Escherichia coli from retail meats carry genes associated with uropathogenic Escherichia coli, but are weakly invasive in human bladder cell culture

Journal of Applied Microbiology

Volumn 110, Issue 5, 2011, Pages 1166-1176

  Xia, X ^a,b   Meng, J ^a,b   Mcdermott, P F ^c   Zhao, S ^c  

^a NORTHWEST A F UNIVERSITY   (China)

^b UNIVERSITY OF MARYLAND   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Adhesion; Invasion; Retail meats; Uropathogenic Escherichia coli; Virulence factor

Indexed keywords

COSTS; ESCHERICHIA COLI; GENES; SALES; TISSUE CULTURE;

E. COLI; INVASION; MULTI-LOCI SEQUENCE TYPING; PATHOGENIC E. COLI; RETAIL MEAT; URINARY TRACT INFECTIONS; UROPATHOGENIC; UROPATHOGENIC ESCHERICHIA COLI; VIRULENCE FACTORS; VIRULENCE GENE;

MEATS;

INTERLEUKIN 6; VIRULENCE FACTOR;

DISEASE TREATMENT; EXCRETION; FECAL COLIFORM; GENE EXPRESSION; GENETIC ANALYSIS; MEAT; MOLECULAR ANALYSIS; PATHOGEN; PUBLIC HEALTH; SECRETION; VIRULENCE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; BLADDER; CELL CULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; ESCHERICHIA COLI; HUMAN; HUMAN TISSUE; MEAT; MULTILOCUS SEQUENCE TYPING; NONHUMAN; TISSUE CULTURE; UROPATHOGENIC ESCHERICHIA COLI;

ESCHERICHIA COLI;

EID: 79953741580     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.04978.x     Document Type: Article

References (42)

1. Bielaszewska, M., Prager, R., Kock, R., Mellmann, A., Zhang, W., Tschape, H., Tarr, P.I. and Karch, H. (2007) Shiga toxin gene loss and transfer in vitro and in vivo during enterohemorrhagic Escherichia coli O26 infection in humans. Appl Environ Microbiol 73, 3144-3150.
2. Billips, B.K., Forrestal, S.G., Rycyk, M.T., Johnson, J.R., Klumpp, D.J. and Schaeffer, A.J. (2007) Modulation of host innate immune response in the bladder by uropathogenic Escherichia coli. Infect Immun 75, 5353-5360.
3. Billips, B.K., Schaeffer, A.J. and Klumpp, D.J. (2008) Molecular basis of uropathogenic Escherichia coli evasion of the innate immune response in the bladder. Infect Immun 76, 3891-3900.
4. Ewers, C., Li, G., Wilking, H., Kiessling, S., Alt, K., Antao, E.M., Laturnus, C., Diehl, I. et al. (2007) Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int J Med Microbiol 297, 163-176.
5. Foxman, B. and Brown, P. (2003) Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 17, 227-241.
6. Girardeau, J.P., Dubourguier, H.C. and Gouet, P. (1982) Effect of glucose and amino acids on expression of K99 antigen in Escherichia coli. J Gen Microbiol 128, 2243-2249.
7. Gunther, N.W.t., Lockatell, V., Johnson, D.E. and Mobley, H.L. (2001) In vivo dynamics of type 1 fimbria regulation in uropathogenic Escherichia coli during experimental urinary tract infection. Infect Immun 69, 2838-2846.
8. Heimer, S.R., Rasko, D.A., Lockatell, C.V., Johnson, D.E. and Mobley, H.L. (2004) Autotransporter genes pic and tsh are associated with Escherichia coli strains that cause acute pyelonephritis and are expressed during urinary tract infection. Infect Immun 72, 593-597.
9. Hilbert, D.W., Pascal, K.E., Libby, E.K., Mordechai, E., Adelson, M.E. and Trama, J.P. (2008) Uropathogenic Escherichia coli dominantly suppress the innate immune response of bladder epithelial cells by a lipopolysaccharide- and Toll-like receptor 4-independent pathway. Microbes Infect 10, 114-121.
10. Hunstad, D.A., Justice, S.S., Hung, C.S., Lauer, S.R. and Hultgren, S.J. (2005) Suppression of bladder epithelial cytokine responses by uropathogenic Escherichia coli. Infect Immun 73, 3999-4006.
11. Jakobsen, L., Hammerum, A.M. and Frimodt-Moller, N. (2010) Virulence of Escherichia coli B2 isolates from meat and animals in a murine model of ascending urinary tract infection (UTI): evidence that UTI is a zoonosis. J Clin Microbiol 48, 2978-2980.
12. Johnson, J.R. and Russo, T.A. (2005) Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli. Int J Med Microbiol 295, 383-404.
13. Johnson, J.R. and Stell, A.L. (2000) Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181, 261-272.
14. Johnson, J.R., Delavari, P., Kuskowski, M. and Stell, A.L. (2001a) Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 183, 78-88.
15. Johnson, J.R., Stell, A.L., Kaster, N., Fasching, C. and O'Bryan, T.T. (2001b) Novel molecular variants of allele I of the Escherichia coli P fimbrial adhesin gene papG. Infect Immun 69, 2318-2327.
16. Johnson, J.R., Murray, A.C., Gajewski, A., Sullivan, M., Snippes, P., Kuskowski, M.A. and Smith, K.E. (2003) Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob Agents Chemother 47, 2161-2168.
17. Johnson, J.R., Delavari, P., O'Bryan, T.T., Smith, K.E. and Tatini, S. (2005a) Contamination of retail foods, particularly turkey, from community markets (Minnesota, 1999-2000) with antimicrobial-resistant and extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 2, 38-49.
18. Johnson, J.R., Kuskowski, M.A., Smith, K., O'Bryan, T.T. and Tatini, S. (2005b) Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J Infect Dis 191, 1040-1049.
19. Johnson, T.J., Wannemuehler, Y., Johnson, S.J., Stell, A.L., Doetkott, C., Johnson, J.R., Kim, K.S., Spanjaard, L. et al. (2008) Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Appl Environ Microbiol 74, 7043-7050.
20. Johnson, J.R., McCabe, J.S., White, D.G., Johnston, B., Kuskowski, M.A. and McDermott, P. (2009) Molecular analysis of Escherichia coli from retail meats (2002-2004) from the United States National Antimicrobial Resistance Monitoring System. Clin Infect Dis 49, 195-201.
21. Johnson, J.R., Johnston, B., Clabots, C., Kuskowski, M.A. and Castanheira, M. (2010) Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 51, 286-294.
22. Kulkarni, R., Dhakal, B.K., Slechta, E.S., Kurtz, Z., Mulvey, M.A. and Thanassi, D.G. (2009) Roles of putative type II secretion and type IV pilus systems in the virulence of uropathogenic Escherichia coli. PLoS ONE 4, e4752.
23. Lau, S.H., Reddy, S., Cheesbrough, J., Bolton, F.J., Willshaw, G., Cheasty, T., Fox, A.J. and Upton, M. (2008) Major uropathogenic Escherichia coli strain isolated in the northwest of England identified by multilocus sequence typing. J Clin Microbiol 46, 1076-1080.
24. Lim, J.K., Gunther, N.W.t., Zhao, H., Johnson, D.E., Keay, S.K. and Mobley, H.L. (1998) In vivo phase variation of Escherichia coli type 1 fimbrial genes in women with urinary tract infection. Infect Immun 66, 3303-3310.
25. Lloyd, A.L., Rasko, D.A. and Mobley, H.L. (2007) Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189, 3532-3546.
26. Manges, A.R., Smith, S.P., Lau, B.J., Nuval, C.J., Eisenberg, J.N., Dietrich, P.S. and Riley, L.W. (2007) Retail meat consumption and the acquisition of antimicrobial resistant Escherichia coli causing urinary tract infections: a case-control study. Foodborne Pathog Dis 4, 419-431.
27. Marrs, C.F., Zhang, L. and Foxman, B. (2005) Escherichia coli mediated urinary tract infections: are there distinct uropathogenic E. coli (UPEC) pathotypes? FEMS Microbiol Lett 252, 183-190.
28. Martinez, J.J., Mulvey, M.A., Schilling, J.D., Pinkner, J.S. and Hultgren, S.J. (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19, 2803-2812.
29. Miyazaki, J., Ba-Thein, W., Kumao, T., Obata Yasuoka, M., Akaza, H. and Hayshi, H. (2002) Type 1, P and S fimbriae, and afimbrial adhesin I are not essential for uropathogenic Escherichia coli to adhere to and invade bladder epithelial cells. FEMS Immunol Med Microbiol 33, 23-26.
30. Mulvey, M.A. (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4, 257-271.
31. Mulvey, M.A., Schilling, J.D., Martinez, J.J. and Hultgren, S.J. (2000) Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci USA 97, 8829-8835.
32. Picard, B., Garcia, J.S., Gouriou, S., Duriez, P., Brahimi, N., Bingen, E., Elion, J. and Denamur, E. (1999) The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67, 546-553.
33. Ramchandani, M., Manges, A.R., DebRoy, C., Smith, S.P., Johnson, J.R. and Riley, L.W. (2005) Possible animal origin of human-associated, multidrug-resistant, uropathogenic Escherichia coli. Clin Infect Dis 40, 251-257.
34. Rodriguez-Siek, K.E., Giddings, C.W., Doetkott, C., Johnson, T.J., Fakhr, M.K. and Nolan, L.K. (2005) Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 151, 2097-2110.
35. Russo, T.A., Stapleton, A., Wenderoth, S., Hooton, T.M. and Stamm, W.E. (1995) Chromosomal restriction fragment length polymorphism analysis of Escherichia coli strains causing recurrent urinary tract infections in young women. J Infect Dis 172, 440-445.
36. Sivick, K.E. and Mobley, H.L. (2010) Waging war against uropathogenic Escherichia coli: winning back the urinary tract. Infect Immun 78, 568-585.
37. Srinivasan, U., Foxman, B. and Marrs, C.F. (2003) Identification of a gene encoding heat-resistant agglutinin in Escherichia coli as a putative virulence factor in urinary tract infection. J Clin Microbiol 41, 285-289.
38. Vincent, C., Boerlin, P., Daignault, D., Dozois, C.M., Dutil, L., Galanakis, C., Reid-Smith, R.J., Tellier, P.P. et al. (2010) Food reservoir for Escherichia coli causing urinary tract infections. Emerg Infect Dis 16, 88-95.
39. Wiles, T.J., Kulesus, R.R. and Mulvey, M.A. (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85, 11-19.
40. Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L.H., Karch, H., Reeves, P.R. et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60, 1136-1151.
41. Xia, X., Meng, J., McDermott, P.F., Ayers, S., Blickenstaff, K., Tran, T.T., Abbott, J., Zheng, J. et al. (2010) Presence and characterization of shiga toxin-producing Escherichia coli and other potentially diarrheagenic E. coli strains in retail meats. Appl Environ Microbiol 76, 1709-1717.
42. Xia, X., Meng, J., Zhao, S., Bodeis-Jones, S., Gaines, S.A., Ayers, S.L. and McDermott, P.F. (2011) Identification and antimicrobial resistance of extraintestinal pathogenic Escherichia coli from retail meats. J Food Prot 74, 38-44.