Molecular variation among type IV pilin (bfpA) genes from diverse enteropathogenic Escherichia coli strains

Infection and Immunity

Volumn 68, Issue 12, 2000, Pages 7028-7038

  Blank, T Eric ^a   Zhong, Hailang ^a   Bell, Alison L ^b   Whittam, Thomas S ^b   Donnenberg, Michael S ^a  

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

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; PILIN;

AMINO ACID SEQUENCE; ANTIGENIC VARIATION; ARTICLE; BACTERIAL GENETICS; BACTERIUM ADHERENCE; BACTERIUM PILUS; CELL AGGREGATION; ELECTROPHORESIS; ESCHERICHIA COLI; GENE CLUSTER; GENE SEQUENCE; GENETIC VARIABILITY; GRAM NEGATIVE INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; VACCINE PRODUCTION;

ALLELES; AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ESCHERICHIA COLI VACCINES; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; SEROTYPING;

EID: 0034444843     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.12.7028-7038.2000     Document Type: Article

References (81)

1. Aho, E. L., J. W. Botten, R. J. Hall, M. K. Larson, and J. K. Ness. 1997. Characterization of a class II pilin expression locus from Neisseria meningitidis: evidence for increased diversity among pilin genes in pathogenic Neisseria species. Infect. Immun. 65:2613-2620.
2. Anantha, R. P., K. D. Stone, and M. S. Donnenberg. 2000. Effects of bfp mutations on biogenesis of functional enteropathogenic Escherichia coli type IV pili. J. Bacteriol. 182:2498-2506.
3. Baldini, M. M., J. B. Kaper, M. M. Levine, D. C. Candy, and H. W. Moon. 1983. Plasmid-mediated adhesion in enteropathogenic Escherichia coli. J. Pediatr. Gastroenterol. Nutr. 2:534-538.
4. Beaudry, M., C. Zhu, J. M. Fairbrother, and J. Harel. 1996. Genotypic and phenotypic characterization of Escherichia coli isolates from dogs manifesting attaching and effacing lesions. J. Clin. Microbiol. 34:144-148.
5. Bieber, D., S. W. Ramer, C. Y. Wu, W. J. Murray, T. Tobe, R. Fernandez, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.
6. Bortolini, M. R., L. R. Trabulsi, R. Keller, G. Frankel, and V. Sperandio. 1999. Lack of expression of bundle-forming pili in some clinical isolates of enteropathogenic Escherichia coli (EPEC) is due to a conserved large deletion in the bfp operon. FEMS Microbiol. Lett. 179:169-174.
7. Cravioto, A., R. J. Gross, S. M. Scotland, and B. Rowe. 1979. An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr. Microbiol. 3:95-99.
8. Cravioto, A., R. E. Reyes, F. Trujillo, F. Uribe, A. Navarro, J. M. De La Roca, J. M. Hernández, G. Pérez, and V. Vázquez. 1990. Risk of diarrhea during the first year of life associated with initial and subsequent colonization by specific enteropathogens. Am. J. Epidemiol. 131:886-904.
9. Cravioto, A., A. Tello, A. Navarro, J. Ruis, H. Villafán, F. Uribe, and C. Eslava. 1991. Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet 337:262-264.
10. Donnenberg, M. S. 1995. Enteropathogenic Escherichia coli, p. 709-726. In M. J. Blaser, P. D. Smith, J. I. Ravdin, H. B. Greenberg, and R. L. Guerrant (ed.), Infections of the gastrointestinal tract. Raven Press, Ltd., New York, N.Y.
11. Donnenberg, M. S., J. A. Girón, J. P. Nataro, and J. B. Kaper. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6:3427-3437.
12. Donnenberg, M. S., and J. P. Nataro. 1995. Methods for studying adhesion of diarrheagenic Escherichia coli. Methods Enzymol. 253:324-336.
13. Donnenberg, M. S., C. O. Tacket, G. Losonsky, G. Frankel, J. P. Nataro, G. Dougan, and M. M. Levine. 1998. Effect of prior experimental human enteropathogenic Escherichia coli infection on illness following homologous and heterologous rechallenge. Infect. Immun. 66:52-58.
14. Drolet, R., J. M. Fairbrother, J. Harel, and P. Hélie. 1994. Attaching and effacing and enterotoxigenic Escherichia coli associated with enteric colibacillosis in the dog. Can. J. Vet. Res. 58:87-92.
15. Forest, K. T., S. A. Dunham, M. Koomey, and J. A. Tainer. 1999. Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol. Microbiol. 31:743-752.
16. Forest, K. T., and J. A. Tainer. 1997. Type-4 pilus-structure: outside to inside and top to bottom - a minireview. Gene 192:165-169.
17. Giles, C., G. Sangster, and J. Smith. 1949. Epidemic gastroenteritis of infants in Aberdeen during 1947. Arch. Dis. Child. 24:45-53.
18. Girón, J. A., M. S. Donnenberg, W. C. Martin, K. G. Jarvis, and J. B. Kaper. 1993. Distribution of the bundle-forming pilus structural gene (bfpA) among enteropathogenic Escherichia coli. J. Infect. Dis. 168:1037-1041.
19. Girón, J. A., A. S. Y. Ho, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254:710-713.
20. Girón, J. A., F. Qadri, T. Azim, K. J. Jarvis, J. B. Kaper, and M. J. Albert. 1995. Monoclonal antibodies specific for the bundle-forming pilus of enteropathogenic Escherichia coli. Infect. Immun. 63:4949-4952.
21. Gomes, T. A. T., M. A. M. Vieira, I. K. Wachsmuth, P. A. Blake, and L. R. Trabulsi. 1989. Serotype-specific prevalence of Escherichia coli strains with EPEC adherence factor genes in infants with and without diarrhea in São Paulo, Brazil. J. Infect. Dis. 160:131-135.
22. Gunzburg, S. T., N. G. Tornieporth, and L. W. Riley. 1995. Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J. Clin. Microbiol. 33:1375-1377.
23. Hahn, H. P. 1997. The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa - a review. Gene 192:99-108.
24. Hales, B. A., C. A. Hart, R. M. Batt, and J. R. Saunders. 1992. The large plasmids found in enterohemorrhagic and enteropathogenic Escherichia coli constitute a related series of transfer-defective Inc F-IIA replicons. Plasmid 28:183-193.
25. Hazes, B., P. A. Sastry, K. Hayakawa, R. J. Read, and R. T. Irvin. 2000. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J. Mol. Biol. 299:1005-1017.
26. Hicks, S., G. Frankel, J. B. Kaper, G. Dougan, and A. D. Phillips. 1998. Role of intimin and bundle-forming pili in enteropathogenic Escherichia coli adhesion to pediatric intestinal tissue in vitro. Infect. Immun. 66:1570-1578.
27. Iredell, J. R., and P. A. Manning. 1994. Biotype-specific tcpA genes in Vibrio cholerae. FEMS Microbiol. Lett. 121:47-54.
28. Kaper, J. B. 1996. Defining EPEC. Rev. Microbiol. São Paulo 27(Suppl. 1):130-133.
29. Kennedy, D. H., G. H. Walker, R. J. Fallon, J. F. Boyd, R. J. Gross, and B. Rowe. 1973. An outbreak of infantile gastroenteritis due to E. coli 0142. J. Clin. Pathol. 26:731-737.
30. Kirn, T. J., M. J. Lafferty, C. M. Sandoe, and R. K. Taylor. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35:896-910.
31. Knutton, S., R. K. Shaw, R. P. Anantha, M. S. Donnenberg, and A. A. Zorgani. 1999. The type IV bundle-forming pilus of enteropathogenic Escherichia coli undergoes dramatic alterations in structure associated with bacterial adherence, aggregation and dispersal. Mol. Microbiol. 33: 499-509.
32. Laporta, M. Z., M. L. M. Silva, I. C. A. Scaletsky, and L. R. Trabulsi. 1986. Plasmids coding for drug resistance and localized adherence to HeLa cells in enteropathogenic Escherichia coli O55:H- and O55:H6. Infect. Immun. 51:715-717.
33. Levine, M. M. 1996. Vaccines against enteropathogenic Escherichia coli. Rev. Microbiol. São Paulo 27(Suppl. 1): 126-129.
34. Levine, M. M., E. J. Bergquist, D. R. Nalin, D. H. Waterman, R. B. Hornick, C. R. Young, S. Sotman, and B. Rowe. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet i:1119-1122.
35. Levine, M. M., J. P. Nataro, H. Karch, M. M. Baldini, J. B. Kaper, R. E. Black, M. L. Clements, and A. D. O'Brien. 1985. The diarrheal response of humans to some classic serotypes of enteropathogenic Escherichia coli is dependent on a plasmid encoding an enteroadhesiveness factor. J. Infect. Dis. 152:550-559.
36. Levine, M. M., V. Prado, R. Robins-Browne, H. Lior, J. B. Kaper, S. L. Moseley, K. Gicquelais, J. P. Nataro, P. Vial, and B. Tall. 1988. Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia coli. J. Infect. Dis. 158:224-228.
37. Loureiro, I., G. Frankel, J. Adu-Bobie, G. Dougan, L. R. Trabulsi, and M. M. Carneiro-Sampaio. 1998. Human colostrum contains IgA antibodies reactive to enteropathogenic Escherichia coli virulence-associated proteins: intimin, BfpA, EspA, and EspB. J. Pediatr. Gastroenterol. Nutr. 27:166-171.
38. Martinez, M. B., C. R. Taddei, A. Ruiz-Tagle, L. R. Trabulsi, and J. A. Girón. 1999. Antibody response of children with enteropathogenic Escherichia coli infection to the bundle-forming pilus and locus of enterocyte effacement-encoded virulence determinants. J. Infect. Dis. 179:269-274.
39. McConnell, M. M., H. Chart, S. M. Scotland, H. R. Smith, G. A. Willshaw, and B. Rowe. 1989. Properties of adherence factor plasmids of enteropathogenic Escherichia coli and the effect of host strain on expression of adherence to HEp-2 cells. J. Gen. Microbiol. 135:1123-1134.
40. McNamara, B. P., and M. S. Donnenberg. 2000. Evidence for specificity in type 4 pilus biogenesis by enteropathogenic Escherichia coli. Microbiology 146:719-729.
41. Meyer, T. F., C. P. Gibbs, and R. Haas. 1990. Variation and control of protein expression in Neisseria. Annu. Rev. Microbiol. 44:451-477.
42. Nagayama, K., Z. Bi, T. Oguchi, V. Takarada, S. Shibata, and T. Honda. 1996. Use of an alkaline phosphatase-conjugated oligonucleotide probe for the gene encoding the bundle-forming pilus of enteropathogenic Escherichia coli. J. Clin. Microbiol. 34:2819-2821.
43. Nandi, B., R. K. Nandy, A. C. Vicente, and A. C. Ghose. 2000. Molecular characterization of a new variant of toxin-coregulated pilus protein (TcpA) in a toxigenic non-O1/non-O139 strain of Vibrio cholerae. Infect. Immun. 68:948-952.
44. 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.
45. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
46. 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.
47. Nataro, J. P., K. O. Maher, P. Mackie, and J. B. Kaper. 1987. Characterization of plasmids encoding the adherence factor of enteropathogenic Escherichia coli. Infect. Immun. 55:2370-2377.
48. Nataro, J. P., I. C. A. Scaletsky, J. B. Kaper, M. M. Levine, and L. R. Trabulsi. 1985. Plasmid-mediated factors conferring diffuse and localized adherence of enteropathogenic Escherichia coli. Infect. Immun. 48:378-383.
49. Nei, M., and T. Gojobori. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3:418-426.
50. Novais, R. C., A. Coelho, C. A. Salles, and A. C. Vicente. 1999. Toxin-coregulated pilus cluster in non-O1, non-toxigenic Vibrio cholerae: evidence of a third allele of pilin gene. FEMS Microbiol. Lett. 171:49-55.
51. Ørskov, F., I. Ørskov, T. A. Rees, and K. Sahab. 1960. Two new E. coli O-antigens: O141 and O142 and two new coli K-antigens: K85 and K86. Acta Pathol. Microbiol. Scand. 48:48-50.
52. Parge, H. E., K. T. Forest, M. J. Hickey, D. A. Christensen, E. D. Getzoff, and J. A. Tainer. 1995. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 378:32-38.
53. Parissi-Crivelli, A., J. M. Parissi-Crivelli, and J. A. Girón. 2000. Recognition of enteropathogenic Escherichia coli virulence determinants by human colostrum and serum antibodies. J. Clin. Microbiol. 38:2696-2700.
54. Reid, S. D., C. J. Herbelin, A. C. Bumhaugh, R. K. Selander, and T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67.
55. Rhine, J. A., and R. K. Taylor. 1994. TcpA pilin sequences and colonization requirements for O1 and O139 Vibrio cholerae. Mol. Microbiol. 13:1013-1020.
56. Robins-Browne, R. M. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9:28-53.
57. Robins-Browne, R. M., W. C. Yam, L. E. O'Gorman, and K. A. Bettelheim. 1993. Examination of archetypal strains of enteropathogenic Escherichia coli for properties associated with bacterial virulence. J. Med. Microbiol. 38:222-226.
58. Sayle, R. A., and E. J. Milner-White. 1995. RASMOL: biomolecular graphics for all. Trends Biochem. Sci. 20:374.
59. Scaletsky, I. C. A., M. L. M. Silva, and L. R. Trabulsi. 1984. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect. Immun. 45:534-536.
60. Schremmer, C., J. E. Lohr, U. Wastlhuber, J. Kösters, K. Ravelshofer, H. Steinrück, and L. H. Wieler. 1999. Enteropathogenic Escherichia coli in Psittaciformes. Avian Pathol. 28:349-354.
61. Schriefer, A., J. R. Maltez, N. Silva, M. Y. Stoeckle, M. Barral-Netto, and L. W. Riley. 1999. Expression of a pilin subunit BfpA of the bundle-forming pilus of enteropathogenic Escherichia coli in an aroA live Salmonella vaccine strain. Vaccine 17:770-778.
62. Seifert, H. S. 1996. Questions about gonococcal pilus phase and antigenic variation. Mol. Microbiol. 21:433-440.
63. Selander, R. K., D. A. Caugant, H. Ochman, J. M. Musser, M. N. Gilmour, and T. S. Whittam. 1986. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51:873-884.
64. Sohel, I., J. L. Puente, W. J. Murray, J. Vuopio-Varkila, and G. K. Schoolnik. 1993. Cloning and characterization of the bundle-forming pilin gene of enteropathogenic Escherichia coli and its distribution in Salmonella serotypes. Mol. Microbiol. 7:563-575.
65. Sohel, I., J. L. Puente, S. W. Ramer, D. Bieber, C.-Y. Wu, and G. K. Schoolnik. 1996. Enteropathogenic Escherichia coli: identification of a gene cluster coding for bundle-forming pilus morphogenesis. J. Bacteriol. 178: 2613-2628.
66. Stone, K. D., H.-Z. Zhang, L. K. Carlson, and M. S. Donnenberg. 1996. A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for biogenesis of a type IV pilus. Mol. Microbiol. 20:325-337.
67. Strom, M. S., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
68. Taylor, J., and R. E. Charter. 1952. The isolation of serological types of Bact. coli in two residential nurseries and their relation to infantile gastroenteritis. J. Pathol. Bacteriol. 64:715-728.
69. Taylor, J., and R. E. Charter. 1955. Escherichia coli O.128 causing gastroenteritis of infants. J. Clin. Pathol. 8:276-281.
70. Tennent, J. M., and J. S. Mattick. 1994. Type 4 fimbriae, p. 127-146. In P. Klemm (ed.), Fimbriae: adhesion, genetics, biogenesis, and vaccines. CRC Press, Inc., Boca Raton, Fla.
71. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
72. Tobe, T., T. Hayashi, C. G. Han, G. K. Schoolnik, E. Ohtsubo, and C. Sasakawa. 1999. Complete DNA sequence and structural analysis of the enteropathogenic Escherichia coli adherence factor plasmid. Infect. Immun. 67:5455-5462.
73. Toledo, M. R., M. Alvariza, J. Murahovschi, S. R. Ramos, and L. R. Trabulsi. 1983. Enteropathogenic Escherichia coli serotypes and endemic diarrhea in infants. Infect. Immun. 39:586-589.
74. Tornieporth, N. G., J. John, K. Salgado, P. de Jesus, E. Latham, M. C. Melo, S. T. Gunzburg, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33:1371-1374.
75. Tsukamoto, T. 1996. PCR methods for detection of enteropathogenic Escherichia coli (localized adherence) and enteroaggregative Escherichia coli. Kansenshogaku Zasshi 70:569-573.
76. Vuopio-Varkila, J., and G. K. Schoolnik. 1991. Localized adherence by enteropathogenic Escherichia coli is an inducible phenotype associated with the expression of new outer membrane proteins. J. Exp. Med. 174:1167-1177.
77. Wall, D., and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10.
78. Whittam, T. S., and E. A. McGraw. 1996. Clonal analysis of EPEC sero-groups. Rev. Microbiol. São Paulo 27(Suppl. 1):7-16.
79. Whittam, T. S., M. L. Wolfe, I. K. Wathsmuth, F. Ørskov, I. Ørskov, and R. A. Wilson. 1993. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect. Immun. 61:1619-1629.
80. Wieler, L. H., E. Vieler, C. Erpenstein, T. Schlapp, H. Steinruck, R. Bauerfeind, A. Byomi, and G. Baljer. 1996. Shiga toxin-producing Escherichia coli strains from bovines: association of adhesion with carriage of eae and other genes. J. Clin. Microbiol. 34:2980-2984.
81. Zhang, H.-Z., and M. S. Donnenberg. 1996. DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol. Microbiol. 21: 787-797.