Login Register Cart 0
Generic placeholder image

Infectious Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5265
ISSN (Online): 2212-3989

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Toxin–Antitoxin Systems and their Role in Maintaining the Pathogenic Potential of Causative Agents of Sapronoses

Author(s): Boris G. Andryukov*, Larisa M. Somova, Nellie F. Timchenko, Marina P. Bynina and Irina N. Lyapun

Volume 20, Issue 5, 2020

Page: [570 - 584] Pages: 15

DOI: 10.2174/1871526519666190715150444

Price: $65

Abstract

In interepidemic periods, causative agents of sapronoses typically employ a variety of mechanisms for maintaining the viability in terrestrial parasitic systems, associated with different adaptive strategies and utilized by their populations to survive. Unlike spore-forming bacteria, causative agents of sapronoses form resistant cell forms: viable but nonculturable (VBNC) cells and persistence (dormant) cells. The implementation of these strategies is mediated by the influence of various stressors of the environment and is characterized by a decrease in metabolism, a change in the morphology and physiology of the bacterial cell, and also the cessation of its replication. While most of the bacterial population is killed under antibiotic exposure, this fraction of pathogens transiently exhibits a phenotypic multidrug-tolerance, causing relapses and chronic courses of many sapronoses. It is important to note that when these resistant cell forms retain virulence and when favorable conditions occur, they are again transformed into active vegetative forms. For this reason, understanding mechanisms, allowing a fraction of the bacterial population to acquire transiently multidrug-tolerance represents an essential step to eradicate these dormant populations. The discovery of the genetic modules of bacterial toxin-antitoxin systems (TAS) in recent years, was proposed to be an ideal and promising candidate to control these complex regulatory molecular mechanisms. Overexpression of the toxins often increases persister frequency in a defined population. In this review, we summarize the scientific data regarding the TAS modules involved in bacterial persistence to be used as antibiotics for the conservation of the pathogenic potential of resistant forms of pathogens of natural focal sapronosis in interepidemic periods.

Keywords: Toxin–antitoxin systems (TAS), toxin–antitoxin genetic module, sapronoses, resistant (dormant) cell form of bacteria, viable but nonculturable (VBNC) cell, persistence, antibiotic resistance.

[1]
Chen, S.; Thompson, K.M.; Francis, M.S. Environmental Regulation of Yersinia Pathophysiology. Front. Cell. Infect. Microbiol., 2016, 6, 25.
[http://dx.doi.org/10.3389/fcimb.2016.00025] [PMID: 26973818]
[2]
Dynamical Systems and Their Applications in BiologyUSA; Providence, Rhode Island, 2001.
[3]
Hubálek, Z.; Rudolf, I. Microbial Zoonoses and Sapronoses; Springer Science & Business Media B.V., 2011, p. 456.
[4]
Kuris, A.M.; Lafferty, K.D.; Sokolow, S.H. Sapronosis: a distinctive type of infectious agent. Trends Parasitol., 2014, 30(8), 386-393.
[http://dx.doi.org/10.1016/j.pt.2014.06.006] [PMID: 25028088]
[5]
Prosser, J.I.; Bohannan, B.J.M.; Curtis, T.P.; Ellis, R.J.; Firestone, M.K.; Freckleton, R.P.; Green, J.L.; Green, L.E.; Killham, K.; Lennon, J.J.; Osborn, A.M.; Solan, M.; van der Gast, C.J.; Young, J.P. The role of ecological theory in microbial ecology. Nat. Rev. Microbiol., 2007, 5(5), 384-392.
[http://dx.doi.org/10.1038/nrmicro1643] [PMID: 17435792]
[6]
Adgamov, R.R.; Timchenko, N.F.; Zaitseva, E.A. Ecological and genetic mechanisms of development of epidemiologically significant strains of sapronoses causative agents. Biol. Bull. Rev., 2013, 3(2), 125-138.
[http://dx.doi.org/10.1134/S2079086413020023]
[7]
van der Does, H.C.; Rep, M. Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol. Plant Microbe Interact., 2007, 20(10), 1175-1182.
[http://dx.doi.org/10.1094/MPMI-20-10-1175] [PMID: 17918619]
[8]
Mecsas, J.; Raupach, B.; Falkow, S. The Yersinia Yops inhibit invasion of Listeria, Shigella and Edwardsiella but not Salmonella into epithelial cells. Mol. Microbiol., 1998, 28(6), 1269-1281.
[http://dx.doi.org/10.1046/j.1365-2958.1998.00891.x] [PMID: 9680215]
[9]
Kędzierska, B.; Hayes, F. Emerging Roles of Toxin-Antitoxin Modules in Bacterial Pathogenesis. Molecules, 2016, 21(6), 21.
[http://dx.doi.org/10.3390/molecules21060790] [PMID: 27322231]
[10]
Van Melderen, L.; Saavedra De Bast, M. Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet., 2009, 5(3)e1000437
[http://dx.doi.org/10.1371/journal.pgen.1000437] [PMID: 19325885]
[11]
Bong-Jin Lee Structure, Biology, and Therapeutic Application of Toxin–Antitoxin Systems in Pathogenic Bacteria. Toxins (Basel), 2016, 8(10), 305.
[http://dx.doi.org/10.3390/toxins8100305]
[12]
Goeders, N.; Chai, R.; Chen, B.; Day, A.; Salmond, G.P. Structure, Evolution, and Functions of Bacterial Type III Toxin-Antitoxin Systems. Toxins (Basel), 2016, 8(10), 282.
[http://dx.doi.org/10.3390/toxins8100282] [PMID: 27690100]
[13]
Wang, X.; Wood, T.K. Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Appl. Environ. Microbiol., 2011, 77(16), 5577-5583.
[http://dx.doi.org/10.1128/AEM.05068-11] [PMID: 21685157]
[14]
Coussens, N.P.; Daines, D.A. Wake me when it’s over - Bacterial toxin-antitoxin proteins and induced dormancy. Exp. Biol. Med. (Maywood), 2016, 241(12), 1332-1342.
[http://dx.doi.org/10.1177/1535370216651938] [PMID: 27216598]
[15]
Anisimov, A.P.; Lindler, L.E.; Pier, G.B. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev., 2004, 17(2), 434-464.
[http://dx.doi.org/10.1128/CMR.17.2.434-464.2004] [PMID: 15084509]
[16]
Lennon, J.T.; Jones, S.E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol., 2011, 9(2), 119-130.
[http://dx.doi.org/10.1038/nrmicro2504] [PMID: 21233850]
[17]
Holden, D.W. Microbiology. Persisters unmasked. Science, 2015, 347(6217), 30-32.
[http://dx.doi.org/10.1126/science.1262033] [PMID: 25554777]
[18]
Maisonneuve, E.; Castro-Camargo, M.; Gerdes, K. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell, 2013, 154(5), 1140-1150.
[http://dx.doi.org/10.1016/j.cell.2013.07.048] [PMID: 23993101]
[19]
Gerdes, K.; Maisonneuve, E. Remarkable functional convergence: Alarmone ppGpp mediates persistence by activating type I and II toxin-antitoxins. Mol. Cell, 2015, 59(1), 1-3.
[http://dx.doi.org/10.1016/j.molcel.2015.06.019] [PMID: 26140365]
[20]
Meredith, H.R.; Srimani, J.K.; Lee, A.J.; Lopatkin, A.J.; You, L. Collective antibiotic tolerance: mechanisms, dynamics and intervention. Nat. Chem. Biol., 2015, 11(3), 182-188.
[http://dx.doi.org/10.1038/nchembio.1754] [PMID: 25689336]
[21]
Fasani, R.A.; Savageau, M.A. Unrelated toxin-antitoxin systems cooperate to induce persistence. J. R. Soc. Interface, 2015, 12(108)20150130
[http://dx.doi.org/10.1098/rsif.2015.0130] [PMID: 26063817]
[22]
Bigger, J.W. Treatment of staphylococcal infections with penicillin by intermittent sterilization. Lancet, 1944, 294, 497-500.
[http://dx.doi.org/10.1016/S0140-6736(00)74210-3]
[23]
Li, L.; Mendis, N.; Trigui, H.; Oliver, J.D.; Faucher, S.P. The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol., 2014, 5, 258.
[http://dx.doi.org/10.3389/fmicb.2014.00258] [PMID: 24917854]
[24]
Balaban, N.Q.; Merrin, J.; Chait, R.; Kowalik, L.; Leibler, S. Bacterial persistence as a phenotypic switch. Science, 2004, 305(5690), 1622-1625.
[http://dx.doi.org/10.1126/science.1099390] [PMID: 15308767]
[25]
Fisher, R.A.; Gollan, B.; Helaine, S. Persistent bacterial infections and persister cells. Nat. Rev. Microbiol., 2017, 15(8), 453-464.
[http://dx.doi.org/10.1038/nrmicro.2017.42] [PMID: 28529326]
[26]
Yang, Q.E.; Walsh, T.R. Toxin-antitoxin systems and their role in disseminating and maintaining antimicrobial resistance. FEMS Microbiol. Rev., 2017, 41(3), 343-353.
[http://dx.doi.org/10.1093/femsre/fux006] [PMID: 28449040]
[27]
Maisonneuve, E.; Shakespeare, L.J.; Jørgensen, M.G.; Gerdes, K. Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. USA, 2011, 108(32), 13206-13211.
[http://dx.doi.org/10.1073/pnas.1100186108] [PMID: 21788497]
[28]
Maisonneuve, E.; Gerdes, K. Molecular mechanisms underlying bacterial persisters. Cell, 2014, 157(3), 539-548.
[http://dx.doi.org/10.1016/j.cell.2014.02.050] [PMID: 24766804]
[29]
Oliver, J.D. The viable but nonculturable state in bacteria. J. Microbiol., 2005, 43(Spec No), 93-100.
[30]
Oliver, J.D. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev., 2010, 34(4), 415-425.
[http://dx.doi.org/10.1111/j.1574-6976.2009.00200.x] [PMID: 20059548]
[31]
Somova, L.M.; Buzoleva, L.S.; Plekhova, N.G. , 2009.
[32]
Nelson, E.J.; Chowdhury, A.; Flynn, J.; Schild, S.; Bourassa, L.; Shao, Y.; LaRocque, R.C.; Calderwood, S.B.; Qadri, F.; Camilli, A. Transmission of Vibrio cholerae is antagonized by lytic phage and entry into the aquatic environment. PLoS Pathog., 2008, 4(10)e1000187
[http://dx.doi.org/10.1371/journal.ppat.1000187] [PMID: 18949027]
[33]
Xu, H.S.; Roberts, N.; Singleton, F.L.; Attwell, R.W.; Grimes, D.J.; Colwell, R.R. Survival and viability of nonculturableEscherichia coli andVibrio cholerae in the estuarine and marine environment. Microb. Ecol., 1982, 8(4), 313-323.
[http://dx.doi.org/10.1007/BF02010671] [PMID: 24226049]
[34]
Chaveerach, P.; ter Huurne, A.A.; Lipman, L.J.; van Knapen, F. Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl. Environ. Microbiol., 2003, 69(1), 711-714.
[http://dx.doi.org/10.1128/AEM.69.1.711-714.2003] [PMID: 12514068]
[35]
Day, A.P.; Oliver, J.D. Changes in membrane fatty acid composition during entry of Vibrio vulnificus into the viable but nonculturable state. J. Microbiol., 2004, 42(2), 69-73.
[36]
Xiao, X.L.; Tian, C.; Yu, Y.G.; Wu, H. Detection of viable but nonculturable Escherichia coli O157:H7 using propidium monoazide treatments and qPCR. Can. J. Microbiol., 2013, 59(3), 157-163.
[http://dx.doi.org/10.1139/cjm-2012-0577] [PMID: 23540333]
[37]
Nowakowska, J.; Oliver, J.D. Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS Microbiol. Ecol., 2013, 84(1), 213-222.
[http://dx.doi.org/10.1111/1574-6941.12052] [PMID: 23228034]
[38]
Baffone, W.; Citterio, B.; Vittoria, E.; Casaroli, A.; Campana, R.; Falzano, L.; Donelli, G. Retention of virulence in viable but non-culturable halophilic Vibrio spp. Int. J. Food Microbiol., 2003, 89(1), 31-39.
[http://dx.doi.org/10.1016/S0168-1605(03)00102-8] [PMID: 14580971]
[39]
Van den Bergh, B.; Michiels, J.E.; Fauvart, M.; Michiels, J. Should we develop screens for multi-drug antibiotic tolerance? Expert Rev. Anti Infect. Ther., 2016, 14(7), 613-616.
[http://dx.doi.org/10.1080/14787210.2016.1194754] [PMID: 27227426]
[40]
Rivers, B.; Steck, T.R. Viable but nonculturable uropathogenic bacteria are present in the mouse urinary tract following urinary tract infection and antibiotic therapy. Urol. Res., 2001, 29(1), 60-66.
[http://dx.doi.org/10.1007/s002400000151] [PMID: 11310218]
[41]
Lleo, M.M.; Ghidini, V.; Tafi, M.C.; Castellani, F.; Trento, I.; Boaretti, M. Detecting the presence of bacterial DNA by PCR can be useful in diagnosing culture-negative cases of infection, especially in patients with suspected infection and antibiotic therapy. FEMS Microbiol. Lett., 2014, 354(2), 153-160.
[http://dx.doi.org/10.1111/1574-6968.12422] [PMID: 24627954]
[42]
Ayrapetyan, M.; Williams, T.C.; Oliver, J.D. Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios. Appl. Environ. Microbiol., 2014, 80(8), 2478-2483.
[http://dx.doi.org/10.1128/AEM.00080-14] [PMID: 24509922]
[43]
Ayrapetyan, M.; Williams, T.C.; Baxter, R.; Oliver, J.D. Viable but Nonculturable and Persister Cells Coexist Stochastically and Are Induced by Human Serum. Infect. Immun., 2015, 83(11), 4194-4203.
[http://dx.doi.org/10.1128/IAI.00404-15] [PMID: 26283335]
[44]
Ayrapetyan, M.; Williams, T.C.; Oliver, J.D. Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol., 2015, 23(1), 7-13.
[http://dx.doi.org/10.1016/j.tim.2014.09.004] [PMID: 25449050]
[45]
Belov, A.B.; Kuzin, A.A. Sapronous infections associated with the provision of medical care: problematic issues in the theory of epidemiology. Perm Medical Journal, 2017, 4(34), 94-102.
[46]
Belov, A.B.; Kulikalova, E.S. Sapronoses: ecology of pathogens, epidemiology and systematics. Epidemiology and Vaccine Prevention., 2016, 86(1), 5-16.
[http://dx.doi.org/10.31631/2073-3046-2016-15-1-5-16]
[47]
Brusinkina, E. Epidemiology of infections associated with the provision of medical care caused by pathogens of the group of sapronoses. Epidemiology and Vaccine Prevention, 2015, 81(2), 50-56.
[http://dx.doi.org/10.31631/2073-3046-2015-14-2-50-56]
[48]
Wood, T.K. Combatting bacterial persister cells. Biotechnol. Bioeng., 2016, 113(3), 476-483.
[PMID: 26264116] [http://dx.doi.org/10.1002/bit.25721]]
[49]
Pienaar, J.A.; Singh, A.; Barnard, T.G. The viable but non-culturable state in pathogenic Escherichia coli: A general review. Afr. J. Lab. Med., 2016, 5(1), 368.
[http://dx.doi.org/10.4102/ajlm.v5i1.368] [PMID: 28879110]
[50]
Hobby, G.L.; Meyer, K.; Chaffee, E. Observations on the mechanism of action of penicillin. Proc Soc Exp Biol NY, 1942, 50, 281-285.
[http://dx.doi.org/10.3181/00379727-50-13773]
[51]
Ogura, T.; Hiraga, S. Mini-F plasmid genes that couple host cell division to plasmid proliferation. Proc. Natl. Acad. Sci. USA, 1983, 80(15), 4784-4788.
[http://dx.doi.org/10.1073/pnas.80.15.4784] [PMID: 6308648]
[52]
Hayes, F. Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science, 2003, 301(5639), 1496-1499.
[http://dx.doi.org/10.1126/science.1088157] [PMID: 12970556]
[53]
Slava, S. Epstein; Springer: USA, 2009. [CrossRef]
[54]
Michiels, J.E.; Van den Bergh, B.; Verstraeten, N.; Michiels, J. Molecular mechanisms and clinical implications of bacterial persistence. Drug Resist. Updat., 2016, 29(148), 76-89.
[PMID: 27912845] [http://dx.doi.org/10.1016/j.drup.2016.10.002]]
[55]
Korch, S.B.; Hill, T.M. Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: effects on macromolecular synthesis and persister formation. J. Bacteriol., 2006, 188(11), 3826-3836.
[http://dx.doi.org/10.1128/JB.01740-05] [PMID: 16707675]
[56]
Brown, B.L.; Grigoriu, S.; Kim, Y.; Arruda, J.M.; Davenport, A.; Wood, T.K.; Peti, W.; Page, R. Three dimensional structure of the MqsR:MqsA complex: a novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties. PLoS Pathog., 2009, 5(12)e1000706
[http://dx.doi.org/10.1371/journal.ppat.1000706] [PMID: 20041169]
[57]
Kim, J-S.; Chowdhury, N.; Yamasaki, R.; Wood, T.K. Viable But Nonculturable and Persistence Describe the Same Bacterial Stress State. Environ. Microbiol., 2018, •••
[http://dx.doi.org/10.1111/1462-2920.14075]]
[58]
Page, R.; Peti, W. Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat. Chem. Biol., 2016, 12(4), 208-214.
[http://dx.doi.org/10.1038/nchembio.2044] [PMID: 26991085]
[59]
Christensen, S.K.; Maenhaut-Michel, G.; Mine, N.; Gottesman, S.; Gerdes, K.; Van Melderen, L. Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: involvement of the yefM-yoeB toxin-antitoxin system. Mol. Microbiol., 2004, 51(6), 1705-1717.
[PMID: 15009896] [http://dx.doi.org/10.1046/j.1365-2958.2003.03941.x]]
[60]
Bamford, R.A.; Smith, A.; Metz, J.; Glover, G.; Titball, R.W.; Pagliara, S. Investigating the physiology of viable but non-culturable bacteria by microfluidics and time-lapse microscopy. BMC Biol., 2017, 15(1), 121.
[http://dx.doi.org/10.1186/s12915-017-0465-4] [PMID: 29262826]
[61]
Moyed, H.S.; Bertrand, K.P. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol., 1983, 155(2), 768-775.
[PMID: 6348026]
[62]
Fozo, E.M.; Kawano, M.; Fontaine, F.; Kaya, Y.; Mendieta, K.S.; Jones, K.L.; Ocampo, A.; Rudd, K.E.; Storz, G. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol. Microbiol., 2008, 70(5), 1076-1093.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06394.x] [PMID: 18710431]
[63]
Vogel, J.; Argaman, L.; Wagner, E.G.; Altuvia, S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr. Biol., 2004, 14(24), 2271-2276.
[http://dx.doi.org/10.1016/j.cub.2004.12.003] [PMID: 15620655]
[64]
Unoson, C.; Wagner, E.G. A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli. Mol. Microbiol., 2008, 70(1), 258-270.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06416.x] [PMID: 18761622]
[65]
Vesper, O.; Amitai, S.; Belitsky, M.; Byrgazov, K.; Kaberdina, A.C.; Engelberg-Kulka, H.; Moll, I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell, 2011, 147(1), 147-157.
[http://dx.doi.org/10.1016/j.cell.2011.07.047] [PMID: 21944167]
[66]
Budde, P.P.; Davis, B.M.; Yuan, J.; Waldor, M.K. Characterization of a higBA toxin-antitoxin locus in Vibrio cholerae. J. Bacteriol., 2007, 189(2), 491-500.
[http://dx.doi.org/10.1128/JB.00909-06] [PMID: 17085558]
[67]
Fineran, P.C.; Blower, T.R.; Foulds, I.J.; Humphreys, D.P.; Lilley, K.S.; Salmond, G.P. The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc. Natl. Acad. Sci. USA, 2009, 106(3), 894-899.
[http://dx.doi.org/10.1073/pnas.0808832106] [PMID: 19124776]
[68]
Masuda, H.; Tan, Q.; Awano, N.; Wu, K.P.; Inouye, M. YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli. Mol. Microbiol., 2012, 84(5), 979-989.
[http://dx.doi.org/10.1111/j.1365-2958.2012.08068.x] [PMID: 22515815]
[69]
Wang, X.; Lord, D.M.; Cheng, H.Y.; Osbourne, D.O.; Hong, S.H.; Sanchez-Torres, V.; Quiroga, C.; Zheng, K.; Herrmann, T.; Peti, W.; Benedik, M.J.; Page, R.; Wood, T.K. A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS. Nat. Chem. Biol., 2012, 8(10), 855-861.
[http://dx.doi.org/10.1038/nchembio.1062] [PMID: 22941047]
[70]
Aakre, C.D.; Phung, T.N.; Huang, D.; Laub, M.T. A bacterial toxin inhibits DNA replication elongation through a direct interaction with the β sliding clamp. Mol. Cell, 2013, 52(5), 617-628.
[http://dx.doi.org/10.1016/j.molcel.2013.10.014] [PMID: 24239291]
[71]
Erental, A.; Sharon, I.; Engelberg-Kulka, H. Two programmed cell death systems in Escherichia coli: an apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol., 2012, 10(3)e1001281
[http://dx.doi.org/10.1371/journal.pbio.1001281] [PMID: 22412352]
[72]
Hall, A.M.; Gollan, B.; Helaine, S. Toxin-antitoxin systems: reversible toxicity. Curr. Opin. Microbiol., 2017, 36, 102-110.
[http://dx.doi.org/10.1016/j.mib.2017.02.003] [PMID: 28279904]
[73]
Lobato-Márquez, D.; Moreno-Córdoba, I.; Figueroa, V.; Díaz-Orejas, R.; García-del Portillo, F. Distinct type I and type II toxin-antitoxin modules control Salmonella lifestyle inside eukaryotic cells. Sci. Rep., 2015, 5, 9374.
[http://dx.doi.org/10.1038/srep09374] [PMID: 25792384]
[74]
Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct, 2009, 4, 19.
[http://dx.doi.org/10.1186/1745-6150-4-19] [PMID: 19493340]
[75]
Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res., 2013, 41(8), 4360-4377.
[http://dx.doi.org/10.1093/nar/gkt157] [PMID: 23470997]
[76]
Brantl, S.; Jahn, N. sRNAs in bacterial type I and type III toxin-antitoxin systems. FEMS Microbiol. Rev., 2015, 39(3), 413-427.
[http://dx.doi.org/10.1093/femsre/fuv003] [PMID: 25808661]
[77]
Conlon, B.P.; Nakayasu, E.S.; Fleck, L.E.; LaFleur, M.D.; Isabella, V.M.; Coleman, K.; Leonard, S.N.; Smith, R.D.; Adkins, J.N.; Lewis, K. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature, 2013, 503(7476), 365-370.
[http://dx.doi.org/10.1038/nature12790] [PMID: 24226776]
[78]
Kaspy, I.; Rotem, E.; Weiss, N.; Ronin, I.; Balaban, N.Q.; Glaser, G. HipA-mediated antibiotic persistence via phosphorylation of the glutamyl-tRNA-synthetase. Nat. Commun., 2013, 4, 3001.
[http://dx.doi.org/10.1038/ncomms4001] [PMID: 24343429]
[79]
Germain, E.; Castro-Roa, D.; Zenkin, N.; Gerdes, K. Molecular mechanism of bacterial persistence by HipA. Mol. Cell, 2013, 52(2), 248-254.
[http://dx.doi.org/10.1016/j.molcel.2013.08.045] [PMID: 24095282]
[80]
Keren, I.; Mulcahy, L.R.; Lewis, K. Persister eradication: lessons from the world of natural products. Methods Enzymol., 2012, 517, 387-406.
[http://dx.doi.org/10.1016/B978-0-12-404634-4.00019-X] [PMID: 23084949]
[81]
Brauner, A.; Fridman, O.; Gefen, O.; Balaban, N.Q. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat. Rev. Microbiol., 2016, 14(5), 320-330.
[http://dx.doi.org/10.1038/nrmicro.2016.34] [PMID: 27080241]
[82]
Brauner, A.; Shoresh, N.; Fridman, O.; Balaban, N.Q. An Experimental Framework for Quantifying Bacterial Tolerance. Biophys. J., 2017, 112(12), 2664-2671.
[http://dx.doi.org/10.1016/j.bpj.2017.05.014] [PMID: 28636922]
[83]
Ronneau, S.; Helaine, S. 2019.
[84]
Berghoff, B.A.; Wagner, E.G.H. RNA-based regulation in type I toxin-antitoxin systems and its implication for bacterial persistence. Curr. Genet., 2017, 63(6), 1011-1016.
[http://dx.doi.org/10.1007/s00294-017-0710-y] [PMID: 28560584]
[85]
Lewis, K. Platforms for antibiotic discovery. Nat. Rev. Drug Discov., 2013, 12(5), 371-387.
[http://dx.doi.org/10.1038/nrd3975] [PMID: 23629505]
[86]
Harms, A.; Fino, C.; Sørensen, M.A.; Semsey, S.; Gerdes, K. Prophages and Growth Dynamics Confound Experimental Results with Antibiotic-Tolerant Persister Cells. MBio, 2017, 8(6), e01964-e17.
[http://dx.doi.org/10.1128/mBio.01964-17] [PMID: 29233898]
[87]
Brooks, T.M.; Unterweger, D.; Bachmann, V.; Kostiuk, B.; Pukatzki, S. Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J. Biol. Chem., 2013, 288(11), 7618-7625.
[http://dx.doi.org/10.1074/jbc.M112.436725] [PMID: 23341465]
[88]
Van Melderen, L. Toxin-antitoxin systems: why so many, what for? Curr. Opin. Microbiol., 2010, 13(6), 781-785.
[http://dx.doi.org/10.1016/j.mib.2010.10.006] [PMID: 21041110]
[89]
Aizenman, E.; Engelberg-Kulka, H.; Glaser, G. An Escherichia coli chromosomal “addiction module” regulated by guanosine [corrected] 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl. Acad. Sci. USA, 1996, 93(12), 6059-6063.
[http://dx.doi.org/10.1073/pnas.93.12.6059] [PMID: 8650219]
[90]
Verstraeten, N.; Knapen, W.J.; Fauvart, M.; Michiels, J. Membrane depolarization-triggered responsive diversification leads to antibiotic tolerance. Microb. Cell, 2015, 2(8), 299-301.
[PMID: 28357305] [http://dx.doi.org/10.15698/mic2015.08.220]]
[91]
Mok, W.W.; Patel, N.H.; Li, Y. Decoding toxicity: deducing the sequence requirements of IbsC, a type I toxin in Escherichia coli. J. Biol. Chem., 2010, 285(53), 41627-41636.
[http://dx.doi.org/10.1074/jbc.M110.149179] [PMID: 20980267]
[92]
Wen, Y.; Behiels, E.; Devreese, B. Toxin-Antitoxin systems: their role in persistence, biofilm formation, and pathogenicity. Pathog. Dis., 2014, 70(3), 240-249.
[http://dx.doi.org/10.1111/2049-632X.12145] [PMID: 24478112]
[93]
Patra, P.; Klumpp, S. Population dynamics of bacterial persistence. PLoS One, 2013, 8(5)e62814
[http://dx.doi.org/10.1371/journal.pone.0062814] [PMID: 23675428]
[94]
Orman, M.A.; Brynildsen, M.P. Erratum: Inhibition of stationary phase respiration impairs persister formation in E. coli. Nat. Commun., 2016, 7, 10756.
[http://dx.doi.org/10.1038/ncomms10756] [PMID: 26883766]
[95]
Potgieter, M.; Bester, J.; Kell, D.B.; Pretorius, E. The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol. Rev., 2015, 39(4), 567-591.
[http://dx.doi.org/10.1093/femsre/fuv013] [PMID: 25940667]
[96]
Thakur, Z.; Dharra, R.; Saini, V.; Kumar, A.; Mehta, P.K. Insights from the protein-protein interaction network analysis of Mycobacterium tuberculosis toxin-antitoxin systems. Bioinformation, 2017, 13(11), 380-387.
[http://dx.doi.org/10.6026/97320630013380] [PMID: 29225431]
[97]
Nguyen, D.; Joshi-Datar, A.; Lepine, F.; Bauerle, E.; Olakanmi, O.; Beer, K.; McKay, G.; Siehnel, R.; Schafhauser, J.; Wang, Y.; Britigan, B.E.; Singh, P.K. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science, 2011, 334(6058), 982-986.
[http://dx.doi.org/10.1126/science.1211037] [PMID: 22096200]
[98]
Lewis, K. Persister cells. Annu. Rev. Microbiol., 2010, 64, 357-372.
[http://dx.doi.org/10.1146/annurev.micro.112408.134306] [PMID: 20528688]
[99]
Levin, B.R.; Concepción-Acevedo, J.; Udekwu, K.I. Persistence: a copacetic and parsimonious hypothesis for the existence of non-inherited resistance to antibiotics. Curr. Opin. Microbiol., 2014, 21, 18-21.
[http://dx.doi.org/10.1016/j.mib.2014.06.016] [PMID: 25090240]
[100]
Ghafourian, S.; Raftari, M.; Sadeghifard, N.; Sekawi, Z. Toxin-antitoxin Systems: Classification, Biological Function and Application in Biotechnology. Curr. Issues Mol. Biol., 2014, 16, 9-14.
[PMID: 23652423]
[101]
Hayes, F.; Kędzierska, B. Regulating toxin-antitoxin expression: controlled detonation of intracellular molecular timebombs. Toxins (Basel), 2014, 6(1), 337-358.
[http://dx.doi.org/10.3390/toxins6010337] [PMID: 24434949]
[102]
Kint, C.I.; Verstraeten, N.; Fauvart, M.; Michiels, J. New-found fundamentals of bacterial persistence. Trends Microbiol., 2012, 20(12), 577-585.
[http://dx.doi.org/10.1016/j.tim.2012.08.009] [PMID: 22959615]
[103]
Dhar, N.; McKinney, J.D. Microbial phenotypic heterogeneity and antibiotic tolerance. Curr. Opin. Microbiol., 2007, 10(1), 30-38.
[http://dx.doi.org/10.1016/j.mib.2006.12.007] [PMID: 17215163]
[104]
Barth, V.C., Jr; Rodrigues, B.Á.; Bonatto, G.D.; Gallo, S.W.; Pagnussatti, V.E.; Ferreira, C.A.S.; de Oliveira, S.D. Heterogeneous persister cells formation in Acinetobacter baumannii. PLoS One, 2013, 8(12)e84361
[http://dx.doi.org/10.1371/journal.pone.0084361] [PMID: 24391945]
[105]
Allison, K.R.; Brynildsen, M.P.; Collins, J.J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature, 2011, 473(7346), 216-220.
[http://dx.doi.org/10.1038/nature10069] [PMID: 21562562]
[106]
Amato, S.M.; Brynildsen, M.P. Persister heterogeneity arising from a single metabolic stress. Curr. Biol., 2015, 25(16), 2090-2098.
[http://dx.doi.org/10.1016/j.cub.2015.06.034] [PMID: 26255847]
[107]
Ruhe, Z.C.; Low, D.A.; Hayes, C.S. Bacterial contact-dependent growth inhibition. Trends Microbiol., 2013, 21(5), 230-237.
[http://dx.doi.org/10.1016/j.tim.2013.02.003] [PMID: 23473845]
[108]
Maleki, A.; Ghafourian, S.; Pakzad, I.; Badakhsh, B.; Sadeghifard, N. mazE antitoxin of toxin antitoxin system and fbpA as reliable targets to eradication of Neisseria meningitidis. Curr. Pharm. Des., 2017.
[PMID: 29237374]
[109]
Jaén-Luchoro, D.; Aliaga-Lozano, F.; Gomila, R.M.; Gomila, M.; Salvà-Serra, F.; Lalucat, J.; Bennasar-Figueras, A. First insights into a type II toxin-antitoxin system from the clinical isolate Mycobacterium sp. MHSD3, similar to epsilon/zeta systems. PLoS One, 2017, 12(12)e0189459
[http://dx.doi.org/10.1371/journal.pone.0189459] [PMID: 29236773]
[110]
Dörr, T.; Vulić, M.; Lewis, K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol., 2010, 8(2)e1000317
[http://dx.doi.org/10.1371/journal.pbio.1000317] [PMID: 20186264]
[111]
Lewis, K.; Shan, Y. Persister Awakening. Mol. Cell, 2016, 63(1), 3-4.
[http://dx.doi.org/10.1016/j.molcel.2016.06.025] [PMID: 27392143]
[112]
Kwan, B.W.; Chowdhury, N.; Wood, T.K. Combatting bacterial infections by killing persister cells with mitomycin C. Environ. Microbiol., 2015, 17(11), 4406-4414.
[http://dx.doi.org/10.1111/1462-2920.12873] [PMID: 25858802]
[113]
Chowdhury, N.; Wood, T.L.; Martínez-Vázquez, M.; García-Contreras, R.; Wood, T.K. DNA-crosslinker cisplatin eradicates bacterial persister cells. Biotechnol. Bioeng., 2016, 113(9), 1984-1992.
[http://dx.doi.org/10.1002/bit.25963] [PMID: 26914280]

Rights & Permissions Print Cite
Article Metrics
12
© 2024 Bentham Science Publishers | Privacy Policy