The BER necessities: The repair of DNA damage in human-adapted bacterial pathogens

Nature Reviews Microbiology

Volumn 13, Issue 2, 2015, Pages 83-94

  Van Der Veen, Stijn ^a   Tang, Christoph M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; DNA GLYCOSYLTRANSFERASE; ENDONUCLEASE; EXONUCLEASE; MYELOPEROXIDASE; PEROXYNITRITE; SUPEROXIDE; URACIL DNA GLYCOSIDASE; BACTERIAL DNA;

3' UNTRANSLATED REGION; DNA BASE COMPOSITION; DNA DAMAGE; DNA REPAIR; DNA STRAND; ESCHERICHIA COLI; EXCISION REPAIR; HELICOBACTER PYLORI; HUMAN; INNATE IMMUNITY; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW; STOMACH MUCOSA; BACTERIAL INFECTION; BACTERIUM; CLASSIFICATION; GENETICS; IMMUNOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS;

BACTERIA; BACTERIAL INFECTIONS; DNA DAMAGE; DNA REPAIR; DNA, BACTERIAL; HUMANS; IMMUNITY, INNATE;

EID: 84923070685     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3391     Document Type: Review

References (120)

1. Eisen, J. A. & Hanawalt, P. C. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 435, 171-213 (1999).
2. Boiteux, S. & Guillet, M. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair (Amst.) 3, 1-12 (2004).
3. Daley, J. M., Zakaria, C. & Ramotar, D. The endonuclease IV family of apurinic/apyrimidinic endonucleases. Mutat. Res. 705, 217-227 (2010).
4. Eisele, N. A. & Anderson, D. M. Host defense and the airway epithelium: frontline responses that protect against bacterial invasion and pneumonia. J. Pathog. 2011, 249802 (2011).
5. Swanson, P. A. et al. Enteric commensal bacteria potentiate epithelial restitution via reactive oxygen species-mediated inactivation of focal adhesion kinase phosphatases. Proc. Natl Acad. Sci. USA 108, 8803-8808 (2011).
6. Kinnula, V. L., Adler, K. B., Ackley, N. J. & Crapo, J. D. Release of reactive oxygen species by guinea pig tracheal epithelial cells in vitro. Am. J. Physiol. 262, L708-L712 (1992).
7. Sibille, Y. & Reynolds, H. Y. Macrophages and polymorphonuclear neutrophils in lung defense and injury. Am. Rev. Respir. Dis. 141, 471-501 (1990).
8. Fialkow, L., Wang, Y. & Downey, G. P. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic. Biol. Med. 42, 153-164 (2007).
9. Goldblatt, D. & Thrasher, A. J. Chronic granulomatous disease. Clin. Exp. Immunol. 122, 1-9 (2000).
10. Gaut, J. P. et al. Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxidants during sepsis. Proc. Natl Acad. Sci. USA 98, 11961-11966 (2001).
11. Nathan, C. & Shiloh, M. U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl Acad. Sci. USA 97, 8841-8848 (2000).
12. Missall, T. A., Lodge, J. K. & McEwen, J. E. Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukaryot. Cell 3, 835-846 (2004).
13. Shiloh, M. U. et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10, 29-38 (1999).
14. Cadet, J. & Wagner, J. R. DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb. Perspect. Biol. 5, a012559 (2013).
15. Burney, S., Caulfield, J. L., Niles, J. C., Wishnok, J. S. & Tannenbaum, S. R. The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res. 424, 37-49 (1999).
16. Szabo, C. & Ohshima, H. DNA damage induced by peroxynitrite: subsequent biological effects. Nitr. Oxide 1, 373-385 (1997).
17. Huffman, J. L., Sundheim, O. & Tainer, J. A. DNA base damage recognition and removal: new twists and grooves. Mutat. Res. 577, 55-76 (2005).
18. Krokan, H. E. & Bjoras, M. Base excision repair. Cold Spring Harb. Perspect. Biol. 5, a012583 (2013).
19. Svilar, D., Goellner, E. M., Almeida, K. H. & Sobol, R. W. Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage. Antioxid. Redox Signal 14, 2491-2507 (2011).
20. Dianov, G. & Lindahl, T. Reconstitution of the DNA base excision-repair pathway. Curr. Biol. 4, 1069-1076 (1994).
21. Mosbaugh, D. W. & Linn, S. Characterization of the action of Escherichia coli DNA polymerase I at incisions produced by repair endodeoxyribonucleases. J. Biol. Chem. 257, 575-583 (1982).
22. Sung, J. S. & Mosbaugh, D. W. Escherichia coli uracil-and ethenocytosine-initiated base excision DNA repair: rate-limiting step and patch size distribution. Biochemistry 42, 4613-4625 (2003).
23. Yao, M. & Kow, Y. W. Cleavage of insertion/deletion mismatches, flap and pseudo-Y DNA structures by deoxyinosine 3′-endonuclease from Escherichia coli. J. Biol. Chem. 271, 30672-30676 (1996).
24. Singh, P. et al. Carbon nanotube-nucleobase hybrids: nanorings from uracil-modified single-walled carbon nanotubes. Chemistry 17, 6772-6780 (2011).
25. Tchou, J. et al. 8-oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc. Natl Acad. Sci. USA 88, 4690-4694 (1991).
26. Tsai-Wu, J. J., Liu, H. F. & Lu, A. L. Escherichia coli MutY protein has both N-glycosylase and apurinic/apyrimidinic endonuclease activities on A.C and A.G mispairs. Proc. Natl Acad. Sci. USA 89, 8779-8783 (1992).
27. Nakamura, T. et al. Structural and dynamic features of the MutT protein in the recognition of nucleotides with the mutagenic 8-oxoguanine base. J. Biol. Chem. 285, 444-452 (2010).
28. Dye, C., Scheele, S., Dolin, P., Pathania, V. & Raviglione, M. C. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282, 677-686 (1999).
29. Subbian, S., Mehta, P. K., Cirillo, S. L., Bermudez, L. E. & Cirillo, J. D. A. Mycobacterium marinum mel2 mutant is defective for growth in macrophages that produce reactive oxygen and reactive nitrogen species. Infect. Immun. 75, 127-134 (2007).
30. Li, Q. et al. Differences in rate and variability of intracellular growth of a panel of Mycobacterium tuberculosis clinical isolates within a human monocyte model. Infect. Immun. 70, 6489-6493 (2002).
31. Sullivan, J. T., Young, E. F., McCann, J. R. & Braunstein, M. The Mycobacterium tuberculosis SecA2 system subverts phagosome maturation to promote growth in macrophages. Infect. Immun. 80, 996-1006 (2012).
32. Nicholson, S. et al. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183, 2293-2302 (1996).
33. Adams, L. B., Dinauer, M. C., Morgenstern, D. E. & Krahenbuhl, J. L. Comparison of the roles of reactive oxygen and nitrogen intermediates in the host response to Mycobacterium tuberculosis using transgenic mice. Tuber Lung Dis. 78, 237-246 (1997).
34. MacMicking, J. D. et al. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl Acad. Sci. USA 94, 5243-5248 (1997).
35. Lee, P. P. et al. Susceptibility to mycobacterial infections in children with X-linked chronic granulomatous disease: a review of 17 patients living in a region endemic for tuberculosis. Pediatr. Infect. Dis. J. 27, 224-230 (2008).
36. Rand, L. et al. The majority of inducible DNA repair genes in Mycobacterium tuberculosis are induced independently of RecA. Mol. Microbiol. 50, 1031-1042 (2003).
37. Davis, E. O. et al. DNA damage induction of recA in Mycobacterium tuberculosis independently of RecA and LexA. Mol. Microbiol. 46, 791-800 (2002).
38. Smollett, K. L. et al. Global analysis of the regulon of the transcriptional repressor LexA, a key component of SOS response in Mycobacterium tuberculosis. J. Biol. Chem. 287, 22004-22014 (2012).
39. Dos Vultos, T., Mestre, O., Tonjum, T. & Gicquel, B. DNA repair in Mycobacterium tuberculosis revisited. FEMS Microbiol. Rev. 33, 471-487 (2009).
40. Kurthkoti, K. & Varshney, U. Distinct mechanisms of DNA repair in mycobacteria and their implications in attenuation of the pathogen growth. Mech. Ageing Dev. 133, 138-146 (2012).
41. Dos Vultos, T., Blazquez, J., Rauzier, J., Matic, I. & Gicquel, B. Identification of Nudix hydrolase family members with an antimutator role in Mycobacterium tuberculosis and Mycobacterium smegmatis. J. Bacteriol. 188, 3159-3161 (2006).
42. Patil, A. G., Sang, P. B., Govindan, A. & Varshney, U. Mycobacterium tuberculosis MutT1 (Rv2985) and ADPRase (Rv1700) proteins constitute a two-stage mechanism of 8-oxo-dGTP and 8-oxo-GTP detoxification and adenosine to cytidine mutation avoidance. J. Biol. Chem. 288, 11252-11262 (2013).
43. Sang, P. B. & Varshney, U. Biochemical properties of MutT2 proteins from Mycobacterium tuberculosis and M. smegmatis and their contrasting antimutator roles in Escherichia coli. J. Bacteriol. 195, 1552-1560 (2013).
44. Jain, R., Kumar, P. & Varshney, U. A distinct role of formamidopyrimidine DNA glycosylase (MutM) in down-regulation of accumulation of G, C mutations and protection against oxidative stress in mycobacteria. DNA Repair (Amst.) 6, 1774-1785 (2007).
45. Olsen, I. et al. Characterization of the major formamidopyrimidine-DNA glycosylase homolog in Mycobacterium tuberculosis and its linkage to variable tandem repeats. FEMS Immunol. Med. Microbiol. 56, 151-161 (2009).
46. Guo, Y. et al. The oxidative DNA glycosylases of Mycobacterium tuberculosis exhibit different substrate preferences from their Escherichia coli counterparts. DNA Repair (Amst.) 9, 177-190 (2010).
47. Hazra, T. K. et al. Characterization of a novel 8-oxoguanine-DNA glycosylase activity in Escherichia coli and identification of the enzyme as endonuclease VIII. J. Biol. Chem. 275, 27762-27767 (2000).
48. Zharkov, D. O. et al. Structural analysis of an Escherichia coli endonuclease VIII covalent reaction intermediate. EMBO J. 21, 789-800 (2002).
49. Sidorenko, V. S., Rot, M. A., Filipenko, M. L., Nevinsky, G. A. & Zharkov, D. O. Novel DNA glycosylases from Mycobacterium tuberculosis. Biochem. (Mosc) 73, 442-450 (2008).
50. Matsumoto, Y., Zhang, Q. M., Takao, M., Yasui, A. & Yonei, S. Escherichia coli Nth and human hNTH1 DNA glycosylases are involved in removal of 8-oxoguanine from 8-oxoguanine/guanine mispairs in DNA. Nucleic Acids Res. 29, 1975-1981 (2001).
51. Vertessy, B. G. & Toth, J. Keeping uracil out of DNA: physiological role, structure and catalytic mechanism of dUTPases. Acc. Chem. Res. 42, 97-106 (2009).
52. Helt, S. S. et al. Mechanism of dTTP inhibition of the bifunctional dCTP deaminase:dUTPase encoded by Mycobacterium tuberculosis. J. Mol. Biol. 376, 554-569 (2008).
53. Lindahl, T. An N-glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proc. Natl Acad. Sci. USA 71, 3649-3653 (1974).
54. Lindahl, T., Ljungquist, S., Siegert, W., Nyberg, B. & Sperens, B. D.N. A. N-glycosidases: properties of uracil-DNA glycosidase from Escherichia coli. J. Biol. Chem. 252, 3286-3294 (1977).
55. Purnapatre, K. & Varshney, U. Uracil DNA glycosylase from Mycobacterium smegmatis and its distinct biochemical properties. Eur. J. Biochem. 256, 580-588 (1998).
56. Sassetti, C. M. & Rubin, E. J. Genetic requirements for mycobacterial survival during infection. Proc. Natl Acad. Sci. USA 100, 12989-12994 (2003).
57. Venkatesh, J., Kumar, P., Krishna, P. S., Manjunath, R. & Varshney, U. Importance of uracil DNA glycosylase in Pseudomonas aeruginosa and Mycobacterium smegmatis, G+C-rich bacteria, in mutation prevention, tolerance to acidified nitrite, and endurance in mouse macrophages. J. Biol. Chem. 278, 24350-24358 (2003).
58. Srinath, T., Bharti, S. K. & Varshney, U. Substrate specificities and functional characterization of a thermo-tolerant uracil DNA glycosylase (UdgB) from Mycobacterium tuberculosis. DNA Repair (Amst.) 6, 1517-1528 (2007).
59. Kumar, P., Bharti, S. K. & Varshney, U. Uracil excision repair in Mycobacterium tuberculosis cell-free extracts. Tuberculosis (Edinb.) 91, 212-218 (2011).
60. Durbach, S. I. et al. DNA alkylation damage as a sensor of nitrosative stress in Mycobacterium tuberculosis. Infect. Immun. 71, 997-1000 (2003).
61. 6 -methylguanine methyltransferase and mutated variants. J. Bacteriol. 195, 2728-2736 (2013).
62. O'Brien, P. J. & Ellenberger, T. The Escherichia coli 3-methyladenine DNA glycosylase AlkA has a remarkably versatile active site. J. Biol. Chem. 279, 26876-26884 (2004).
63. Cole, S. T. et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998).
64. Loeb, L. A. Apurinic sites as mutagenic intermediates. Cell 40, 483-484 (1985).
65. Puri, R. V., Singh, N., Gupta, R. K. & Tyagi, A. K. Endonuclease IV is the major apurinic/apyrimidinic endonuclease in Mycobacterium tuberculosis and is important for protection against oxidative damage. PLoS ONE 8, e71535 (2013).
66. Takeuchi, M., Lillis, R., Demple, B. & Takeshita, M. Interactions of Escherichia coli endonuclease IV and exonuclease III with abasic sites in DNA. J. Biol. Chem. 269, 21907-21914 (1994).
67. Kusters, J. G., van Vliet, A. H. & Kuipers, E. J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19, 449-490 (2006).
68. Salama, N. R., Hartung, M. L. & Muller, A. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nature Rev. Microbio. 11, 385-399 (2013).
69. Allen, L. A., Beecher, B. R., Lynch, J. T., Rohner, O. V. & Wittine, L. M. Helicobacter pylori disrupts NADPH oxidase targeting in human neutrophils to induce extracellular superoxide release. J. Immunol. 174, 3658-3667 (2005).
70. Chaturvedi, R. et al. Induction of polyamine oxidase 1 by Helicobacter pylori causes macrophage apoptosis by hydrogen peroxide release and mitochondrial membrane depolarization. J. Biol. Chem. 279, 40161-40173 (2004).
71. Xu, H. et al. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res. 64, 8521-8525 (2004).
72. Alm, R. A. et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176-180 (1999).
73. Tomb, J. F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547 (1997).
74. García-Ortíz, M. V. et al. Unexpected role for Helicobacter pylori DNA polymerase I as a source of genetic variability. PLoS Genet. 7, e1002152 (2011).
75. Linz, B. et al. A mutation burst during the acute phase of Helicobacter pylori infection in humans and rhesus macaques. Nature Commun. 5, 4165 (2014).
76. O'Rourke, E. J. et al. Pathogen DNA as target for host-generated oxidative stress: role for repair of bacterial DNA damage in Helicobacter pylori colonization. Proc. Natl Acad. Sci. USA 100, 2789-2794 (2003).
77. O'Rourke, E. J. et al. A novel 3-methyladenine DNA glycosylase from Helicobacter pylori defines a new class within the endonuclease III family of base excision repair glycosylases. J. Biol. Chem. 275, 20077-20083 (2000).
78. Eichman, B. F., O'Rourke, E. J., Radicella, J. P. & Ellenberger, T. Crystal structures of 3-methyladenine DNA glycosylase MagIII and the recognition of alkylated bases. EMBO J. 22, 4898-4909 (2003).
79. Baldwin, D. N. et al. Identification of Helicobacter pylori genes that contribute to stomach colonization. Infect. Immun. 75, 1005-1016 (2007).
80. Mathieu, A., O'Rourke, E. J. & Radicella, J. P. Helicobacter pylori genes involved in avoidance of mutations induced by 8-oxoguanine. J. Bacteriol. 188, 7464-7469 (2006).
81. Huang, S., Kang, J. & Blaser, M. J. Antimutator role of the DNA glycosylase mutY gene in Helicobacter pylori. J. Bacteriol. 188, 6224-6234 (2006).
82. Eutsey, R., Wang, G. & Maier, R. J. Role of a MutY DNA glycosylase in combating oxidative DNA damage in Helicobacter pylori. DNA Repair (Amst.) 6, 19-26 (2007).
83. Pinto, A. V. et al. Suppression of homologous and homeologous recombination by the bacterial MutS2 protein. Mol. Cell 17, 113-120 (2005).
84. 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. 58, 166-176 (2005).
85. Stephens, D. S. Uncloaking the meningococcus: dynamics of carriage and disease. Lancet 353, 941-942 (1999).
86. Cartwright, K. A., Stuart, J. M., Jones, D. M. & Noah, N. D. The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol. Infect. 99, 591-601 (1987).
87. Christensen, H., May, M., Bowen, L., Hickman, M. & Trotter, C. L. Meningococcal carriage by age: a systematic review and meta-analysis. Lancet Infect. Dis. 10, 853-861 (2010).
88. Criss, A. K. & Seifert, H. S. A bacterial siren song: intimate interactions between Neisseria and neutrophils. Nature Rev. Microbiol. 10, 178-190 (2012).
89. Carpenter, E. P. et al. AP endonuclease paralogues with distinct activities in DNA repair and bacterial pathogenesis. EMBO J. 26, 1363-1372 (2007).
90. Nagorska, K. et al. A network of enzymes involved in repair of oxidative DNA damage in Neisseria meningitidis. Mol. Microbiol. 83, 1064-1079 (2012).
91. Morelle, S., Carbonnelle, E., Matic, I. & Nassif, X. Contact with host cells induces a DNA repair system in pathogenic Neisseriae. Mol. Microbiol. 55, 853-861 (2005).
92. Davidsen, T. & Tønjum, T. Meningococcal genome dynamics. Nature Rev. Microbiol. 4, 11-22 (2006).
93. Tibballs, K. L. et al. Characterization of the meningococcal DNA glycosylase Fpg involved in base excision repair. BMC Microbiol. 9, 7 (2009).
94. Silhan, J. et al. Specialization of an Exonuclease III family enzyme in the repair of 3′ DNA lesions during base excision repair in the human pathogen Neisseria meningitidis. Nucleic Acids Res. 40, 2065-2075 (2012).
95. Demple, B. & Harrison, L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63, 915-948 (1994).
96. Davidsen, T., Tuven, H. K., Bjoras, M., Rodland, E. A. & Tonjum, T. Genetic interactions of DNA repair pathways in the pathogen Neisseria meningitidis. J. Bacteriol. 189, 5728-5737 (2007).
97. Davidsen, T., Bjoras, M., Seeberg, E. C. & Tonjum, T. Antimutator role of DNA glycosylase MutY in pathogenic Neisseria species. J. Bacteriol. 187, 2801-2809 (2005).
98. Sanders, L. H., Sudhakaran, J. & Sutton, M. D. The GO system prevents ROS-induced mutagenesis and killing in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 294, 89-96 (2009).
99. LeCuyer, B. E., Criss, A. K. & Seifert, H. S. Genetic characterization of the nucleotide excision repair system of Neisseria gonorrhoeae. J. Bacteriol. 192, 665-673 (2010).
100. Fischer, W. & Haas, R. The RecA protein of Helicobacter pylori requires a posttranslational modification for full activity. J. Bacteriol. 186, 777-784 (2004).
101. Orillard, E., Radicella, J. P. & Marsin, S. Biochemical and cellular characterization of Helicobacter pylori RecA, a protein with high-level constitutive expression. J. Bacteriol. 193, 6490-6497 (2011).
102. Yesilkaya, H., Andisi, V. F., Andrew, P. W. & Bijlsma, J. J. Streptococcus pneumoniae and reactive oxygen species: an unusual approach to living with radicals. Trends Microbiol. 21, 187-195 (2013).
103. Ambur, O. H. et al. Genome dynamics in major bacterial pathogens. FEMS Microbiol. Rev. 33, 453-470 (2009).
104. Lesterlin, C., Ball, G., Schermelleh, L. & Sherratt, D. J. RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506, 249-253 (2014).
105. Pitcher, R. S. et al. NHEJ protects mycobacteria in stationary phase against the harmful effects of desiccation. DNA Repair (Amst.) 6, 1271-1276 (2007).
106. Prieto, A. I., Ramos-Morales, F. & Casadesus, J. Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174, 575-584 (2006).
107. Thompson, S. A. & Blaser, M. J. Isolation of the Helicobacter pylori recA gene and involvement of the recA region in resistance to low pH. Infect. Immun. 63, 2185-2193 (1995).
108. Thompson, S. A., Latch, R. L. & Blaser, J. M. Molecular characterization of the Helicobacter pylori uvr B gene. Gene 209, 113-122 (1998).
109. Yi, C. & He, C. DNA repair by reversal of DNA damage. Cold Spring Harb. Perspect. Biol. 5, a012575 (2013).
110. Krokan, H. E., Standal, R. & Slupphaug, G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 325, 1-16 (1997).
111. Friedman, J. I. & Stivers, J. T. Detection of damaged DNA bases by DNA glycosylase enzymes. Biochemistry 49, 4957-4967 (2010).
112. Berti, P. J. & McCann, J. A. Toward a detailed understanding of base excision repair enzymes: transition state and mechanistic analyses of N-glycoside hydrolysis and N-glycoside transfer. Chem. Rev. 106, 506-555 (2006).
113. Mol, C. D., Hosfield, D. J. & Tainer, J. A. Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: the 3′ ends justify the means. Mutat. Res. 460, 211-229 (2000).
114. Kisker, C., Kuper, J. & Van Houten, B. Prokaryotic nucleotide excision repair. Cold Spring Harb. Perspect. Biol. 5, a012591 (2013).
115. Deaconescu, A. M. et al. Structural basis for bacterial transcription-coupled DNA repair. Cell 124, 507-520 (2006).
116. Jiricny, J. Postreplicative mismatch repair. Cold Spring Harb. Perspect. Biol. 5, a012633 (2013).
117. Ayora, S. et al. Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol. Rev. 35, 1055-1081 (2011).
118. Jasin, M. & Rothstein, R. Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol. 5, a012740 (2013).
119. Pitcher, R. S., Brissett, N. C. & Doherty, A. J. Nonhomologous end-joining in bacteria: a microbial perspective. Annu. Rev. Microbiol. 61, 259-282 (2007).
120. Nohmi, T. Environmental stress and lesion-bypass DNA polymerases. Annu. Rev. Microbiol. 60, 231-253 (2006).