Enzymes involved in DNA ligation and end-healing in the radioresistant bacterium Deinococcus radiodurans

BMC Molecular Biology

Volumn 8, Issue , 2007, Pages

  Blasius, Melanie ^a   Buob, Rebecca ^a   Shevelev, Igor V ^a,b   Hubscher, Ulrich ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5' POLYNUCLEOTIDE KINASE; ADENOSINE TRIPHOSPHATE; BACTERIAL DNA; LYSINE; MANGANESE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NUCLEOTIDYLTRANSFERASE; PHOSPHOTRANSFERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; UNCLASSIFIED DRUG; ADENOSINE PHOSPHATE; BACTERIAL PROTEIN; POLYNUCLEOTIDE 5' HYDROXYL KINASE; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GENETICS; CATALYSIS; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; MOLECULAR CLONING; NONHUMAN; OPERON; PROTEIN EXPRESSION; RADIOSENSITIVITY; SEQUENCE HOMOLOGY; SPECIES COMPARISON; AMINO ACID SEQUENCE; DEINOCOCCUS; DNA DAMAGE; GENETICS; HUMAN; IONIZING RADIATION; METABOLISM; MOLECULAR GENETICS; RADIATION EXPOSURE; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS; ESCHERICHIA COLI;

ADENOSINE MONOPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DEINOCOCCUS; DNA DAMAGE; DNA LIGASES; DNA REPAIR; DNA, BACTERIAL; HUMANS; MANGANESE; MOLECULAR SEQUENCE DATA; NAD; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE; RADIATION, IONIZING; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 34948840017     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-8-69     Document Type: Article

References (36)

1. Cox MM Battista JR Deinococcus radiodurans - the consummate survivor Nat Rev Microbiol 2005, 3(11):882-892 10.1038/nrmicro1264 16261171
2. Daly MJ Gaidamakova EK Matrosova VY Vasilenko A Zhai M Leapman RD Lai B Ravel B Li SM Kemner KM Fredrickson JK Protein oxidation implicated as the primary determinant of bacterial radioresistance PLoS Biol 2007, 5(4):e92 1828145 17373858 10.1371/journal.pbio.0050092
3. Daly MJ Gaidamakova EK Matrosova VY Vasilenko A Zhai M Venkateswaran A Hess M Omelchenko MV Kostandarithes HM Makarova KS Wackett LP Fredrickson JK Ghosal D Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance Science 2004, 306(5698):1025-1028 10.1126/science.1103185 15459345
4. Bowater R Doherty AJ Making ends meet: Repairing breaks in bacterial DNA by non-homologous end-joining PLoS Genet 2006, 2(2):e8 1378119 16518468 10.1371/journal.pgen.0020008
5. Weller GR Kysela B Roy R Tonkin LM Scanlan E Della M Devine SK Day JP Wilkinson A d'Adda di Fagagna F Devine KM Bowater RP Jeggo PA Jackson SP Doherty AJ Identification of a DNA nonhomologous end-joining complex in bacteria Science 2002, 297(5587):1686-1689 10.1126/science.1074584 12215643
6. Zahradka K Slade D Bailone A Sommer S Averbeck D Petranovic M Lindner AB Radman M Reassembly of shattered chromosomes in Deinococcus radiodurans Nature 2006, 443(7111):569-573 17006450
7. Wilkinson A Day J Bowater R Bacterial DNA ligases Mol Microbiol 2001, 40(6):1241-1248 10.1046/j.1365-2958.2001.02479.x 11442824
8. Liu Y Zhou J Omelchenko MV Beliaev AS Venkateswaran A Stair J Wu L Thompson DK Xu D Rogozin IB Gaidamakova EK Zhai M Makarova KS Koonin EV Daly MJ Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation Proc Natl Acad Sci USA 2003, 100(7):4191-4196 153069 12651953 10.1073/pnas.0630387100
9. Makarova KS Aravind L Wolf YI Tatusov RL Minton KW Koonin EV Daly MJ Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics Microbiol Mol Biol Rev 2001, 65(1):44-79 99018 11238985 10.1128/ MMBR.65.1.44-79.2001
10. Omelchenko MV Wolf YI Gaidamakova EK Matrosova VY Vasilenko A Zhai M Daly MJ Koonin EV Makarova KS Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: Divergent routes of adaptation to thermophily and radiation resistance BMC Evol Biol 2005, 5:57 1274311 16242020 10.1186/1471-2148-5-57
11. Henner WD Grunberg SM Haseltine WA Sites and structure of gamma radiation-induced DNA strand breaks J Biol Chem 1982, 257(19):11750-11754 7118909
12. Henner WD Rodriguez LO Hecht SM Haseltine WA gamma Ray induced deoxyribonucleic acid strand breaks. 3′ Glycolate termini J Biol Chem 1983, 258(2):711-713 6822504
13. Amitsur M Levitz R Kaufmann G Bacteriophage T4 anticodon nuclease, polynucleotide kinase and RNA ligase reprocess the host lysine tRNA Embo J 1987, 6(8):2499-2503 553660 2444436
14. Audebert M Salles B Weinfeld M Calsou P Involvement of polynucleotide kinase in a poly(ADP-ribose) polymerase-1-dependent DNA double-strand breaks rejoining pathway J Mol Biol 2006, 356(2):257-265 10.1016/ j.jmb.2005.11.028 16364363
15. Chappell C Hanakahi LA Karimi-Busheri F Weinfeld M West SC Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining Embo J 2002, 21(11):2827-2832 126026 12032095 10.1093/emboj/21.11.2827
16. Whitehouse CJ Taylor RM Thistlethwaite A Zhang H Karimi-Busheri F Lasko DD Weinfeld M Caldecott KW XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair Cell 2001, 104(1):107-117 10.1016/S0092-8674(01)00195-7 11163244
17. Martins A Shuman S An end-healing enzyme from Clostridium thermocellum with 5' kinase, 2',3' phosphatase, and adenylyltransferase activities Rna 2005, 11(8):1271-1280 1370810 15987807 10.1261/rna.2690505
18. Aravind L Koonin EV The HD domain defines a new superfamily of metal-dependent phosphohydrolases Trends Biochem Sci 1998, 23(12):469-472 10.1016/S0968-0004(98)01293-6 9868367
19. Blondal T Hjorleifsdottir S Aevarsson A Fridjonsson OH Skirnisdottir S Wheat JO Hermannsdottir AG Hreggvidsson GO Smith AV Kristjansson JK Characterization of a 5′-polynucleotide kinase/ 3′-phosphatase from bacteriophage RM378 J Biol Chem 2005, 280(7):5188-5194 10.1074/jbc.M409211200 15579472
20. Wang LK Shuman S Mutational analysis defines the 5′-kinase and 3′-phosphatase active sites of T4 polynucleotide kinase Nucleic Acids Res 2002, 30(4):1073-1080 100346 11842120 10.1093/nar/30.4.1073
21. Doherty AJ Suh SW Structural and mechanistic conservation in DNA ligases Nucleic Acids Res 2000, 28(21):4051-4058 113121 11058099 10.1093/nar/ 28.21.4051
22. Weller GR Doherty AJ A family of DNA repair ligases in bacteria? FEBS Lett 2001, 505(2):340-342 10.1016/S0014-5793(01)02831-9 11566200
23. Leibowitz PJ Schwartzberg LS Bruce AK The in vivo association of manganese with the chromosome of Micrococcus radiodurans Photochem Photobiol 1976, 23(1):45-50 178008
24. Evans DM Moseley BE Identification and initial characterisation of a pyrimidine dimer UV endonuclease (UV endonuclease beta) from Deinococcus radiodurans; a DNA-repair enzyme that requires manganese ions Mutat Res 1985, 145(3):119-128 3838572
25. Lecointe F Shevelev IV 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(6):1721-1730 10.1111/j.1365-2958.2004.04233.x 15341650
26. Blasius M Shevelev I Jolivet E Sommer S Hubscher U DNA polymerase X from Deinococcus radiodurans possesses a structure-modulated 3′→5′ exonuclease activity involved in radioresistance Mol Microbiol 2006, 60(1):165-176 10.1111/j.1365-2958.2006.05077.x 16556228
27. Jilani A Ramotar D Slack C Ong C Yang XM Scherer SW Lasko DD Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3′-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage J Biol Chem 1999, 274(34):24176-24186 10.1074/jbc.274.34.24176 10446192
28. Nick McElhinny SA Snowden CM McCarville J Ramsden DA Ku recruits the XRCC4-ligase IV complex to DNA ends Mol Cell Biol 2000, 20(9):2996-3003 85565 10757784 10.1128/MCB.20.9.2996-3003.2000
29. Narumi I Satoh K Cui S Funayama T Kitayama S Watanabe H PprA: A novel protein from Deinococcus radiodurans that stimulates DNA ligation Mol Microbiol 2004, 54(1):278-285 10.1111/j.1365-2958.2004.04272.x 15458422
30. Murakami M Narumi I Satoh K Furukawa A Hayata I Analysis of interaction between DNA and Deinococcus radiodurans PprA protein by Atomic force microscopy Biochim Biophys Acta 2006, 1764(1):20-23 16309981
31. Turko IV Francis SH Corbin JD Potential roles of conserved amino acids in the catalytic domain of the cGMP-binding cGMP-specific phosphodiesterase J Biol Chem 1998, 273(11):6460-6466 10.1074/ jbc.273.11.6460 9497379
32. Eggington JM Haruta N Wood EA Cox MM The single-stranded DNA-binding protein of Deinococcus radiodurans BMC Microbiol 2004, 4:2 331404 14718065 10.1186/1471-2180-4-2
33. Smirnova E Toueille M Markkanen E Hubscher U The human checkpoint sensor and alternative DNA clamp Rad9-Rad1-Hus1 modulates the activity of DNA ligase I, a component of the long-patch base excision repair machinery Biochem J 2005, 389(Pt 1):13-17 1184534 15871698
34. Shuman S Schwer B RNA capping enzyme and DNA ligase: A superfamily of covalent nucleotidyl transferases Mol Microbiol 1995, 17(3):405-410 10.1111/j.1365-2958.1995.mmi_17030405.x 8559059
35. Thompson JD Higgins DG Gibson TJ CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 1994, 22(22):4673-4680 308517 7984417 10.1093/nar/22.22.4673
36. Marchler-Bauer A Bryant SH CD-Search: Protein domain annotations on the fly Nucleic Acids Res 2004: 32 Web Server W327-331 441592 15215404 10.1093/nar/gkh454