Connecting Replication and Repair: YoaA, a Helicase-Related Protein, Promotes Azidothymidine Tolerance through Association with Chi, an Accessory Clamp Loader Protein

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During the replication of the cell’s genetic material, difficulties are often encountered. These problems require the recruitment of special proteins to repair DNA so that replication can be completed. The failure to do so causes cell death or deleterious changes to the cell’s genetic material. In humans, these genetic changes can promote cancer formation. Our study identifies a repair protein that is recruited to problem sites by interactions with the replication machinery. These interactions provide a means by which the cell can sense, respond to and repair damage that interferes with the completion of DNA replication.

Vyšlo v časopise: Connecting Replication and Repair: YoaA, a Helicase-Related Protein, Promotes Azidothymidine Tolerance through Association with Chi, an Accessory Clamp Loader Protein. PLoS Genet 11(11): e32767. doi:10.1371/journal.pgen.1005651
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005651

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Zdroje

1. Goodman MF. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Ann Rev Biochem. 2002; 71 : 17–50. 12045089

2. Goldfless SJ, Morag AS, Belisle KA, Sutera VA, Lovett ST. DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol Cell. 2006;21 : 595–604. 16507358

3. Michel B, Boubakri H, Baharoglu Z, LeMasson M, Lestini R. Recombination proteins and rescue of arrested replication forks. DNA Repair .2007;6 : 967–980. 17395553

4. Persky NS, Lovett ST. Mechanisms of recombination: lessons from E. coli. Crit Rev Biochem Mol Biol. 2008;43 : 347–370. doi: 10.1080/10409230802485358 19016098

5. Shereda RD, Kozlov AG, Lohman TM, Cox MM, Keck JL. SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol. 2008;43 : 289–318. doi: 10.1080/10409230802341296 18937104

6. Cooper DL, Lovett ST. Toxicity and tolerance mechanisms for azidothymidine, a replication gap-promoting agent, in Escherichia coli. DNA Repair. 2011;10 : 260–270. doi: 10.1016/j.dnarep.2010.11.007 21145792

7. Richardson CC, Lehman IR, Kornberg A. A deoxyribonucleic acid phosphatase-exonuclease from Escherichia coli. II. Characterization of the exonuclease activity. J Biol Chem. 1964;239 : 251–258. 14114851

8. Saka K, Tadenuma M, Nakade S, Tanaka N, Sugawara H, Nishikawa K, et al. A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Res. 2005;12 : 63–68. 16106753

9. Butland G, Peregrin-Alvarez J, Li J, Yang W, Yang X, Canadien V, et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature. 2005;433 : 531–537. 15690043

10. Kurth I, O'Donnell M. Replisome dynamics during chromosome duplication. EcoSal Plus. 2009. Available: http://www.asmscience.org/content/journal/ecosalplus/10.1128/ecosalplus.4.4.2 doi: 10.1128/ecosalplus.4.4.2

11. Gulbis JM, Kazmirski SL, Finkelstein J, Kelman Z, O'Donnell M, Kuriyan J. Crystal structure of the chi:psi sub-assembly of the Escherichia coli DNA polymerase clamp-loader complex. Eur J Biochem. 2004;271 : 439–449. 14717711

12. Xiao H, Dong Z, O'Donnell M. DNA polymerase III accessory proteins. IV. Characterization of chi and psi. J Biol Chem. 1993;268 : 11779–11784. 8505305

13. Kelman Z, Yuzhakov A, Andjelkovic J, O'Donnell M. Devoted to the lagging strand-the chi subunit of DNA polymerase III holoenzyme contacts SSB to promote processive elongation and sliding clamp assembly. EMBO J. 1998;17 : 2436–2449. 9545254

14. Olson MW, Dallmann HG, McHenry CS. DnaX complex of Escherichia coli DNA polymerase III holoenzyme. The chi psi complex functions by increasing the affinity of tau and gamma for delta delta' to a physiologically relevant range. J Biol Chem. 1995;270 : 29570–29577. 7494000

15. Glover B, McHenry C. The chi psi subunits of DNA polymerase III holoenzyme bind to single-stranded DNA-binding protein (SSB) and facilitate replication of an SSB-coated template. J Biol Chem. 1998;273 : 23476–23484. 9722585

16. Yuan Q, McHenry CS. Strand displacement by DNA polymerase III occurs through a tau-psi-chi link to single-stranded DNA-binding protein coating the lagging strand template. J Biol Chem. 2009;284 : 31672–31679. doi: 10.1074/jbc.M109.050740 19749191

17. Yuzhakov A, Kelman Z, O'Donnell M. Trading places on DNA—a three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell. 1999;96 : 153–163. 9989506

18. Anderson S, Williams C, O'Donnell M, Bloom L. A function for the psi subunit in loading the Escherichia coli DNA polymerase sliding clamp. J Biol Chem. 2007;282 : 7035–7045. 17210572

19. Viguera E, Petranovic M, Zahradka D, Germain K, Ehrlich DS, Michel B. Lethality of bypass polymerases in Escherichia coli cells with a defective clamp loader complex of DNA polymerase III. Mol Microbiol. 2003;50 : 193–204. 14507374

20. Reyes-Lamothe R, Sherratt DJ, Leake MC. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science. 2010;328 : 498–501. doi: 10.1126/science.1185757 20413500

21. Koonin EV. Escherichia coli dinG gene encodes a putative DNA helicase related to a group of eukaryotic helicases including Rad3 protein. Nucleic Acids Res. 1993;21 : 1497. 8385320

22. Voloshin ON, Vanevski F, Khil PP, Camerini-Otero RD. Characterization of the DNA damage-inducible helicase DinG from Escherichia coli. J Biol Chem. 2003;278 : 28284–28293. 12748189

23. Voloshin ON, Camerini-Otero RD. The DinG protein from Escherichia coli is a structure-specific helicase. J Biol Chem. 2007;282 : 18437–18447. 17416902

24. Ren B, Duan X, Ding H. Redox control of the DNA damage-inducible protein DinG helicase activity via its iron-sulfur cluster. J Biol Chem. 2009;284 : 4829–4835. doi: 10.1074/jbc.M807943200 19074432

25. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, et al. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 2005;12 : 291–299. 16769691

26. Naue N, Fedorov R, Pich A, Manstein DJ, Curth U. Site-directed mutagenesis of the chi subunit of DNA polymerase III and single-stranded DNA-binding protein of E. coli reveals key residues for their interaction. Nucleic Acids Res. 2011;39 : 1398–1407. doi: 10.1093/nar/gkq988 20972214

27. White MF. Structure, function and evolution of the XPD family of iron-sulfur-containing 5'—>3' DNA helicases. Biochem Soc Trans. 2009;37 : 547–551. doi: 10.1042/BST0370547 19442249

28. Fijalkowska I, Schaaper RM. Mutants in the Exo I motif of Escherichia coli dnaQ: defective proofreading and inviability due to error catastrophe. Proc Natl Acad Sci USA. 1996;93 : 2856–2861. 8610131

29. Jonczyk P, Nowicka A, Fijałkowska IJ, Schaaper RM, Cieśla Z. In vivo protein interactions within the Escherichia coli DNA polymerase III core. J Bacteriol. 1998;180 : 1563–1566. 9515927

30. Lewis LK, Jenkins ME, Mount DW. Isolation of DNA damage-inducible promoters in Escherichia coli: regulation of polB (dinA), dinG, and dinH by LexA repressor. J Bacteriol. 1992;174 : 3377–3385. 1577702

31. Lewis LK, Mount DW. Interaction of LexA repressor with the asymmetric dinG operator and complete nucleotide sequence of the gene. J Bacteriol. 1992;174 : 5110–5116. 1629168

32. Thakur RS, Desingu A, Basavaraju S, Subramanya S, Rao DN, Nagaraju G. Mycobacterium tuberculosis DinG is a structure-specific helicase that unwinds G4 DNA: implications for targeting G4 DNA as a novel therapeutic approach. J Biol Chem. 2014;289 : 25112–25136. doi: 10.1074/jbc.M114.563569 25059658

33. Boubakri H, de Septenville AL, Viguera E, Michel B. The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 2010;29 : 145–157. doi: 10.1038/emboj.2009.308 19851282

34. Burdett V, Baitinger C, Viswanathan M, Lovett ST, Modrich P. In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair. Proc Natl Acad Sci USA. 2001;98 : 6765–6770. 11381137

35. Hersh MN, Morales LD, Ross KJ, Rosenberg SM. Single-strand-specific exonucleases prevent frameshift mutagenesis by suppressing SOS induction and the action of DinB/DNA polymerase IV in growing cells. J Bacteriol. 2006;188 : 2336–2342. 16547019

36. Dutra BE, Sutera VA Jr., Lovett ST. RecA-independent recombination is efficient but limited by exonucleases. Proc Natl Acad Sci USA. 2007;104 : 216–221. 17182742

37. Eriksson S, Xu B, Clayton DA. Efficient incorporation of anti-HIV deoxynucleotides by recombinant yeast mitochondrial DNA polymerase. J Biol Chem. 1995;270 : 18929–18934. 7642550

38. Johnson AA, Ray AS, Hanes J, Suo Z, Colacino JM, Anderson KS, Johnson KA. Toxicity of antiviral nucleoside analogs and the human mitochondrial DNA polymerase. J Biol Chem. 2001;276 : 40847–40857. 11526116

39. Miller J. A short course in bacterial genetics. Cold Spring Harbor, NY: Cold Spring Harbor Press; 1992.

40. Dower WJ, Miller JF, Ragsdale CW. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988;16 : 6127–6145. 3041370

41. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006;2 : 2006 0008. 16738554

42. Lovett ST, Kolodner RD. Nucleotide sequence of the Escherichia coli recJ chromosomal region and construction of recJ-overexpression plasmids. J Bacteriol. 1991;173 : 353–364. 1987126