Abstract
Escherichia coli 73-1 (serotype O73:H33) and 5-2 (serotype O89:H-) isolated from patients with diarrhea adhered to tissue culture cells (HeLa and HEp-2) as well as coverslips (plastic and glass) in a diffuse pattern. Adherence of strain 73-1 was mediated by a 110-kbp plasmid designated pEDA1 and correlated with D-mannose-resistant hemagglutinin (MRHA) detected with bovine, sheep, or human erythrocytes. The MRHA region was duplicated on pEDA1 and mediated the production of the 57-kDa outer membrane protein whose N-terminal amino acid sequence was hydrophobic. In accordance with MRHA and adherence, the 57-kDa outer membrane protein was observed best at 37 degrees C and to a lesser extent at 25 degrees C. In human intestine, adherence to mucus and colonic epithelium was obvious. No detectable pili were observed. The enteroaggregative E. coli heat-stable enterotoxin 1 (EAST1) gene, whose nucleotide sequence was 99.1% homologous to that of enteroaggregative E. coli, was present adjacent to the MRHA region on pEDA1. Strain 5-2 also exhibited MRHA activities and adherence and had sequences corresponding to those of the MRHA region and EAST1 gene. The data suggest that strain 73-1 (and strain 5-2), which has characteristics of both diffusely adhering E. coli and enteroaggregative E. coli, possesses a novel hemagglutinin associated with diffuse adherence.
Full Text
The Full Text of this article is available as a PDF (2.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baudry B., Savarino S. J., Vial P., Kaper J. B., Levine M. M. A sensitive and specific DNA probe to identify enteroaggregative Escherichia coli, a recently discovered diarrheal pathogen. J Infect Dis. 1990 Jun;161(6):1249–1251. doi: 10.1093/infdis/161.6.1249. [DOI] [PubMed] [Google Scholar]
- Benz I., Schmidt M. A. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect Immun. 1989 May;57(5):1506–1511. doi: 10.1128/iai.57.5.1506-1511.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benz I., Schmidt M. A. Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126:H27). Infect Immun. 1992 Jan;60(1):13–18. doi: 10.1128/iai.60.1.13-18.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bilge S. S., Clausen C. R., Lau W., Moseley S. L. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol. 1989 Aug;171(8):4281–4289. doi: 10.1128/jb.171.8.4281-4289.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Broome-Smith J. K., Edelman A., Yousif S., Spratt B. G. The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding protein 1A and 1B of Escherichia coli K12. Eur J Biochem. 1985 Mar 1;147(2):437–446. doi: 10.1111/j.1432-1033.1985.tb08768.x. [DOI] [PubMed] [Google Scholar]
- Clément J. M., Hofnung M. Gene sequence of the lambda receptor, an outer membrane protein of E. coli K12. Cell. 1981 Dec;27(3 Pt 2):507–514. doi: 10.1016/0092-8674(81)90392-5. [DOI] [PubMed] [Google Scholar]
- Echeverria P., Savarino S. J., Yamamoto T. Escherichia coli diarrhoea. Baillieres Clin Gastroenterol. 1993 Jun;7(2):243–262. doi: 10.1016/0950-3528(93)90042-q. [DOI] [PubMed] [Google Scholar]
- Girón J. A., Jones T., Millán-Velasco F., Castro-Muñoz E., Zárate L., Fry J., Frankel G., Moseley S. L., Baudry B., Kaper J. B. Diffuse-adhering Escherichia coli (DAEC) as a putative cause of diarrhea in Mayan children in Mexico. J Infect Dis. 1991 Mar;163(3):507–513. doi: 10.1093/infdis/163.3.507. [DOI] [PubMed] [Google Scholar]
- Harayama S., Tsuda M., Iino T. High frequency mobilization of the chromosome of Escherichia coli by a mutant of plasmid RP4 temperature-sensitive for maintenance. Mol Gen Genet. 1980;180(1):47–56. doi: 10.1007/BF00267351. [DOI] [PubMed] [Google Scholar]
- Jallat C., Livrelli V., Darfeuille-Michaud A., Rich C., Joly B. Escherichia coli strains involved in diarrhea in France: high prevalence and heterogeneity of diffusely adhering strains. J Clin Microbiol. 1993 Aug;31(8):2031–2037. doi: 10.1128/jcm.31.8.2031-2037.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kado C. I., Liu S. T. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. doi: 10.1128/jb.145.3.1365-1373.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knutton S., Shaw R. K., Bhan M. K., Smith H. R., McConnell M. M., Cheasty T., Williams P. H., Baldwin T. J. Ability of enteroaggregative Escherichia coli strains to adhere in vitro to human intestinal mucosa. Infect Immun. 1992 May;60(5):2083–2091. doi: 10.1128/iai.60.5.2083-2091.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LENNOX E. S. Transduction of linked genetic characters of the host by bacteriophage P1. Virology. 1955 Jul;1(2):190–206. doi: 10.1016/0042-6822(55)90016-7. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
- Levine M. M., Prado V., Robins-Browne R., Lior H., Kaper J. B., Moseley S. L., Gicquelais K., Nataro J. P., Vial P., Tall B. Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia coli. J Infect Dis. 1988 Jul;158(1):224–228. doi: 10.1093/infdis/158.1.224. [DOI] [PubMed] [Google Scholar]
- Masuda N., Sakagawa E., Ohya S. Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 1995 Mar;39(3):645–649. doi: 10.1128/AAC.39.3.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nataro J. P., Deng Y., Maneval D. R., German A. L., Martin W. C., Levine M. M. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun. 1992 Jun;60(6):2297–2304. doi: 10.1128/iai.60.6.2297-2304.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nataro J. P., Kaper J. B., Robins-Browne R., Prado V., Vial P., Levine M. M. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J. 1987 Sep;6(9):829–831. doi: 10.1097/00006454-198709000-00008. [DOI] [PubMed] [Google Scholar]
- Nataro J. P., Scaletsky I. C., Kaper J. B., Levine M. M., Trabulsi L. R. Plasmid-mediated factors conferring diffuse and localized adherence of enteropathogenic Escherichia coli. Infect Immun. 1985 May;48(2):378–383. doi: 10.1128/iai.48.2.378-383.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nataro J. P., Yikang D., Giron J. A., Savarino S. J., Kothary M. H., Hall R. Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect Immun. 1993 Mar;61(3):1126–1131. doi: 10.1128/iai.61.3.1126-1131.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nowicki B., Labigne A., Moseley S., Hull R., Hull S., Moulds J. The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun. 1990 Jan;58(1):279–281. doi: 10.1128/iai.58.1.279-281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Savarino S. J., Fasano A., Robertson D. C., Levine M. M. Enteroaggregative Escherichia coli elaborate a heat-stable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest. 1991 Apr;87(4):1450–1455. doi: 10.1172/JCI115151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Savarino S. J., Fasano A., Watson J., Martin B. M., Levine M. M., Guandalini S., Guerry P. Enteroaggregative Escherichia coli heat-stable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3093–3097. doi: 10.1073/pnas.90.7.3093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scaletsky I. C., Silva M. L., Trabulsi L. R. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun. 1984 Aug;45(2):534–536. doi: 10.1128/iai.45.2.534-536.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smit J., Kamio Y., Nikaido H. Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. J Bacteriol. 1975 Nov;124(2):942–958. doi: 10.1128/jb.124.2.942-958.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swanson T. N., Bilge S. S., Nowicki B., Moseley S. L. Molecular structure of the Dr adhesin: nucleotide sequence and mapping of receptor-binding domain by use of fusion constructs. Infect Immun. 1991 Jan;59(1):261–268. doi: 10.1128/iai.59.1.261-268.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tacket C. O., Moseley S. L., Kay B., Losonsky G., Levine M. M. Challenge studies in volunteers using Escherichia coli strains with diffuse adherence to HEp-2 cells. J Infect Dis. 1990 Aug;162(2):550–552. doi: 10.1093/infdis/162.2.550. [DOI] [PubMed] [Google Scholar]
- Vial P. A., Mathewson J. J., DuPont H. L., Guers L., Levine M. M. Comparison of two assay methods for patterns of adherence to HEp-2 cells of Escherichia coli from patients with diarrhea. J Clin Microbiol. 1990 May;28(5):882–885. doi: 10.1128/jcm.28.5.882-885.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vial P. A., Robins-Browne R., Lior H., Prado V., Kaper J. B., Nataro J. P., Maneval D., Elsayed A., Levine M. M. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988 Jul;158(1):70–79. doi: 10.1093/infdis/158.1.70. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Echeverria P. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infect Immun. 1996 Apr;64(4):1441–1445. doi: 10.1128/iai.64.4.1441-1445.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto T., Echeverria P., Yokota T. Drug resistance and adherence to human intestines of enteroaggregative Escherichia coli. J Infect Dis. 1992 Apr;165(4):744–749. doi: 10.1093/infdis/165.4.744. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Endo S., Yokota T., Echeverria P. Characteristics of adherence of enteroaggregative Escherichia coli to human and animal mucosa. Infect Immun. 1991 Oct;59(10):3722–3739. doi: 10.1128/iai.59.10.3722-3739.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto T., Koyama Y., Matsumoto M., Sonoda E., Nakayama S., Uchimura M., Paveenkittiporn W., Tamura K., Yokota T., Echeverria P. Localized, aggregative, and diffuse adherence to HeLa cells, plastic, and human small intestines by Escherichia coli isolated from patients with diarrhea. J Infect Dis. 1992 Dec;166(6):1295–1310. doi: 10.1093/infdis/166.6.1295. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Yokota T. Electron microscopic study of Vibrio cholerae O1 adherence to the mucus coat and villus surface in the human small intestine. Infect Immun. 1988 Oct;56(10):2753–2759. doi: 10.1128/iai.56.10.2753-2759.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto T., Yokota T., Kaji A. Molecular organization of heat-labile enterotoxin genes originating in Escherichia coli of human origin and construction of heat-labile toxoid-producing strains. J Bacteriol. 1981 Dec;148(3):983–987. doi: 10.1128/jb.148.3.983-987.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]