Trade-offs between drug toxicity and benefit in the multi-antibiotic resistance system underlie optimal growth of E. coli

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Wood, Kevin B ^a   Cluzel, Philippe ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTIINFECTIVE AGENT; SALICYLIC ACID DERIVATIVE;

ANTIBIOTIC RESISTANCE; ARTICLE; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; ESCHERICHIA COLI; GROWTH, DEVELOPMENT AND AGING; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SYSTEMS BIOLOGY;

ANTI-BACTERIAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI; MICROBIAL SENSITIVITY TESTS; SALICYLATES; STRESS, PHYSIOLOGICAL; SYSTEMS BIOLOGY;

EID: 84861392612     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-48     Document Type: Article

References (42)

1. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 2004, 10(12 Suppl):S122-S129.
2. Alekshun MN, Levy SB. The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol 1999, 7(10):410-413. 10.1016/S0966-842X(99)01589-9, 10498949.
3. Cohen SP, Hachler H, Levy SB. Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol 1993, 175(5):1484-1492. 193236, 8383113.
4. Cohen SP, Levy SB, Foulds J, Rosner JL. Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar- independent pathway. J Bacteriol 1993, 175(24):7856-7862. 206962, 7504664.
5. Critzer FJ, Dsouza DH, Golden DA. Transcription analysis of stx1, marA, and eaeA genes in Escherichia coli O157:H7 treated with sodium benzoate. J Food Prot 2008, 71(7):1469-1474.
6. Herbert D, Paramasivan CN, Venkatesan P, Kubendiran G, Prabhakar R, Mitchison DA. Bactericidal action of ofloxacin, sulbactam-ampicillin, rifampin, and isoniazid on logarithmic- and stationary-phase cultures of Mycobacterium tuberculosis. Antimicrob Agents Chemother 1996, 40(10):2296-2299. 163523, 8891133.
7. Potenski CJ, Gandhi M, Matthews KR. Exposure of Salmonella Enteritidis to chlorine or food preservatives decreases [corrected] susceptibility to antibiotics. FEMS Microbiol Lett 2003, 220(2):181-186. 10.1016/S0378-1097(03)00099-5, 12670679.
8. Tavio MM, Vila J, Perilli M, Casanas LT, Macia L, Amicosante G, de Jimenez Anta MT. Enhanced active efflux, repression of porin synthesis and development of Mar phenotype by diazepam in two enterobacteria strains. J Med Microbiol 2004, 53(Pt 11):1119-1122.
9. Viveiros M, Jesus A, Brito M, Leandro C, Martins M, Ordway D, Molnar AM, Molnar J, Amaral L. Inducement and reversal of tetracycline resistance in Escherichia coli K-12 and expression of proton gradient-dependent multidrug efflux pump genes. Antimicrob Agents Chemother 2005, 49(8):3578-3582. 10.1128/AAC.49.8.3578-3582.2005, 1196278, 16048990.
10. Greco WR, Bravo G, Parsons JC. The search for synergy: a critical review from a response surface perspective. Pharmacol Rev 1995, 47(2):331-385.
11. Bliss CI. The calculation of microbial assays. Bacteriol Rev 1956, 20(4):243-258. 180866, 13403845.
12. Loewe S. The problem of synergism and antagonism of combined drugs. Arzneimittelforschung 1953, 3(6):285-290.
13. Chait R, Craney A, Kishony R. Antibiotic interactions that select against resistance. Nature 2007, 446(7136):668-671. 10.1038/nature05685, 17410176.
14. Hegreness M, Shoresh N, Damian D, Hartl D, Kishony R. Accelerated evolution of resistance in multidrug environments. Proc Natl Acad Sci USA 2008, 105(37):13977-13981. 10.1073/pnas.0805965105, 2544564, 18779569.
15. Michel JB, Yeh PJ, Chait R, Moellering RC, Kishony R. Drug interactions modulate the potential for evolution of resistance. Proc Natl Acad Sci USA 2008, 105(39):14918-14923. 10.1073/pnas.0800944105, 2567468, 18815368.
16. Chait R, Shrestha S, Shah AK, Michel JB, Kishony R. A differential drug screen for compounds that select against antibiotic resistance. PLoS One 2010, 5(12):e15179. 10.1371/journal.pone.0015179, 2999542, 21209699.
17. Torella JP, Chait R, Kishony R. Optimal drug synergy in antimicrobial treatments. PLoS Comput Biol 2010, 6(6):e1000796. 10.1371/journal.pcbi.1000796, 2880566, 20532210.
18. Levy SB. Active efflux mechanisms for antimicrobial resistance. Antimicrob Agents Chemother 1992, 36(4):695-703. 10.1128/AAC.36.4.695, 189356, 1503431.
19. Levy SB. Active efflux, a common mechanism for biocide and antibiotic resistance. J Appl Microbiol 2002, 92(Suppl):65S-71S.
20. Okusu H, Ma D, Nikaido H. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J Bacteriol 1996, 178(1):306-308. 177656, 8550435.
21. Wall ME, Markowitz DA, Rosner JL, Martin RG. Model of transcriptional activation by MarA in Escherichia coli. PLoS Comput Biol 2009, 5(12):e1000614. 10.1371/journal.pcbi.1000614, 2787020, 20019803.
22. Cohen SP, Hooper DC, Wolfson JS, Souza KS, McMurry LM, Levy SB. Endogenous active efflux of norfloxacin in susceptible Escherichia coli. Antimicrob Agents Chemother 1988, 32(8):1187-1191. 10.1128/AAC.32.8.1187, 172374, 3056253.
23. Cohen SP, McMurry LM, Hooper DC, Wolfson JS, Levy SB. Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob Agents Chemother 1989, 33(8):1318-1325. 10.1128/AAC.33.8.1318, 172647, 2679373.
24. Cohen SP, McMurry LM, Levy SB. marA locus causes decreased expression of OmpF porin in multiple-antibiotic-resistant (Mar) mutants of Escherichia coli. J Bacteriol 1988, 170(12):5416-5422. 211632, 2848006.
25. McMurry LM, George AM, Levy SB. Active efflux of chloramphenicol in susceptible Escherichia coli strains and in multiple-antibiotic-resistant (Mar) mutants. Antimicrob Agents Chemother 1994, 38(3):542-546. 10.1128/AAC.38.3.542, 284495, 8203852.
26. Rosner JL. Nonheritable resistance to chloramphenicol and other antibiotics induced by salicylates and other chemotactic repellents in Escherichia coli K-12. Proc Natl Acad Sci USA 1985, 82(24):8771-8774. 10.1073/pnas.82.24.8771, 391519, 3909154.
27. Price CT, Lee IR, Gustafson JE. The effects of salicylate on bacteria. Int J Biochem Cell Biol 2000, 32(10):1029-1043. 10.1016/S1357-2725(00)00042-X, 11091136.
28. Fitzgerald JB, Schoeberl B, Nielsen UB, Sorger PK. Systems biology and combination therapy in the quest for clinical efficacy. Nat Chem Biol 2006, 2(9):458-466. 10.1038/nchembio817, 16921358.
29. Yeh P, Tschumi AI, Kishony R. Functional classification of drugs by properties of their pairwise interactions. Nat Genet 2006, 38(4):489-494. 10.1038/ng1755, 16550172.
30. Lehar J, Zimmermann GR, Krueger AS, Molnar RA, Ledell JT, Heilbut AM, Short GF, Giusti LC, Nolan GP, Magid OA, et al. Chemical combination effects predict connectivity in biological systems. Mol Syst Biol 2007, 3:80. 1828746, 17332758.
31. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006, 2:2006 0008. 1681482, 16738554.
32. Fralick JA. Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli. J Bacteriol 1996, 178(19):5803-5805. 178425, 8824631.
33. Alekshun MN, Levy SB, Mealy TR, Seaton BA, Head JF. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 A resolution. Nat Struct Biol 2001, 8(8):710-714. 10.1038/90429, 11473263.
34. Li F, Sethi G. Targeting transcription factor NF-kappaB to overcome chemoresistance and radioresistance in cancer therapy. Biochim Biophys Acta 2010, 1805(2):167-180.
35. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141(1):69-80. 10.1016/j.cell.2010.02.027, 2851638, 20371346.
36. George AM, Levy SB. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J Bacteriol 1983, 155:531-540. 217720, 6348022.
37. Alekshun MN, Levy SB. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob Agents Chemother 1997, 41:2067-2075. 164072, 9333027.
38. Maneewannakul K, Levy S. Identification of mar mutants among quinolone-resistant clinical isolates of Escherichia coli. Antimicrob Agents Chemother 1996, 40:1695-1698. 163397, 8807064.
39. Guet C, Bruneaux L, Oikonomou P, Cluzel P. In preparation 2011, 18.
40. Le TT, Emonet T, Harlepp S, Guet CC, Cluzel P. Dynamical determinants of druginducible gene expression in a single bacterium. Biophys J 2006, 90:3315-3321. 10.1529/biophysj.105.073353, 1432126, 16461398.
41. Lutz R, Bujard H. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 1997, 25:1203-1210. 10.1093/nar/25.6.1203, 146584, 9092630.
42. Elf J, Nilsson K, Tenson T, Ehrenberg M. Bistable bacterial growth rate in response to antibiotics with low membrane permeability. Phys Rev Lett 2006, 97:258104.