Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7

Journal of Clinical Investigation

Volumn 117, Issue 11, 2007, Pages 3519-3529

  Xicohtencatl Cortes, Juan ^a   Monteiro Neto, Valério ^a,b   Ledesma, Maria A ^a   Jordan, Dianna M ^c   Francetic, Olivera ^d   Kaper, James B ^e   Puente, José Luis ^f   Girón, Jorge A ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b CEUMA UNIVERSITY   (Brazil)

^c IOWA STATE UNIVERSITY   (United States)

^d INSTITUT PASTEUR   (France)

^e University of Maryland School of Medicine Center for Vaccine Development   (United States)

^f INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; INTIMIN; NUCLEOLIN; PROTEIN HEPA; PROTEIN SUBUNIT; PROTEIN TIR; RECEPTOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BACTERIUM PILUS; BCPA GENE; CELL ULTRASTRUCTURE; CYTOTOXICITY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI; ESCHERICHIA COLI O157; GENE; GENE INACTIVATION; HEMOLYTIC UREMIC SYNDROME; HEMORRHAGIC COLI PILUS; HEMORRHAGIC COLITIS; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SERODIAGNOSIS;

EID: 36049037184     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI30727     Document Type: Article

References (64)

1. Riley, L.W., et al. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308:681-685.
2. Griffin, P.M., et al. 1988. Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann. Intern. Med. 109:705-712.
3. Kaper, J.B., Gansheroff, L.J., Wachtel, M.R., and O'Brien, A.D. 1998. Intimin-mediated adherence of Shiga Toxin-producing Escherichia coli and attaching-and-effacing pathogens. In Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains. J.B. Kaper and A.D. O'Brien, editors. American Society for Microbiology. Washington, DC, USA. 148-156.
4. Kaper, J.B., Nataro, J.P., and Mobley, H.L. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
5. Nataro, J.P., and Kaper, J.B. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
6. Paton, J.C., and Paton, A.W. 1998. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
7. Tarr, P.I., Gordon, C.A., and Chandler, W.L. 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 365:1073-1086.
8. Caprioli, A., Morabito, S., Brugere, H., and Oswald, E. 2005. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet. Res. 36:289-311.
9. Borczyk, A.A., Karmali, M.A., Lior, H., and Duncan, L.M. 1987. Bovine reservoir for verotoxin-producing Escherichia coli O157:H7. Lancet. 1:98.
10. Cody, S.H., et al. 1999. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann. Intern. Med. 130:202-209.
11. Crump, J.A., et al. 2002. An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm. N. Engl. J. Med. 347:555-560.
12. Karmali, M.A., Steele, B.T., Petric, M., and Lim, C. 1983. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet. 1:619-620.
13. Paton, A.W., Srimanote, P., Woodrow, M.C., and Paton, J.C. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009.
14. McKee, M.L., Melton-Celsa, A.R., Moxley, R.A., Francis, D.H., and O'Brien, A.D. 1995. Enterohemorrhagic Escherichia coli O157:H7 requires intimin to colonize the gnotobiotic pig intestine and to adhere to HEp-2 cells. Infect. Immun. 63:3739-3744.
15. Tarr, P.I., et al. 2000. Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect. Immun. 68:1400-1407.
16. Nicholls, L., Grant, T.H.R., and Robins-Browne, R.M. 2000. Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol. Microbiol. 35:275-288.
17. Ashkenazi, S., May, L., LaRocco, M., Lopez, E.L., and Cleary, T.G. 1991. The effect of postnatal age on the adherence of enterohemorrhagic Escherichia coli to rabbit intestinal cells. Pediatr. Res. 29:14-19.
18. Dean-Nystrom, E.A., Bosworth, B.T., Cray, W.C., Jr., and Moon, H.W. 1997. Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect. Immun. 65:1842-1848.
19. Stavric, S., Buchanan, B., and Gleeson, T.M. 1993. Intestinal colonization of young chicks with Escherichia coli O157:H7 and other verotoxin-producing serotypes. J. Appl. Bacteriol. 74:557-563.
20. Naylor, S.W., et al. 2003. Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect. Immun. 71:1505-1512.
21. Donnenberg, M.S., et al. 1993. The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J. Clin. Invest. 92:1418-1424.
22. Frankel, G., et al. 1996. The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J. Biol. Chem. 271:20359-20364.
23. Kenny, B., and Finlay, B.B. 1997. Intimin-dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase Cgamma1. Infect. Immun. 65:2528-2536.
24. Robinson, C.M., Sinclair, J.F., Smith, M.J., and O'Brien, A.D. 2006. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc. Natl. Acad. Sci. U. S. A. 103:9667-9672.
25. Torres, A.G., and Kaper, J.B. 2003. Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect. Immun. 71:4985-4995.
26. Hayashi, T., et al. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8:11-22.
27. Perna, N.T., et al. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature. 409:529-533.
28. Low, A.S., et al. 2006. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157:H7. Environ. Microbiol. 8:1033-1047.
29. Brunder, W., Khan, A.S., Hacker, J., and Karch, H. 2001. Novel type of fimbriae encoded by the large plasmid of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:H(-). Infect. Immun. 69:4447-4457.
30. Torres, A.G., et al. 2002. Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 70:5416-5427.
31. Kim, S.H., and Kim, Y.H. 2004. Escherichia coli O157: H7 adherence to HEp-2 cells is implicated with curli expression and outer membrane integrity. J. Vet. Sci. 5:119-124.
32. Low, A.S., et al. 2006. Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 74:2233-2244.
33. Srimanote, P., Paton, A.W., and Paton, J.C. 2002. Characterization of a novel type IV pilus locus encoded on the large plasmid of locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 70:3094-3100.
34. Jordan, D.M., et al. 2004. Long polar fimbriae contribute to colonization by Escherichia coli O157:H7 in vivo. Infect. Immun. 72:6168-6171.
35. Rendon, M.A., et al. 2007. Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc. Natl. Acad. Sci. U. S. A. 104:10637-10642.
36. Craig, L., Pique, M.E., and Tainer, J.A. 2004. Type IV pilus structure and bacterial pathogenicity. Nat. Rev. Microbiol. 2:363-378.
37. Mattick, J.S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289-314.
38. Winther-Larsen, H.C., et al. 2001. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl. Acad. Sci. U. S. A. 98:15276-15281.
39. Giron, J.A., Ho, A.S., and Schoolnik, G.K. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science. 254:710-713.
40. Taylor, R.K., Miller, V.L., Furlong, D.B., and Mekalanos, J.J. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. U. S. A. 84:2833-2837.
41. Paranjpye, R.N., and Strom, M.S. 2005. A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect. Immun. 73:1411-1422.
42. Guinee, P.A., Jansen, W.H., and Agterberg, C.M. 1976. Detection of the K99 antigen by means of agglutination and immunoelectrophoresis in Escherichia coli isolates from calves and its correlation with entertoxigenicity. Infect. Immun. 13:1369-1377.
43. Giron, J.A., Levine, M.M., and Kaper, J.B. 1994. Longus: a long pilus ultrastructure produced by human enterotoxigenic Escherichia coli. Mol. Microbiol. 12:71-82.
44. Gismero-Ordonez, J., Dall'Agnol, M., Trabulsi, L.R., and Giron, J.A. 2002. Expression of the bundle-forming pilus by enteropathogenic Escherichia coli strains of heterologous serotypes. J. Clin. Microbiol. 40:2291-2296.
45. de Oliveira-Garcia, D., et al. 2002. Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. Emerg. Infect. Dis. 8:918-923.
46. Blattner, F.R., et al. 1997. The complete genome sequence of Escherichia coli K-12. Science. 277:1453-1474.
47. Francetic, O., Lory, S., and Pugsley, A.P. 1998. A second prepilin peptidase gene in Escherichia coli K-12. Mol. Microbiol. 27:763-775.
48. Strom, M.S., and Lory, S. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
49. Sauvonnet, N., Gounon, P., and Pugsley, A.P. 2000. PpdD type IV pilin of Escherichia coli K-12 can be assembled into pili in Pseudomonas aeruginosa. J. Bacteriol. 182:848-854.
50. Sundin, C., Wolfgang, M.C., Lory, S., Forsberg, A., and Frithz-Lindsten, E. 2002. Type IV pili are not specifically required for contact dependent translocation of exoenzymes by Pseudomonas aeruginosa. Microb. Pathog. 33:265-277.
51. Nougayrede, J.P., and Donnenberg, M.S. 2004. Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol. 6:1097-1111.
52. Hicks, S., Frankel, G., Kaper, J.B., Dougan, G., and Phillips, A.D. 1998. Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect. Immun. 66:1570-1578.
53. Puente, J.L., Bieber, D., Ramer, S.W., Murray, W., and Schoolnik, G.K. 1996. The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Mol. Microbiol. 20:87-100.
54. Edwards, R.A., and Puente, J.L. 1998. Fimbrial expression in enteric bacteria: a critical step in intestinal pathogenesis. Trends Microbiol. 6:282-287.
55. Sauvonnet, N., Vignon, G., Pugsley, A.P., and Gounon, P. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
56. Datsenko, K.A., and Wanner, B.L. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
57. Sambrook, J., and Russell, D.W. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York, USA. 854 pp.
58. Giron, J.A., Torres, A.G., Freer, E., and Kaper, J.B. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361-379.
59. Parissi-Crivelli, A., Parissi-Crivelli, J.M., and Giron, J.A. 2000. Recognition of enteropathogenic Escherichia coli virulence determinants by human colostrum and serum antibodies. J. Clin. Microbiol. 38:2696-2700.
60. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
61. Giron, J.A., Ho, A.S., and Schoolnik, G.K. 1993. Characterization of fimbriae produced by enteropathogenic Escherichia coli. J. Bacteriol. 175:7391-7403.
62. Jarvis, K.G., and Kaper, J.B. 1996. Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect. Immun. 64:4826-4829.
63. Tzipori, S., et al. 1987. Role of a 60-megadalton plasmid and Shiga-like toxins in the pathogenesis of infection caused by enterohemorrhagic Escherichia coli O157:H7 in gnotobiotic piglets. Infect. Immun. 55:3117-3125.
64. Roulland-Dussoix, D., and Boyer, H.W. 1969. The Escherichia coli B restriction endonuclease. Biochim. Biophys. Acta. 195:219-229.