Shiga toxin 2a and Enteroaggregative Escherichia coli – A deadly combination

Gut Microbes

Volumn 6, Issue 4, 2015, Pages 272-278

  Boisen, Nadia ^a   Melton Celsa, Angela R ^a   Scheutz, Flemming ^a   O’Brien, Alison D ^b   Nataro, James P ^c  

^a STATENS SERUM INSTITUT   (Denmark)

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

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Diarrhea; Enteroaggregative Escherichia coli (EAEC); Mechanisms of pathogenesis of gut microbes; O104:H4; Shiga toxin; Virulence

Indexed keywords

EXTENDED SPECTRUM BETA LACTAMASE; VEROTOXIN 2;

ARTICLE; BACTERIAL VIRULENCE; DIARRHEA; DIARRHEAGENIC ESCHERICHIA COLI; DOWN REGULATION; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENTEROBACTERIACEAE; ENTEROINVASIVE ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; GENE EXPRESSION; HEMOLYTIC UREMIC SYNDROME; HUMAN; INFECTIOUS DIARRHEA; NONHUMAN; ANIMAL; BIOLOGICAL MODEL; EPIDEMIC; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; EUROPE; GENETICS; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PLASMID;

ANIMALS; DISEASE OUTBREAKS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; EUROPE; HUMANS; MODELS, BIOLOGICAL; PLASMIDS; SHIGA TOXIN 2;

EID: 84944458227     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2015.1054591     Document Type: Article

References (74)

1. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet [Internet] 2012 [cited 2014 Jul 10]; 379:2151-61. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 22579125; PMID:22579125; http://dx.doi.org/10.1016/ S0140-6736(12)60560-1
2. Petri WA, Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL. Enteric infections, diarrhea, and their impact on function and development. J Clin Invest [Internet] 2008 [cited 2015 Feb 15]; 118:1277-90. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD2276781&toolDpmcentrez&rendertypeD abstract; PMID:18382740; http://dx.doi.org/10.1172/ JCI34005
3. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet [Internet] 2013 [cited 2014 Apr 29]; 382:209-22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 23680352; PMID:23680352; http://dx.doi.org/ 10.1016/S0140-6736(13)60844-2
4. Farthing MJ. Diarrhoea: a significant worldwide problem. Int J Antimicrob Agents [Internet] 2000 [cited 2015 Feb 15]; 14:65-9. Available from: http://www.ncbi.nlm.nih. gov/pubmed/10717503; PMID:10717503; http://dx.doi. org/10.1016/S0924-8579(99)00149-1
5. Wanke CA. To know Escherichia coli is to know bacterial diarrheal disease. Clin Infect Dis [Internet] 2001 [cited 2015 Feb 15]; 32:1710-2. Available from: http:// www.ncbi.nlm.nih.gov/pubmed/11360212; PMID:11360212; http://dx.doi.org/10.1086/320763
6. Bryce J, Boschi-Pinto C, Shibuya K, Black RE. WHO estimates of the causes of death in children. Lancet [Internet] 2005; [cited 2015 Feb 3]; 365:1147-52. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 15794969; PMID:15794969; http://dx.doi.org/ 10.1016/S0140-6736(05)71877-8
7. Riley LW. The epidemiologic, clinical, and microbiologic features of hemorrhagic colitis. Annu Rev Microbiol [Internet] 1987 [cited 2015 Feb 15]; 41:383-407. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 3318674; PMID:3318674; http://dx.doi.org/10.1146/ annurev.mi.41.100187.002123
8. Watanabe H, Wada A, Inagaki Y, Itoh K, Tamura K. Outbreaks of enterohaemorrhagic Escherichia coli O157:H7 infection by two different genotype strains in Japan, 1996. Lancet [Internet] 1996 [cited 2015 Feb 15]; 348:831-2. Available from: http://www.ncbi.nlm. nih.gov/pubmed/8814014; PMID:8814014; http://dx. doi.org/10.1016/S0140-6736(05)65257-9
9. Karmali MA, Steele BT, Petric M, Lim C. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet [Internet] 1983 [cited 2015 Feb 9]; 1:619-20. Available from: http://www.ncbi.nlm. nih.gov/pubmed/6131302; PMID:6131302; http://dx. doi.org/10.1016/S0140-6736(83)91795-6
10. O'Brien AO, Lively TA, Chen ME, Rothman SW, Formal SB. Escherichia coli O157:H7 strains associated with haemorrhagic colitis in the United States produce a Shigella dysenteriae 1 (SHIGA) like cytotoxin. Lancet [Internet] 1983 [cited 2015 Feb 15]; 1:702. Available from: http://www.ncbi.nlm.nih.gov/pubmed/6132054; http://dx.doi.org/10.1016/S0140-6736(83)91987-6
11. Siegler RL. Postdiarrheal Shiga toxin-mediated hemolytic uremic syndrome. JAMA [Internet] 2003 [cited 2015 Mar 29]; 290:1379-81. Available from: http://www.ncbi. nlm.nih.gov/pubmed/12966132; PMID:12966132; http://dx.doi.org/10.1001/jama.290.10.1379
12. Paton JC, Paton AW. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev [Internet] 1998 [cited 2015Mar 29]; 11:450-79. Available from: http://www.pubmedcentral.nih.gov/articleren der.fcgi?artidD88891&toolDpmcentrez&rendertypeD abstract; PMID:9665978
13. Scheutz F, Teel LD, Beutin L, PiérardD, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol [Internet] 2012 [cited 2015 Mar 29]; 50:2951-63. Available from: http://jcm.asm.org/content/ 50/9/2951.long; PMID:22760050; http://dx.doi.org/ 10.1128/JCM.00860-12
14. Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis [Internet] 2011 [cited 2014 May 8]; 11:671-6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 21703928; PMID:21703928; http://dx.doi.org/ 10.1016/S1473-3099(11)70165-7
15. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, et al. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med [Internet] 2011 [cited 2014 May 13]; 365:1771-80. Available from: http://www.ncbi.nlm. nih.gov/pubmed/21696328; PMID:21696328; http:// dx.doi.org/10.1056/NEJMoa1106483
16. Scheutz F,NielsenEM, Frimodt-Møller J,BoisenN,Morabito S, Tozzoli R, Nataro JP, Caprioli A. 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 [Internet] 2011 [cited 2014 May 13]; 16; pii: 19889. Available from: http://www.ncbi.nlm.nih. gov/pubmed/21699770;PMID:21699770
17. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, Deleré Y, an der Heiden M, Adlhoch C, Dreesman J, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med [Internet] 2011 [cited 2014 May 2]; 365:1763-70. Available from: http://www.ncbi.nlm. nih.gov/pubmed/22029753; PMID:22029753; http:// dx.doi.org/10.1056/NEJMoa1106482
18. Gould LH, Demma L, Jones TF, Hurd S, Vugia DJ, Smith K, Shiferaw B, Segler S, Palmer A, Zansky S, et al. Hemolytic uremic syndrome and death in persons with Escherichia coli O157:H7 infection, foodborne diseases active surveillance network sites, 2000-2006. Clin Infect Dis [Internet] 2009 2009[cited 2015 Feb 15]; 49:1480-5. Available from: http://www.ncbi.nlm. nih.gov/pubmed/19827953; PMID:19827953; http:// dx.doi.org/10.1086/644621
19. Alpers K, Werber D, Frank C, Koch J, Friedrich AW, Karch H, An DER Heiden M, Prager R, Fruth A, Bielaszewska M, et al. Sorbitol-fermenting enterohaemorrhagic Escherichia coli O157:H-causes another outbreak of haemolytic uraemic syndrome in children. Epidemiol Infect [Internet] 2009 [cited 2015 Feb 15]; 137:389-95. Available from: http:// www.ncbi.nlm.nih.gov/pubmed/19021923; PMID:19021923; http://dx.doi.org/10.1017/ S0950268808001465
20. Tzipori S, Wachsmuth IK, Chapman C, Birden R, Brittingham J, Jackson C, Hogg J. The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157:H7 in gnotobiotic piglets. J Infect Dis [Internet] 1986 [cited 2015 Feb 15]; 154:712-6. Available from: http://www. ncbi.nlm.nih.gov/pubmed/3528323; PMID:3528323; http://dx.doi.org/10.1093/infdis/154.4.712
21. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A [Internet] 1995 [cited 2015 Feb 2]; 92:1664-8. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD42580&toolDpmcentrez&rendertypeD abstract; PMID:7878036; http://dx.doi.org/10.1073/ pnas.92.5.1664
22. Dallman T, Smith GP, O'Brien B, Chattaway MA, Finlay D, Grant KA, Jenkins C. Characterization of a verocytotoxin-producing enteroaggregative Escherichia coli serogroup O111:H21 strain associated with a household outbreak in Northern Ireland. J Clin Microbiol [Internet] 2012 [cited 2014 May 13]; 50:4116-9. Available from: http://www.pubmedcentral.nih.gov/arti clerender.fcgi?artidD3502983&toolDpmcentrez& rendertypeDabstract; PMID:23035193; http://dx.doi. org/10.1128/JCM.02047-12
23. Vashakidze E, Megrelishvili T, Pachkoria E, Tevzadze L, Lashkarashvili M. Enterohemorrhagic E. coli and hemolytic uremic syndrome in Georgia. Georgian Med News 2010; 38-41.
24. Morabito S, Karch H, Mariani-Kurkdjian P, Schmidt H, Minelli F, Bingen E, Caprioli A. Enteroaggregative, Shiga toxin-producing Escherichia coli O111:H2 associated with an outbreak of hemolytic-uremic syndrome. J Clin Microbiol [Internet] 1998 [cited 2015 Feb 15]; 36:840-2. Available from: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artidD104641&toolDpmcentrez& rendertypeDabstract; PMID:9508328
25. Adachi JA, Jiang ZD, Mathewson JJ, Verenkar MP, Thompson S, Martinez-Sandoval F, Steffen R, Ericsson CD, DuPont HL. Enteroaggregative Escherichia coli as a major etiologic agent in traveler's diarrhea in 3 regions of the world. Clin Infect Dis [Internet] 2001 [cited 2014May 13]; 32:1706-9. Available from: http://www.ncbi.nlm.nih.gov/ pubmed/11360211; PMID:11360211; http://dx.doi.org/ 10.1086/320756
26. Okeke IN, Lamikanra A, SteinrückH, Kaper JB. Characterization of Escherichia coli strains from cases of childhood diarrhea in provincial southwestern Nigeria. J Clin Microbiol [Internet] 2000 [cited 2014 May 13]; 38:7-12. Available from: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artidD86005&toolDpmcentrez &rendertypeDabstract; PMID:10618054
27. Fang GD, Lima AA,Martins CV,Nataro JP, Guerrant RL. Etiology and epidemiology of persistent diarrhea in northeastern Brazil: a hospital-based, prospective, case-control study. J Pediatr Gastroenterol Nutr [Internet] 1995 [cited 2014 May 13]; 21:137-44. Available from: http://www. ncbi.nlm.nih.gov/pubmed/7472898; PMID:7472898; http://dx.doi.org/10.1097/00005176-199508000-00003
28. Bhan MK, Raj P, Levine MM, Kaper JB, Bhandari N, Srivastava R, Kumar R, Sazawal S. Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis [Internet] 1989 [cited 2014 May 6]; 159:1061-4. Available from: http://www. ncbi.nlm.nih.gov/pubmed/2656875; PMID:2656875; http://dx.doi.org/10.1093/infdis/159.6.1061
29. 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 [Internet] 1998 [cited 2014 May 13]; 178:185-90. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 9652439; PMID:9652439; http://dx.doi.org/10.1086/ 515595
30. Sahl JW, Steinsland H, Redman JC, Angiuoli SV, Nataro JP, Sommerfelt H, Rasko DA. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect Immun [Internet] 2011 [cited 2014 May 9]; 79:950-60. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD3028850&toolD pmcentrez&rendertypeDabstract; PMID:21078854; http://dx.doi.org/10.1128/IAI.00932-10
31. Valentiner-Branth P, Steinsland H, Fischer TK, Perch M, Scheutz F, Dias F, Aaby P, Mølbak K, Sommerfelt H. Cohort study of Guinean children: incidence, pathogenicity, conferred protection, and attributable risk for enteropathogens during the first 2 years of life. J Clin Microbiol [Internet] 2003 [cited 2014 May 13]; 41:4238-45. Available from: http://www.pubmedcentral.nih.gov/articleren der.fcgi?artidD193811&toolDpmcentrez&rendertypeD abstract; PMID:12958251; http://dx.doi.org/10.1128/ JCM.41.9.4238-4245.2003
32. Boisen N, Scheutz F, Rasko D a, Redman JC, Persson S, Simon J, Kotloff KL, Levine MM, Sow S, Tamboura B, et al. Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J Infect Dis [Internet] 2012; 205:431-44. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD3256949&toolD pmcentrez&rendertypeDabstract; http://dx.doi.org/ 10.1093/infdis/jir757
33. Lima IFN, Boisen N, Quetz J, da S, Havt A, de Carvalho EB, Soares AM, Lima NL, Mota RMS, Nataro JP, Guerrant RL, et al. Prevalence of enteroaggregative Escherichia coli and its virulence-related genes in a casecontrol study among children from north-eastern Brazil. J Med Microbiol [Internet] 2013 [cited 2014 May 9]; 62:683-93. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD3709657&toolD pmcentrez&rendertypeDabstract; PMID:23429698; http://dx.doi.org/10.1099/jmm.0.054262-0
34. 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 [Internet] 2000 [cited 2014 May 13]; 181:252-60. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10608774; PMID:10608774; http://dx.doi.org/10.1086/315204
35. 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 [Internet] 2009 [cited 2014 May 13]; 80:294-301. Available from: http://www.pubmedcentral.nih.gov/arti clerender.fcgi?artidD2660206&toolDpmcentrez& rendertypeDabstract; PMID:19190229
36. Jenkins C, van Ijperen C, Dudley EG, Chart H, Willshaw GA, Cheasty T, Smith HR, Nataro JP. Use of a microarray to assess the distribution of plasmid and chromosomal virulence genes in strains of enteroaggregative Escherichia coli. FEMS Microbiol Lett [Internet] 2005 [cited 2014 May 13]; 253:119-24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 16243450; PMID:16243450; http://dx.doi.org/ 10.1016/j.femsle.2005.09.040
37. Nataro JP, Yikang D, Yingkang D, Walker K. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol [Internet] 1994 [cited 2014 May 13]; 176:4691-9. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD196291&toolD pmcentrez&rendertypeDabstract; PMID:7913930
38. Bernier C, Gounon P, Le Bouguénec C. Identification of an aggregative adhesion fimbria (AAF) type IIIencoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun [Internet] 2002 [cited 2014 May 13]; 70:4302-11. Available from: http:// www.pubmedcentral.nih.gov/articlerender.fcgi?artid D128174&toolDpmcentrez&rendertypeDabstract; PMID:12117939; http://dx.doi.org/10.1128/ IAI.70.8.4302-4311.2002
39. 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 [Internet] 2008 [cited 2014 May 13]; 76:3281-92. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD2446688&toolDpmcentrez&rendertypeD abstract; PMID:18443096; http://dx.doi.org/10.1128/ IAI.01646-07
40. Czeczulin JR, Balepur S, Hicks S, Phillips A, Hall R, Kothary MH, Navarro-Garcia F, Nataro JP. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun [Internet] 1997 [cited 2014 May 13]; 65:4135-45. Available from: http:// www.pubmedcentral.nih.gov/articlerender.fcgi?artid D175595&toolDpmcentrez&rendertypeDabstract; PMID:9317019
41. Henderson IR, Hicks S, Navarro-Garcia F, Elias WP, Philips AD, Nataro JP. Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect Immun [Internet] 1999 [cited 2014 May 13]; 67:5338-44. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD96889&toolDpmcentrez&rendertypeD abstract; PMID:10496914
42. 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 [Internet] 1993 [cited 2014 May 13]; 61:1126-31. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD302849&toolDpmcentrez&rendertypeD abstract; PMID:8094379
43. Jønsson R, Struve C, Boisen N, Mateiu RV, Santiago AE, Jenssen H, Nataro JP, Krogfelt KA. A novel Aggregative Adherence Fimbriae (AAF/V) of Enteroaggregative Escherichia coli (EAEC). Infect Immun [Internet] 2015 [cited 2015 Feb 15]; Available from: http://www.ncbi.nlm.nih. gov/pubmed/25624357;PMID:25624357
44. Strauman MC, Harper JM, Harrington SM, Boll EJ, Nataro JP. Enteroaggregative Escherichia coli disrupts epithelial cell tight junctions. Infect Immun [Internet] 2010 [cited 2014 May 8]; 78:4958-64. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi? artidD2976312&toolDpmcentrez&rendertypeDabstra ct; PMID:20823198; http://dx.doi.org/10.1128/ IAI.00580-10
45. 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 [Internet] 2005 [cited 2014 May 13]; 7:1565-78. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 16207244; PMID:16207244; http://dx.doi.org/ 10.1111/j.1462-5822.2005.00588.x
46. Sheikh J, Czeczulin JR, Harrington S, Hicks S, Henderson IR, Le Bouguénec C, Gounon P, Phillips A, Nataro JP. A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest [Internet] 2002 [cited 2014 May 13]; 110:1329-37. Available from: http:// www.pubmedcentral.nih.gov/articlerender.fcgi?artidD 151617&toolDpmcentrez&rendertypeDabstract; PMID:12417572; http://dx.doi.org/10.1172/ JCI16172
47. Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol [Internet] 2006 [cited 2014 May 13]; 61:1267-82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 16925558; PMID:16925558; http://dx.doi.org/ 10.1111/j.1365-2958.2006.05281.x
48. Santiago AE, Ruiz-Perez F, Jo NY, Vijayakumar V, Gong MQ, Nataro JP. A large family of antivirulence regulators modulates the effects of transcriptional activators in Gram-negative pathogenic bacteria. PLoS Pathog [Internet] 2014 [cited 2015 Feb 15]; 10: e1004153. Available from: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artidD4038620&toolD pmcentrez&rendertypeDabstract; PMID:24875828
49. Dutta PR, Cappello R, Navarro-García F, Nataro JP. Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect Immun [Internet] 2002 [cited 2014 May 13]; 70:7105-13. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD133081&toolDpmcentrez&rendertypeD abstract; PMID:12438392; http://dx.doi.org/10.1128/ IAI.70.12.7105-7113.2002
50. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin C-S, Iliopoulos D, et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med [Internet] 2011 [cited 2014 May 13]; 365:709-17. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD3168948&toolD pmcentrez&rendertypeDabstract; PMID:21793740; http://dx.doi.org/10.1056/NEJMoa1106920
51. Henderson IR, Navarro-Garcia F, Nataro JP. The great escape: structure and function of the autotransporter proteins. Trends Microbiol [Internet] 1998 [cited 2014 May 13]; 6:370-8. Available from: http://www.ncbi. nlm.nih.gov/pubmed/9778731; PMID:9778731; http://dx.doi.org/10.1016/S0966-842X(98)01318-3
52. Zangari T, Melton-Celsa AR, Panda A, Boisen N, Smith MA, Tatarov I, De Tolla LJ, Nataro JP, O'Brien AD. Virulence of the Shiga toxin type 2-expressing Escherichia coli O104:H4 German outbreak isolate in two animal models. Infect Immun [Internet] 2013 [cited 2014 May 13]; 81:1562-74. Available from: http://www.ncbi.nlm.nih.gov/ pubmed/23439303; PMID:23439303; http://dx.doi.org/ 10.1128/IAI.01310-12
53. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol [Internet] 2004 [cited 2014 Apr 28]; 2:123-40. Available from: http://www.ncbi.nlm.nih. gov/pubmed/15040260; PMID:15040260; http://dx.doi. org/10.1038/nrmicro818
54. Nataro JP, Deng Y, Cookson S, Cravioto A, Savarino SJ, Guers LD, Levine MM, Tacket CO. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis [Internet] 1995 [cited 2014 May 13]; 171:465-8. Available from: http://www. ncbi.nlm.nih.gov/pubmed/7844392; PMID:7844392; http://dx.doi.org/10.1093/infdis/171.2.465
55. Itoh Y, Nagano I, Kunishima M, Ezaki T. Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol [Internet] 1997 [cited 2015 Feb 15]; 35:2546-50. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi? artidD230008&toolDpmcentrez&rendertypeDabstract; PMID:9316905
56. Cobeljić M, Miljković-Selimović B, Paunović-Todosijević D, Velicković Z, Lepsanović Z, Zec N, Savić D, Ilić R, Konstantinović S, Jovanović B, et al. Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol Infect [Internet] 1996 [cited 2015 Feb 15]; 117:11-6. Available from: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artidD2271665&tool Dpmcentrez&rendertypeDabstract; PMID:8760945; http://dx.doi.org/10.1017/S0950268800001072
57. Smith HR, Cheasty T, Rowe B. Enteroaggregative Escherichia coll and outbreaks of gastroenteritis in UK. Lancet [Internet] 1997 [cited 2015 Feb 15]; 350:814-5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 9298029; PMID:9298029; http://dx.doi.org/10.1016/ S0140-6736(05)62611-6
58. Scavia G, StaffolaniM, Fisichella S, Striano G, Colletta S, Ferri G, Escher M, Minelli F, Caprioli A. Enteroaggregative Escherichia coli associated with a foodborne outbreak of gastroenteritis. J Med Microbiol [Internet] 2008 [cited 2015 Feb 15]; 57:1141-6. Available from: http://www. ncbi.nlm.nih.gov/pubmed/18719185; PMID:18719185; http://dx.doi.org/10.1099/jmm.0.2008/001362-0
59. Roche JK, Cabel A, Sevilleja J, Nataro J, Guerrant RL. Enteroaggregative Escherichia coli (EAEC) impairs growth while malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J Infect Dis [Internet] 2010 [cited 2015 Feb 15]; 202:506-14. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD2919845&toolD pmcentrez&rendertypeDabstract; PMID:20594107; http://dx.doi.org/10.1086/654894
60. Steiner TS, Lima AA, Nataro JP, Guerrant RL. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis [Internet] 1998 [cited 2014 May 13]; 177:88-96. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 9419174; PMID:9419174; http://dx.doi.org/10.1086/ 513809
61. Olesen B, Scheutz F, Andersen RL, Menard M, Boisen N, Johnston B, Hansen DS, Krogfelt KA, Nataro JP, Johnson JR. Enteroaggregative Escherichia coli O78: H10, the Cause of an Outbreak of Urinary Tract Infection. J Clin Microbiol [Internet] 2012 [cited 2014 May 13]; 50:3703-11. Available from: http://www.pubmed central.nih.gov/articlerender.fcgi?artidD3486220&tool Dpmcentrez&rendertypeDabstract; PMID:22972830; http://dx.doi.org/10.1128/JCM.01909-12
62. Hicks S, Candy DC, Phillips AD. Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun [Internet] 1996 [cited 2015 Feb 15]; 64:4751-60. Available from: http:// www.pubmedcentral.nih.gov/articlerender.fcgi?artidD 174442&toolDpmcentrez&rendertypeDabstract; PMID:8890236
63. Tzipori S, Montanaro J, Robins-Browne RM, Vial P, Gibson R, Levine MM. Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect Immun [Internet] 1992 [cited 2015 Feb 15]; 60:5302-6. Available from: http://www.pubmed central.nih.gov/articlerender.fcgi?artidD258311&tool Dpmcentrez&rendertypeDabstract; PMID:1452364
64. 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 [Internet] 2002 [cited 2014 May 13]; 40:4185-90. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi? artidD139678&toolDpmcentrez&rendertypeDabstract; PMID:12409395; http://dx.doi.org/10.1128/ JCM.40.11.4185-4190.2002
65. Bouckenooghe AR, Dupont HL, Jiang ZD, Adachi J, Mathewson JJ, Verenkar MP, Rodrigues S, Steffen R. Markers of enteric inflammation in enteroaggregative Escherichia coli diarrhea in travelers. Am J Trop Med Hyg [Internet] 2000 [cited 2015 Feb 15]; 62:711-3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/ 11304060; PMID:11304060
66. Steiner TS, Nataro JP, Poteet-Smith CE, Smith JA, Guerrant RL. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin Invest [Internet] 2000 [cited 2014 May 13]; 105:1769-77. Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artidD378507&toolDpmcentrez&rendertypeD abstract; PMID:10862792; http://dx.doi.org/10.1172/ JCI8892
67. Boll EJ, Struve C, Sander A, Demma Z, Nataro JP, McCormick BA, Krogfelt KA. The fimbriae of enteroaggregative Escherichia coli induce epithelial inflammation in vitro and in a human intestinal xenograft model. J Infect Dis [Internet] 2012 [cited 2014 May 3]; 206:714-22. Available from: http://jid.oxfordjour nals.org/content/early/2012/06/21/infdis.jis417; PMID:22723643; http://dx.doi.org/10.1093/infdis/ jis417
68. Boisen N, Hansen A-M, Melton-Celsa AR, Zangari T, Mortensen NP, Kaper JB, O'Brien AD, Nataro JP. 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. J Infect Dis [Internet] 2014 [cited 2014 Nov 15]; 210 (12):1909-19; Available from: http://www.ncbi.nlm. nih.gov/pubmed/25038258; PMID:25038258
69. 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 [Internet] 1999 [cited 2014 May 13]; 67:2184-92. Available from: http://www.pub medcentral.nih.gov/articlerender.fcgi?artidD115956 &toolDpmcentrez&rendertypeDabstract
70. Frankel G, Phillips AD. Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. CellMicrobiol [Internet] 2008 [cited 2014 May 13]; 10:549-56. Available from: http://www.ncbi.nlm. nih.gov/pubmed/18053003; PMID:18053003; http://dx. doi.org/10.1111/j.1462-5822.2007.01103.x
71. DeVinney R, Puente JL, Gauthier A, Goosney D, Finlay BB. Enterohaemorrhagic and enteropathogenic Escherichia coli use a different Tir-based mechanism for pedestal formation. Mol Microbiol [Internet] 2001 [cited 2014 May 13]; 41:1445-58. Available from: http://www.ncbi. nlm.nih.gov/pubmed/11580847; PMID:11580847; http://dx.doi.org/10.1046/j.1365-2958.2001.02617.x
72. 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 [Internet] 1999 [cited 2014 May 13]; 67:5985-93. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD96984&tool Dpmcentrez&rendertypeDabstract; PMID:10531258
73. Hurley BP, Thorpe CM, Acheson DW. Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect Immun [Internet] 2001 [cited 2014 May 13]; 69:6148-55. Available from: http://www.pubmedcentral.nih.gov/arti clerender.fcgi?artidD98745&toolDpmcentrez &rendertypeDabstract; PMID:11553554; http://dx. doi.org/10.1128/IAI.69.10.6148-6155.2001
74. Zhang W, Bielaszewska M, Kunsmann L, Mellmann A, Bauwens A, Köck R, Kossow A, Anders A, Gatermann S, Karch H. Lability of the pAA virulence plasmid in escherichia coli O104:H4: implications for virulence in humans. PLoS One [Internet] 2013 [cited 2014 May 13]; 8:e66717. Available from: http://www.pubmedcen tral.nih.gov/articlerender.fcgi?artidD3689698&tool Dpmcentrez&rendertypeDabstract; PMID:23805269; http://dx.doi.org/10.1371/journal.pone.0066717