Bacterial DNA repair by non-homologous end joining

Nature Reviews Microbiology

Volumn 5, Issue 11, 2007, Pages 852-861

  Shuman, Stewart ^a   Glickman, Michael S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA POLYMERASE; DOUBLE STRANDED DNA; KU ANTIGEN; PHOSPHATASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE D; UNCLASSIFIED DRUG;

BASE PAIRING; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE INSERTION; HOMOLOGOUS RECOMBINATION; MYCOBACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; VIRUS CELL INTERACTION;

BACTERIAL PHYSIOLOGY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, BACTERIAL; RECOMBINATION, GENETIC;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE;

EID: 35348890199     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1768     Document Type: Review

References (56)

1. Cromie, G. A., Connelly, J. C. & Leach, D. R. F. Recombination at double-strand breaks and DNA ends: Conserved mechanisms from phage to humans. Mol. Cell 8, 1163-1174 (2001).
2. Daley, J. M., Palmbos, P. L. Wu, D. & Wilson, T. E. Nonhomologous end joining in yeast. Annu. Rev. Genet. 39, 431-451 (2005).
3. Lieber, M. R., Yu, L & Raghavan, S. C. Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. DNA Repair 5, 1234-1245 (2006).
4. Lusetti, S. L & Cox, M. M. The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71, 71-100 (2002).
5. Takata, M. et al. Homologous recombination and nonhomologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17, 5497-5508 (1998).
6. Ferreira, M. G. & Cooper, J. P. Two modes of DNA double-strand break repair are reciprocally regulated through fission yeast cell cycle. Genes Dev. 18, 2249-2254 (2004).
7. Bertocci, B., De Smet, A., Weill, J. C. & Reynaud, C. A. Nonoverlapping functions of DNA polymerases Mu, Lambda, and terminal deoxynucleotidyltransferase during immunoglobulin V(D)J recombination in vivo. Immunity 25, 31-41 (2006).
8. Aravind, L. & Koonin, E. V. Prokaryotic homologs of the eukaryotic DNA end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res. 11, 1365-1374 (2001).
9. Doherty, A. J., Jackson, S. P. & Weller, G. R. Identification of bacterial homologues of the Ku DNA repair proteins. FEBS Lett. 500, 186-188 (2001).
10. d'Adda di Fagagna, F., Weller, G. R., Doherty, A. J. & Jackson, S. P. The Gam protein of bacteriophage Mu is an ortholog of eukaryotic Ku. EMBO Rep. 4, 47-52 (2003).
11. Cheng, C. & Shuman, S. Characterization of an ATP-dependent DNA ligase encoded by Haemophilus influenzae. Nucleic Acids Res. 25, 1369-1375 (1997).
12. Magnet, S. & Blanchard, J. S. Mechanistic and kinetic study of the ATP-dependent DNA ligase of Neisseria meningitidis. Biochemistry 43, 710-717 (2004).
13. Weller, G. R. et al. Identification of a DNA nonhomologous end-joining complex in bacteria. Science 297, 1686-1689 (2002).
14. Gong, C., Martins, A., Bongiorno, P., Glickman, M. & Shuman, S. Biochemical and genetic analysis of the four DNA ligases of mycobacteria. J. Biol. Chem. 279, 20594-20606 (2004).
15. Weller, G. R. & Doherty A. J. A family of DNA repair ligases in bacteria? FEBS Lett. 505, 340-342 (2001).
16. Della, M. et al. Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science 306, 683-685 (2004).
17. Gone, C. et al. Mechanism of nonhomologous end-joining in mycobacteria: A low fidelity repair system driven by Ku, ligase D and ligase C. Nature Struct. Mol. Biol. 12, 304-312 (2005).
18. Korycka-Machala, M. et al. Distinct DNA repair pathways involving RecA and nonhomologous end joining in Mycobacterium smegmatis. FEMS Microbiol. Lett. 258, 83-91 (2006).
19. Wang, S. T. et al. The forespore line of gene expression in Bacillus subtilis. J. Mol. Biol. 358, 16-37 (2006).
20. Moeller, R. et al. Role of DNA repair by nonhomologous end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV, and ionizing radiation. J. Bacteriol. 189 3306-3311 (2007).
21. Stephanou, N. C. et al. Mycobacterial nonhomologous end joining mediates mutagenic repair of chromosomal double-strand DNA breaks. J. Bacteriol. 189, 5237-5246 (2007).
22. Pitcher, R. S. et al. NHEJ protects mycobacteria in stationary phase against the harmful effects of dessication. DNA Repair 6 1271-1276 (2007).
23. Zhu, H. & Shuman, S. A primer-dependent polymerase function of Pseudomonas aeruginosa ATP-dependent DNA ligase (LigD). J. Biol. Chem. 280, 418-427 (2005).
24. Zhu, H. & Shuman, S. Novel 3′-ribonuclease and 3′-phosphatase activities of the bacterial nonhomologous end-joining protein, DNA ligase D. J. Biol. Chem. 280, 25973-25981 (2005).
25. Zhu, H. & Shuman, S. Characterization of Agrobacterium tumefaciens DNA ligases C and D. Nucleic Acids Res. 35, 3631-3645 (2007).
26. Akey D. et al. Crystal structure and nonhomologous end joining function of the ligase domain of Mycobocterium DNA ligase D. J. Biol. Chem. 281, 13412-13423 (2006).
27. Zhu, H. et al. Atomic structure and nonhomologous end-joining function of the polymerase component of bacterial DNA ligase D. Proc. Natl Acad. Sci. USA 103, 1711-1716 (2006).
28. Pitcher, R. S. et al. Structure and function of a mycobacterial NHEJ DNA repair polymerase. J. Mol. Biol. 366, 391-405 (2007).
29. Lehman, I. R. DNA ligase: Structure, mechanism, and function. Science 186, 790-797 (1974).
30. Nandakumar, J., Nair, P. A. & Shuman, S. Last stop on the road to repair: Structure of E. coli DNA ligase bond to nicked DNA-adenylate. Mol. Cell 26, 257-271 (2007).
31. + synthesis within a bacterial DNA ligase crystal. Structure 12 1449-1459 (2004).
32. +. J. Biol. Chem. 277, 9685-9700 (2002).
33. Pascal, J. M., O'Brien, P. J., Tomkinson, A. E. & Ellenberger, T. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432, 473-478 (2004).
34. Pitcher, R. S., Tonkin, L. M., Green, A. J. &.Doherty A. J. Domain structure of a NHEJ repair figase from Mycobacterium tuberculosis. J. Mol. Biol. 351, 531-544 (2005).
35. Yakovleva, L. & Shuman, S. Nucleotide misincorporation, 3′-mismatch extension, and responses to abasic sites and DNA adducts by the polymerase component of bacterial DNA ligase D. J. Biol. Chem. 281, 25026-25040 (2006).
36. Augustin, M. A., Huber, R. & Kaiser, J. T. Crystal structure of a DNA-dependent RNA polymerase (DNA primase). Nature Struct. Biol. 8, 57-61 (2001).
37. Ito, N., Nureki, O., Shirouzu, M., Yokoyama, S. & Hanaola, F. Crystal structure of the Pyrococcus horikoshii DNA primase-UTP complex: implications for the mechanism of primer synthesis. Genes Cells 8, 913-923 (2003).
38. Ramadan, K., Shevelev, I. & Hübscher, U. The DNA-polymerase-X family: controllers of DNA quality? Nature Rev. Mol. Cell. Biol. 5, 1038-1043 (2004).
39. Zhu, H. & Shuman, S. Essential constituents of the 3′-phosphoesterase domain of bacterial DNA-ligase D, a nonhomologous end-joining enzyme. J. Biol. Chem. 280, 33707-33715 (2005).
40. Zhu, H. & Shuman, S. Substrate specificity and structure-function analysis of the 3′-phosphoesterase component of the bacterial NHEJ protein, DNA Ligase D. J. Biol. Chem. 281, 13873-13881 (2006).
41. Jacobs, M. A. et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 100, 14339-14344 (2003).
42. Darwin, K. H. & Nathan, C. F. Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun. 73, 4581-4587 (2005).
43. Boschoff, H. I., Reed, M. B., Barry, C. E. & Mizrahi, V. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell 113, 183-193 (2003).
44. Cirz, R. T. et al. Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol. 3, 1024-1033 (2005).
45. Gandhi, N. R. et al. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368, 1575-1580 (2006).
46. Wayne, L. G. Synchronized replication of Mycobacterium tuberculosis. Infect. Immun. 17, 528-530 (1977).
47. Dick, T., Lee, B. H. & Murugasu-Oei, B. Oxygen depletion induced dormancy in Mycobacterium smegmatis. FEMS Microbiol. Lett. 163 159-164 (1998).
48. Li, L. et al. Role of the non-homologous DNA end joining pathway in the early steps of retroviral infection. EMBO J. 20, 3272-3281 (2001).
49. Skalka, A. M. & Katz, R. A. Retroviral DNA integration and the DNA damage response. Cell Death Differ. 12, 871-978 (2005).
50. Muylaert, I. & Elias, P. Knockdown of DNA ligase IV/XRCC4 by RNA interference inhibits herpes simplex virus type I DNA replication. J. Biol. Chem. 282, 10865-10872 (2007).
51. Pitcher, R. S. et al. Mycobacteriophage exploit NHEJ to facilitate genome circularization. Mol. Cell 23, 743-748 (2006).
52. Martinez, J. J., Seveau, S., Veiga, S., Matsuyama, S. & Cossart, P. Ku70, a component of DNA-dependent protein kinase, is a mammalian receptor for Rickettsio conorii. Cell 123, 1013-1023 (2005).
53. Sinha, K. M., Stephanou, N. C., Gao, F., Glickman, M. S. & Shuman, S. Mycobacterial UvrD1 is a Ku-dependent DNA helicase that plays a role in multiple DNA repair events, including double-strand break repair. J. Biol. Chem. 282, 15114-15125 (2007).
54. Velankar, S. S., Soultanas, P., Dillingham, M. S., Subramanya, H. S. & Wigley, D. B. Crystal structure of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 87, 75-84 (1999).
55. Lee, J. Y. & Yang, W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349-1360 (2006).
56. Curti, E., Smerdon, S. J. & Davis, E. O. Characterization of the helicase activity and substrate specificity of Mycobacterium tuberculosis UvrD. J. Bacteriol. 189, 1542-1555 (2007).