The AcrAB RND efflux system from the live vaccine strain of Francisella tularensis is a multiple drug efflux system that is required for virulence in mice

FEMS Microbiology Letters

Volumn 279, Issue 2, 2008, Pages 226-233

  Bina, Xiaowen R ^a   Lavine, Christy L ^a   Miller, Mark A ^a   Bina, James E ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Antibiotic resistance; Efflux; Francisella; RND; Virulence

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; CARBENICILLIN; CEFOPERAZONE; CHLORAMPHENICOL; CHOLIC ACID; CIPROFLOXACIN; DEOXYCHOLIC ACID; DODECYL SULFATE SODIUM; ERYTHROMYCIN; GENOMIC DNA; GENTAMICIN; KANAMYCIN; NALIDIXIC ACID; POLYMYXIN B; RIFAMPICIN; TETRACYCLINE; TRITON X 100;

ACRAB GENE; ACTIVE TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; COLONY FORMING UNIT; CONTROLLED STUDY; DSBB GENE; ESCHERICHIA COLI; FRANCISELLA TULARENSIS; GENE MUTATION; GRAM NEGATIVE BACTERIUM; GRAM NEGATIVE INFECTION; LIVER; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SPLEEN; STRAIN IDENTIFICATION;

ANIMALS; ANTI-BACTERIAL AGENTS; FEMALE; FRANCISELLA TULARENSIS; LETHAL DOSE 50; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED BALB C; MUTAGENESIS, INSERTIONAL; SURVIVAL ANALYSIS; TULAREMIA; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; MURINAE; MUS;

EID: 38349144550     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2007.01033.x     Document Type: Article

References (42)

1. Alexeyev MF Shokolenko IN (1995) RP4 oriT and RP4 oriT-R6K oriV DNA cassettes for construction of specialized vectors. Biotechniques 19 : 22 24, 26.
2. Anda P, Segura del Pozo J, Diaz Garcia JM, Escudero R, Garcia Pena FJ, Lopez Velasco MC, Sellek RE, Jimenez Chillaron MR, Sanchez Serrano LP Martinez Navarro JF (2001) Waterborne outbreak of tularemia associated with crayfish fishing. Emerg Infect Dis 7 : (3 Suppl) : 575 582.
3. Bina JE, Provenzano D, Wang C, Bina XR Mekalanos JJ (2006a) Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch Microbiol 186 : 171 181.
4. Bina XR, Wang C, Miller MA Bina JE (2006b) The Bla2 beta-lactamase from the live-vaccine strain of Francisella tularensis encodes a functional protein that is only active against penicillin-class beta-lactam antibiotics. Arch Microbiol 186 : 219 228.
5. Buckley AM, Webber MA, Cooles S, Randall LP, La Ragione RM, Woodward MJ Piddock LJ (2006) The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol 8 : 847 856.
6. Chan YY Chua KL (2005) The Burkholderia pseudomallei BpeAB-OprB efflux pump: expression and impact on quorum sensing and virulence. J Bacteriol 187 : 4707 4719.
7. Cross JT Jacobs RF (1993) Tularemia: treatment failures with outpatient use of ceftriaxone. Clin Infect Dis 17 : 976 980.
8. Cross JT Penn RL (2000) Francisella tularensis (tularemia). Principles and Practice of Infectious Diseases, 5th edn (Mandell GL, Bennett JE Dolin R, eds) Churchill Livingston, Philadelphia.
9. Curiale MS Levy SB (1982) Two complementation groups mediate tetracycline resistance determined by Tn10. J Bacteriol 151 : 209 215.
10. Ellis J, Oyston PC, Green M Titball RW (2002) Tularemia. Clin Microbiol Rev 15 : 631 646.
11. Elzer PH, Kovach ME, Phillips RW, Robertson GT, Peterson KM Roop RM II. (1995) In vivo and in vitro stability of the broad-host-range cloning vector pBBR1MCS in six Brucella species. Plasmid 33 : 51 57.
12. Evans ME (1985) Francisella tularensis. Infect Contr 6 : 381 383.
13. Fernandez-Recio J, Walas F, Federici L, Venkatesh Pratap J, Bavro VN, Miguel RN, Mizuguchi K Luisi B (2004) A model of a transmembrane drug-efflux pump from Gram-negative bacteria. FEBS Lett 578 : 5 9.
14. Francis E (1937) Sources of infection and seasonal incidence of tularemia in man. Publ Health Rep 52 : 103.
15. Gil H, Platz GJ, Forestal CA, Monfett M, Bakshi CS, Sellati TJ, Furie MB, Benach JL Thanassi DG (2006) Deletion of TolC orthologs in Francisella tularensis identifies roles in multidrug resistance and virulence. Proc Natl Acad Sci USA 103 : 12897 12902.
16. Greco D, Allegrini G, Tizzi T, Ninu E, Lamanna A Luzi S (1987) A waterborne tularemia outbreak. Eur J Epidemiol 3 : 35 38.
17. Hirakata Y, Srikumar R, Poole K, Gotoh N, Suematsu T, Kohno S, Kamihira S, Hancock RE Speert DP (2002) Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J Exp Med 196 : 109 118.
18. Jerse AE, Sharma ND, Simms AN, Crow ET, Snyder LA Shafer WM (2003) A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect Immun 71 : 5576 5582.
19. Kadokura H, Katzen F Beckwith J (2003) Protein disulfide bond formation in prokaryotes. Annu Rev Biochem 72 : 111 135.
20. Karpoff SP Antononoff NI (1936) The spread of tularemia through water as a new factor in its epidemiology. J Bacteriol 32 : 243.
21. Kawula TH, Hall JD, Fuller JR Craven RR (2004) Use of transposon-transposase complexes to create stable insertion mutant strains of Francisella tularensis LVS. Appl Environ Microbiol 70 : 6901 6904.
22. Li XZ, Nikaido H Poole K (1995) Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39 : 1948 1953.
23. Lin J, Sahin O, Michel LO Zhang Q (2003) Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun 71 : 4250 4259.
24. Lomovskaya O, Zgurskaya HI, Totrov M Watkins WJ (2007) Waltzing transporters and 'the dance macabre' between humans and bacteria. Nat Rev Drug Discov 6 : 56 65.
25. Ma D, Cook DN, Alberti M, Pon NG, Nikaido H Hearst JE (1995) Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol 16 : 45 55.
26. Maier TM, Havig A, Casey M, Nano FE, Frank DW Zahrt TC (2004) Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl Environ Microbiol 70 : 7511 7519.
27. Maier TM, Casey MS, Becker RH, Dorsey CW, Glass EM, Maltsev N, Zahrt TC Frank DW (2007) Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 75 : 5376 5389.
28. Nishino K, Latifi T Groisman EA (2006) Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol Microbiol 59 : 126 141.
29. Piddock LJ (2006a) Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 19 : 382 402.
30. Piddock LJ (2006b) Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4 : 629 636.
31. Raivio TL (2005) Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol 56 : 1119 1128.
32. Saier MH Jr. Paulsen IT (2001) Phylogeny of multidrug transporters. Semin Cell Dev Biol 12 : 205 213.
33. Sjostedt A (2007) Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann NY Acad Sci 1105 : 1 29.
34. Stahler FN, Odenbreit S, Haas R, Wilrich J, Van Vliet AH, Kusters JG, Kist M Bereswill S (2006) The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect Immun 74 : 3845 3852.
35. Su J, Yang J, Zhao D, Kawula TH, Banas JA Zhang JR (2007) Genome-wide identification of Francisella tularensis virulence determinants. Infect Immun 75 : 3089 3101.
36. Syrjala H, Kujala P, Myllyla V Salminen A (1985) Airborne transmission of tularemia in farmers. Scand J Infect Dis 17 : 371 375.
37. Szybalski W (1952) Gradient plate technique for study of bacteria resistance. Science 116 : 46 48.
38. Tarnvik A (1989) Nature of protective immunity to Francisella tularensis. Rev Infect Dis 11 : 440 451.
39. Tempel R, Lai XH, Crosa L, Kozlowicz B Heffron F (2006) Attenuated Francisella novicida transposon mutants protect mice against wild-type challenge. Infect Immun 74 : 5095 5105.
40. Teutsch SM, Martone WJ, Brink EW, Potter ME, Eliot G, Hoxsie R, Craven RB Kaufmann AF (1979) Pneumonic tularemia on Martha's Vineyard. New England J Med 301 : 826 828.
41. Van Bambeke F, Glupczynski Y, Plesiat P, Pechere JC Tulkens PM (2003) Antibiotic efflux pumps in prokaryotic cells: occurrence, impact on resistance and strategies for the future of antimicrobial therapy. J Antimicrob Chemother 51 : 1055 1065.
42. Weiss DS, Brotcke A, Henry T, Margolis JJ, Chan K Monack DM (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci USA 104 : 6037 6042.