Complete and SOS-Mediated Response of Staphylococcus aureus to the Antibiotic Ciprofloxacin
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Staphylococcus aureus infections can be difficult to treat due to both multidrug resistance and the organism's remarkable ability to persist in the host. Persistence and the evolution of resistance may be related to several complex regulatory networks, such as the SOS response, which modifies transcription in response to environmental stress. To understand how S. aureus persists during antibiotic therapy and eventually emerges resistant, we characterized its global transcriptional response to ciprofloxacin. We found that ciprofloxacin induces prophage mobilization as well as significant alterations in metabolism, most notably the up-regulation of the tricarboxylic acid cycle. In addition, we found that ciprofloxacin induces the SOS response, which we show, by comparison of a wild-type strain and a non-SOS-inducible lexA mutant strain, includes the derepression of 16 genes. While the SOS response of S. aureus is much more limited than those of Escherichia coli and Bacillus subtilis , it is similar to that of Pseudomonas aeruginosa and includes RecA, LexA, several hypothetical proteins, and a likely error-prone Y family polymerase whose homologs in other bacteria are required for induced mutation. We also examined induced mutation and found that either the inability to derepress the SOS response or the lack of the LexA-regulated polymerase renders S. aureus unable to evolve antibiotic resistance in vitro in response to UV damage. The data suggest that up-regulation of the tricarboxylic acid cycle and induced mutation facilitate S. aureus persistence and evolution of resistance during antibiotic therapy.
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dinB is not part of the S. aureus SOS regulon.
“In contrast, the mutant lacking functional dinB (which is not part of the S. aureus SOS regulon [62]) had only a slight defect in H2O2-induced SCV formation (Fig. 3A).”
From Staphylococcus aureus Adapts to Oxidative Stress by Producing H <sub>2</sub> O <sub>2</sub> -Resistant Small-Colony Variants via the SOS Response (2015) · cites this paper as [62]
Cites
Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., & Ellenberger, T. (2005) · doi:10.1128/9781555816704 · Cited by 5,683 · see citing works
McKinney, J. D., zu Bentrup, K. H., Muñoz‐Elías, E. J., Miczák, A., Chen, B., Chan, W.-T., Swenson, D. L., Sacchettini, J. C., Jacobs, W. R., & Russell, D. G. (2000) · Nature · doi:10.1038/35021074 · Cited by 1,361 · see citing works
DNA gyrase, topoisomerase IV, and the 4-quinolones
Drlica, K., & Zhao, X. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.3.377-392.1997 · Cited by 1,272 · see citing works
Arnaud, M., Chastanet, A., & Débarbouillé, M. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.11.6887-6891.2004 · Cited by 953 · see citing works
Courcelle, J., Khodursky, A., Peter, B., Brown, P. O., & Hanawalt, P. C. (2001) · Genetics · doi:10.1093/genetics/158.1.41 · Cited by 853 · see citing works
The glyoxylate cycle is required for fungal virulence
Lorenz, M. C., & Fink, G. R. (2001) · Nature · doi:10.1038/35083594 · Cited by 745 · see citing works
SOS Response Induction by ß-Lactams and Bacterial Defense Against Antibiotic Lethality
Miller, C., Thomsen, L. E., Gaggero, C., Mosseri, R., Ingmer, H., & Cohen, S. N. (2004) · Science · doi:10.1126/science.1101630 · Cited by 584 · see citing works
Inhibition of Mutation and Combating the Evolution of Antibiotic Resistance
Cirz, R. T., Chin, J. K., Andes, D. R., de Crécy‐Lagard, V., Craig, W. A., & Romesberg, F. E. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030176 · Cited by 576 · see citing works
Self-citationVoyich, J. M., Braughton, K. R., Sturdevant, D. E., Whitney, A. R., Saïd-Salim, B., Porcella, S. F., Long, R. D., Dorward, D. W., Gardner, D. J., Kreiswirth, B. N., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.6.3907 · Cited by 563 · see citing works
Bacteriophage Control of Bacterial Virulence
Wagner, P. L., & Waldor, M. K. (2002) · Infection and Immunity · doi:10.1128/iai.70.8.3985-3993.2002 · Cited by 500 · see citing works
Boshoff, H. I., Reed, M. B., Barry, C. E., & Mizrahi, V. (2003) · Cell · doi:10.1016/s0092-8674(03)00270-8 · Cited by 411 · see citing works
Napolitano, R. L., Janel‐Bintz, R., Wagner, J. E., & Fuchs, R. P. (2000) · The EMBO Journal · doi:10.1093/emboj/19.22.6259 · Cited by 403 · see citing works
Maiques, E., Úbeda, C., Campoy, S., Salvador, N., Lasa, Í., Novick, R. P., Barbé, J., & Penadés, J. R. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.7.2726-2729.2006 · Cited by 365 · see citing works
Cirz, R. T., O’Neill, B. M., Hammond, J. A., Head, S. R., & Romesberg, F. E. (2006) · Journal of Bacteriology · doi:10.1128/jb.00807-06 · Cited by 277 · see citing works
Self-citationEvolvability is a selectable trait
Earl, D. J., & Deem, M. W. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404656101 · Cited by 240 · see citing works
Genetic Composition of the Bacillus subtilis SOS System
Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L. E., Canny, S., Chachu, K. A., Colavito, S. A., Fuller, S. N., Groban, E. S., Hensley, L. A., et al. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.22.7655-7666.2005 · Cited by 206 · see citing works
Somerville, G. A., Chaussee, M. S., Morgan, C. I., Fitzgerald, J. R., Dorward, D. W., Reitzer, L. J., & Musser, J. M. (2002) · Infection and Immunity · doi:10.1128/iai.70.11.6373-6382.2002 · Cited by 196 · see citing works
A Sliding-Clamp Toolbelt Binds High- and Low-Fidelity DNA Polymerases Simultaneously
Indiani, C., McInerney, P., Georgescu, R. E., Goodman, M. F., & O’Donnell, M. E. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.08.011 · Cited by 194 · see citing works
IANDOLO, J. J., Worrell, V. E., Groicher, K. H., Qian, Y., Tian, R., Kenton, S., Dorman, A., Ji, H., Lin, S., Loh, P., et al. (2002) · Gene · doi:10.1016/s0378-1119(02)00481-x · Cited by 162 · see citing works
Mismatch repair protein MutL becomes limiting during stationary-phase mutationPreprint
Harris, R. S., Feng, G., Ross, K. J., Sidhu, R., Thulin, C., Longerich, S., Szigety, S. K., Winkler, M. E., & Rosenberg, S. M. (1997) · Genes & Development · doi:10.1101/gad.11.18.2426 · Cited by 151 · see citing works
Easy cloning of mini-Tn10 insertions from the Bacillus subtilis chromosome
Steinmetz, M. O., & Richter, R. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.6.1761-1763.1994 · Cited by 143 · see citing works
NATURAL HISTORY OF 338 TREATED AND UNTREATED PATIENTS WITH STAPHYLOCOCCAL SEPTICÆMIA
Smith, I. M., & Vickers, A. B. (1960) · The Lancet · doi:10.1016/s0140-6736(60)92303-5 · Cited by 143 · see citing works
Stress resistance in Staphylococcus aureus
Clements, M. O., & Foster, S. J. (1999) · Trends in Microbiology · doi:10.1016/s0966-842x(99)01607-8 · Cited by 136 · see citing works
An SOS-regulated operon involved in damage-inducible mutagenesis in Caulobacter crescentus
Galhardo, R. S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki551 · Cited by 125 · see citing works
Hersh, M. N., Ponder, R. G., Hastings, P. J., & Rosenberg, S. M. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2004.01.020 · Cited by 121 · see citing works
Eleaume, H., & Jabbouri, S. (2004) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2004.07.015 · Cited by 118 · see citing works
Sung, H., Yeamans, G., Ross, C. A., & Yasbin, R. E. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.7.2153-2160.2003 · Cited by 110 · see citing works
SIGNIFICANCE OF HYPERMETHIONÆMIA IN ACUTE TYROSINOSIS
Gaull, G., Rassin, D. K., Sturman, J. A., & Scriver, C. (1968) · The Lancet · doi:10.1016/s0140-6736(68)92343-x · Cited by 109 · see citing works
Radman, M., Matic, I., & Taddei, F. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08874.x · Cited by 109 · see citing works
Coping with replication ‘train wrecks’ in Escherichia coli using Pol V, Pol II and RecA proteins
Goodman, M. F. (2000) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)01564-4 · Cited by 107 · see citing works
Induction and Inhibition of Ciprofloxacin Resistance-Conferring Mutations in Hypermutator Bacteria
Cirz, R. T., & Romesberg, F. E. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.50.1.220-225.2006 · Cited by 105 · see citing works
Self-citationGoranov, A. I., Kuester-Schoeck, E., Wang, J. D., & Grossman, A. D. (2006) · Journal of Bacteriology · doi:10.1128/jb.00342-06 · Cited by 98 · see citing works
Gérard, H. C., Freise, J., Wang, Z., Roberts, G. G., Rudy, D., Krauße‐Opatz, B., Köhler, L., Zeidler, H. K., Schumacher, H. R., Whittum‐Hudson, J. A., et al. (2002) · Microbes and Infection · doi:10.1016/s1286-4579(01)01504-0 · Cited by 95 · see citing works
Begun, J., Sifri, C. D., Goldman, S., Calderwood, S. B., & Ausubel, F. M. (2005) · Infection and Immunity · doi:10.1128/iai.73.2.872-877.2005 · Cited by 94 · see citing works
Köhler, C., Wolff, S., Albrecht, D., Fuchs, S., Becher, D., Büttner, K., Engelmann, S., & Hecker, M. (2005) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.08.002 · Cited by 87 · see citing works
Roth, J. R., Kofoid, E., Roth, F. P., Berg, O. G., Seger, J., & Andersson, D. I. (2003) · Genetics · doi:10.1093/genetics/163.4.1483 · Cited by 66 · see citing works
The role of the SOS response in bacteria exposed to zidovudine or trimethoprim
Lewin, C. S., & Amyes, S. G. B. (1991) · Journal of Medical Microbiology · doi:10.1099/00222615-34-6-329 · Cited by 58 · see citing works
[20] Cleavage of LexA repressor
Little, J. W., Kim, B., Roland, K. L., Smith, M. H., Lin, L.-L., & Slilaty, S. N. (1994) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(94)44022-0 · Cited by 58 · see citing works
Distinctive genetic features exhibited by the Y‐family DNA polymerases in Bacillus subtilis
Duigou, S., Ehrlich, S. D., Noirot, P. H., & Noirot‐Gros, M. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04259.x · Cited by 57 · see citing works
Somerville, G. A., Mikoryak, C., & Reitzer, L. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.4.1072-1078.1999 · Cited by 52 · see citing works
Pedraza‐Reyes, M., & Yasbin, R. E. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.19.6485-6491.2004 · Cited by 48 · see citing works
Binding of the Bacillus subtilis LexA protein to the SOS operator
Groban, E. S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki939 · Cited by 40 · see citing works
Induction of the SOS gene (umuC) by 4-quinolone antibacterial drugs
Power, E. G. M., & Phillips, I. R. (1992) · Journal of Medical Microbiology · doi:10.1099/00222615-36-2-78 · Cited by 38 · see citing works
Dassy, B., & Fournier, J. M. (1996) · Infection and Immunity · doi:10.1128/iai.64.7.2408-2414.1996 · Cited by 26 · see citing works
Schmid, A., Howell, H. A., Battista, J. R., Peterson, S. N., & Lidstrom, M. E. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.10.3339-3351.2005 · Cited by 25 · see citing works
Self-citationTHOMPSON, J. K., & HART, M. G. R. (1981) · Microbiology · doi:10.1099/00221287-124-1-147 · Cited by 13 · see citing works
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Beceiro, A., Tomás, M., & Bou, G. (2013) · Clinical Microbiology Reviews · doi:10.1128/cmr.00059-12 · Cited by 1,078 · see citing works
Bacterial stress responses as determinants of antimicrobial resistance
Poole, K. (2012) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dks196 · Cited by 515 · see citing works
Microbial Persistence and the Road to Drug Resistance
Cohen, N. R., Lobritz, M. A., & Collins, J. J. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.05.009 · Cited by 459 · see citing works
Quinolones: Mechanism, Lethality and Their Contributions to Antibiotic Resistance
Bush, N. G., Díez-Santos, I., Abbott, L. R., & Maxwell, A. (2020) · Molecules · doi:10.3390/molecules25235662 · Cited by 431 · see citing works
Intracellular Staphylococcus aureus persisters upon antibiotic exposure
Peyrusson, F., Varet, H., Nguyen, T. K., Legendre, R., Sismeiro, O., Coppée, J.-Y., Wolz, C., Tenson, T., & Van Bambeke, F. (2020) · Nature Communications · doi:10.1038/s41467-020-15966-7 · Cited by 392 · see citing works
Sully, E. K., Małachowa, N., Elmore, B. O., Alexander, S. M., Femling, J., Gray, B. M., DeLeo, F. R., Otto, M. J., Cheung, A. L., Edwards, B. S., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004174 · Cited by 394 · see citing works
Global Fluoroquinolone Resistance Epidemiology and Implictions for Clinical Use
Dalhoff, A. (2012) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2012/976273 · Cited by 357 · see citing works
Evolution of antibiotic resistance at non-lethal drug concentrations
Andersson, D. I., & Hughes, D. (2012) · Drug Resistance Updates · doi:10.1016/j.drup.2012.03.005 · Cited by 337 · see citing works
Bacterial persisters: molecular mechanisms and therapeutic development
Niu, H., Gu, J., & Zhang, Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01866-5 · Cited by 334 · see citing works
The bacterial LexA transcriptional repressor
Butala, M., Žgur-Bertok, D., & Busby, S. J. W. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8378-6 · Cited by 315 · see citing works
Concentration-dependent activity in natural environments
Bernier, S. P., & Surette, M. G. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00020 · Cited by 261 · see citing works
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Gaupp, R., Ledala, N., & Somerville, G. A. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00033 · Cited by 253 · see citing works
Podlesek, Z., & Bertok, D. Ž. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.01785 · Cited by 243 · see citing works
Slager, J., Kjos, M., Attaiech, L., & Veening, J.-W. (2014) · Cell · doi:10.1016/j.cell.2014.01.068 · Cited by 237 · see citing works
Staphylococcus aureus Transcriptome Architecture: From Laboratory to Infection-Mimicking Conditions
Mäder, U., Nicolas, P., Depke, M., Pané‐Farré, J., Débarbouillé, M., van der Kooi‐Pol, M. M., Guérin, C., Dérozier, S., Hiron, A., Jarmer, H. Ø., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005962 · Cited by 203 · see citing works
Simmons, L. A., Foti, J. J., Cohen, S., & Walker, G. (2008) · EcoSal Plus · doi:10.1128/ecosalplus.5.4.3 · Cited by 208 · see citing works
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Papkou, A., Hedge, J., Kapel, N., Young, B., & MacLean, R. C. (2020) · Nature Communications · doi:10.1038/s41467-020-17735-y · Cited by 167 · see citing works
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Lenhart, J. S., Schroeder, J. W., Walsh, B. W., & Simmons, L. A. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05020-11 · Cited by 165 · see citing works
Friedman, M. (2015) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.5b00778 · Cited by 164 · see citing works
Selection of resistance at lethal and non-lethal antibiotic concentrations
Hughes, D., & Andersson, D. I. (2012) · Current Opinion in Microbiology · doi:10.1016/j.mib.2012.07.005 · Cited by 161 · see citing works
Painter, K. L., Strange, E., Parkhill, J., Bamford, K. B., Armstrong-James, D., & Edwards, A. M. (2015) · Infection and Immunity · doi:10.1128/iai.03016-14 · Cited by 153 · see citing works
Evaluating evolutionary models of stress-induced mutagenesis in bacteria
MacLean, R. C., Barceló, C. T., & Moxon, R. E. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3415 · Cited by 144 · see citing works
Andreoni, F., Toyofuku, M., Menzi, C., Kalawong, R., Shambat, S. M., François, P., Zinkernagel, A. S., & Eberl, L. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01439-18 · Cited by 143 · see citing works
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Daly, S. M., Elmore, B. O., Kavanaugh, J. S., Triplett, K. D., Figueroa, M., Raja, H. A., El‐Elimat, T., Crosby, H. A., Femling, J., Cech, N. B., et al. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.04564-14 · Cited by 141 · see citing works
Collins, J. A., & Osheroff, N. (2024) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.4c00128 · Cited by 133 · see citing works
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Rapacka-Zdończyk, A., Woźniak, A., Michalska, K., Pierański, M. K., Ogonowska, P., Grinholc, M., & Nakonieczna, J. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.642609 · Cited by 128 · see citing works
Okaiyeto, S. A., Sutar, P. P., Chen, C., Ni, J., Wang, J., MUJUMDAR, A. S., Zhang, J., Xu, M.-Q., Fang, X., Zhang, C., et al. (2024) · Agriculture Communications · doi:10.1016/j.agrcom.2024.100027 · Cited by 123 · see citing works
DNA Damage Triggers Genetic Exchange in Helicobacter pylori
Dorer, M. S., Fero, J., & Salama, N. R. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001026 · Cited by 121 · see citing works
Key Role of Mfd in the Development of Fluoroquinolone Resistance in Campylobacter jejuni
Han, J., Şahin, O., Barton, Y.-W., & Zhang, Q. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000083 · Cited by 120 · see citing works
Nnadozie, C. F., Kumari, S., & Bux, F. (2017) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-017-9438-x · Cited by 119 · see citing works
The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis
van der Veen, S., van Schalkwijk, S., Douwe Molenaar, B., de Vos, W. M., Abee, T., & Wells-Bennik, M. H. J. (2009) · Microbiology · doi:10.1099/mic.0.035196-0 · Cited by 118 · see citing works
Interplay of antibiotic resistance and food-associated stress tolerance in foodborne pathogens
Liao, X., Ma, Y., Daliri, E. B., Koseki, S., Wei, S., Liu, D., Ye, X., Chen, S., & Ding, T. (2019) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2019.11.006 · Cited by 114 · see citing works
Wolf, C., Hochgräfe, F., Kusch, H., Albrecht, D., Hecker, M., & Engelmann, S. (2008) · PROTEOMICS · doi:10.1002/pmic.200701062 · Cited by 115 · see citing works
Impact of Antibiotics with Various Target Sites on the Metabolome of Staphylococcus aureus
Dörries, K., Schlueter, R., & Lalk, M. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.03104-14 · Cited by 103 · see citing works
Absolute quantification of microbial proteomes at different states by directed mass spectrometry
Schmidt, A., Beck, M., Malmström, J. A., Lam, H., Claassen, M., Campbell, D. S., & Aebersold, R. H. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.37 · Cited by 101 · see citing works
Mesak, L. R., Miao, V., & DAVIES, J. E. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01599-07 · Cited by 101 · see citing works
Mo, C. Y., Manning, S. A., Roggiani, M., Culyba, M. J., Samuels, A. N., Sniegowski, P., Goulian, M., & Kohli, R. M. (2016) · mSphere · doi:10.1128/msphere.00163-16 · Cited by 98 · see citing works
A Multi-Omic View of Host-Pathogen-Commensal Interplay in Salmonella-Mediated Intestinal Infection
Kaiser, B. L. D., Li, J., Sanford, J. A., Kim, Y., Kronewitter, S. R., Jones, M. B., Peterson, C. T., Peterson, S. N., Frank, B. C., Purvine, S. O., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067155 · Cited by 83 · see citing works
Self-citationRobinson, A., Brzoska, A. J., Turner, K. M., Withers, R., Harry, E. J., Lewis, P. J., & Dixon, N. E. (2010) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00048-09 · Cited by 83 · see citing works
Respiration and Small Colony Variants of Staphylococcus aureus
Proctor, R. A. (2019) · Microbiology Spectrum · doi:10.1128/microbiolspec.gpp3-0069-2019 · Cited by 80 · see citing works
Phenotypic heterogeneity in persisters: a novel ‘hunker’ theory of persistence
Urbaniec, J., Xu, Y., Hu, Y., Hingley‐Wilson, S., & McFadden, J. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab042 · Cited by 80 · see citing works
Pag, U., Oedenkoven, M., Sass, V., Shai, Y., Валерьевна, Ш. О., Antcheva, N., Tossi, A., & Sahl, H. (2008) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm479 · Cited by 79 · see citing works
Novel Inhibitors of E. coli RecA ATPase Activity
Sexton, J. Z., Wigle, T. J., He, Q., Hughes, M. A., Smith, G. R., Singleton, S. F., Williams, A. L., & Yeh, L.-A. (2010) · Current Chemical Genomics · doi:10.2174/1875397301004010034 · Cited by 76 · see citing works
Sass, V., Pag, U., Tossi, A., Bierbaum, G., & Sahl, H. (2008) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2008.01.011 · Cited by 74 · see citing works
SOS response and its regulation on the fluoroquinolone resistance.
Qin, T., Kang, H., Ma, P., Li, P.-P., Huang, L., & Gu, B. (2015) · PubMed Central · doi:10.3978/j.issn.2305-5839.2015.12.09 · Cited by 74 · see citing works
Controlling Mutation: Intervening in Evolution as a Therapeutic Strategy
Cirz, R. T., & Romesberg, F. E. (2007) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409230701597741 · Cited by 71 · see citing works
Self-citationQuinolone Resistance Reversion by Targeting the SOS Response
Recacha, E., Machuca, J., de Alba, P. D., Ramos-Guelfo, M. S., Docobo-Pérez, F., Rodríguez-Beltrán, J., Blázquez, J., Pascual, Á., & Rodríguez-Martínez, J. M. (2017) · mBio · doi:10.1128/mbio.00971-17 · Cited by 71 · see citing works
Zwicker, P., Schleusener, J., Lohan, S. B., Busch, L., Sicher, C., Einfeldt, S., Kneissl, M., Kühl, A. A., Keck, C. M., Witzel, C., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-06397-z · Cited by 71 · see citing works
Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens
Kelly, B. G., Vespermann, A., & Bolton, D. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2008.02.007 · Cited by 69 · see citing works
Wigle, T. J., Sexton, J. Z., Gromova, A. V., Hadimani, M. B., Hughes, M. A., Smith, G. R., Yeh, L.-A., & Singleton, S. F. (2009) · SLAS DISCOVERY · doi:10.1177/1087057109342126 · Cited by 69 · see citing works
Characterization of the SOS Regulon ofCaulobacter crescentus
da Rocha, R. P., Paquola, A. C. M., Marques, M. V., Menck, C. F. M., & Galhardo, R. S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01419-07 · Cited by 63 · see citing works
Benson, M. A., Lilo, S., Wasserman, G. A., Thoendel, M., Smith, A. P., Horswill, A. R., Fraser, J. D., Novick, R. P., Shopsin, B., & Torres, V. J. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07720.x · Cited by 62 · see citing works
Bacterial pleomorphism and competition in a relative humidity gradient
de Goffau, M. C., Yang, X., van Dijl, J. M., & Harmsen, H. J. M. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01802.x · Cited by 61 · see citing works
Are Sewage Treatment Plants Promoting Antibiotic Resistance?
Jury, K. L., Khan, S. J., Vancov, T., Stuetz, R. M., & Ashbolt, N. J. (2011) · Critical Reviews in Environmental Science and Technology · doi:10.1080/10643380902772589 · Cited by 58 · see citing works
Yeo, W., Arya, R., Kim, K. K., Jeong, H., Cho, K. H., & Bae, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-20617-5 · Cited by 58 · see citing works
DNA Repair in Staphylococcus aureus
Ha, K. P., & Edwards, A. M. (2021) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00091-21 · Cited by 57 · see citing works
Fleury, B., Kelley, W. L., Lew, D., Götz, F., Proctor, R. A., & Vaudaux, P. E. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-76 · Cited by 57 · see citing works
Tuchscherr, L. P. N., Löffler, B., Buzzola, F. R., & Sordelli, D. O. (2010) · Future Microbiology · doi:10.2217/fmb.10.147 · Cited by 57 · see citing works
Schröder, W., Goerke, C., & Wolz, C. (2012) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dks456 · Cited by 56 · see citing works
Current challenges in the application of the UV-LED technology for food decontamination
Soro, A. B., Shokri, S., Nicolau‐Lapeña, I., Ekhlas, D., Burgess, C. M., Whyte, P., Bolton, D., Bourke, P., & Tiwari, B. K. (2022) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2022.12.003 · Cited by 56 · see citing works
Grinholc, M., Rodziewicz, A., Forys, K., Rapacka-Zdończyk, A., Kawiak, A., Domachowska, A., Gołuński, G., Wolz, C., Mesak, L. R., Becker, K., et al. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-6863-z · Cited by 55 · see citing works
Phage against the Machine: The SIE-ence of Superinfection Exclusion
Bucher, M. J., & Czyż, D. M. (2024) · Viruses · doi:10.3390/v16091348 · Cited by 52 · see citing works
Nagel, M., Reuter, T., Jansen, A., Szekat, C., & Bierbaum, G. (2010) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2010.08.021 · Cited by 51 · see citing works
Actinorhodin is a redox‐active antibiotic with a complex mode of action against G ram‐positive cells
Mak, S., & Nodwell, J. R. (2017) · Molecular Microbiology · doi:10.1111/mmi.13837 · Cited by 51 · see citing works
Didier, J.-P., Villet, R. A., Huggler, E., Lew, D. P., Hooper, D. C., Kelley, W. L., & Vaudaux, P. E. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01407-10 · Cited by 50 · see citing works
Ravcheev, D. A., Best, A. A., Tintle, N., DeJongh, M., Osterman, A. L., Novichkov, P. S., & Rodionov, D. A. (2011) · Journal of Bacteriology · doi:10.1128/jb.00350-11 · Cited by 49 · see citing works
Sending out an SOS - the bacterial DNA damage response
Lima-Noronha, M. A., Fonseca, D. L. H., Oliveira, R. S., Freitas, R. R., Park, J. H., & Galhardo, R. S. (2022) · Genetics and Molecular Biology · doi:10.1590/1678-4685-gmb-2022-0107 · Cited by 37 · see citing works
Gan, R., Wu, X., He, W., Liu, Z., Wu, S., Chen, C., Chen, S., Xiang, Q., Deng, Z., Liang, D., et al. (2014) · Scientific Reports · doi:10.1038/srep06642 · Cited by 47 · see citing works
The relevance of persisters in tuberculosis drug discovery
Mandal, S., Njikan, S., Kumar, A., Early, J. V., & Parish, T. (2019) · Microbiology · doi:10.1099/mic.0.000760 · Cited by 47 · see citing works
Petek, M., Baebler, Š., Kuzman, D., Rotter, A., Podlesek, Z., Gruden, K., Ravnikar, M., & Urleb, U. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-159 · Cited by 47 · see citing works
Insights into the complex levels of regulation imposed on Escherichia coli DNA polymerase V
Goodman, M. F., McDonald, J. P., Jaszczur, M. M., & Woodgate, R. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.05.005 · Cited by 46 · see citing works
Szabó, J. E., Németh, V., Papp‐Kádár, V., Nyíri, K., Leveles, I., Bendes, Á. Á., Zagyva, I., Róna, G., Pálinkás, H. L., Besztercei, B., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku882 · Cited by 45 · see citing works
Type III-A CRISPR immunity promotes mutagenesis of staphylococci
Mo, C. Y., Mathai, J., Rostøl, J. T., Varble, A., Banh, D. V., & Marraffini, L. A. (2021) · Nature · doi:10.1038/s41586-021-03440-3 · Cited by 44 · see citing works
Gottschalk, S., Ifrah, D., Søndergaard, S. L., Gottlieb, C. T., Cohn, M. T., Hiasa, H., Hansen, P. B., Gram, L., Ingmer, H., & Thomsen, L. E. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-192 · Cited by 41 · see citing works
Antibiotics trigger initiation of SCCmec transfer by inducing SOS responses
Liu, P., Wu, Z., Xue, H., & Zhao, X. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx153 · Cited by 40 · see citing works
New insights into the structures and interactions of bacterial Y-family DNA polymerases
Timinskas, K., & Venclovas, Č. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz198 · Cited by 40 · see citing works
Bacterial SOS response: a food safety perspective
van der Veen, S., & Abee, T. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.11.012 · Cited by 40 · see citing works
Computational analysis of LexA regulons in Cyanobacteria
Li, S., Xu, M., & Su, Z. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-527 · Cited by 39 · see citing works
Denève-Larrazet, C., Bouttier, S., Dupuy, B., Barbut, F., Collignon, A., & Janoir, C. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00532-09 · Cited by 39 · see citing works
Effect of combined oxidative and nitrosative stresses on Staphylococcus aureus transcriptome
Nobre, L. S., & Saraiva, L. M. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-4730-3 · Cited by 38 · see citing works
Canfield, G. S., Schwingel, J. M., Foley, M. H., Vore, K. L., Boonanantanasarn, K., Gill, A. L., Sutton, M. D., & Gill, S. R. (2012) · Journal of Bacteriology · doi:10.1128/jb.00733-12 · Cited by 38 · see citing works
Proulx, M. K., Palace, S. G., Gandra, S., Torres, B., Weir, S. K., Stiles, T., Ellison, R. T., & Goguen, J. D. (2015) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiv512 · Cited by 38 · see citing works
SosA inhibits cell division in Staphylococcus aureus in response to DNA damage
Bojer, M. S., Wacnik, K., Kjelgaard, P., Gallay, C., Bottomley, A. L., Cohn, M., Lindahl, G., Frees, D., Veening, J., Foster, S., et al. (2018) · bioRxiv · doi:10.1111/mmi.14350 · Cited by 34 · see citing works
Lima, M. C., de Barros, M., Scatamburlo, T. M., Polveiro, R. C., de Castro, L. K., Guimarães, S. H. S., da Costa, S. L., da Costa, M. M., & Moreira, M. A. S. (2020) · BMC Microbiology · doi:10.1186/s12866-020-01793-9 · Cited by 38 · see citing works
Butterfield, J. M., Tsuji, B. T., Brown, J. E., Ashley, E. D., Hardy, D. J., Brown, K., Forrest, A., & Lodise, T. P. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00407-11 · Cited by 37 · see citing works
Zhu, X., Feng, T., Chen, Y., Xiao, Y. C., Wen, W. N., Wang, S., Wang, D., Zhang, X., Liang, J., & Xiong, H. (2024) · Small · doi:10.1002/smll.202310247 · Cited by 36 · see citing works
Mutational Consequences of Ciprofloxacin in Escherichia coli
Song, L. Y., Goff, M., Davidian, C., Mao, Z., London, M., Lam, K., Yung, M., & Miller, J. H. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01415-16 · Cited by 36 · see citing works
Cohabitation of Two DifferentlexARegulons inPseudomonas putida
Abella, M., Campoy, S., Erill, I., Rojo, F., & Barbé, J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01213-07 · Cited by 35 · see citing works
Activation of the SOS response increases the frequency of small colony variants
Vestergaard, M. R., Paulander, W., & Ingmer, H. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1735-2 · Cited by 34 · see citing works
Veiga, H., Jousselin, A., Schäper, S., Saraiva, B. M., Marques, L. B., Reed, P., Wilton, J., Pereira, P. M., Filipe, S. R., & Pinho, M. G. (2023) · The EMBO Journal · doi:10.15252/embj.2022112140 · Cited by 34 · see citing works
Baicalein Suppresses the SOS Response System of Staphylococcus Aureus Induced by Ciprofloxacin
Peng, Q., Zhou, S., Yao, F., Hou, B., Huang, Y., Hua, D., Zheng, Y., & Yuanshu, Q. (2011) · Cellular Physiology and Biochemistry · doi:10.1159/000335791 · Cited by 34 · see citing works
Chen, Z., Luong, T. T., & Lee, C. Y. (2007) · Journal of Bacteriology · doi:10.1128/jb.01079-07 · Cited by 34 · see citing works
Varhimo, E., Savijoki, K., Jalava, J., Kuipers, O. P., & Varmanen, P. (2007) · Journal of Bacteriology · doi:10.1128/jb.00473-07 · Cited by 34 · see citing works
In Vitro Synergy of Biochanin A and Ciprofloxacin against Clinical Isolates of Staphylococcus aureus
Liu, G., Liang, J., Wang, X., Li, Z., Wang, W., Guo, N., Wu, X., Shen, F., Xing, M., Liu, L., et al. (2011) · Molecules · doi:10.3390/molecules16086656 · Cited by 33 · see citing works
Reducing the Bottleneck in Discovery of Novel Antibiotics
Jones, M. B., Nierman, W. C., Shan, Y., Frank, B. C., Spoering, A. L., Ling, L. L., Peoples, A. J., Zullo, A. M., Lewis, K., & Nelson, K. E. (2016) · Microbial Ecology · doi:10.1007/s00248-016-0889-3 · Cited by 33 · see citing works
Self-citationPlata, K. B., Riosa, S., Singh, C. R., Rosato, R. R., & Rosato, A. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061083 · Cited by 33 · see citing works
An exclusion list based label‐free proteome quantification approach using an LTQ Orbitrap
Muntel, J., Hecker, M., & Becher, D. (2012) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.6147 · Cited by 33 · see citing works
Mohiuddin, S. G., Ghosh, S., Kavousi, P., & Orman, M. A. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.02024-22 · Cited by 32 · see citing works
Cooper, B., Islam, N., Xu, Y., Beard, H. S., Garrett, W. M., Gu, G., & Nou, X. (2018) · PROTEOMICS · doi:10.1002/pmic.201700461 · Cited by 32 · see citing works
Tattevin, P., Basuino, L., & Chambers, H. F. “. (2009) · Research in Microbiology · doi:10.1016/j.resmic.2009.03.003 · Cited by 32 · see citing works
- Authors
- Cirz, R. T., Jones, M. B., Gingles, N. A., Minogue, T. D., Jarrahi, B., Peterson, S. N., & Romesberg, F. E.
- Affiliations
- Scripps Research Institute (US)
- Pathogen Functional Genomics Resource Center (PFGRC), The Institute for Genomic Research, Rockville, Maryland 20850
- Corresponding author
- Romesberg, Floyd E.
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2007-01-15
- Volume
- 189
- Issue
- 2
- Pages
- 531-539
- ISSN
- 0021-9193 (ISSN-L)
- 1098-5530
- PMC
- PMC1797410
- OpenAlex
- W1991848397
- Cited by
- 273
- References
- 46
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 22 · 2023: 15 · 2022: 14 · 2021: 20 · 2020: 19 · 2019: 14 · 2018: 13 · 2017: 8 · 2016: 12 · 2015: 11 · 2014: 10 · 2013: 16 · 2012: 17
- FWCI
- 6.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Bacteriology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (n01ai15447-36-0-3)
- Office of Naval Research
- National Institute of Allergy and Infectious Diseases (N01 AI015447)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- Staphylococcus aureus, ciprofloxacin, SOS response, antibiotic resistance, bacterial persistence, TCA cycle, LexA, RecA, induced mutation, UV damage
- MeSH terms
- Anti-Bacterial Agents, Bacterial Proteins, Ciprofloxacin, Citric Acid Cycle, Mutation, SOS Response, Genetics, Staphylococcus aureus, Ultraviolet Rays, Gene Expression Regulation, Bacterial, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Drug Resistance, Bacterial
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