Staphylococcus aureus Dormancy: Waiting for Insurgency

Page: [1898 - 1915] Pages: 18

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Abstract

Relapse infection usually results from resistance to the antibiotic, acquired genes, or persister cells. Persister cells are formed through mutation, reduced activity or metabolically inactive pathways induced by antibiotics, harassing conditions, low ATP, and malnutrition. These factors provide the ground for bacteria to grow slowly. Such a slow growth rate makes traditional antibiotics ineffective against persister cells. Staphylococcus aureus (S. aureus), in addition to this form, can be observed in Small Colony Variants (SCVs), L-forms, and dormant, all of which are characterized by at least one feature, i.e., slow growth. Despite their slow growth, they are metabolically active in terms of stringent SOS and cell wall stress responses. The stress response involves resistance against harassing conditions, and it survives until it is reactivated later. The present study aims to discuss the mechanisms of all persister cell formations, circumstances involved, gene mutation, and adoptable strategies against it.

Graphical Abstract

[1]
Muliukin, A.L.; Suzina, N.E.; Mel’nikov, V.G.; Gal’chenko, V.F. Dormant state and phenotypic variability of Staphylococcus aureus and corynebacterium pseudodiphtheriticum. Mikrobiologiia, 2014, 83(1), 15-27.
[PMID: 25423730]
[2]
Lewis, K. Persister cells, dormancy and infectious disease. Nat. Rev. Microbiol., 2007, 5(1), 48-56.
[http://dx.doi.org/10.1038/nrmicro1557] [PMID: 17143318]
[3]
Vázquez-Laslop, N.; Lee, H.; Neyfakh, A.A. Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J. Bacteriol., 2006, 188(10), 3494-3497.
[http://dx.doi.org/10.1128/JB.188.10.3494-3497.2006] [PMID: 16672603]
[4]
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]
[5]
Blair, J.M.A.; Webber, M.A.; Baylay, A.J.; Ogbolu, D.O.; Piddock, L.J.V. Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol., 2015, 13(1), 42-51.
[http://dx.doi.org/10.1038/nrmicro3380] [PMID: 25435309]
[6]
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]
[7]
Balaban, N.Q.; Helaine, S.; Lewis, K.; Ackermann, M.; Aldridge, B.; Andersson, D.I.; Brynildsen, M.P.; Bumann, D.; Camilli, A.; Collins, J.J.; Dehio, C.; Fortune, S.; Ghigo, J.M.; Hardt, W.D.; Harms, A.; Heinemann, M.; Hung, D.T.; Jenal, U.; Levin, B.R.; Michiels, J.; Storz, G.; Tan, M.W.; Tenson, T.; Van Melderen, L.; Zinkernagel, A. Definitions and guidelines for research on antibiotic persistence. Nat. Rev. Microbiol., 2019, 17(7), 441-448.
[http://dx.doi.org/10.1038/s41579-019-0196-3] [PMID: 30980069]
[8]
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]
[9]
Luidalepp, H.; Jõers, A.; Kaldalu, N.; Tenson, T. Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J. Bacteriol., 2011, 193(14), 3598-3605.
[http://dx.doi.org/10.1128/JB.00085-11] [PMID: 21602347]
[10]
Wilmaerts, D.; Windels, E.M.; Verstraeten, N.; Michiels, J. General mechanisms leading to persister formation and awakening. Trends Genet., 2019, 35(6), 401-411.
[http://dx.doi.org/10.1016/j.tig.2019.03.007] [PMID: 31036343]
[11]
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]
[12]
Donegan, N.P.; Thompson, E.T.; Fu, Z.; Cheung, A.L. Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus. J. Bacteriol., 2010, 192(5), 1416-1422.
[http://dx.doi.org/10.1128/JB.00233-09] [PMID: 20038589]
[13]
Habib, G.; Zhu, J.; Sun, B. A novel type I toxin-antitoxin system modulates persister cell formation in Staphylococcus aureus. Int. J. Med. Microbiol., 2020, 310(2), 151400.
[http://dx.doi.org/10.1016/j.ijmm.2020.151400] [PMID: 32001143]
[14]
Maisonneuve, E.; Castro-Camargo, M.; Gerdes, K. RETRACTED:(p) ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity; Elsevier: Amsterdam, Netherlands, 2013.
[15]
Irving, S.E.; Choudhury, N.R.; Corrigan, R.M. The stringent response and physiological roles of (pp)pGpp in bacteria. Nat. Rev. Microbiol., 2021, 19(4), 256-271.
[http://dx.doi.org/10.1038/s41579-020-00470-y] [PMID: 33149273]
[16]
Conlon, B.P.; Rowe, S.E.; Gandt, A.B.; Nuxoll, A.S.; Donegan, N.P.; Zalis, E.A.; Clair, G.; Adkins, J.N.; Cheung, A.L.; Lewis, K. Persister formation in Staphylococcus aureus is associated with ATP depletion. Nat. Microbiol., 2016, 1(5), 16051.
[http://dx.doi.org/10.1038/nmicrobiol.2016.51]
[17]
Peyrusson, F.; Varet, H.; Nguyen, T.K.; Legendre, R.; Sismeiro, O.; Coppée, J.Y.; Wolz, C.; Tenson, T.; Van Bambeke, F. Intracellular Staphylococcus aureus persisters upon antibiotic exposure. Nat. Commun., 2020, 11(1), 2200.
[http://dx.doi.org/10.1038/s41467-020-15966-7] [PMID: 32366839]
[18]
Dengler, V.; Meier, P.S.; Heusser, R.; Berger-Bächi, B.; McCallum, N. Induction kinetics of the Staphylococcus aureus cell wall stress stimulon in response to different cell wall active antibiotics. BMC Microbiol., 2011, 11(1), 16.
[http://dx.doi.org/10.1186/1471-2180-11-16] [PMID: 21251258]
[19]
Fernandes, P.B.; Reed, P.; Monteiro, J.M.; Pinho, M.G. Revisiting the role of VraTSR in Staphylococcus aureus response to cell wall-targeting antibiotics. J. Bacteriol., 2022, 204(8), e00162-22.
[http://dx.doi.org/10.1128/jb.00162-22] [PMID: 35862765]
[20]
Rajput, A.; Seif, Y.; Choudhary, K.S.; Dalldorf, C.; Poudel, S.; Monk, J.M.; Palsson, B.O. Pangenome analytics reveal two-component systems as conserved targets in ESKAPEE pathogens. mSystems, 2021, 6(1), e00981-20.
[http://dx.doi.org/10.1128/mSystems.00981-20] [PMID: 33500331]
[21]
Geiger, T.; Kästle, B.; Gratani, F.L.; Goerke, C.; Wolz, C. Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J. Bacteriol., 2014, 196(4), 894-902.
[http://dx.doi.org/10.1128/JB.01201-13] [PMID: 24336937]
[22]
Han, J.; Liu, Z.; Xu, T.; Shi, W.; Xu, X.; Wang, S. A novel LysR-type global regulator rpva controls persister formation and virulence in Staphylococcus aureus. bioRxiv, 2019, 861500.
[23]
Waters, E.M.; Rowe, S.E.; O’Gara, J.P.; Conlon, B.P. Convergence of Staphylococcus aureus persister and biofilm research: Can biofilms be defined as communities of adherent persister cells? PLoS Pathog., 2016, 12(12), e1006012.
[http://dx.doi.org/10.1371/journal.ppat.1006012] [PMID: 28033390]
[24]
Hogan, S.; Zapotoczna, M.; Stevens, N.T.; Humphreys, H.; O’Gara, J.P.; O’Neill, E. in vitro approach for identification of the most effective agents for antimicrobial lock therapy in the treatment of intravascular catheter-related infections caused by Staphylococcus aureus. Antimicrob. Agents Chemother., 2016, 60(5), 2923-2931.
[http://dx.doi.org/10.1128/AAC.02885-15] [PMID: 26926633]
[25]
Prax, M.; Mechler, L.; Weidenmaier, C.; Bertram, R. Glucose augments killing efficiency of daptomycin challenged Staphylococcus aureus persisters. PLoS One, 2016, 11(3), e0150907.
[http://dx.doi.org/10.1371/journal.pone.0150907] [PMID: 26960193]
[26]
Kubistova, L.; Dvoracek, L.; Tkadlec, J.; Melter, O.; Licha, I. Environmental stress affects the formation of Staphylococcus aureus persisters tolerant to antibiotics. Microb. Drug Resist., 2018, 24(5), 547-555.
[http://dx.doi.org/10.1089/mdr.2017.0064] [PMID: 28813617]
[27]
Kang, C.K.; Kim, Y.K.; Jung, S.I.; Park, W.B.; Song, K.H.; Park, K.H.; Choe, P.G.; Jang, H.C.; Lee, S.; Kim, Y.S.; Kwak, Y.G.; Kwon, K.T.; Kiem, S.; Kim, C.J.; Kim, E.S.; Kim, H.B. agr functionality affects clinical outcomes in patients with persistent methicillin-resistant Staphylococcus aureus bacteraemia. Eur. J. Clin. Microbiol. Infect. Dis., 2017, 36(11), 2187-2191.
[http://dx.doi.org/10.1007/s10096-017-3044-2] [PMID: 28639163]
[28]
Xu, T.; Wang, X.Y.; Cui, P.; Zhang, Y.M.; Zhang, W.H.; Zhang, Y. The Agr quorum sensing system represses persister formation through regulation of phenol soluble modulins in Staphylococcus aureus. Front. Microbiol., 2017, 8, 2189.
[http://dx.doi.org/10.3389/fmicb.2017.02189] [PMID: 29163457]
[29]
Nasser, A.; Moradi, M.; Jazireian, P.; Safari, H.; Alizadeh-Sani, M.; Pourmand, M.R.; Azimi, T. Staphylococcus aureus versus neutrophil: Scrutiny of ancient combat. Microb. Pathog., 2019, 131, 259-269.
[http://dx.doi.org/10.1016/j.micpath.2019.04.026] [PMID: 31002964]
[30]
Schnaith, A.; Kashkar, H.; Leggio, S.A.; Addicks, K.; Krönke, M.; Krut, O. Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J. Biol. Chem., 2007, 282(4), 2695-2706.
[http://dx.doi.org/10.1074/jbc.M609784200] [PMID: 17135247]
[31]
Nguyen, T.K.; Peyrusson, F.; Dodémont, M.; Pham, N.H.; Nguyen, H.A.; Tulkens, P.M.; Van Bambeke, F. The persister character of clinical isolates of Staphylococcus aureus contributes to faster evolution to resistance and higher survival in THP-1 monocytes: A study with moxifloxacin. Front. Microbiol., 2020, 11, 587364.
[http://dx.doi.org/10.3389/fmicb.2020.587364] [PMID: 33329458]
[32]
Grosz, M.; Kolter, J.; Paprotka, K.; Winkler, A.C.; Schäfer, D.; Chatterjee, S.S.; Geiger, T.; Wolz, C.; Ohlsen, K.; Otto, M.; Rudel, T.; Sinha, B.; Fraunholz, M. Cytoplasmic replication of Staphylococcus aureus upon phagosomal escape triggered by phenolsoluble modulin α. Cell. Microbiol., 2014, 16(4), 451-465.
[http://dx.doi.org/10.1111/cmi.12233] [PMID: 24164701]
[33]
Rollin, G.; Tan, X.; Tros, F.; Dupuis, M.; Nassif, X.; Charbit, A.; Coureuil, M. Intracellular survival of Staphylococcus aureus in endothelial cells: A matter of growth or persistence. Front. Microbiol., 2017, 8, 1354.
[http://dx.doi.org/10.3389/fmicb.2017.01354] [PMID: 28769913]
[34]
Johnson, P.J.T.; Levin, B.R. Pharmacodynamics, population dynamics, and the evolution of persistence in Staphylococcus aureus. PLoS Genet., 2013, 9(1), e1003123.
[http://dx.doi.org/10.1371/journal.pgen.1003123] [PMID: 23300474]
[35]
Keren, I.; Kaldalu, N.; Spoering, A.; Wang, Y.; Lewis, K. Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett., 2004, 230(1), 13-18.
[http://dx.doi.org/10.1016/S0378-1097(03)00856-5] [PMID: 14734160]
[36]
Mechler, L.; Herbig, A.; Paprotka, K.; Fraunholz, M.; Nieselt, K.; Bertram, R. A novel point mutation promotes growth phasedependent daptomycin tolerance in Staphylococcus aureus. Antimicrob. Agents Chemother., 2015, 59(9), 5366-5376.
[http://dx.doi.org/10.1128/AAC.00643-15] [PMID: 26100694]
[37]
Pandey, S.; Sahukhal, G.S.; Elasri, M.O. The msaABCR operon regulates persister formation by modulating energy metabolism in Staphylococcus aureus. Front. Microbiol., 2021, 12, 657753.
[http://dx.doi.org/10.3389/fmicb.2021.657753] [PMID: 33936014]
[38]
Mina, E.G.; Marques, C.N.H. Interaction of Staphylococcus aureus persister cells with the host when in a persister state and following awakening. Sci. Rep., 2016, 6(1), 31342.
[http://dx.doi.org/10.1038/srep31342] [PMID: 27506163]
[39]
Peschel, A.; Jack, R.W.; Otto, M.; Collins, L.V.; Staubitz, P.; Nicholson, G.; Kalbacher, H.; Nieuwenhuizen, W.F.; Jung, G.; Tarkowski, A.; van Kessel, K.P.M.; van Strijp, J.A.G. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J. Exp. Med., 2001, 193(9), 1067-1076.
[http://dx.doi.org/10.1084/jem.193.9.1067] [PMID: 11342591]
[40]
Pinel-Marie, M.L.; Brielle, R.; Riffaud, C.; Germain-Amiot, N.; Polacek, N.; Felden, B. RNA antitoxin SprF1 binds ribosomes to attenuate translation and promote persister cell formation in Staphylococcus aureus. Nat. Microbiol., 2021, 6(2), 209-220.
[http://dx.doi.org/10.1038/s41564-020-00819-2] [PMID: 33398097]
[41]
Allan, E.J.; Hoischen, C.; Gumpert, J. Bacterial L‐Forms. Adv. Appl. Microbiol., 2009, 68, 1-39.
[http://dx.doi.org/10.1016/S0065-2164(09)01201-5] [PMID: 19426852]
[42]
Han, J.; Shi, W.; Xu, X.; Wang, S.; Zhang, S.; He, L.; Sun, X.; Zhang, Y. Conditions and mutations affecting Staphylococcus aureus L-form formation. Microbiology, 2015, 161(1), 57-66.
[http://dx.doi.org/10.1099/mic.0.082354-0] [PMID: 25361600]
[43]
Han, J.; He, L.; Shi, W.; Xu, X.; Wang, S.; Zhang, S.; Zhang, Y. Glycerol uptake is important for L-form formation and persistence in Staphylococcus aureus. PLoS One, 2014, 9(9), e108325.
[http://dx.doi.org/10.1371/journal.pone.0108325] [PMID: 25251561]
[44]
Singh, M.; Matsuo, M.; Sasaki, T.; Hishinuma, T.; Yamamoto, N.; Morimoto, Y.; Kirikae, T.; Hiramatsu, K. RNA sequencing identifies a common physiology in vancomycin-and ciprofloxacintolerant Staphylococcus aureus induced by ileS mutations. Antimicrob. Agents Chemother., 2020, 64(10), e00827-20.
[http://dx.doi.org/10.1128/AAC.00827-20] [PMID: 32690649]
[45]
Xu, Y.; Zhang, B.; Wang, L.; Jing, T.; Chen, J.; Xu, X.; Zhang, W.; Zhang, Y.; Han, J. Unusual features and molecular pathways of Staphylococcus aureus L-form bacteria. Microb. Pathog., 2020, 140, 103970.
[http://dx.doi.org/10.1016/j.micpath.2020.103970] [PMID: 31918001]
[46]
Kawai, Y.; Mickiewicz, K.; Errington, J. Lysozyme counteracts β-lactam antibiotics by promoting the emergence of L-form bacteria. Cell, 2018, 172(5), 1038-1049.e10.
[http://dx.doi.org/10.1016/j.cell.2018.01.021] [PMID: 29456081]
[47]
Kawai, Y.; Mercier, R.; Mickiewicz, K.; Serafini, A.; Sório de Carvalho, L.P.; Errington, J. Crucial role for central carbon metabolism in the bacterial L-form switch and killing by β-lactam antibiotics. Nat. Microbiol., 2019, 4(10), 1716-1726.
[http://dx.doi.org/10.1038/s41564-019-0497-3] [PMID: 31285586]
[48]
Kawai, Y.; Mercier, R.; Mickiewicz, K.; Serafini, A.; de Carvalho, L.P.S.; Errington, J. Cell wall inhibition in L-forms or via β-lactam antibiotics induces reactive oxygen-mediated bacterial killing through increased glycolytic flux. Nat. Microbiol., 2019, 4(10), 1716.
[http://dx.doi.org/10.1038/s41564-019-0497-3] [PMID: 31285586]
[49]
Burke, T.P. The unexpected effects of the combination of antibiotics and immunity. Cell, 2018, 172(5), 891-893.
[http://dx.doi.org/10.1016/j.cell.2018.02.003] [PMID: 29474916]
[50]
Kawai, Y.; Mercier, R.; Wu, L.J.; Domínguez-Cuevas, P.; Oshima, T.; Errington, J. Cell growth of wall-free L-form bacteria is limited by oxidative damage. Curr. Biol., 2015, 25(12), 1613-1618.
[http://dx.doi.org/10.1016/j.cub.2015.04.031] [PMID: 26051891]
[51]
Bezrukov, F.; Prados, J.; Renzoni, A.; Panasenko, O.O. MazF toxin causes alterations in Staphylococcus aureus transcriptome, translatome and proteome that underlie bacterial dormancy. Nucleic Acids Res., 2021, 49(4), 2085-2101.
[http://dx.doi.org/10.1093/nar/gkaa1292] [PMID: 33544858]
[52]
Yee, R.; Cui, P.; Xu, T.; Shi, W.; Feng, J.; Zhang, W. Identification of a novel gene argJ involved in arginine biosynthesis critical for persister formation in Staphylococcus aureus. bioRxiv, 2017, 114827.
[53]
Wortham, B.W.; Oliveira, M.A.; Patel, C.N. Polyamines in bacteria: Pleiotropic effects yet specific mechanisms. Adv Exp Med Biol., 2007, 603(106), 115.
[http://dx.doi.org/10.1007/978-0-387-72124-8_9]
[54]
Habib, G.; Zhu, Q.; Sun, B. Bioinformatics and functional assessment of toxin-antitoxin systems in Staphylococcus aureus. Toxins, 2018, 10(11), 473.
[http://dx.doi.org/10.3390/toxins10110473] [PMID: 30441856]
[55]
Panasenko, O.O.; Bezrukov, F.; Komarynets, O.; Renzoni, A. YjbH solubility controls Spx in Staphylococcus aureus: Implication for MazEF toxin-antitoxin system regulation. Front. Microbiol., 2020, 11, 113.
[http://dx.doi.org/10.3389/fmicb.2020.00113] [PMID: 32117138]
[56]
Frees, D.; Gerth, U.; Ingmer, H. Clp chaperones and proteases are central in stress survival, virulence and antibiotic resistance of Staphylococcus aureus. Int. J. Med. Microbiol., 2014, 304(2), 142-149.
[http://dx.doi.org/10.1016/j.ijmm.2013.11.009] [PMID: 24457183]
[57]
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]
[58]
Gunaratnam, G.; Tuchscherr, L.; Elhawy, M.I.; Bertram, R.; Eisenbeis, J.; Spengler, C.; Tschernig, T.; Löffler, B.; Somerville, G.A.; Jacobs, K.; Herrmann, M.; Bischoff, M. ClpC affects the intracellular survival capacity of Staphylococcus aureus in nonprofessional phagocytic cells. Sci. Rep., 2019, 9(1), 16267.
[http://dx.doi.org/10.1038/s41598-019-52731-3] [PMID: 31700127]
[59]
Tuchscherr, L.; Löffler, B.; Proctor, R.A. Persistence of Staphylococcus aureus: Multiple metabolic pathways impact the expression of virulence factors in Small-Colony Variants (SCVs). Front. Microbiol., 2020, 11, 1028.
[http://dx.doi.org/10.3389/fmicb.2020.01028] [PMID: 32508801]
[60]
Proctor, R. Respiration and small colony variants of Staphylococcus aureus. Microbiol. Spectr., 2019, 7(3), 7.3.22.
[http://dx.doi.org/10.1128/microbiolspec.GPP3-0069-2019] [PMID: 31198131]
[61]
Tuchscherr, L.; Bischoff, M.; Lattar, S.M.; Noto Llana, M.; Pförtner, H.; Niemann, S.; Geraci, J.; Van de Vyver, H.; Fraunholz, M.J.; Cheung, A.L.; Herrmann, M.; Völker, U.; Sordelli, D.O.; Peters, G.; Löffler, B. Sigma factor SigB is crucial to mediate Staphylococcus aureus adaptation during chronic infections. PLoS Pathog., 2015, 11(4), e1004870.
[http://dx.doi.org/10.1371/journal.ppat.1004870] [PMID: 25923704]
[62]
Guérillot, R.; Kostoulias, X.; Donovan, L.; Li, L.; Carter, G.P.; Hachani, A.; Vandelannoote, K.; Giulieri, S.; Monk, I.R.; Kunimoto, M.; Starrs, L.; Burgio, G.; Seemann, T.; Peleg, A.Y.; Stinear, T.P.; Howden, B.P. Unstable chromosome rearrangements in Staphylococcus aureus cause phenotype switching associated with persistent infections. Proc. Natl. Acad. Sci. USA, 2019, 116(40), 20135-20140.
[http://dx.doi.org/10.1073/pnas.1904861116] [PMID: 31527262]
[63]
Xia, G.; Wolz, C. Phages of Staphylococcus aureus and their impact on host evolution. Infect. Genet. Evol., 2014, 21, 593-601.
[http://dx.doi.org/10.1016/j.meegid.2013.04.022] [PMID: 23660485]
[64]
Lee, J.; Zilm, P.S.; Kidd, S.P. Novel research models for Staphylococcus aureus small colony variants (SCV) development: Copathogenesis and growth rate. Front. Microbiol., 2020, 11, 321.
[http://dx.doi.org/10.3389/fmicb.2020.00321] [PMID: 32184775]
[65]
Chatterjee, I.; Becker, P.; Grundmeier, M.; Bischoff, M.; Somerville, G.A.; Peters, G.; Sinha, B.; Harraghy, N.; Proctor, R.A.; Herrmann, M. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol., 2005, 187(13), 4488-4496.
[http://dx.doi.org/10.1128/JB.187.13.4488-4496.2005] [PMID: 15968059]
[66]
Kriegeskorte, A.; Grubmüller, S.; Huber, C.; Kahl, B.C.; von Eiff, C.; Proctor, R.A.; Peters, G.; Eisenreich, W.; Becker, K. Staphylococcus aureus small colony variants show common metabolic features in central metabolism irrespective of the underlying auxotrophism. Front. Cell. Infect. Microbiol., 2014, 4, 141.
[http://dx.doi.org/10.3389/fcimb.2014.00141] [PMID: 25374845]
[67]
Zhang, P.; Wright, J.A.; Osman, A.A.; Nair, S.P. An aroD ochre mutation results in a Staphylococcus aureus small colony variant that can undergo phenotypic switching via two alternative mechanisms. Front. Microbiol., 2017, 8, 1001.
[http://dx.doi.org/10.3389/fmicb.2017.01001] [PMID: 28620368]
[68]
Bogut, A.; Magryś, A. The road to success of coagulase-negative staphylococci: Clinical significance of small colony variants and their pathogenic role in persistent infections. Eur. J. Clin. Microbiol. Infect. Dis., 2021, 40(11), 2249-2270.
[http://dx.doi.org/10.1007/s10096-021-04315-1] [PMID: 34296355]
[69]
Batko, I.Z.; Flannagan, R.S.; Guariglia-Oropeza, V.; Sheldon, J.R.; Heinrichs, D.E. Hemin-dependent siderophore utilization promotes iron-restricted growth of the Staphylococcus aureus hemB small colony variant. J. Bacteriol., 2021, 203(24), e00458-21.
[http://dx.doi.org/10.1128/JB.00458-21] [PMID: 34606375]
[70]
Sifri, C.D.; Baresch-Bernal, A.; Calderwood, S.B.; von Eiff, C. Virulence of Staphylococcus aureus small colony variants in the Caenorhabditis elegans infection model. Infect. Immun., 2006, 74(2), 1091-1096.
[http://dx.doi.org/10.1128/IAI.74.2.1091-1096.2006] [PMID: 16428756]
[71]
Ou, J.J.J.; Drilling, A.J.; Cooksley, C.; Bassiouni, A.; Kidd, S.P.; Psaltis, A.J.; Wormald, P.J.; Vreugde, S. Reduced innate immune response to a Staphylococcus aureus small colony variant compared to its wild-type parent strain. Front. Cell. Infect. Microbiol., 2016, 6, 187.
[http://dx.doi.org/10.3389/fcimb.2016.00187] [PMID: 28083514]
[72]
Wong Fok Lung, T.; Monk, I.R.; Acker, K.P.; Mu, A.; Wang, N.; Riquelme, S.A.; Pires, S.; Noguera, L.P.; Dach, F.; Gabryszewski, S.J.; Howden, B.P.; Prince, A. Staphylococcus aureus small colony variants impair host immunity by activating host cell glycolysis and inducing necroptosis. Nat. Microbiol., 2019, 5(1), 141-153.
[http://dx.doi.org/10.1038/s41564-019-0597-0] [PMID: 31686028]
[73]
Wu, M.; von Eiff, C.; Al Laham, N.; Tsuji, B.T. Vancomycin and daptomycin pharmacodynamics differ against a site-directed Staphylococcus epidermidis mutant displaying the small-colony-variant phenotype. Antimicrob. Agents Chemother., 2009, 53(9), 3992-3995.
[http://dx.doi.org/10.1128/AAC.01597-08] [PMID: 19564372]
[74]
Nakaminami, H.; Chen, C.; Truong-Bolduc, Q.C.; Kim, E.S.; Wang, Y.; Hooper, D.C. Efflux transporter of siderophore staphyloferrin A in Staphylococcus aureus contributes to bacterial fitness in abscesses and epithelial cells. Infect. Immun., 2017, 85(8), e00358-17.
[http://dx.doi.org/10.1128/IAI.00358-17] [PMID: 28559406]
[75]
Christmas, B.A.F.; Rolfe, M.D.; Rose, M.; Green, J. Staphylococcus aureus adaptation to aerobic low-redox-potential environments: Implications for an intracellular lifestyle. Microbiology, 2019, 165(7), 779-791.
[http://dx.doi.org/10.1099/mic.0.000809] [PMID: 31100054]
[76]
Kleinert, F.; Kallies, R.; Hort, M.; Zweynert, A.; Szekat, C.; Nagel, M.; Bierbaum, G. Influence of IS 256 on genome variability and formation of small-colony variants in Staphylococcus aureus. Antimicrob. Agents Chemother., 2017, 61(8), e00144-17.
[http://dx.doi.org/10.1128/AAC.00144-17] [PMID: 28584147]
[77]
Bui, L.M.G.; Kidd, S.P. A full genomic characterization of the development of a stable Small Colony Variant cell-type by a clinical Staphylococcus aureus strain. Infect. Genet. Evol., 2015, 36, 345-355.
[http://dx.doi.org/10.1016/j.meegid.2015.10.011] [PMID: 26458527]
[78]
Bui, L.M.G.; Hoffmann, P.; Turnidge, J.D.; Zilm, P.S.; Kidd, S.P. Prolonged growth of a clinical Staphylococcus aureus strain selects for a stable small-colony-variant cell type. Infect. Immun., 2015, 83(2), 470-481.
[http://dx.doi.org/10.1128/IAI.02702-14] [PMID: 25385795]
[79]
Bui, L.M.G.; Turnidge, J.D.; Kidd, S.P. The induction of Staphylococcus aureus biofilm formation or Small Colony Variants is a strain-specific response to host-generated chemical stresses. Microbes Infect., 2015, 17(1), 77-82.
[http://dx.doi.org/10.1016/j.micinf.2014.09.009] [PMID: 25284682]
[80]
Norström, T.; Lannergård, J.; Hughes, D. Genetic and phenotypic identification of fusidic acid-resistant mutants with the small-colony-variant phenotype in Staphylococcus aureus. Antimicrob. Agents Chemother., 2007, 51(12), 4438-4446.
[http://dx.doi.org/10.1128/AAC.00328-07] [PMID: 17923494]
[81]
Tan, X.; Coureuil, M.; Ramond, E.; Euphrasie, D.; Dupuis, M.; Tros, F.; Meyer, J.; Nemazanyy, I.; Chhuon, C.; Guerrera, I.C.; Ferroni, A.; Sermet-Gaudelus, I.; Nassif, X.; Charbit, A.; Jamet, A. Chronic Staphylococcus aureus lung infection correlates with proteogenomic and metabolic adaptations leading to an increased intracellular persistence. Clin. Infect. Dis., 2019, 69(11), 1937-1945.
[http://dx.doi.org/10.1093/cid/ciz106] [PMID: 30753350]
[82]
Sendi, P.; Proctor, R.A. Staphylococcus aureus as an intracellular pathogen: The role of small colony variants. Trends Microbiol., 2009, 17(2), 54-58.
[http://dx.doi.org/10.1016/j.tim.2008.11.004] [PMID: 19162480]
[83]
Proctor, R.A.; von Eiff, C.; Kahl, B.C.; Becker, K.; McNamara, P.; Herrmann, M.; Peters, G. Small colony variants: A pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat. Rev. Microbiol., 2006, 4(4), 295-305.
[http://dx.doi.org/10.1038/nrmicro1384] [PMID: 16541137]
[84]
An, Y.; Wang, Y.; Zhan, J.; Tang, X.; Shen, K.; Shen, F.; Wang, C.; Luan, W.; Wang, X.; Wang, X.; Liu, M.; Zheng, Q.; Yu, L. Fosfomycin protects mice from Staphylococcus aureus pneumonia caused by α-hemolysin in extracellular vesicles by inhibiting MAPK-regulated NLRP3 inflammasomes. Front. Cell. Infect. Microbiol., 2019, 9, 253.
[http://dx.doi.org/10.3389/fcimb.2019.00253] [PMID: 31380296]
[85]
Peterson, M.L.; Schlievert, P.M. Glycerol monolaurate inhibits the effects of Gram-positive select agents on eukaryotic cells. Biochemistry, 2006, 45(7), 2387-2397.
[http://dx.doi.org/10.1021/bi051992u] [PMID: 16475828]
[86]
Nasser, A.; Azimi, T.; Ostadmohammadi, S.; Ostadmohammadi, S. A comprehensive review of bacterial osteomyelitis with emphasis on Staphylococcus aureus. Microb. Pathog., 2020, 148, 104431.
[http://dx.doi.org/10.1016/j.micpath.2020.104431] [PMID: 32801004]
[87]
Atalla, H.; Gyles, C.; Mallard, B. Staphylococcus aureus small colony variants (SCVs) and their role in disease. Anim. Health Res. Rev., 2011, 12(1), 33-45.
[http://dx.doi.org/10.1017/S1466252311000065] [PMID: 21676339]
[88]
Leimer, N.; Rachmühl, C.; Palheiros Marques, M.; Bahlmann, A.S.; Furrer, A.; Eichenseher, F.; Seidl, K.; Matt, U.; Loessner, M.J.; Schuepbach, R.A.; Zinkernagel, A.S. Nonstable Staphylococcus aureus small-colony variants are induced by low pH and sensitized to antimicrobial therapy by phagolysosomal alkalinization. J. Infect. Dis., 2016, 213(2), 305-313.
[http://dx.doi.org/10.1093/infdis/jiv388] [PMID: 26188074]
[89]
Häffner, N.; Bär, J.; Dengler Haunreiter, V.; Mairpady Shambat, S.; Seidl, K.; Crosby, H.A.; Horswill, A.R.; Zinkernagel, A.S. Intracellular environment and agr system affect colony size heterogeneity of Staphylococcus aureus. Front. Microbiol., 2020, 11, 1415.
[http://dx.doi.org/10.3389/fmicb.2020.01415] [PMID: 32695082]
[90]
Hammer, N.D.; Reniere, M.L.; Cassat, J.E.; Zhang, Y.; Hirsch, A.O.; Indriati Hood, M.; Skaar, E.P. Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. MBio, 2013, 4(4), e00241-13.
[http://dx.doi.org/10.1128/mBio.00241-13] [PMID: 23900169]
[91]
Garcia, L.G.; Lemaire, S.; Kahl, B.C.; Becker, K.; Proctor, R.A.; Denis, O.; Tulkens, P.M.; Van Bambeke, F. Antibiotic activity against small-colony variants of Staphylococcus aureus: Review of in vitro, animal and clinical data. J. Antimicrob. Chemother., 2013, 68(7), 1455-1464.
[http://dx.doi.org/10.1093/jac/dkt072] [PMID: 23485724]
[92]
Tuchscherr, L.; Medina, E.; Hussain, M.; Völker, W.; Heitmann, V.; Niemann, S.; Holzinger, D.; Roth, J.; Proctor, R.A.; Becker, K.; Peters, G.; Löffler, B. Staphylococcus aureus phenotype switching: An effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med., 2011, 3(3), 129-141.
[http://dx.doi.org/10.1002/emmm.201000115] [PMID: 21268281]
[93]
Kim, J.S.; Yamasaki, R.; Song, S.; Zhang, W.; Wood, T.K. Single cell observations show persister cells wake based on ribosome content. Environ. Microbiol., 2018, 20(6), 2085-2098.
[http://dx.doi.org/10.1111/1462-2920.14093] [PMID: 29528544]
[94]
Wood, T.K.; Song, S.; Yamasaki, R. Ribosome dependence of persister cell formation and resuscitation. J. Microbiol., 2019, 57(3), 213-219.
[http://dx.doi.org/10.1007/s12275-019-8629-2] [PMID: 30806978]
[95]
Prossliner, T.; Skovbo Winther, K.; Sørensen, M.A.; Gerdes, K. Ribosome Hibernation. Annu. Rev. Genet., 2018, 52(1), 321-348.
[http://dx.doi.org/10.1146/annurev-genet-120215-035130] [PMID: 30476446]
[96]
Yoshida, H.; Shimada, T.; Ishihama, A. Coordinated hibernation of transcriptional and translational apparatus during growth transition of Escherichia coli to stationary phase. mSystems, 2018, 3(5), e00057-18.
[http://dx.doi.org/10.1128/mSystems.00057-18] [PMID: 30225374]
[97]
Matzov, D.; Aibara, S.; Basu, A.; Zimmerman, E.; Bashan, A.; Yap, M.N.F.; Amunts, A.; Yonath, A.E. The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat. Commun., 2017, 8(1), 723.
[http://dx.doi.org/10.1038/s41467-017-00753-8] [PMID: 28959035]
[98]
Khusainov, I.; Vicens, Q.; Bochler, A.; Grosse, F.; Myasnikov, A.; Ménétret, J.F.; Chicher, J.; Marzi, S.; Romby, P.; Yusupova, G.; Yusupov, M.; Hashem, Y. Structure of the 70S ribosome from human pathogen Staphylococcus aureus. Nucleic Acids Res., 2016, 44(21), 10491-10504.
[http://dx.doi.org/10.1093/nar/gkw933]
[99]
Basu, A.; Yap, M.N.F. Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res., 2016, 44(10), 4881-4893.
[http://dx.doi.org/10.1093/nar/gkw180] [PMID: 27001516]
[100]
Basu, A.; Yap, M.N.F. Disassembly of the Staphylococcus aureus hibernating 100S ribosome by an evolutionarily conserved GTPase. Proc. Natl. Acad. Sci. USA, 2017, 114(39), E8165-E8173.
[http://dx.doi.org/10.1073/pnas.1709588114] [PMID: 28894000]
[101]
Basu, A.; Shields, K.E.; Yap, M.N.F. The hibernating 100S complex is a target of ribosome-recycling factor and elongation factor G in Staphylococcus aureus. J. Biol. Chem., 2020, 295(18), 6053-6063.
[http://dx.doi.org/10.1074/jbc.RA119.012307] [PMID: 32209660]
[102]
Zundel, M.A.; Basturea, G.N.; Deutscher, M.P. Initiation of ribosome degradation during starvation in Escherichia coli. RNA, 2009, 15(5), 977-983.
[http://dx.doi.org/10.1261/rna.1381309] [PMID: 19324965]
[103]
Yoshida, H.; Nakayama, H.; Maki, Y.; Ueta, M.; Wada, C.; Wada, A. Functional sites of ribosome modulation factor (RMF) involved in the formation of 100S Ribosome. Front. Mol. Biosci., 2021, 8, 661691.
[http://dx.doi.org/10.3389/fmolb.2021.661691] [PMID: 34012979]
[104]
Khusainov, I.; Fatkhullin, B.; Pellegrino, S.; Bikmullin, A.; Liu, W.; Gabdulkhakov, A.; Shebel, A.A.; Golubev, A.; Zeyer, D.; Trachtmann, N.; Sprenger, G.A.; Validov, S.; Usachev, K.; Yusupova, G.; Yusupov, M. Mechanism of ribosome shutdown by RsfS in Staphylococcus aureus revealed by integrative structural biology approach. Nat. Commun., 2020, 11(1), 1656.
[http://dx.doi.org/10.1038/s41467-020-15517-0] [PMID: 32245971]
[105]
Pascoe, B.; Dams, L.; Wilkinson, T.S.; Harris, L.G.; Bodger, O.; Mack, D.; Davies, A.P. Dormant cells of Staphylococcus aureus are resuscitated by spent culture supernatant. PLoS One, 2014, 9(2), e85998.
[http://dx.doi.org/10.1371/journal.pone.0085998] [PMID: 24523858]
[106]
Guo, L.; Xu, R.; Zhao, Y.; Liu, D.; Liu, Z.; Wang, X.; Chen, H.; Kong, M.G. Gas plasma pre-treatment increases antibiotic sensitivity and persister eradication in methicillin-resistant Staphylococcus aureus. Front. Microbiol., 2018, 9, 537.
[http://dx.doi.org/10.3389/fmicb.2018.00537] [PMID: 29628915]
[107]
Shen, F.; Tang, X.; Cheng, W.; Wang, Y.; Wang, C.; Shi, X.; An, Y.; Zhang, Q.; Liu, M.; Liu, B.; Yu, L. Fosfomycin enhances phagocyte-mediated killing of Staphylococcus aureus by extracellular traps and reactive oxygen species. Sci. Rep., 2016, 6(1), 19262.
[http://dx.doi.org/10.1038/srep19262] [PMID: 26778774]
[108]
Schmidt, N.W.; Deshayes, S.; Hawker, S.; Blacker, A.; Kasko, A.M.; Wong, G.C.L. Engineering persister-specific antibiotics with synergistic antimicrobial functions. ACS Nano, 2014, 8(9), 8786-8793.
[http://dx.doi.org/10.1021/nn502201a] [PMID: 25130648]
[109]
Hurdle, J.G.; O’Neill, A.J.; Chopra, I.; Lee, R.E. Targeting bacterial membrane function: An underexploited mechanism for treating persistent infections. Nat. Rev. Microbiol., 2011, 9(1), 62-75.
[http://dx.doi.org/10.1038/nrmicro2474] [PMID: 21164535]
[110]
Khan, F.; Pham, D.T.N.; Tabassum, N.; Oloketuyi, S.F.; Kim, Y.M. Treatment strategies targeting persister cell formation in bacterial pathogens. Crit. Rev. Microbiol., 2020, 46(6), 665-688.
[http://dx.doi.org/10.1080/1040841X.2020.1822278] [PMID: 33022189]
[111]
Hu, Y.; Coates, A.R.M. Enhancement by novel anti-methicillinresistant Staphylococcus aureus compound HT61 of the activity of neomycin, gentamicin, mupirocin and chlorhexidine: in vitro and in vivo studies. J. Antimicrob. Chemother., 2013, 68(2), 374-384.
[http://dx.doi.org/10.1093/jac/dks384] [PMID: 23042813]
[112]
Kim, W.; Conery, A.L.; Rajamuthiah, R.; Fuchs, B.B.; Ausubel, F.M.; Mylonakis, E. Identification of an antimicrobial agent effective against methicillin-resistant Staphylococcus aureus persisters using a fluorescence-based screening strategy. PLoS One, 2015, 10(6), e0127640.
[http://dx.doi.org/10.1371/journal.pone.0127640] [PMID: 26039584]
[113]
Ghosh, C.; Manjunath, G.B.; Konai, M.M.; Uppu, D.S.S.M.; Hoque, J.; Paramanandham, K.; Shome, B.R.; Haldar, J. Arylalkyl-lysines: Agents that kill planktonic cells, persister cells, biofilms of MRSA and protect mice from skin-infection. PLoS One, 2015, 10(12), e0144094.
[http://dx.doi.org/10.1371/journal.pone.0144094] [PMID: 26669634]
[114]
Jennings, M.C.; Ator, L.E.; Paniak, T.J.; Minbiole, K.P.C.; Wuest, W.M. Biofilm-eradicating properties of quaternary ammonium amphiphiles: Simple mimics of antimicrobial peptides. ChemBioChem, 2014, 15(15), 2211-2215.
[http://dx.doi.org/10.1002/cbic.201402254] [PMID: 25147134]
[115]
Ooi, N.; Miller, K.; Randall, C.; Rhys-Williams, W.; Love, W.; Chopra, I. XF-70 and XF-73, novel antibacterial agents active against slow-growing and non-dividing cultures of Staphylococcus aureus including biofilms. J. Antimicrob. Chemother., 2010, 65(1), 72-78.
[http://dx.doi.org/10.1093/jac/dkp409] [PMID: 19889790]
[116]
Reza, A.; Farid, A.J.; Zamberi, S.; Amini, R.; Sajedeh, K.; Ahmad, N. Dynamics of bacteriophages as a promising antibiofilm agents. J. Pure Appl. Microbiol., 2014, 8(2), 1015-1019.
[117]
Maleki, F.; Hadadi, M.H.; Rezaei, F.; Mohamadi, H.R.; Khosravi, A.; Nasser, A. Classification and replication mechanism of Staphylococcus phage. Biosci. Biotechnol. Res. Asia, 2015, 12(1), 481-486.
[http://dx.doi.org/10.13005/bbra/1689]
[118]
Nasser, A.; Soltan Dallal, M.M.; Jahanbakhshi, S.; Azimi, T.; Nikouei, L. Staphylococcus aureus: Biofilm formation and strategies against it. Curr. Pharm. Biotechnol., 2022, 23(5), 664-678.
[PMID: 34238148]
[119]
Azimi, T.; Mosadegh, M.; Nasiri, M.J.; Sabour, S.; Karimaei, S.; Nasser, A. Phage therapy as a renewed therapeutic approach to mycobacterial infections: A comprehensive review. Infect. Drug Resist., 2019, 12, 2943-2959.
[http://dx.doi.org/10.2147/IDR.S218638] [PMID: 31571947]
[120]
Tkhilaishvili, T.; Lombardi, L.; Klatt, A.B.; Trampuz, A.; Di Luca, M. Bacteriophage Sb-1 enhances antibiotic activity against biofilm, degrades exopolysaccharide matrix and targets persisters of Staphylococcus aureus. Int. J. Antimicrob. Agents, 2018, 52(6), 842-853.
[http://dx.doi.org/10.1016/j.ijantimicag.2018.09.006] [PMID: 30236955]
[121]
Rodríguez, L.; Martínez, B.; Zhou, Y.; Rodríguez, A.; Donovan, D.M.; García, P. Lytic activity of the virion-associated peptidoglycan hydrolase HydH5 of Staphylococcus aureusbacteriophage vB_SauS-phiIPLA88. BMC Microbiol., 2011, 11(1), 138.
[http://dx.doi.org/10.1186/1471-2180-11-138] [PMID: 21682850]
[122]
Nasser, A.; Azizian, R.; Tabasi, M.; Khezerloo, J.K.; Heravi, F.S.; Kalani, M.T.; Sadeghifard, N.; Amini, R.; Pakzad, I.; Radmanesh, A.; Jalilian, F.A. Specification of bacteriophage isolated against clinical methicillin-resistant Staphylococcus aureus. Osong Public Health Res. Perspect., 2019, 10(1), 20-24.
[http://dx.doi.org/10.24171/j.phrp.2019.10.1.05] [PMID: 30847267]
[123]
Latka, A.; Maciejewska, B.; Majkowska-Skrobek, G.; Briers, Y.; Drulis-Kawa, Z. Bacteriophage-encoded virion-associated enzymes to overcome the carbohydrate barriers during the infection process. Appl. Microbiol. Biotechnol., 2017, 101(8), 3103-3119.
[http://dx.doi.org/10.1007/s00253-017-8224-6] [PMID: 28337580]
[124]
Gutiérrez, D.; Ruas-Madiedo, P.; Martínez, B.; Rodríguez, A.; García, P. Effective removal of staphylococcal biofilms by the endolysin LysH5. PLoS One, 2014, 9(9), e107307.
[http://dx.doi.org/10.1371/journal.pone.0107307] [PMID: 25203125]
[125]
Schuch, R.; Khan, B.K.; Raz, A.; Rotolo, J.A.; Wittekind, M. Bacteriophage lysin CF-301, a potent antistaphylococcal biofilm agent. Antimicrob. Agents Chemother., 2017, 61(7), e02666-16.
[http://dx.doi.org/10.1128/AAC.02666-16] [PMID: 28461319]
[126]
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]
[127]
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]
[128]
Moreira, W.; Aziz, D.B.; Dick, T. Boromycin kills mycobacterial persisters without detectable resistance. Front. Microbiol., 2016, 7, 199.
[http://dx.doi.org/10.3389/fmicb.2016.00199] [PMID: 26941723]
[129]
Lee, J.H.; Kim, Y.G.; Gwon, G.; Wood, T.K.; Lee, J. Halogenated indoles eradicate bacterial persister cells and biofilms. AMB Express, 2016, 6(1), 123.
[http://dx.doi.org/10.1186/s13568-016-0297-6] [PMID: 27921270]
[130]
McCall, I.C.; Shah, N.; Govindan, A.; Baquero, F.; Levin, B.R. Antibiotic killing of diversely generated populations of nonreplicating bacteria. Antimicrob. Agents Chemother., 2019, 63(7), e02360-18.
[http://dx.doi.org/10.1128/AAC.02360-18] [PMID: 31036690]
[131]
Yee, R.; Yuan, Y.; Tarff, A.; Brayton, C.; Gour, N.; Feng, J. A drug combination approach targeting both growing bacteria and dormant persisters eradicate persistent Staphylococcus aureus biofilm infection. bioRxiv, 2019, 686097.
[http://dx.doi.org/10.1101/686097]
[132]
Morgera, F; Antcheva, N; Pacor, S; Quaroni, L; Berti, F; Vaccari, L. Structuring and interactions of human β‐defensins 2 and 3 with model membranes. J. Peptide. Sci., 2008, 14(4), 518-523.
[http://dx.doi.org/10.1002/psc.981]
[133]
Omardien, S.; Drijfhout, J.W.; Vaz, F.M.; Wenzel, M.; Hamoen, L.W.; Zaat, S.A.J.; Brul, S. Bactericidal activity of amphipathic cationic antimicrobial peptides involves altering the membrane fluidity when interacting with the phospholipid bilayer. Biochim. Biophys. Acta Biomembr., 2018, 1860(11), 2404-2415.
[http://dx.doi.org/10.1016/j.bbamem.2018.06.004] [PMID: 29902419]
[134]
de Breij, A.; Riool, M.; Cordfunke, R.A.; Malanovic, N.; de Boer, L.; Koning, R.I.; Ravensbergen, E.; Franken, M.; van der Heijde, T.; Boekema, B.K.; Kwakman, P.H.S.; Kamp, N.; El Ghalbzouri, A.; Lohner, K.; Zaat, S.A.J.; Drijfhout, J.W.; Nibbering, P.H. The antimicrobial peptide SAAP-148 combats drug-resistant bacteria and biofilms. Sci. Transl. Med., 2018, 10(423), eaan4044.
[http://dx.doi.org/10.1126/scitranslmed.aan4044] [PMID: 29321257]
[135]
Brezden, A.; Mohamed, M.F.; Nepal, M.; Harwood, J.S.; Kuriakose, J.; Seleem, M.N.; Chmielewski, J. Dual targeting of intracellular pathogenic bacteria with a cleavable conjugate of kanamycin and an antibacterial cell-penetrating peptide. J. Am. Chem. Soc., 2016, 138(34), 10945-10949.
[http://dx.doi.org/10.1021/jacs.6b04831] [PMID: 27494027]
[136]
Wexselblatt, E; Oppenheimer-Shaanan, Y; Kaspy, I; London, N; Schueler-Furman, O; Yavin, E Relacin, a novel antibacterial agent targeting the stringent response. PLoS Pathog., 2012, 8(9), e1002925.
[http://dx.doi.org/10.1371/journal.ppat.1002925]