Heat-resistant agglutinin 1 is an accessory enteroaggregative Escherichia coli colonization factor

Journal of Bacteriology

Volumn 191, Issue 15, 2009, Pages 4934-4942

  Bhargava, Samhita ^a   Johnson, Brandon B ^a   Hwang, Jennifer ^a   Harris, Tamia A ^a   George, Anu S ^a   Muir, Amanda ^a   Dorff, Justin ^a   Okeke, Iruka N ^a  

^a HAVERFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLUTININ; AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; GENE PRODUCT; GENOMIC DNA; KANAMYCIN; OUTER MEMBRANE PROTEIN; STREPTOMYCIN; TETRACYCLINE;

ACUTE DIARRHEA; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BIOFILM; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DELETION MUTANT; DNA SEQUENCE; ENTEROAGGREGATIVE ESCHERICHIA COLI; ESCHERICHIA COLI; ESCHERICHIA COLI K 12; FIMBRIA; HEAT TOLERANCE; HRA1 GENE; HUMAN; HUMAN CELL; MOLECULAR CLONING; NONHUMAN; PERU; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WESTERN BLOTTING; WILD TYPE;

ADHESINS, BACTERIAL; ANIMALS; BIOFILMS; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; SEQUENCE DELETION;

CAENORHABDITIS ELEGANS; ESCHERICHIA COLI;

EID: 67749101200     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01831-08     Document Type: Article

References (55)

1. Aballay, A., E. Drenkard, L. R. Hilbun, and F. M. Ausubel. 2003. Caenorhabditis elegans innate immune response triggered by Salmonella enterica requires intact LPS and is mediated by a MAPK signaling pathway. Curr. Biol. 13:47-52.
2. Aballay, A., P. Yorgey, and F. M. Ausubel. 2000. Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr. Biol. 10:1539-1542.
3. Baldo, L., N. Lo, and J. H. Werren. 2005. Mosaic nature of the Wolbachia surface protein. J. Bacteriol. 187:5406-5418.
4. Bernier, C., P. Gounon, and C. Le Bouguenec. 2002. 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. 70:4302-4311.
5. Bhardwaj, R., S. Majumdar, N. K. Ganguly, N. Taneja, S. Dutta, T. Ramamurthy, and A. Chakraborti. 2006. Characterization of adhesin variants in Indian isolates of enteroaggregative Escherichia coli. FEMS Microbiol. Lett. 258:274-283.
6. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
7. Bouzari, S., A. Jafari, and M. Zarepour. 2005. Distribution of virulence related genes among enteroaggregative Escherichia coli isolates: using multiplex PCR and hybridization. Infect. Genet. Evol. 5:79-83.
8. Cerna, J. F., J. P. Nataro, and T. Estrada-Garcia. 2003. Multiplex PCR for detection of three plasmid-borne genes of enteroaggregative Escherichia coli strains. J. Clin. Microbiol. 41:2138-2140.
9. Chart, H., H. R. Smith, and B. Rowe. 1995. 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. 132:17-22.
10. Clarke, S. C., R. D. Haigh, P. P. E. Freestone, and P. H. Williams. 2003. Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin. Microbiol. Rev. 16:365-378.
11. Cohen, M. B., J. P. Nataro, D. I. Bernstein, J. Hawkins, N. Roberts, and M. A. Staat. 2005. Prevalence of diarrheagenic Escherichia coli in acute childhood enteritis: a prospective controlled study. J. Pediatr. 146:54-61.
12. Cravioto, A., R. Gross, S. Scotland, and B. Rowe. 1979. An adhesive factor found in strains of Escherichia coli belonging to the traditional enteropathogenic serotypes. Curr. Microbiol. 3:95-99.
13. Czeczulin, J., T. Whittam, I. Henderson, F. Navarro-Garcia, and J. Nataro. 1999. Phylogenetic analysis of virulence genes in enteroaggregative and diffusely-adherent Escherichia coli. Infect. Immun. 67:2692-2699.
14. Czeczulin, J. R., S. Balepur, S. Hicks, A. Phillips, R. Hall, M. H. Kothary, F. Navarro-Garcia, and J. P. Nataro. 1997. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect. Immun. 65:4135-4145.
15. Diard, M., S. Baeriswyl, O. Clermont, S. Gouriou, B. Picard, F. Taddei, E. Denamur, and I. Matic. 2007. Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect. 9:214-223.
16. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
17. Dudley, E. G., C. Abe, J. M. Ghigo, P. Latour-Lambert, J. C. Hormazabal, and J. P. Nataro. 2006. An IncI1 plasmid contributes to the adherence of the atypical enteroaggregative Escherichia coli strain C1096 to cultured cells and abiotic surfaces. Infect. Immun. 74:2102-2114.
18. Fagan, R. P., M. A. Lambert, and S. G. Smith. 2007. The Hek outer membrane protein of Escherichia coli strain RS218 binds to proteoglycan and utilizes a single extracellular loop for adherence, invasion and autoaggregation. Infect. Immun. 76:1135-1142.
19. Fagan, R. P., and S. G. Smith. 2007. The Hek outer membrane protein of Escherichia coli is an auto-aggregating adhesin and invasin. FEMS Microbiol. Lett. 269:248-255.
20. Fleckenstein, J. M., J. T. Holland, and D. L. Hasty. 2002. Interaction of an outer membrane protein of enterotoxigenic Escherichia coli with cell surface heparan sulfate proteoglycans. Infect. Immun. 70:1530-1537.
21. Fleckenstein, J. M., D. J. Kopecko, R. L. Warren, and E. A. Elsinghorst. 1996. Molecular characterization of the tia invasion locus from enterotoxigenic Escherichia coli. Infect. Immun. 64:2256-2265.
22. Hasman, H., T. Chakraborty, and P. Klemm. 1999. Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J. Bacteriol. 181:4834-4841.
23. Henk, M. C. 2004. Method for collecting air-water interface microbes suitable for subsequent microscopy and molecular analysis in both research and teaching laboratories. Appl. Environ. Microbiol. 70:2486-2493.
24. Huang, D. B., J. P. Nataro, H. L. DuPont, P. P. Kamat, A. D. Mhatre, P. C. Okhuysen, and T. Chiang. 2006. Enteroaggregative Escherichia coli is a cause of acute diarrheal illness: a meta-analysis. Clin. Infect. Dis. 43:556-563.
25. Huang, D. B., P. C. Okhuysen, Z. D. Jiang, and H. L. DuPont. 2004. Enteroaggregative Escherichia coli: an emerging enteric pathogen. Am. J. Gastroenterol. 99:383-389.
26. Huppertz, H. I., S. Rutkowski, S. Aleksic, and H. Karch. 1997. Acute and chronic diarrhoea and abdominal colic associated with enteroaggregative Escherichia coli in young children living in western Europe. Lancet 349:1660-1662.
27. Imuta, N., J. Nishi, K. Tokuda, R. Fujiyama, K. Manago, M. Iwashita, J. Sarantuya, and Y. Kawano. 2007. The Escherichia coli efflux pump TolC promotes aggregation of enteroaggregative E. coli 042. Infect. Immun. 76:1247-1256.
28. Jenkins, C., H. Chart, G. A. Willshaw, T. Cheasty, and D. S. Tompkins. 2007. Association of putative pathogenicity genes with adherence characteristics and fimbrial genotypes in typical enteroaggregative Escherichia coli from patients with and without diarrhoea in the United Kingdom. Eur. J. Clin. Microbiol. Infect. Dis. 26:901-906.
29. Lutwyche, P., R. Rupps, J. Cavanagh, R. A. Warren, and D. E. Brooks. 1994. Cloning, sequencing, and viscometric adhesion analysis of heat-resistant agglutinin 1, an integral membrane hemagglutinin from Escherichia coli O9:H10:K99. Infect. Immun. 62:5020-5026.
30. Mellies, J. L., A. M. Barron, K. R. Haack, A. S. Korson, and D. A. Oldridge. 2006. The global regulator Ler is necessary for enteropathogenic Escherichia coli colonization of Caenorhabditis elegans. Infect. Immun. 74:64-72.
31. Ménard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
32. Metcalf, W. W., W. Jiang, and B. L. Wanner. 1994. Use of the REP technique for allele replacement to construct new Escherichia coli hosts for maintenance of R6K gamma origin plasmids at different copy numbers. Gene 138:1-7.
33. Monteiro-Neto, V., L. C. Campos, A. J. Ferreira, T. A. Gomes, and L. R. Trabulsi. 1997. Virulence properties of Escherichia coli O111:H12 strains. FEMS Microbiol. Lett. 146:123-128.
34. Moreira, C. G., S. M. Carneiro, J. P. Nataro, L. R. Trabulsi, and W. P. Elias. 2003. Role of type I fimbriae in the aggregative adhesion pattern of enteroaggregative Escherichia coli. FEMS Microbiol. Lett. 226:79-85.
35. Nataro, J. P., M. M. Baldini, J. B. Kaper, R. E. Black, N. Bravo, and M. M. Levine. 1985. Detection of an adherence factor of enteropathogenic Escherichia coli with a DNA probe. J. Infect. Dis. 152:560-565.
36. Nataro, J. P., Y. Deng, S. Cookson, A. Cravioto, S. J. Savarino, L. D. Guers, M. M. Levine, and C. O. Tacket. 1995. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J. Infect. Dis. 171:465-468.
37. Nataro, J. P., Y. Deng, D. R. Maneval, A. L. German, W. C. Martin, and M. M. Levine. 1992. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect. Immun. 60:2297-2304.
38. Nataro, J. P., J. B. Kaper, R. Robins-Browne, V. Prado, P. Vial, and M. M. Levine. 1987. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6:829-831.
39. Nataro, J. P., D. Yikang, J. A. Giron, S. J. Savarino, M. H. Kothary, and R. Hall. 1993. Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect. Immun. 61:1126-1131.
40. Okeke, I. N., and J. P. Nataro. 2001. Enteroaggregative Escherichia coli. Lancet Infect. Dis. 1:304-313.
41. Okeke, I., A. Lamikanra, J. Czeczulin, F. Dubovsky, J. Kaper, and J. Nataro. 2000. Heterogeneous virulence of enteroaggregative Escherchia coli strains isolated from children in southwest Nigeria. J. Infect. Dis. 181:252-260.
42. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
43. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Schembri, M. A., D. Dalsgaard, and P. Klemm. 2004. Capsule shields the function of short bacterial adhesins. J. Bacteriol. 186:1249-1257.
45. Sheikh, J., J. R. Czeczulin, S. Harrington, S. Hicks, I. R. Henderson, C. Le Bouguenec, P. Gounon, A. Phillips, and J. P. Nataro. 2002. A novel dispersin protein in enteroaggregative Escherichia coli. J. Clin. Investig. 110:1329-1337.
46. Sheikh, J., S. Hicks, M. Dall'Agnol, A. D. Phillips, and J. P. Nataro. 2001. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol. Microbiol. 41:983-997.
47. Simon, U., R. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
48. Srinivasan, U., B. Foxman, and C. F. Marrs. 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.
49. Steiner, T., J. Nataro, C. Poteet-Smith, J. Smith, and R. Guerrant. 2000. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Investig. 105:1769-1777.
50. Tan, M. W., S. Mahajan-Miklos, and F. M. Ausubel. 1999. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 96:715-720.
51. Tompkins, D. S., M. J. Hudson, H. R. Smith, R. P. Eglin, J. G. Wheeler, M. M. Brett, R. J. Owen, J. S. Brazier, P. Cumberland, V. King, and P. E. Cook. 1999. A study of infectious intestinal disease in England: microbiological findings in cases and controls. Commun. Dis. Public Health 2:108-113.
52. Torres, A. G., J. A. Giron, N. T. Perna, V. Burland, F. R. Blattner, F. Avelino-Flores, and J. B. Kaper. 2002. Identification and characterization of lpfABCC′DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 70:5416-5427.
53. Torres, A. G., X. Zhou, and J. B. Kaper. 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect. Immun. 73:18-29.
54. Velarde, J. J., K. M. Varney, K. G. Inman, M. Farfan, E. Dudley, J. Fletcher, D. J. Weber, and J. P. Nataro. 2007. Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Mol. Microbiol. 66:1123-1135.
55. Vial, P. A., J. J. Mathewson, H. L. DuPont, L. Guers, and M. M. Levine. 1990. Comparison of two assay methods for patterns of adherence to HEp-2 cells of Escherichia coli from patients with diarrhea. J. Clin. Microbiol. 28:882-885.