Abstract
Infections with Mycobacterium tuberculosis, the causative agent of tuberculosis, are difficult to treat using currently available chemotherapeutics. Clinicians agree on the urgent need for novel drugs to treat tuberculosis. In this mini review, we summarize data that prompts the consideration of DNA repair-associated proteins as targets for the development of new antitubercular compounds. We discuss data, including gene expression data, that highlight the importance of DNA repair genes during the pathogenic cycle as well as after exposure to antimicrobials currently in use. Specifically, we report experiments on determining the essentiality of DNA repair-related genes. We report the availability of protein crystal structures and summarize discovered protein inhibitors. Further, we describe phenotypes of available gene mutants of M. tuberculosis and model organisms Mycobacterium bovis and Mycobacterium smegmatis. We summarize experiments regarding the role of DNA repair-related proteins in pathogenesis and virulence performed both in vitro and in vivo during the infection of macrophages and animals. We detail the role of DNA repair genes in acquiring mutations, which influence the rate of drug resistance acquisition.
Keywords: DNA repair, Mycobacterium tuberculosis, crystal structure, inhibitor, drug resistance, mutation rate.
[2]
Płocinska, R.; Korycka-Machala, M.; Plocinski, P.; Dziadek, J. Mycobacterial DNA replication as a target for antituberculosis drug discovery. Curr. Top. Med. Chem., 2017, 17(19), 2129-2142.
[3]
Gorna, A.E.; Bowater, R.P.; Dziadek, J. DNA repair systems and the pathogenesis of Mycobacterium tuberculosis: varying activities at different stages of infection. Clin. Sci. Lond. Engl, 2010, 119(5), 187-202.
[4]
Fu, L.M.; Fu-Liu, C.S. The gene expression data of Mycobacterium tuberculosis based on Affymetrix gene chips provide insight into regulatory and hypothetical genes. BMC Microbiol., 2007, 7(1), 37.
[5]
van der Veen, S.; Tang, C.M. The BER necessities: the repair of DNA damage in human-adapted bacterial pathogens. Nat. Rev. Microbiol., 2015, 13(2), 83-94.
[6]
Helt, S.S.; Thymark, M.; Harris, P.; Aagaard, C.; Dietrich, J.; Larsen, S.; Willemoes, M. Mechanism of dTTP inhibition of the bifunctional dCTP deaminase:dUTPase encoded by Mycobacterium tuberculosis. J. Mol. Biol., 2008, 376(2), 554-569.
[7]
Sassetti, C.M.; Boyd, D.H.; Rubin, E.J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol., 2003, 48(1), 77-84.
[8]
Pecsi, I.; Hirmondo, R.; Brown, A.C.; Lopata, A.; Parish, T.; Vertessy, B.G.; Tóth, J. The dUTPase enzyme is essential in Mycobacterium smegmatis. PLoS One, 2012, 7(5), e37461.
[9]
Dubnau, E.; Fontán, P.; Manganelli, R.; Soares-Appel, S.; Smith, I. Mycobacterium tuberculosis genes induced during infection of human macrophages. Infect. Immun., 2002, 70(6), 2787-2795.
[10]
Chan, S.; Segelke, B.; Lekin, T.; Krupka, H.; Cho, U.S.; Kim, M-Y.; So, M.; Kim, C-Y.; Naranjo, C.M.; Rogers, Y.C.; Park, M.S.; Waldo, G.S.; Pashkov, I.; Cascio, D.; Perry, J.L.; Sawaya, M.R. Crystal structure of the Mycobacterium tuberculosis dUTPase: insights into the catalytic mechanism. J. Mol. Biol., 2004, 341(2), 503-517.
[11]
Varga, B.; Barabás, O.; Takács, E.; Nagy, N.; Nagy, P.; Vértessy, B.G. Active site of mycobacterial dUTPase: structural characteristics and a built-in sensor. Biochem. Biophys. Res. Commun., 2008, 373(1), 8-13.
[12]
Ramalho, T.C.; Caetano, M.S.; Josa, D.; Luz, G.P.; Freitas, E.A.; da Cunha, E.F. Molecular modeling of Mycobacterium tuberculosis dUTpase: docking and catalytic mechanism studies. J. Biomol. Struct. Dyn., 2011, 28(6), 907-917.
[13]
Schnöller, D.; Pénzes, C.B.; Horváti, K.; Bősze, S.; Hudecz, F.; Kiss, É. Membrane affinity of new antitubercular drug candidates using a phospholipid langmuir monolayer model and LB technique. Colloid Polym. Sci., 2011, 138, 131-137.
[14]
Horváti, K.; Bacsa, B.; Szabó, N.; Dávid, S.; Mező, G.; Grolmusz, V.; Vértessy, B.; Hudecz, F.; Bősze, S. Enhanced cellular uptake of a new, in silico identified antitubercular candidate by peptide conjugation. Bioconjug. Chem., 2012, 23(5), 900-907.
[15]
Kiss, É.; Gyulai, G.; Pénzes, C.B.; Idei, M.; Horváti, K.; Bacsa, B.; Bősze, S. Tuneable surface modification of PLGA nanoparticles carry-ing new antitubercular drug candidate. COLLOIDS Surf. -. Physicochem. Eng. Asp., 2014, 458, 178-186.
[16]
Horváti, K.; Bacsa, B.; Szabó, N.; Fodor, K.; Balka, G.; Rusvai, M.; Kiss, É.; Mező, G.; Grolmusz, V.; Vértessy, B.; Hudecz, F.; Bősze, S. Antimycobacterial activity of peptide conjugate of pyridopyrimidine derivative against Mycobacterium tuberculosis in a series of in vitro and in vivo models. Tuberculosis (Edinb.), 2015, 95(Suppl. 1), S207-S211.
[17]
Dutta, N.K.; Mehra, S.; Didier, P.J.; Roy, C.J.; Doyle, L.A.; Alvarez, X.; Ratterree, M.; Be, N.A.; Lamichhane, G.; Jain, S.K.; Lacey, M.R.; Lackner, A.A.; Kaushal, D. Genetic requirements for the survival of Tubercle Bacilli in primates. J. Infect. Dis., 2010, 201(11), 1743-1752.
[18]
Sassetti, C.M.; Rubin, E.J. Genetic requirements for mycobacterial survival during infection. Proc. Natl. Acad. Sci. USA, 2003, 100(22), 12989-12994.
[19]
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., 2003, 278(27), 24350-24358.
[20]
Kurthkoti, K.; Kumar, P.; Jain, R.; Varshney, U. Important role of the nucleotide excision repair pathway in Mycobacterium smegmatis in conferring protection against commonly encountered DNA-damaging agents. Microbiol. Read. Engl., 2008, 154(Pt 9), 2776-2785.
[21]
Malshetty, V.S.; Jain, R.; Srinath, T.; Kurthkoti, K.; Varshney, U. Synergistic effects of UdgB and Ung in mutation prevention and protection against commonly encountered DNA damaging agents in Mycobacterium smegmatis. Microbiol. Read. Engl., 2010, 156(Pt 3), 940-949.
[22]
Talaat, A.M.; Ward, S.K.; Wu, C-W.; Rondon, E.; Tavano, C.; Bannantine, J.P.; Lyons, R.; Johnston, S.A. Mycobacterial Bacilli are metabolically active during chronic tuberculosis in murine lungs: insights from genome-wide transcriptional profiling. J. Bacteriol., 2007, 189(11), 4265-4274.
[23]
Puri, R.V.; Singh, N.; Gupta, R.K.; Tyagi, A.K.; Endonuclease, I.V.; Endonuclease, I.V. Is the major apurinic/apyrimidinic endonuclease in Mycobacterium tuberculosis and is important for protection against oxidative damage. PLoS One, 2013, 8(8), e71535.
[24]
Wiid, I.; Grundlingh, R.; Bourn, W.; Bradley, G.; Harington, A.; Hoal-van Helden, E.G.; van Helden, P.O. (6)-alkylguanine-DNA alkyltransferase DNA repair in mycobacteria: pathogenic and non-pathogenic species differ. Tuberculosis (Edinb.), 2002, 82(2-3), 45-53.
[25]
Boshoff, H.I.; Myers, T.G.; Copp, B.R.; McNeil, M.R.; Wilson, M.A.; Barry, C.E., III The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem., 2004, 279(38), 40174-40184.
[26]
Schnappinger, D.; Ehrt, S.; Voskuil, M.I.; Liu, Y.; Mangan, J.A.; Monahan, I.M.; Dolganov, G.; Efron, B.; Butcher, P.D.; Nathan, C.; Schoolnik, G.K. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: Insights into the phagosomal environment. J. Exp. Med., 2003, 198(5), 693-704.
[27]
Durbach, S.I.; Springer, B.; Machowski, E.E.; North, R.J.; Papavinasasundaram, K.G.; Colston, M.J.; Böttger, E.C.; Mizrahi, V. DNA alkylation damage as a sensor of nitrosative stress in Mycobacterium tuberculosis. Infect. Immun., 2003, 71(2), 997-1000.
[28]
Wanner, R.M.; Castor, D.; Güthlein, C.; Böttger, E.C.; Springer, B.; Jiricny, J. The uracil DNA glycosylase UdgB of Mycobacterium smegmatis protects the organism from the mutagenic effects of cytosine and adenine deamination. J. Bacteriol., 2009, 191(20), 6312-6319.
[29]
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.), 2007, 6(12), 1774-1785.
[30]
Kurthkoti, K.; Srinath, T.; Kumar, P.; Malshetty, V.S.; Sang, P.B.; Jain, R.; Manjunath, R.; Varshney, U. A distinct physiological role of MutY in mutation prevention in mycobacteria. Microbiol. Read. Engl., 2010, 156(Pt 1), 88-93.
[31]
Nouvel, L.X.; Kassa-Kelembho, E.; Dos Vultos, T.; Zandanga, G.; Rauzier, J.; Lafoz, C.; Martin, C.; Blazquez, J.; Talarmin, A.; Gicquel, B. Multidrug-resistant Mycobacterium tuberculosis, Bangui, Central African Republic. Emerg. Infect. Dis., 2006, 12(9), 1454-1456.
[32]
Ebrahimi-Rad, M.; Bifani, P.; Martin, C.; Kremer, K.; Samper, S.; Rauzier, J.; Kreiswirth, B.; Blazquez, J.; Jouan, M.; van Soolingen, D.; Gicquel, B. Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family. Emerg. Infect. Dis., 2003, 9(7), 838-845.
[33]
Olano, J.; López, B.; Reyes, A.; Lemos, M.P.; Correa, N.; Del Portillo, P.; Barrera, L.; Robledo, J.; Ritacco, V.; Zambrano, M.M. Mutations in DNA repair genes are associated with the Haarlem lineage of Mycobacterium tuberculosis independently of their antibiotic resistance. Tuberculosis (Edinb.), 2007, 87(6), 502-508.
[34]
Lari, N.; Rindi, L.; Bonanni, D.; Tortoli, E.; Garzelli, C. Mutations in mutT genes of Mycobacterium tuberculosis isolates of Beijing genotype. J. Med. Microbiol., 2006, 55(Pt 5), 599-603.
[35]
Houghton, J.; Townsend, C.; Williams, A.R.; Rodgers, A.; Rand, L.; Walker, K.B.; Böttger, E.C.; Springer, B.; Davis, E.O. Important role for Mycobacterium tuberculosis UvrD1 in pathogenesis and persistence apart from its function in nucleotide excision repair. J. Bacteriol., 2012, 194(11), 2916-2923.
[36]
Graham, J.E.; Clark-Curtiss, J.E. Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc. Natl. Acad. Sci. USA, 1999, 96(20), 11554-11559.
[37]
Rossi, F.; Khanduja, J.S.; Bortoluzzi, A.; Houghton, J.; Sander, P.; Güthlein, C.; Davis, E.O.; Springer, B.; Böttger, E.C.; Relini, A.; Penco, A.; Muniyappa, K.; Rizzi, M. The biological and structural characterization of Mycobacterium tuberculosis UvrA provides novel insights into its mechanism of action. Nucleic Acids Res., 2011, 39(16), 7316-7328.
[38]
Darwin, K.H.; Nathan, C.F. Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun., 2005, 73(8), 4581-4587.
[39]
Güthlein, C.; Wanner, R.M.; Sander, P.; Davis, E.O.; Bosshard, M.; Jiricny, J.; Böttger, E.C.; Springer, B. Characterization of the mycobacterial NER system reveals novel functions of the uvrD1 helicase. J. Bacteriol., 2009, 191(2), 555-562.
[40]
Lamichhane, G.; Zignol, M.; Blades, N.J.; Geiman, D.E.; Dougherty, A.; Grosset, J.; Broman, K.W.; Bishai, W.R. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA, 2003, 100(12), 7213-7218.
[41]
Griffin, J.E.; Gawronski, J.D.; Dejesus, M.A.; Ioerger, T.R.; Akerley, B.J.; Sassetti, C.M. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog., 2011, 7(9), e1002251.
[42]
Rengarajan, J.; Bloom, B.R.; Rubin, E.J. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc. Natl. Acad. Sci. USA, 2005, 102(23), 8327-8332.
[43]
Parulekar, R.S.; Barage, S.H.; Jalkute, C.B.; Dhanavade, M.J.; Fandilolu, P.M.; Sonawane, K.D. Homology modeling, molecular docking and DNA binding studies of nucleotide excision repair UvrC protein from M. tuberculosis. Protein J., 2013, 32(6), 467-476.
[44]
Sinha, K.M.; Stephanou, N.C.; Unciuleac, M-C.; Glickman, M.S.; Shuman, S. Domain requirements for DNA unwinding by mycobacterial UvrD2, an essential DNA helicase. Biochemistry, 2008, 47(36), 9355-9364.
[45]
Williams, A.; Güthlein, C.; Beresford, N.; Böttger, E.C.; Springer, B.; Davis, E.O. UvrD2 is essential in Mycobacterium tuberculosis, but its helicase activity is not required. J. Bacteriol., 2011, 193(17), 4487-4494.
[46]
Kazarian, K.; Cassani, C.; Rizzi, M. Expression, purification and characterization of UvrD2 helicase from Mycobacterium tuberculosis. Protein Expr. Purif., 2010, 69(2), 215-218.
[47]
Mazloum, N.; Stegman, M.A.; Croteau, D.L.; Van Houten, B.; Kwon, N.S.; Ling, Y.; Dickinson, C.; Venugopal, A.; Towheed, M.A.; Nathan, C. Identification of a chemical that inhibits the mycobacterial UvrABC complex in nucleotide excision repair. Biochemistry, 2011, 50(8), 1329-1335.
[48]
Watkins, H.A.; Baker, E.N. Structural and functional characterization of an RNase HI domain from the bifunctional protein Rv2228c from Mycobacterium tuberculosis. J. Bacteriol., 2010, 192(11), 2878-2886.
[49]
Minias, A.E.; Brzostek, A.M.; Korycka-Machala, M.; Dziadek, B.; Minias, P.; Rajagopalan, M.; Madiraju, M.; Dziadek, J. RNase HI is essential for survival of Mycobacterium smegmatis. PLoS One, 2015, 10(5), e0126260.
[50]
Gupta, R.; Chatterjee, D.; Glickman, M.S.; Shuman, S. Division of labor among Mycobacterium smegmatis RNase H enzymes: RNase H1 activity of RnhA or RnhC is essential for growth whereas RnhB and RnhA guard against killing by hydrogen peroxide in stationary phase. Nucleic Acids Res., 2017, 45(1), 1-14.
[51]
Gupta, R.; Barkan, D.; Redelman-Sidi, G.; Shuman, S.; Glickman, M.S. Mycobacteria exploit three genetically distinct DNA double-strand break repair pathways. Mol. Microbiol., 2011, 79(2), 316-330.
[52]
Gupta, R.; Unciuleac, M-C.; Shuman, S.; Glickman, M.S. Homologous recombination mediated by the mycobacterial AdnAB helicase without end resection by the AdnAB nucleases. Nucleic Acids Res., 2017, 45(2), 762-774.
[53]
Waddell, S.J.; Stabler, R.A.; Laing, K.; Kremer, L.; Reynolds, R.C.; Besra, G.S. The use of microarray analysis to determine the gene expression profiles of Mycobacterium tuberculosis in response to anti-bacterial compounds. Tuberculosis (Edinb.), 2004, 84(3-4), 263-274.
[54]
Datta, S.; Prabu, M.M.; Vaze, M.B.; Ganesh, N.; Chandra, N.R.; Muniyappa, K.; Vijayan, M. Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-AlF(4): implications for decreased ATPase activity and molecular aggregation. Nucleic Acids Res., 2000, 28(24), 4964-4973.
[55]
Chandran, A.V.; Prabu, J.R.; Nautiyal, A.; Patil, K.N.; Muniyappa, K.; Vijayan, M. Structural studies on Mycobacterium tuberculosis RecA: molecular plasticity and interspecies variability. J. Biosci., 2015, 40(1), 13-30.
[56]
Szulc-Kielbik, I.; Brzezinska, M.; Kielbik, M.; Brzostek, A.; Dziadek, J.; Kania, K.; Sulowska, Z.; Krupa, A.; Klink, M. Mycobacterium tuberculosis RecA is indispensable for inhibition of the mitogen-activated protein kinase-dependent bactericidal activity of THP-1-derived macrophages in vitro. FEBS J., 2015, 282(7), 1289-1306.
[57]
Brzostek, A.; Szulc, I.; Klink, M.; Brzezinska, M.; Sulowska, Z.; Dziadek, J. Either non-homologous ends joining or homologous recombination is required to repair double-strand breaks in the genome of macrophage-internalized Mycobacterium tuberculosis. PLoS One, 2014, 9(3), e92799.
[58]
Heaton, B.E.; Barkan, D.; Bongiorno, P.; Karakousis, P.C.; Glickman, M.S. Deficiency of double-strand DNA break repair does not impair Mycobacterium tuberculosis virulence in multiple animal models of infection. Infect. Immun., 2014, 82(8), 3177-3185.
[59]
Sander, P.; Papavinasasundaram, K.G.; Dick, T.; Stavropoulos, E.; Ellrott, K.; Springer, B.; Colston, M.J.; Böttger, E.C. Mycobacterium bovis BCG recA deletion mutant shows increased susceptibility to DNA-damaging agents but wild-type survival in a mouse infection model. Infect. Immun., 2001, 69(6), 3562-3568.
[60]
Mo, C.Y.; Manning, S.A.; Roggiani, M.; Culyba, M.J.; Samuels, A.N.; Sniegowski, P.D.; Goulian, M.; Kohli, R.M. Systematically altering bacterial SOS activity under stress reveals therapeutic strategies for potentiating antibiotics. MSphere, 2016, 1(4), 1.
[61]
Alam, M.K.; Alhhazmi, A.; DeCoteau, J.F.; Luo, Y.; Geyer, C.R. RecA inhibitors potentiate antibiotic activity and block evolution of antibiotic resistance. Cell Chem. Biol., 2016, 23(3), 381-391.
[62]
Nautiyal, A.; Patil, K.N.; Muniyappa, K. Suramin is a potent and selective inhibitor of Mycobacterium tuberculosis RecA protein and the SOS response: RecA as a potential target for antibacterial drug discovery. J. Antimicrob. Chemother., 2014, 69(7), 1834-1843.
[63]
Zhang, L.; Zheng, Y.; Callahan, B.; Belfort, M.; Liu, Y. Cisplatin inhibits protein splicing, suggesting inteins as therapeutic targets in mycobacteria. J. Biol. Chem., 2011, 286(2), 1277-1282.
[64]
Rienksma, R.A.; Suarez-Diez, M.; Mollenkopf, H-J.; Dolganov, G.M.; Dorhoi, A.; Schoolnik, G.K.; Martins Dos Santos, V.A.; Kaufmann, S.H.; Schaap, P.J.; Gengenbacher, M. Comprehensive insights into transcriptional adaptation of intracellular mycobacteria by microbe-enriched dual RNA sequencing. BMC Genomics, 2015, 16, 34.
[65]
Namouchi, A.; Gómez-Muñoz, M.; Frye, S.A.; Moen, L.V.; Rognes, T.; Tønjum, T.; Balasingham, S.V. The Mycobacterium tuberculosis transcriptional landscape under genotoxic stress. BMC Genomics, 2016, 17(1), 791.
[66]
Long, Q.; Du, Q.; Fu, T.; Drlica, K.; Zhao, X.; Xie, J. Involvement of Holliday junction resolvase in fluoroquinolone-mediated killing of Mycobacterium smegmatis. Antimicrob. Agents Chemother., 2015, 59(3), 1782-1785.
[67]
Prabu, J.R.; Thamotharan, S.; Khanduja, J.S.; Alipio, E.Z.; Kim, C-Y.; Waldo, G.S.; Terwilliger, T.C.; Segelke, B.; Lekin, T.; Toppani, D.; Hung, L-W.; Yu, M.; Bursey, E.; Muniyappa, K.; Chandra, N.R.; Vijayan, M. Structure of Mycobacterium tuberculosis RuvA, a protein involved in recombination. Acta Crystallograph. Sect. F Struct. Biol. Cryst. Commun., 2006, 62(Pt 8), 731-734.
[68]
Prabu, J.R.; Thamotharan, S.; Khanduja, J.S.; Chandra, N.R.; Muniyappa, K.; Vijayan, M. Crystallographic and modelling studies on Mycobacterium tuberculosis RuvA Additional role of RuvB-binding domain and inter species variability. Biochim. Biophys. Acta, 2009, 1794(7), 1001-1009.
[69]
Glickman, M.S. Double-strand DNA break repair in mycobacteria. Microbiol. Spectr., 2014, 2(5), 2.
[70]
Lieber, M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 2010, 79, 181-211.
[71]
Della, M.; Palmbos, P.L.; Tseng, H-M.; Tonkin, L.M.; Daley, J.M.; Topper, L.M.; Pitcher, R.S.; Tomkinson, A.E.; Wilson, T.E.; Doherty, A.J. Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science, 2004, 306(5696), 683-685.
[72]
Weller, G.R.; Kysela, B.; Roy, R.; Tonkin, L.M.; Scanlan, E.; Della, M.; Devine, S.K.; Day, J.P.; Wilkinson, A.; d’Adda di Fagagna, F.; Devine, K.M.; Bowater, R.P.; Jeggo, P.A.; Jackson, S.P.; Doherty, A.J. Identification of a DNA nonhomologous end-joining complex in bacteria. Science, 2002, 297(5587), 1686-1689.
[73]
Korycka-Machala, M.; Brzostek, A.; Rozalska, S.; Rumijowska-Galewicz, A.; Dziedzic, R.; Bowater, R.; Dziadek, J. Distinct DNA repair pathways involving RecA and nonhomologous end joining in Mycobacterium smegmatis. FEMS Microbiol. Lett., 2006, 258(1), 83-91.
[74]
Pitcher, R.S.; Brissett, N.C.; Picher, A.J.; Andrade, P.; Juarez, R.; Thompson, D.; Fox, G.C.; Blanco, L.; Doherty, A.J. Structure and function of a mycobacterial NHEJ DNA repair polymerase. J. Mol. Biol., 2007, 366(2), 391-405.
[75]
Stephanou, N.C.; Gao, F.; Bongiorno, P.; Ehrt, S.; Schnappinger, D.; Shuman, S.; Glickman, M.S. Mycobacterial nonhomologous end joining mediates mutagenic repair of chromosomal double-strand DNA breaks. J. Bacteriol., 2007, 189(14), 5237-5246.
[76]
Bowater, R.; Doherty, A.J. Making ends meet: repairing breaks in bacterial DNA by non-homologous end-joining. PLoS Genet., 2006, 2(2), e8.
[77]
Weller, G.R.; Doherty, A.J. A family of DNA repair ligases in bacteria? FEBS Lett., 2001, 505(2), 340-342.
[78]
Akey, D.; Martins, A.; Aniukwu, J.; Glickman, M.S.; Shuman, S.; Berger, J.M. Crystal structure and nonhomologous end-joining function of the ligase component of Mycobacterium DNA ligase D. J. Biol. Chem., 2006, 281(19), 13412-13423.
[79]
Padiadpu, J.; Vashisht, R.; Chandra, N. Protein-protein interaction networks suggest different targets have different propensities for triggering drug resistance. Syst. Synth. Biol., 2010, 4(4), 311-322.
[80]
Ilina, E.N.; Shitikov, E.A.; Ikryannikova, L.N.; Alekseev, D.G.; Kamashev, D.E.; Malakhova, M.V.; Parfenova, T.V.; Afanas’ev, M.V.; Ischenko, D.S.; Bazaleev, N.A.; Smirnova, T.G.; Larionova, E.E.; Chernousova, L.N.; Beletsky, A.V.; Mardanov, A.V.; Ravin, N.V.; Skryabin, K.G.; Govorun, V.M. Comparative genomic analysis of Mycobacterium tuberculosis drug resistant strains from Russia. PLoS One, 2013, 8(2), e56577.
[81]
Raman, K.; Yeturu, K.; Chandra, N. targetTB: a target identification pipeline for Mycobacterium tuberculosis through an interactome, reactome and genome-scale structural analysis. BMC Syst. Biol., 2008, 2, 109.
[82]
Gordhan, B.G.; Andersen, S.J.; De Meyer, A.R.; Mizrahi, V. Construction by homologous recombination and phenotypic characterization of a DNA polymerase domain polA mutant of Mycobacterium smegmatis. Gene, 1996, 178(1-2), 125-130.
[83]
Talaat, A.M.; Lyons, R.; Howard, S.T.; Johnston, S.A. The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc. Natl. Acad. Sci. USA, 2004, 101(13), 4602-4607.
[84]
Warner, D.F.; Ndwandwe, D.E.; Abrahams, G.L.; Kana, B.D.; Machowski, E.E.; Venclovas, C.; Mizrahi, V. Essential roles for imuA′- and imuB-encoded accessory factors in DnaE2-dependent mutagenesis in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA, 2010, 107(29), 13093-13098.
[85]
Boshoff, H.I.; Reed, M.B.; Barry, C.E., III; Mizrahi, V. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. Cell, 2003, 113(2), 183-193.
[86]
Keren, I.; Minami, S.; Rubin, E.; Lewis, K. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. MBio, 2011, 2(3), e00100-e00111.
[87]
Jadaun, A.; Sudhakar, D.R.; Subbarao, N.; Dixit, A. In silico screening for novel inhibitors of DNA polymerase III alpha subunit of Mycobacterium tuberculosis (MtbDnaE2, H37Rv). PLoS One, 2015, 10(3), e0119760.
[88]
Gobec, S.; Plantan, I.; Mravljak, J.; Wilson, R.A.; Besra, G.S.; Kikelj, D. Phosphonate inhibitors of antigen 85C, a crucial enzyme involved in the biosynthesis of the Mycobacterium tuberculosis cell wall. Bioorg. Med. Chem. Lett., 2004, 14(13), 3559-3562.
[89]
Sriram, D.; Yogeeswari, P.; Srichakravarthy, N.; Bal, T.R. Synthesis of stavudine amino acid ester prodrugs with broad-spectrum chemotherapeutic properties for the effective treatment of HIV/AIDS. Bioorg. Med. Chem. Lett., 2004, 14(5), 1085-1087.
[90]
Chhabra, G.; Dixit, A.; Garg, C. L. DNA polymerase III α subunit from Mycobacterium tuberculosis H37Rv: Homology modeling and molecular docking of its inhibitor. Bioinformation, 2011, 6(2), 69-73.
[91]
Rock, J.M.; Lang, U.F.; Chase, M.R.; Ford, C.B.; Gerrick, E.R.; Gawande, R.; Coscolla, M.; Gagneux, S.; Fortune, S.M.; Lamers, M.H. DNA replication fidelity in Mycobacterium tuberculosis is mediated by an ancestral prokaryotic proofreader. Nat. Genet., 2015, 47(6), 677-681.
[92]
Castañeda-García, A.; Prieto, A.I.; Rodríguez-Beltrán, J.; Alonso, N.; Cantillon, D.; Costas, C.; Pérez-Lago, L.; Zegeye, E.D.; Herranz, M.; Plociński, P.; Tonjum, T.; García de Viedma, D.; Paget, M.; Waddell, S.J.; Rojas, A.M.; Doherty, A.J.; Blázquez, J. A non-canonical mismatch repair pathway in prokaryotes. Nat. Commun., 2017, 8, 14246.
[93]
Goodman, M.F. Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem., 2002, 71, 17-50.
[94]
Karakousis, P.C.; Williams, E.P.; Bishai, W.R. Altered expression of isoniazid-regulated genes in drug-treated dormant Mycobacterium tuberculosis. J. Antimicrob. Chemother., 2008, 61(2), 323-331.
[95]
Kana, B.D.; Abrahams, G.L.; Sung, N.; Warner, D.F.; Gordhan, B.G.; Machowski, E.E.; Tsenova, L.; Sacchettini, J.C.; Stoker, N.G.; Kaplan, G.; Mizrahi, V. Role of the DinB homologs Rv1537 and Rv3056 in Mycobacterium tuberculosis. J. Bacteriol., 2010, 192(8), 2220-2227.
[96]
Ordonez, H.; Uson, M.L.; Shuman, S. Characterization of three mycobacterial DinB (DNA polymerase IV) paralogs highlights DinB2 as naturally adept at ribonucleotide incorporation. Nucleic Acids Res., 2014, 42(17), 11056-11070.
[97]
Ordonez, H.; Shuman, S. Mycobacterium smegmatis DinB2 misincorporates deoxyribonucleotides and ribonucleotides during templated synthesis and lesion bypass. Nucleic Acids Res., 2014, 42(20), 12722-12734.
[98]
Foti, J.J.; Devadoss, B.; Winkler, J.A.; Collins, J.J.; Walker, G.C. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science, 2012, 336(6079), 315-319.
[99]
Wilkinson, A.; Day, J.; Bowater, R. Bacterial DNA ligases. Mol. Microbiol., 2001, 40(6), 1241-1248.
[102]
Sriskanda, V.; Moyer, R.W.; Shuman, S. NAD+-dependent DNA ligase encoded by a eukaryotic virus. J. Biol. Chem., 2001, 276(39), 36100-36109.
[103]
Khanam, T.; Ramachandran, R. Exploiting bacterial DNA repair systems as drug targets: a review of the current scenario with focus on mycobacteria. J. Indian Inst. Sci., 2014, 94(1), 149-168.
[104]
Lehman, I.R. DNA ligase: structure, mechanism, and function. Science, 1974, 186(4166), 790-797.
[105]
Gong, C.; Martins, A.; Bongiorno, P.; Glickman, M.; Shuman, S. Biochemical and genetic analysis of the four DNA ligases of mycobacteria. J. Biol. Chem., 2004, 279(20), 20594-20606.
[106]
Srivastava, S.K.; Dube, D.; Tewari, N.; Dwivedi, N.; Tripathi, R.P.; Ramachandran, R. Mycobacterium tuberculosis NAD+-dependent DNA ligase is selectively inhibited by glycosylamines compared with human DNA ligase I. Nucleic Acids Res., 2005, 33(22), 7090-7101.
[107]
Srivastava, S.K.; Tripathi, R.P.; Ramachandran, R. NAD+-dependent DNA Ligase (Rv3014c) from Mycobacterium tuberculosis. Crystal structure of the adenylation domain and identification of novel inhibitors. J. Biol. Chem., 2005, 280(34), 30273-30281.
[108]
Korycka-Machala, M.; Rychta, E.; Brzostek, A.; Sayer, H.R.; Rumijowska-Galewicz, A.; Bowater, R.P.; Dziadek, J. Evaluation of NAD(+) -dependent DNA ligase of mycobacteria as a potential target for antibiotics. Antimicrob. Agents Chemother., 2007, 51(8), 2888-2897.
[109]
Ciarrocchi, G.; MacPhee, D.G.; Deady, L.W.; Tilley, L. Specific inhibition of the eubacterial DNA ligase by arylamino compounds. Antimicrob. Agents Chemother., 1999, 43(11), 2766-2772.
[110]
Brötz-Oesterhelt, H.; Knezevic, I.; Bartel, S.; Lampe, T.; Warnecke-Eberz, U.; Ziegelbauer, K.; Häbich, D.; Labischinski, H. Specific and potent inhibition of NAD+-dependent DNA ligase by pyridochromanones. J. Biol. Chem., 2003, 278(41), 39435-39442.
[111]
Mills, S.D.; Eakin, A.E.; Buurman, E.T.; Newman, J.V.; Gao, N.; Huynh, H.; Johnson, K.D.; Lahiri, S.; Shapiro, A.B.; Walkup, G.K.; Yang, W.; Stokes, S.S. Novel bacterial NAD+-dependent DNA ligase inhibitors with broad-spectrum activity and antibacterial efficacy in vivo. Antimicrob. Agents Chemother., 2011, 55(3), 1088-1096.
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