Increased survival of antibiotic-resistant Escherichia coli inside macrophages

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 1, 2013, Pages 189-195

  Miskinyte, Migla ^a   Gordo, Isabel ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING) A; NALIDIXIC ACID; PROTEIN; RIFAMPICIN; RNA POLYMERASE BETA SUBUNIT; RPSL PROTEIN; STREPTOMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ESCHERICHIA COLI; GENE MUTATION; GROWTH RATE; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; SURVIVAL;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL LINE; DNA GYRASE; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENETIC FITNESS; MACROPHAGES; MICE; MICROBIAL VIABILITY; NALIDIXIC ACID; POINT MUTATION; RIBOSOMAL PROTEINS; RIFAMPIN; STREPTOMYCIN;

EID: 84872035293     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01632-12     Document Type: Article

References (55)

1. Denamur E, Picard B, Tenaillon O. 2010. Population genetics of pathogenic Escherichia coli, p 269-286. In Bacterial population genetics in infectious disease. John Wiley & Sons, Inc, New York, NY.
2. Rolhion N, Darfeuille-Michaud A. 2007. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm. Bowel Dis. 13:1277-1283. (Pubitemid 47597778)
3. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140. (Pubitemid 39490066)
4. Bailey JK, Pinyon JL, Anantham S, Hall RM. 2010. Commensal Escherichia coli of healthy humans: a reservoir for antibiotic-resistance determinants. J. Med. Microbiol. 59:1331-1339.
5. Levert M, Zamfir O, Clermont O, Bouvet O, Lespinats S, Hipeaux MC, Branger C, Picard B, Saint-Ruf C, Norel F, Balliau T, Zivy M, Le Nagard H, Cruveiller S, Chane-Woon-Ming B, Nilsson S, Gudelj I, Phan K, Ferenci T, Tenaillon O, Denamur E. 2010. Molecular and evolutionary bases of within-patient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Pathog. 6:e1001125. doi:10.1371/journal.ppat.1001125.
6. Andersson DI, Hughes D. 2010. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8:260-271.
7. Maclean RC, Hall AR, Perron GG, Buckling A. 2010. The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nat. Rev. Genet. 11:405-414.
8. Gagneux S, Long CD, Small PM, Van T, Schoolnik GK, Bohannan BJ. 2006. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312:1944-1946. (Pubitemid 43993719)
9. Trindade S, Sousa A, Xavier KB, Dionisio F, Ferreira MG, Gordo I. 2009. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet. 5:e1000578. doi:10.1371/journal.pgen.1000578.
10. Bataillon T, Zhang T, Kassen R. 2011. Cost of adaptation and fitness effects of beneficial mutations in Pseudomonas fluorescens. Genetics 189:939-949.
11. Hall AR, Iles JC, Maclean RC. 2011. The fitness cost of rifampicin resistance in Pseudomonas aeruginosa depends on demand for RNA polymerase. Genetics 187:817-822.
12. Macvanin M, Bjorkman J, Eriksson S, Rhen M, Andersson DI, Hughes D. 2003. Fusidic acid-resistant mutants of Salmonella enterica serovar Typhimurium with low fitness in vivo are defective in RpoS induction. Antimicrob. Agents Chemother. 47:3743-3749. (Pubitemid 37484982)
13. Paulander W, Maisnier-Patin S, Andersson DI. 2009. The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source, and RpoS (σS). Genetics 183:539-546.
14. Trindade S, Sousa A, Gordo I. 2012. Antibiotic resistance and stress in the light of Fisher's model. Evolution doi:10.1111/j.1558-5646.2012.01722.x.
15. Adams KN, Takaki K, Connolly LE, Wiedenhoft H, Winglee K, Humbert O, Edelstein PH, Cosma CL, Ramakrishnan L. 2011. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145:39-53.
16. Bjorkman J, Hughes D, Andersson DI. 1998. Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 95:3949-3953. (Pubitemid 28173234)
17. Bjorkholm B, Sjolund M, Falk PG, Berg OG, Engstrand L, Andersson DI. 2001. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 98:14607-14612. (Pubitemid 33121439)
18. Enne VI, Delsol AA, Roe JM, Bennett PM. 2004. Rifampicin resistance and its fitness cost in Enterococcus faecium. J. Antimicrob. Chemother. 53:203-207. (Pubitemid 38239951)
19. Giraud E, Cloeckaert A, Baucheron S, Mouline C, Chaslus-Dancla E. 2003. Fitness cost of fluoroquinolone resistance in Salmonella enterica serovar Typhimurium. J. Med. Microbiol. 52:697-703. (Pubitemid 36981479)
20. Luo N, Pereira S, Sahin O, Lin J, Huang S, Michel L, Zhang Q. 2005. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl. Acad. Sci. U. S. A. 102:541-546. (Pubitemid 40282701)
21. Hegreness M, Shoresh N, Hartl D, Kishony R. 2006. An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311:1615-1617.
22. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. (Pubitemid 30412767)
23. Thomason LC, Costantino N, Court DL. 2007. E. coli genome manipulation by P1 transduction. Curr. Protoc. Mol. Biol. Chapter 1:Unit 117.
24. Elena SF, Lenski RE. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457-469. (Pubitemid 36648145)
25. Maree AF, Keulen W, Boucher CA, De Boer RJ. 2000. Estimating relative fitness in viral competition experiments. J. Virol. 74:11067-11072. (Pubitemid 32223971)
26. Hamrick TS, Havell EA, Horton JR, Orndorff PE. 2000. Host and bacterial factors involved in the innate ability of mouse macrophages to eliminate internalized unopsonized Escherichia coli. Infect. Immun. 68:125-132. (Pubitemid 30016687)
27. Lim AC, Mak KCN, Ng NUT, Ng TKK. 2007. Multiple modes of protection against hydrogen peroxide-induced oxidative damage in stationary and exponential phase Escherichia coli by DNA-binding protein (Dps). J. Exp. Microbiol. Immunol. 11:86-92.
28. Ferenci T. 2005. Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol. Microbiol. 57:1-8. (Pubitemid 40896592)
29. De Paepe M, Gaboriau-Routhiau V, Rainteau D, Rakotobe S, Taddei F, Cerf-Bensussan N. 2011. Trade-off between bile resistance and nutritional competence drives Escherichia coli diversification in the mouse gut. PLoS Genet. 7:e1002107. doi:10.1371/journal.pgen.1002107.
30. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S. 2000. Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J. Bacteriol. 182:5225-5230.
31. Crofton J, Mitchison DA. 1948. Streptomycin resistance in pulmonary tuberculosis. BMJ 2:1009-1015.
32. Barreto A, Guimaraes B, Radhouani H, Araujo C, Goncalves A, Gaspar E, Rodrigues J, Igrejas G, Poeta P. 2009. Detection of antibiotic resistant Escherichia coli and Enterococcus spp. in stool of healthy growing children in Portugal. J. Basic Microbiol. 49:503-512.
33. Hong S, Choi YH, Choo YA, Choi Y, Choi SY, Kim DW, Lee BK, Park MS. 2010. Genetic characterization of atypical Shigella flexneri isolated in Korea. J. Microbiol. Biotechnol. 20:1457-1462.
34. Rahmani F, Fooladi AA, Marashi SM, Nourani MR. 2012. Drug resistance in Vibrio cholerae strains isolated from clinical specimens. Acta Microbiol. Immunol. Hung. 59:77-84.
35. Tseng JT, Bryan LE, Van Den Elzen HM. 1972. Mechanisms and spectrum of streptomycin resistance in a natural population of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2:136-141.
36. Sreevatsan S, Pan X, Stockbauer KE, Williams DL, Kreiswirth BN, Musser JM. 1996. Characterization of rpsL and rrs mutations in streptomycin-resistant Mycobacterium tuberculosis isolates from diverse geographic localities. Antimicrob. Agents Chemother. 40:1024-1026. (Pubitemid 26115243)
37. Zaher HS, Green R. 2010. Hyperaccurate and error-prone ribosomes exploit distinct mechanisms during tRNA selection. Mol. Cell 39:110-120.
38. Bilgin N, Claesens F, Pahverk H, Ehrenberg M. 1992. Kinetic properties of Escherichia coli ribosomes with altered forms of S12. J. Mol. Biol. 224:1011-1027.
39. Okamoto-Hosoya Y, Hosaka T, Ochi K. 2003. An aberrant protein synthesis activity is linked with antibiotic overproduction in rpsL mutants of Streptomyces coelicolor A3(2). Microbiology 149:3299-3309. (Pubitemid 37442012)
40. Ballesteros M, Fredriksson A, Henriksson J, Nystrom T. 2001. Bacterial senescence: protein oxidation in non-proliferating cells is dictated by the accuracy of the ribosomes. EMBO J. 20:5280-5289. (Pubitemid 32910922)
41. Cabiscol E, Tamarit J, Ros J. 2000. Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 3:3-8.
42. Liu G, Xu X, He L, Ding Z, Gu Y, Zhang J, Zhou L. 2011. Primary antibiotic resistance of Helicobacter pylori isolated from Beijing children. Helicobacter 16:356-362.
43. Sekiguchi J, Miyoshi-Akiyama T, Augustynowicz-Kopec E, Zwolska Z, Kirikae F, Toyota E, Kobayashi I, Morita K, Kudo K, Kato S, Kuratsuji T, Mori T, Kirikae T. 2007. Detection of multidrug resistance in Mycobacterium tuberculosis. J. Clin. Microbiol. 45:179-192. (Pubitemid 46106425)
44. Yesilyurt M, Kilic S, Celebi B, Celik M, Gul S, Erdogan F, Ozel G. 2011. Antimicrobial susceptibilities of Francisella tularensis subsp. holarctica strains isolated from humans in the Central Anatolia region of Turkey. J. Antimicrob. Chemother. 66:2588-2592.
45. Cavusoglu C, Turhan A, Akinci P, Soyler I. 2006. Evaluation of the Genotype MTBDR assay for rapid detection of rifampin and isoniazid resistance in Mycobacterium tuberculosis isolates. J. Clin. Microbiol. 44:2338-2342. (Pubitemid 44092395)
46. Tan Y, Hu Z, Zhao Y, Cai X, Luo C, Zou C, Liu X. 2012. The beginning of the rpoB gene in addition to the rifampin resistance determination region might be needed for identifying rifampin/rifabutin cross-resistance in multidrug-resistant Mycobacterium tuberculosis isolates from Southern China. J. Clin. Microbiol. 50:81-85.
47. Kawamura N, Kurokawa K, Ito T, Hamamoto H, Koyama H, Kaito C, Sekimizu K. 2005. Participation of Rho-dependent transcription termination in oxidative stress sensitivity caused by an rpoB mutation. Genes Cells 10:477-487. (Pubitemid 40590365)
48. Maughan H, Galeano B, Nicholson WL. 2004. Novel rpoB mutations conferring rifampin resistance on Bacillus subtilis: global effects on growth, competence, sporulation, and germination. J. Bacteriol. 186:2481-2486. (Pubitemid 38451852)
49. Perkins AE, Nicholson WL. 2008. Uncovering new metabolic capabilities of Bacillus subtilis using phenotype profiling of rifampin-resistant rpoB mutants. J. Bacteriol. 190:807-814. (Pubitemid 351170923)
50. Zhou YN, Jin DJ. 1998. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like "stringent" RNA polymerases in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 95:2908-2913. (Pubitemid 128617610)
51. Ghosh AR, Thanasekaran K, Roy S. 2011. Nalidixic acid-resistant Shigella sonnei infection among dysenteric children in Port Blair. J. Microbiol. Antimicrob. 3:87-93.
52. Kumar Y, Sharma A, Mani KR. 2009. High level of resistance to nalidixic acid in Salmonella enterica serovar Typhi in Central India. J. Infect. Dev. Countries 3:467-469.
53. Wu TL, Su LH, Chia JH, Kao TM, Chiu CH, Kuo AJ, Sun CF. 2002. Molecular epidemiology of nalidixic acid-resistant campylobacter isolates from humans and poultry by pulsed-field gel electrophoresis and flagellin gene analysis. Epidemiol. Infect. 129:227-231.
54. Hopkins KL, Arnold C, Threlfall EJ. 2007. Rapid detection of gyrA and parC mutations in quinolone-resistant Salmonella enterica using pyrosequencing technology. J. Microbiol. Methods 68:163-171. (Pubitemid 46054328)
55. Petersen A, Aarestrup FM, Olsen JE. 2009. The in vitro fitness cost of antimicrobial resistance in Escherichia coli varies with the growth conditions. FEMS Microbiol. Lett. 299:53-59.