Autotransporters and virulence of enteroaggregative E. coli

Gut Microbes

Volumn 2, Issue 1, 2011, Pages

  Navarro Garcia, Fernando ^a   Elias, Waldir P ^b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

Autotransporter; Diarrhea; EAEC; Enteroaggregative; Escherichia coli; SPATE; Virulence factors

Indexed keywords

AUTOTRANSPORTER PROTEIN; CYTOKINE; CYTOTOXIN; ENTEROAGGREGATIVE HEAT STABLE TOXIN 1; ENTEROTOXIN; FLAGELLIN; HEMOLYSIN; HYALURONIDASE; OUTER MEMBRANE PROTEIN; PILIN; PLASMID ENCODED TOXIN; PROTEIN; PROTEIN INVOLVED IN COLONIZATION; SHIGELLA ENTEROTOXIN 1; TOXIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; SERINE PROTEINASE;

BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BIOFILM; BIOGENESIS; CYTOTOXICITY; DIARRHEA; ENDOCYTOSIS; ENTEROAGGREGATIVE ESCHERICHIA COLI; EPITHELIUM CELL; ESCHERICHIA COLI INFECTION; FIMBRIA; GENE CONTROL; HUMAN; INTESTINE MUCOSA; MUCOSA INFLAMMATION; NONHUMAN; PLASMID; PROTEIN DEGRADATION; REVIEW; BACTERIUM ADHERENCE; CELL LINE; ESCHERICHIA COLI; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL ADHESION; CARRIER PROTEINS; CELL LINE; ENTEROTOXINS; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; HUMANS; SERINE PROTEASES; VIRULENCE; VIRULENCE FACTORS;

EID: 79956222838     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.2.1.14933     Document Type: Review

References (120)

1. Clarke SC. Diarrhoeagenic Escherichia coli-an emerging problem? Diagn Microbiol Infect Dis 2001; 41:93-8.
2. Black EP, Hirneisen KA, Hoover DG, Kniel KE. Fate of Escherichia coli O157: H7 in ground beef following high-pressure processing and freezing. J Appl Microbiol 2010; 108:1352-60.
3. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2:123-40.
4. Nataro JP, Kaper JB, Robins-Browne R, Prado V, Vial P, Levine MM. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J 1987; 6:829-31.
5. Gioppo NM, Elias WP Jr, Vidotto MC, Linhares RE, Saridakis HO, Gomes TA, et al. Prevalence of HEp-2 cell-adherent Escherichia coli and characterisation of enteroaggregative E. coli and chain-like adherent E. coli isolated from children with and without diarrhoea, in Londrina, Brazil. FEMS Microbiol Lett 2000; 190:293-8.
6. Gomes TA, Vieira MA, Abe CM, Rodrigues D, Griffin PM, Ramos SR. Adherence patterns and adherencerelated DNA sequences in Escherichia coli isolates from children with and without diarrhea in Sao Paulo city, Brazil. J Clin Microbiol 1998; 36:3609-13.
7. Knutton S, Shaw RK, Bhan MK, Smith HR, McConnell MM, Cheasty T, et al. Ability of enteroaggregative Escherichia coli strains to adhere in vitro to human intestinal mucosa. Infect Immun 1992; 60:2083-91.
8. Cravioto A, Gross RJ, Scotland SM, Rowe B. An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile entropathogenic serotypes. Curr Microbiol 1979; 3:95-9.
9. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998; 11:142-201.
10. Kaur P, Chakraborti A, Asea A. Enteroaggregative Escherichia coli: an emerging enteric food borne pathogen. Interdiscip Perspect Infect Dis 2010; 254159.
11. Okhuysen PC, Dupont HL. Enteroaggregative Escherichia coli (EAEC): a cause of acute and persistent diarrhea of worldwide importance. J Infect Dis 202:503-5.
12. Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, et al. Diarrheagenic Escherichia coli infection in Baltimore, Maryland and New Haven, Connecticut. Clin Infect Dis 2006; 43:402-7.
13. Harrington SM, Dudley EG, Nataro JP. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett 2006; 254:12-8.
14. Okeke IN, Nataro JP. Enteroaggregative Escherichia coli. Lancet Infect Dis 2001; 1:304-13.
15. Huang DB, Nataro JP, DuPont HL, Kamat PP, Mhatre AD, Okhuysen PC, et al. Enteroaggregative Escherichia coli is a cause of acute diarrheal illness: a meta-analysis. Clin Infect Dis 2006; 43:556-63.
16. Weintraub A. Enteroaggregative Escherichia coli: epidemiology, virulence and detection. J Med Microbiol 2007; 56:4-8.
17. Wilson A, Evans J, Chart H, Cheasty T, Wheeler JG, Tompkins D, et al. Characterisation of strains of enteroaggregative Escherichia coli isolated during the infectious intestinal disease study in England. Eur J Epidemiol 2001; 17:1125-30.
18. 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 1998; 177:88-96.
19. Nataro JP, Deng Y, Cookson S, Cravioto A, Savarino SJ, Guers LD, et al. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis 1995; 171:465-8.
20. Hicks S, Candy DC, Phillips AD. Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect Immun 1996; 64:4751-60.
21. Nataro JP, Hicks S, Phillips AD, Vial PA, Sears CL. T84 cells in culture as a model for enteroaggregative Escherichia coli pathogenesis. Infect Immun 1996; 64:4761-8.
22. 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 1992; 60:5302-6.
23. Bernier C, Gounon P, Le Bouguenec 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 2002; 70:4302-11.
24. 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.
25. Czeczulin JR, Balepur S, Hicks S, Phillips A, Hall R, Kothary MH, et al. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun 1997; 65:4135-45.
26. Debroy C, Yealy J, Wilson RA, Bhan MK, Kumar R. Antibodies raised against the outer membrane protein interrupt adherence of enteroaggregative Escherichia coli. Infect Immun 1995; 63:2873-9.
27. Dudley EG, Abe C, Ghigo JM, Latour-Lambert P, Hormazabal JC, Nataro JP. An IncI1 plasmid contributes to the adherence of the atypical enteroaggregative Escherichia coli strain C1096 to cultured cells and abiotic surfaces. Infect Immun 2006; 74:2102-14.
28. Monteiro-Neto V, Bando SY, Moreira-Filho CA, Giron JA. Characterization of an outer membrane protein associated with haemagglutination and adhesive properties of enteroaggregative Escherichia coli O111:H12. Cell Microbiol 2003; 5:533-47.
29. Nataro JP, Deng Y, Maneval DR, German AL, Martin WC, Levine MM. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun 1992; 60:2297-304.
30. Wai SN, Takade A, Amako K. The hydrophobic surface protein layer of enteroaggregative Escherichia coli strains. FEMS Microbiol Lett 1996; 135:17-22.
31. Chart H, Smith HR, Rowe B. Enteroaggregative strains of Escherichia coli belonging to serotypes O126:H27 and O44:H18 express antigenically similar 18 kDa outer membrane-associated proteins. FEMS Microbiol Lett 1995; 132:17-22.
32. Suzart S, Guth BE, Pedroso MZ, Okafor UM, Gomes TA. Diversity of surface structures and virulence genetic markers among enteroaggregative Escherichia coli (EAEC) strains with and without the EAEC DNA probe sequence. FEMS Microbiol Lett 2001; 201:163-8.
33. Bhargava S, Johnson BB, Hwang J, Harris TA, George AS, Muir A, et al. Heat-resistant agglutinin 1 is an accessory enteroaggregative Escherichia coli colonization factor. J Bacteriol 2009; 191:4934-42.
34. Vial PA, Robins-Browne R, Lior H, Prado V, Kaper JB, Nataro JP, et al. Characterization of enteroadherentaggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis 1988; 158:70-9.
35. Elias WP Jr, Czeczulin JR, Henderson IR, Trabulsi LR, Nataro JP. Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J Bacteriol 1999; 181:1779-85.
36. Servin AL. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Clin Microbiol Rev 2005; 18:264-92.
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 1994; 176:4691-9.
38. Savarino SJ, Fox P, Deng Y, Nataro JP. Identification and characterization of a gene cluster mediating enteroaggregative Escherichia coli aggregative adherence fimbria I biogenesis. J Bacteriol 1994; 176:4949-57.
39. Farfan MJ, Inman KG, Nataro JP. The major pilin subunit of the AAF/II fimbriae from enteroaggregative Escherichia coli mediates binding to extracellular matrix proteins. Infect Immun 2008; 76:4378-84.
40. Cobeljic M, Miljkovic-Selimovic B, Paunovic-Todosijevic D, Velickovic Z, Lepsanovic Z, Zec N, et al. Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol Infect 1996; 117:11-6.
41. Czeczulin JR, Whittam TS, Henderson IR, Navarro-Garcia F, Nataro JP. Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli. Infect Immun 1999; 67:2692-9.
42. Zamboni A, Fabbricotti SH, Fagundes-Neto U, Scaletsky IC. Enteroaggregative Escherichia coli virulence factors are found to be associated with infantile diarrhea in Brazil. J Clin Microbiol 2004; 42:1058-63.
43. Uber AP, Trabulsi LR, Irino K, Beutin L, Ghilardi AC, Gomes TA, et al. Enteroaggregative Escherichia coli from humans and animals differ in major phenotypical traits and virulence genes. FEMS Microbiol Lett 2006; 256:251-7.
44. Pereira AC, Britto-Filho JD, Jose de Carvalho J, de Luna MG, Rosa AC. Enteroaggregative Escherichia coli (EAEC) strains enter and survive within cultured intestinal epithelial cells. Microb Pathog 2008; 45:310-4.
45. Chaudhuri RR, Sebaihia M, Hobman JL, Webber MA, Leyton DL, Goldberg MD, et al. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One 2010; 5:8801.
46. Avelino F, Saldana Z, Islam S, Monteiro-Neto V, Dall'Agnol M, Eslava CA, et al. The majority of enteroaggregative Escherichia coli strains produce the E. coli common pilus when adhering to cultured epithelial cells. Int J Med Microbiol 300:440-8.
47. Moreira CG, Carneiro SM, Nataro JP, Trabulsi LR, Elias WP. Role of type I fimbriae in the aggregative adhesion pattern of enteroaggregative Escherichia coli. FEMS Microbiol Lett 2003; 226:79-85.
48. Sheikh J, Czeczulin JR, Harrington S, Hicks S, Henderson IR, Le Bouguenec C, et al. A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 2002; 110:1329-37.
49. Nishi J, Sheikh J, Mizuguchi K, Luisi B, Burland V, Boutin A, et al. The export of coat protein from enteroaggregative Escherichia coli by a specific ATPbinding cassette transporter system. J Biol Chem 2003; 278:45680-9.
50. Velarde JJ, Varney KM, Inman KG, Farfan M, Dudley E, Fletcher J, et al. Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Mol Microbiol 2007; 66:1123-35.
51. Monteiro BT, Campos LC, Sircili MP, Franzolin MR, Bevilacqua LF, Nataro JP, et al. The dispersinencoding gene (aap) is not restricted to enteroaggregative Escherichia coli. Diagn Microbiol Infect Dis 2009; 65:81-4.
52. 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.
53. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010; 8:26-38.
54. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004; 68:692-744.
55. 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.
56. Savarino SJ, Fasano A, Watson J, Martin BM, Levine MM, Guandalini S, et al. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc Natl Acad Sci USA 1993; 90:3093-7.
57. Eslava C, Navarro-Garcia F, Czeczulin JR, Henderson IR, Cravioto A, Nataro JP. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 1998; 66:3155-63.
58. Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP. Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 1999; 67:5587-96.
59. Behrens M, Sheikh J, Nataro JP. Regulation of the overlapping pic/set locus in Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 2002; 70:2915-25.
60. Fasano A, Noriega FR, Maneval DR Jr, Chanasongcram S, Russell R, Guandalini S, et al. Shigella enterotoxin 1: an enterotoxin of Shigella flexneri 2a active in rabbit small intestine in vivo and in vitro. J Clin Invest 1995; 95:2853-61.
61. Mueller M, Grauschopf U, Maier T, Glockshuber R, Ban N. The structure of a cytolytic alpha-helical toxin pore reveals its assembly mechanism. Nature 2009; 459:726-30.
62. Eslava C, Villaseca JM, Morales R, Navarro A, Cravioto A. Identification of a protein with toxigenic activity produced by enteroaggregative Escherichia coli. Abstracs of the 93rd General Meeting of the American Society for Microbiology, Washington DC 1993; 44.
63. Navarro-Garcia F, Eslava C, Villaseca JM, Lopez-Revilla R, Czeczulin JR, Srinivas S, et al. In vitro effects of a high-molecular-weight heat-labile enterotoxin from enteroaggregative Escherichia coli. Infect Immun 1998; 66:3149-54.
64. Jose J, Meyer TF. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol Mol Biol Rev 2007; 71:600-19.
65. Henderson IR, Navarro-Garcia F, Nataro JP. The great escape: structure and function of the autotransporter proteins. Trends Microbiol 1998; 6:370-8.
66. Maurer J, Jose J, Meyer TF. Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J Bacteriol 1999; 181:7014-20.
67. Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 2003; 47:1367-83.
68. Jacob-Dubuisson F, Locht C, Antoine R. Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 2001; 40:306-13.
69. Roggenkamp A, Ackermann N, Jacobi CA, Truelzsch K, Hoffmann H, Heesemann J. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 2003; 185:3735-44.
70. van der Woude MW, Henderson IR. Regulation and function of Ag43 (flu). Annu Rev Microbiol 2008; 62:153-69.
71. Stegmeier JF, Gluck A, Sukumaran S, Mantele W, Andersen C. Characterisation of YtfM, a second member of the Omp85 family in Escherichia coli. Biol Chem 2007; 388:37-46.
72. Knowles TJ, McClelland DM, Rajesh S, Henderson IR, Overduin M. Secondary structure and (1)H, (13)C and (15)N backbone resonance assignments of BamC, a component of the outer membrane protein assembly machinery in Escherichia coli. Biomol NMR Assign 2009; 3:203-6.
73. Knowles TJ, Jeeves M, Bobat S, Dancea F, McClelland D, Palmer T, et al. Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol Microbiol 2008; 68:1216-27.
74. Yen MR, Tseng YH, Nguyen EH, Wu LF, Saier MH Jr. Sequence and phylogenetic analyses of the twinarginine targeting (Tat) protein export system. Arch Microbiol 2002; 177:441-50.
75. Valle J, Mabbett AN, Ulett GC, Toledo-Arana A, Wecker K, Totsika M, et al. UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J Bacteriol 2008; 190:4147-61.
76. Wanke CA, Cronan S, Goss C, Chadee K, Guerrant RL. Characterization of binding of Escherichia coli strains which are enteropathogens to small-bowel mucin. Infect Immun 1990; 58:794-800.
77. Bellini EM, Elias WP, Gomes TA, Tanaka TL, Taddei CR, Huerta R, et al. Antibody response against plasmid-encoded toxin (Pet) and the protein involved in intestinal colonization (Pic) in children with diarrhea produced by enteroaggregative Escherichia coli. FEMS Immunol Med Microbiol 2005; 43:259-64.
78. Vilhena-Costa AB, Piazza RM, Nara JM, Trabulsi LR, Martinez MB. Slot blot immunoassay as a tool for plasmid-encoded toxin detection in enteroaggregative Escherichia coli culture supernatants. Diagn Microbiol Infect Dis 2006; 55:101-6.
79. Ulises HC, Tatiana G, Karlen G, Guillermo MH, Juan XC, Carlos E. Peptide sequences identified by phage display are immunodominant functional motifs of Pet and Pic serine proteases secreted by Escherichia coli and Shigella flexneri. Peptides 2009; 30:2127-35.
80. 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 1999; 67:5338-44.
81. Navarro-Garcia 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.
82. Navarro-Garcia F, Canizalez-Roman A, Luna J, Sears C, Nataro JP. Plasmid-encoded toxin of enteroaggregative Escherichia coli is internalized by epithelial cells. Infect Immun 2001; 69:1053-60.
83. Navarro-Garcia F, Canizalez-Roman A, Vidal JE, Salazar MI. Intoxication of epithelial cells by plasmidencoded toxin requires clathrin-mediated endocytosis. Microbiology 2007; 153:2828-38.
84. Navarro-Garcia F, Canizalez-Roman A, Burlingame KE, Teter K, Vidal JE. Pet, a non-AB toxin, is transported and translocated into epithelial cells by a retrograde trafficking pathway. Infect Immun 2007; 75:2101-9.
85. Bennett V, Gilligan DM. The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu Rev Cell Biol 1993; 9:27-66.
86. Djabali K. Cytoskeletal proteins connecting intermediate filaments to cytoplasmic and nuclear periphery. Histol Histopathol 1999; 14:501-9.
87. Canizalez-Roman A, Navarro-Garcia F. Fodrin CaMbinding domain cleavage by Pet from enteroaggregative Escherichia coli leads to actin cytoskeletal disruption. Mol Microbiol 2003; 48:947-58.
88. Navarro-Garcia F. Enteroaggregative Escherichia coli plasmid-encoded toxin. Future Microbiol 2010; 5:1005-13.
89. Betancourt-Sanchez M, Navarro-Garcia F. Pet secretion, internalization and induction of cell death during infection of epithelial cells by enteroaggregative Escherichia coli. Microbiology 2009; 155:2895-906.
90. Rajakumar K, Sasakawa C, Adler B. Use of a novel approach, termed island probing, identifies the Shigella flexneri she pathogenicity island which encodes a homolog of the immunoglobulin A protease-like family of proteins. Infect Immun 1997; 65:4606-14.
91. Gutierrez-Jimenez J, Arciniega I, Navarro-Garcia F. The serine protease motif of Pic mediates a dose-dependent mucolytic activity after binding to sugar constituents of the mucin substrate. Microb Pathog 2008; 45:115-23.
92. Parham NJ, Srinivasan U, Desvaux M, Foxman B, Marrs CF, Henderson IR. PicU, a second serine protease autotransporter of uropathogenic Escherichia coli. FEMS Microbiol Lett 2004; 230:73-83.
93. Heimer SR, Rasko DA, Lockatell CV, Johnson DE, Mobley HL. Autotransporter genes pic and tsh are associated with Escherichia coli strains that cause acute pyelonephritis and are expressed during urinary tract infection. Infect Immun 2004; 72:593-7.
94. Navarro-Garcia F, Gutierrez-Jimenez J, Garcia-Tovar C, Castro LA, Salazar-Gonzalez H, Cordova V. Pic, an autotransporter protein secreted by different pathogens in the Enterobacteriaceae family, is a potent mucus secretagogue. Infect Immun 2010; 78:4101-9.
95. Harrington SM, Sheikh J, Henderson IR, Ruiz-Perez F, Cohen PS, Nataro JP. The Pic protease of enteroaggregative Escherichia coli promotes intestinal colonization and growth in the presence of mucin. Infect Immun 2009; 77:2465-73.
96. Fasano A, Noriega FR, Liao FM, Wang W, Levine MM. Effect of shigella enterotoxin 1 (ShET1) on rabbit intestine in vitro and in vivo. Gut 1997; 40:505-11.
97. Ludwig A, von Rhein C, Bauer S, Huttinger C, Goebel W. Molecular analysis of cytolysin A (ClyA) in pathogenic Escherichia coli strains. J Bacteriol 2004; 186:5311-20.
98. Lithgow JK, Haider F, Roberts IS, Green J. Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol Microbiol 2007; 66:685-98.
99. von Rhein C, Hunfeld KP, Ludwig A. Serologic evidence for effective production of cytolysin A in Salmonella enterica serovars typhi and paratyphi A during human infection. Infect Immun 2006; 74:6505-8.
100. von Rhein C, Bauer S, Simon V, Ludwig A. Occurrence and characteristics of the cytolysin A gene in Shigella strains and other members of the family Enterobacteriaceae. FEMS Microbiol Lett 2008; 287:143-8.
101. Menard LP, Lussier JG, Lepine F, Paiva de Sousa C, Dubreuil JD. Expression, purification and biochemical characterization of enteroaggregative Escherichia coli heat-stable enterotoxin 1. Protein Expr Purif 2004; 33:223-31.
102. Piva IC, Pereira AL, Ferraz LR, Silva RS, Vieira AC, Blanco JE, et al. Virulence markers of enteroaggregative Escherichia coli isolated from children and adults with diarrhea in Brasilia, Brazil. J Clin Microbiol 2003; 41:1827-32.
103. Greenberg RN, Hill M, Crytzer J, Krause WJ, Eber SL, Hamra FK, et al. Comparison of effects of uroguanylin, guanylin and Escherichia coli heat-stable enterotoxin STa in mouse intestine and kidney: evidence that uroguanylin is an intestinal natriuretic hormone. J Investig Med 1997; 45:276-82.
104. Fasano A. Toxins and the gut: role in human disease. Gut 2002; 50:9-14.
105. Savarino SJ, Fasano A, Robertson DC, Levine MM. Enteroaggregative Escherichia coli elaborate a heatstable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest 1991; 87:1450-5.
106. Bouckenooghe AR, Dupont HL, Jiang ZD, Adachi J, Mathewson JJ, Verenkar MP, et al. Markers of enteric inflammation in enteroaggregative Escherichia coli diarrhea in travelers. Am J Trop Med Hyg 2000; 62:711-3.
107. Greenberg DE, Jiang ZD, Steffen R, Verenker MP, DuPont HL. Markers of inflammation in bacterial diarrhea among travelers, with a focus on enteroaggregative Escherichia coli pathogenicity. J Infect Dis 2002; 185:944-9.
108. 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 2000; 105:1769-77.
109. Jiang ZD, 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.
110. Huang DB, DuPont HL, Jiang ZD, Carlin L, Okhuysen PC. Interleukin-8 response in an intestinal HCT-8 cell line infected with enteroaggregative and enterotoxigenic Escherichia coli. Clin Diagn Lab Immunol 2004; 11:548-51.
111. Plancon L, Du Merle L, Le Friec S, Gounon P, Jouve M, Guignot J, et al. Recognition of the cellular beta1-chain integrin by the bacterial AfaD invasin is implicated in the internalization of afa-expressing pathogenic Escherichia coli strains. Cell Microbiol 2003; 5:681-93.
112. Cota E, Chen HA, Anderson KL, Simpson P, Du Merle L, Bernier-Febreau C, et al. Complete resonance assignments of the 'donor-strand complemented' AfaD: the afimbrial invasin from Diffusely Adherent E. coli. J Biomol NMR 2004; 29:411-2.
113. Kucharzik T, Hudson JT, 3rd, Lugering A, Abbas JA, Bettini M, Lake JG, et al. Acute induction of human IL-8 production by intestinal epithelium triggers neutrophil infiltration without mucosal injury. Gut 2005; 54:1565-72.
114. Sansonetti PJ, Arondel J, Huerre M, Harada A, Matsushima K. Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect Immun 1999; 67:1471-80.
115. Madara JL, Patapoff TW, Gillece-Castro B, Colgan SP, Parkos CA, Delp C, et al. 5'-adenosine monophosphate is the neutrophil-derived paracrine factor that elicits chloride secretion from T84 intestinal epithelial cell monolayers. J Clin Invest 1993; 91:2320-5.
116. Khan MA, Kang J, Steiner TS. Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires Toll-like receptor 5-dependent p38 MAP kinase activation. Immunology 2004; 112:651-60.
117. Donnelly MA, Steiner TS. Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of toll-like receptor 5. J Biol Chem 2002; 277:40456-61.
118. Jiang ZD, Okhuysen PC, Guo DC, He R, King TM, DuPont HL, et al. Genetic susceptibility to enteroaggregative Escherichia coli diarrhea: polymorphism in the interleukin-8 promotor region. J Infect Dis 2003; 188:506-11.
119. Jiang ZD, DuPont HL, Garey K, Price M, Graham G, Okhuysen P, et al. A common polymorphism in the interleukin 8 gene promoter is associated with Clostridium difficile diarrhea. Am J Gastroenterol 2006; 101:1112-6.
120. Garey K, Jiang ZD, Ghantoji S, Tam VH, Arora V, Dupont HL. A common polymorphism in the interleukin-8 gene promoter is associated with an increased risk for recurrent Clostridium difficile infection. Clin Infect Dis 2010; 15:1406-10.