2628.
33. Wang L., Xu G., Chen H., Zhao Y., Xu N., Tian B., Hua Y. DrRRA: a novel response regulator essential for the extreme radioresistance of Deinococcus radiodurans. Mol. Microbiol. 2008, 67:1211-1222.
34. Kabsch W. Xds. Acta Crystallogr. D: Biol. Crystallogr. 2010, 66:125-132.
35. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., McCoy A.J., Moriarty N.W., Oeffner R., Read R.J., Richardson D.C., Richardson J.S., Terwilliger T.C., Zwart P.H. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D: Biol. Crystallogr. 2010, 66:213-221.
36. Emsley P., Lohkamp B., Scott W.G., Cowtan K. Features and development of Coot. Acta Crystallogr. D: Biol. Crystallogr. 2010, 66:486-501.
37. Baker N.A., Sept D., Joseph S., Holst M.J., McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10037-10041.
38. Fukui K., Kosaka H., Kuramitsu S., Masui R. Nuclease activity of the MutS homologue MutS2 from Thermus thermophilus is confined to the Smr domain. Nucleic Acids Res. 2007, 35:850-860.
39. Fukui K., Masui R., Kuramitsu S. Thermus thermophilus MutS2, a MutS paralogue, possesses an endonuclease activity promoted by MutL. J. Biochem. 2004, 135:375-384.
40. Bauman J.D., Patel D., Baker S.F., Vijayan R.S., Xiang A., Parhi A.K., Martinez-Sobrido L., LaVoie E.J., Das K., Arnold E. Crystallographic fragment screening and structure-based optimization yields a new class of influenza endonuclease inhibitors. ACS Chem. Biol. 2013, 8:2501-2508.
41. Schmidt B.H., Burgin A.B., Deweese J.E., Osheroff N., Berger J.M. A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 2010, 465:641-644.
42. Sui M.J., Tsai L.C., Hsia K.C., Doudeva L.G., Ku W.Y., Han G.W., Yuan H.S. Metal ions and phosphate binding in the H-N-H motif: crystal structures of the nuclease domain of ColE7/Im7 in complex with a phosphate ion and different divalent metal ions. Protein Sci. Publ. Protein Soc. 2002, 11:2947-2957.
43. Repar J., Cvjetan S., Slade D., Radman M., Zahradka D., Zahradka K. RecA protein assures fidelity of DNA repair and genome stability in Deinococcus radiodurans. DNA Repair 2010, 9:1151-1161.
44. Schlesinger D.J. Role of RecA in DNA damage repair in Deinococcus radiodurans. FEMS Microbiol. Lett. 2007, 274:342-347.
45. Jolivet E., Lecointe F., Coste G., Satoh K., Narumi I., Bailone A., Sommer S. Limited concentration of RecA delays DNA double-strand break repair in Deinococcus radiodurans R1. Mol. Microbiol. 2006, 59:338-349.
46. Satoh K., Kikuchi M., Ishaque A.M., Ohba H., Yamada M., Tejima K., Onodera T., Narumi I. The role of Deinococcus radiodurans RecFOR proteins in homologous recombination. DNA Repair 2012, 11:410-418.
47. Bentchikou E., Servant P., Coste G., Sommer S. A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet. 2010, 6:e1000774.
48. Huang L., Hua X., Lu H., Gao G., Tian B., Shen B., Hua Y. Three tandem HRDC domains have synergistic effect on the RecQ functions in Deinococcus radiodurans. DNA Repair 2007, 6:167-176.
49. Tanaka M., Earl A.M., Howell H.A., Park M.J., Eisen J.A., Peterson S.N., Battista J.R. Analysis of Deinococcus radiodurans's transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 2004, 168:21-33.
50. Ngo K.V., Molzberger E.T., Chitteni-Pattu S., Cox M.M. Regulation of Deinococcus radiodurans RecA protein function via modulation of active and inactive nucleoprotein filament states. J. Biol. Chem. 2013, 288:21351-21366.
51. Kim J.I., Cox M.M. The RecA proteins of Deinococcus radiodurans and Escherichia coli promote DNA strand exchange via inverse pathways. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:7917-7921.
52. Kanvah S., Joseph J., Schuster G.B., Barnett R.N., Cleveland C.L., Landman U. Oxidation of DNA: damage to nucleobases. Acc. Chem. Res. 2010, 43:280-287.
53. Waris G., Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog. 2006, 5:14.
54. Markillie L.M., Varnum S.M., Hradecky P., Wong K.K. Targeted mutagenesis by duplication insertion in the radioresistant bacterium Deinococcus radiodurans: radiation sensitivities of catalase (katA) and superoxide dismutase (sodA) mutants. J. Bacteriol. 1999, 181:666-669.
55. Jung I.L., Kim I.G. Thiamine protects against paraquat-induced damage: scavenging activity of reactive oxygen species. Environ. Toxicol. Pharmacol. 2003, 15:19-26.
56. Fukui K., Takahata Y., Nakagawa N., Kuramitsu S., Masui R. Analysis of a nuclease activity of catalytic domain of Thermus thermophilus MutS2 by high-accuracy mass spectrometry. Nucleic Acids Res. 2007, 35:e100.
57. Culotta V.C., Daly M.J. Manganese complexes: diverse metabolic routes to oxidative stress resistance in prokaryotes and yeast. Antioxidants Redox Signal. 2013, 19:933-944.
58. Daly M.J. Death by protein damage in irradiated cells. DNA Repair 2012, 11:12-21.
59. Heinz K., Marx A. Lesion bypass activity of DNA polymerase A from the extremely radioresistant organism Deinococcus radiodurans. J. Biol. Chem. 2007, 282:10908-10914.
60. Lecointe F., Shevelev I.V., Bailone A., Sommer S., Hubscher U. Involvement of an X family DNA polymerase in double-stranded break repair in the radioresistant organism Deinococcus radiodurans. Mol. Microbiol. 2004, 53:1721-1730.
61. Khairnar N.P., Misra H.S. DNA polymerase X from Deinococcus radiodurans implicated in bacterial tolerance to DNA damage is characterized as a short patch base excision repair polymerase. Microbiology 2009, 155:3005-3014.