The presence of the pAA plasmid in the German O104:H4 Shiga toxin type 2a (Stx2a)-producing enteroaggregative Escherichia coli strain promotes the translocation of Stx2a across an epithelial cell monolayer

Journal of Infectious Diseases

Volumn 210, Issue 12, 2014, Pages 1909-1919

  Boisen, Nadia ^a   Hansen, Anne Marie ^b   Melton Celsa, Angela R ^c   Zangari, Tonia ^c   Mortensen, Ninell Pollas ^d,e   Kaper, James B ^b   O'Brien, Alison D ^c   Nataro, James P ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d RTI INTERNATIONAL   (United States)

^e OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Diarrhea; Enteroaggregative Escherichia coli (EAEC); O104:H4; PAA plasmid; Shiga toxin

Indexed keywords

INTERLEUKIN 8; SHIGA TOXIN; SHIGA TOXIN TYPE 2A; UNCLASSIFIED DRUG; AGGR PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; TRANSACTIVATOR PROTEIN; VEROTOXIN 2; VIRULENCE FACTOR;

AGGA GENE; AGGR GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CONTROLLED STUDY; CYTOKINE RELEASE; ENTEROAGGREGATIVE ESCHERICHIA COLI; EPITHELIUM CELL; GENE DELETION; GENETIC CODE; HUMAN; HUMAN CELL; MACACA FASCICULARIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; SEPA GENE; TOXIN ANALYSIS; TRANSPORT KINETICS; CELL LINE; CLASSIFICATION; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; GENOTYPE; GERMANY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PROTEIN TRANSPORT; SECRETION (PROCESS); SEROTYPE;

BACTERIAL ADHESION; CELL LINE; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENOTYPE; GERMANY; HUMANS; INTERLEUKIN-8; PLASMIDS; PROTEIN TRANSPORT; SEROGROUP; SHIGA TOXIN 2; TRANS-ACTIVATORS; VIRULENCE FACTORS;

EID: 84927651869     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu399     Document Type: Article

References (50)

1. Adachi JA, Jiang ZD, Mathewson JJ, et al. Enteroaggregative Escherichia coli as a major etiologic agent in traveler's diarrhea in 3 regions of the world. Clin Infect Dis 2001;32:1706-9.
2. Okeke IN, Lamikanra A, Steinrück H, Kaper JB. Characterization of Escherichia coli strains from cases of childhood diarrhea in provincial southwestern Nigeria. J Clin Microbiol 2000;38:7-12.
3. Fang GD, Lima AA, Martins CV, Nataro JP, Guerrant RL. Etiology and epidemiology of persistent diarrhea in northeastern Brazil: a hospitalbased, prospective, case-control study. J Pediatr Gastroenterol Nutr 1995;21:137-44.
4. Bhan MK, Raj P, Levine MM, et al. Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis 1989;159:1061-4.
5. Wanke CA, Mayer H, Weber R, Zbinden R, Watson DA, Acheson D. Enteroaggregative Escherichia coli as a potential cause of diarrheal disease in adults infected with human immunodeficiency virus. J Infect Dis 1998;178:185-90.
6. Sahl JW, Steinsland H, Redman JC, et al. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect Immun 2011;79:950-60.
7. Valentiner-Branth P, Steinsland H, Fischer TK, et al. Cohort study of Guinean children: incidence, pathogenicity, conferred protection, and attributable risk for enteropathogens during the first 2 years of life. J Clin Microbiol 2003;41:4238-45.
8. Boisen N, Scheutz F, Rasko DA, et al. Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J Infect Dis 2012;205:431-44.
9. Lima I F N, Boisen N, Quetz Jda S, et al. Prevalence of enteroaggregative Escherichia coli and its virulence-related genes in a case-control study among children from north-eastern Brazil. J Med Microbiol 2013;62(Pt 5):683-93.
10. Okeke IN, Lamikanra A, Czeczulin J, Dubovsky F, Kaper JB, Nataro JP. Heterogeneous virulence of enteroaggregative Escherichia coli strains isolated from children in Southwest Nigeria. J Infect Dis 2000;181:252-60.
11. Boisen N, Ruiz-Perez F, Scheutz F, Krogfelt KA, Nataro JP. Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am J Trop Med Hyg 2009;80:294-301.
12. Jenkins C, van Ijperen C, Dudley EG, et al. Use of a microarray to assess the distribution of plasmid and chromosomal virulence genes in strains of enteroaggregative Escherichia coli. FEMS Microbiol Lett 2005;253:119-24.
13. Nataro JP, Yikang D, Yingkang D, Walker K. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol 1994;176:4691-9.
14. Bernier C, Gounon P, Le Bouguénec C. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun 2002;70:4302-11.
15. Boisen N, Struve C, Scheutz F, Krogfelt KA, Nataro JP. New adhesin of enteroaggregative Escherichia coli related to the Afa/Dr/AAF family. Infect Immun 2008;76:3281-92.
16. Czeczulin JR, Balepur S, Hicks S, et al. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun 1997;65:4135-45.
17. Henderson IR, Hicks S, Navarro-Garcia F, Elias WP, Philips AD, Nataro JP. Involvement of the enteroaggregative Escherichia coli plasmidencoded toxin in causing human intestinal damage. Infect Immun 1999;67:5338-44.
18. Nataro JP, Yikang D, Giron JA, Savarino SJ, Kothary MH, Hall R. Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect Immun 1993;61:1126-31.
19. Strauman MC, Harper JM, Harrington SM, Boll EJ, Nataro JP. Enteroaggregative Escherichia coli disrupts epithelial cell tight junctions. Infect Immun 2010;78:4958-64.
20. Harrington SM, Strauman MC, Abe CM, Nataro JP. Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli. Cell Microbiol 2005;7:1565-78.
21. Dutta PR, Cappello R, Navarro-García F, Nataro JP. Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect Immun 2002;70:7105-13.
22. Frank C, Werber D, Cramer JP, et al. Epidemic profile of Shigatoxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 2011;365:1771-80.
23. Scheutz F, Nielsen EM, Frimodt-Møller J, et al. Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill 2011;16.
24. Bielaszewska M, Mellmann A, Zhang W, et al. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 2011;11:671-6.
25. Rasko DA, Webster DR, Sahl JW, et al. Origins of the E.coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 2011;365:709-17.
26. Donnenberg MS, Kaper JB. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 1991;59:4310-7.
27. Sheikh J, Hicks S, Dall'Agnol M, Phillips AD, Nataro JP. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 2001;41:983-97.
28. Gentry MK, Dalrymple JM. Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol 1980;12:361-6.
29. Schmitt CK, McKee ML, O'Brien AD. Two copies of Shiga-like toxin II-related genes common in enterohemorrhagic Escherichia coli strains are responsible for the antigenic heterogeneity of the O157:H-strain E32511. Infect Immun 1991;59:1065-73.
30. Hicks S, Candy D, Phillips A. Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun 1996;64:4751-60.
31. Zangari T, Melton-Celsa AR, Panda A, et al. Virulence of the Shiga toxin type 2-expressing Escherichia coli O104:H4 German outbreak isolate in two animal models. Infect Immun 2013;81:1562-74.
32. Jiang Z-D, Greenberg D, Nataro JP, Steffen R, DuPont HL. Rate of occurrence and pathogenic effect of enteroaggregative Escherichia coli virulence factors in international travelers. J Clin Microbiol 2002;40:4185-90.
33. Tran S-L, Billoud L, Lewis SB, Phillips AD, Schüller S. Shiga toxin production and translocation during microaerobic human colonic infection with Shiga toxin-producing E.coli O157:H7 and O104:H4. Cell Microbiol 2014;16:1255-66.
34. Acheson DW, Moore R, De Breucker S, et al. Translocation of Shiga toxin across polarized intestinal cells in tissue culture. Infect Immun 1996;64:3294-300.
35. Hurley BP, Thorpe CM, Acheson DW. Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect Immun 2001;69:6148-55.
36. Trachtman H, Austin C, Lewinski M, Stahl R A K. Renal and neurological involvement in typical Shiga toxin-associated HUS. Nat Rev Nephrol 2012;8:658-69.
37. Frankel G, Phillips AD. Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 2008;10:549-56.
38. DeVinney R, Puente JL, Gauthier A, Goosney D, Finlay BB. Enterohaemorrhagic and enteropathogenic Escherichia coli use a different Tirbased mechanism for pedestal formation. Mol Microbiol 2001;41:1445-58.
39. Navarro-García F, Sears C, Eslava C, Cravioto A, Nataro JP. Cytoskeletal effects induced by pet, the serine protease enterotoxin of enteroaggregative Escherichia coli. Infect Immun 1999;67:2184-92.
40. Thorpe CM, Hurley BP, Lincicome LL, Jacewicz MS, Keusch GT, Acheson DW. Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect Immun 1999;67:5985-93.
41. Benjelloun-Touimi Z, Sansonetti PJ, Parsot C. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol Microbiol 1995;17:123-35.
42. Boll EJ, Struve C, Sander A, et al. The fimbriae of enteroaggregative Escherichia coli induce epithelial inflammation in vitro and in a human intestinal xenograft model. J Infect Dis 2012;206:714-22.
43. Hurley BP, Jacewicz M, Thorpe CM, et al. Shiga toxins 1 and 2 translocate differently across polarized intestinal epithelial cells. Infect Immun 1999;67:6670-7.
44. Zhang W, Bielaszewska M, Kunsmann L, et al. Lability of the pAA Virulence Plasmid in Escherichia coli O104:H4: Implications for Virulence in Humans. PLoS One 2013;8:e66717.
45. Munera D, Ritchie JM, Hatzios SK, et al. Autotransporters but not pAA are critical for rabbit colonization by Shiga toxin-producing Escherichia coli O104:H4. Nat Commun 2014;5:3080.
46. Griffin PM, Ostroff SM, Tauxe RV, et al. Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann Intern Med 1988;109:705-12.
47. Simons RW, Houman F, Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 1987;53:85-96.
48. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB, Young CR SS. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1978;311:1119-22.
49. Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 1995;177:4121-30.
50. Harrison LM, Rallabhandi P, Michalski J, et al. Vibrio cholerae flagellins induce toll-like receptor 5-mediated interleukin-8 production through mitogen-activated protein kinase and NF-kappaB activation. Infect Immun 2008;76:5524-34.