Abstract
An Escherichia coli strain (serotype O127a:H2) that had been isolated from a child with diarrhea in Thailand and that was negative for the virulence factors of the four categories of diarrheagenic E. coli (enterotoxigenic, enteropathogenic, enteroinvasive, and enterohemorrhagic) and that showed an aggregative pattern of adherence to HeLa cells was investigated for adherence to native or Formalin-fixed human and animal mucosa. The hemagglutinating activity and adherence ability of the bacteria were resistant to D-mannose and were strictly regulated by environmental conditions. Genetic data supported the close relation between the hemagglutinating activity and adherence ability. In accordance with the adherence pattern on tissue-cultured cells, the bacteria adhered to human and animal mucosa, as evidenced by a direct gold-labeling analysis. In human intestines, Formalin-fixed mucous coatings, epithelial cells of colonic mucosa, epithelial cells of ileal single lymphoid follicles and Peyer's patches, and the absorptive cells of jejunal or ileal villi provided adherence targets. Adherence to M cells in the Peyer's patch-associated epithelium was also confirmed. The adherence levels to native jejunal or ileal human villi were low, as was the case with the corresponding Formalin-fixed villi. In human urinary tract, the superficial epithelial cells of both native and Formalin-fixed ureter provided striking adherence targets. In animal (porcine and rabbit) small intestines, the bacteria adhered to the native villi to a lesser extent than to the Formalin-fixed villi. The adherence levels were compared with those of enterotoxigenic E. coli with colonization factor antigen (CFA)/I pili or CFA/II pili. The data suggested unique mucosa adherence characteristics of the enteroaggregative E. coli strain. The possibility of the adherence ability as a virulence factor was discussed.
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- Baldini M. M., Nataro J. P., Kaper J. B. Localization of a determinant for HEp-2 adherence by enteropathogenic Escherichia coli. Infect Immun. 1986 Apr;52(1):334–336. doi: 10.1128/iai.52.1.334-336.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bhan M. K., Khoshoo V., Sommerfelt H., Raj P., Sazawal S., Srivastava R. Enteroaggregative Escherichia coli and Salmonella associated with nondysenteric persistent diarrhea. Pediatr Infect Dis J. 1989 Aug;8(8):499–502. doi: 10.1097/00006454-198908000-00005. [DOI] [PubMed] [Google Scholar]
- Bhan M. K., Raj P., Levine M. M., Kaper J. B., Bhandari N., Srivastava R., Kumar R., Sazawal S. Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis. 1989 Jun;159(6):1061–1064. doi: 10.1093/infdis/159.6.1061. [DOI] [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]
- Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fujita K., Yamamoto T., Yokota T., Kitagawa R. In vitro adherence of type 1-fimbriated uropathogenic Escherichia coli to human ureteral mucosa. Infect Immun. 1989 Aug;57(8):2574–2579. doi: 10.1128/iai.57.8.2574-2579.1989. [DOI] [PMC free article] [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]
- Jones G. W., Abrams G. D., Freter R. Adhesive properties of Vibrio cholerae: adhesion to isolated rabbit brush border membranes and hemagglutinating activity. Infect Immun. 1976 Jul;14(1):232–239. doi: 10.1128/iai.14.1.232-239.1976. [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., Baldwin T., Williams P. H., McNeish A. S. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun. 1989 Apr;57(4):1290–1298. doi: 10.1128/iai.57.4.1290-1298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knutton S., Lloyd D. R., McNeish A. S. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun. 1987 Jan;55(1):69–77. doi: 10.1128/iai.55.1.69-77.1987. [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]
- 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]
- Mathewson J. J., Johnson P. C., DuPont H. L., Morgan D. R., Thornton S. A., Wood L. V., Ericsson C. D. A newly recognized cause of travelers' diarrhea: enteroadherent Escherichia coli. J Infect Dis. 1985 Mar;151(3):471–475. doi: 10.1093/infdis/151.3.471. [DOI] [PubMed] [Google Scholar]
- Mathewson J. J., Johnson P. C., DuPont H. L., Satterwhite T. K., Winsor D. K. Pathogenicity of enteroadherent Escherichia coli in adult volunteers. J Infect Dis. 1986 Sep;154(3):524–527. doi: 10.1093/infdis/154.3.524. [DOI] [PubMed] [Google Scholar]
- Moon H. W., Whipp S. C., Argenzio R. A., Levine M. M., Giannella R. A. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun. 1983 Sep;41(3):1340–1351. doi: 10.1128/iai.41.3.1340-1351.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakasone N., Iwanaga M. Quantitative evaluation of colonizing ability of Vibrio cholerae O1. Microbiol Immunol. 1987;31(8):753–761. doi: 10.1111/j.1348-0421.1987.tb03137.x. [DOI] [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]
- Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology. 1974 Feb;66(2):189–203. [PubMed] [Google Scholar]
- Owen R. L., Pierce N. F., Apple R. T., Cray W. C., Jr M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis. 1986 Jun;153(6):1108–1118. doi: 10.1093/infdis/153.6.1108. [DOI] [PubMed] [Google Scholar]
- Roth J., Bendayan M., Orci L. Ultrastructural localization of intracellular antigens by the use of protein A-gold complex. J Histochem Cytochem. 1978 Dec;26(12):1074–1081. doi: 10.1177/26.12.366014. [DOI] [PubMed] [Google Scholar]
- Rothbaum R., McAdams A. J., Giannella R., Partin J. C. A clinicopathologic study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology. 1982 Aug;83(2):441–454. [PubMed] [Google Scholar]
- Sack R. B. Enterotoxigenic Escherichia coli: identification and characterization. J Infect Dis. 1980 Aug;142(2):279–286. doi: 10.1093/infdis/142.2.279. [DOI] [PubMed] [Google Scholar]
- Scaletsky I. C., Silva M. L., Toledo M. R., Davis B. R., Blake P. A., Trabulsi L. R. Correlation between adherence to HeLa cells and serogroups, serotypes, and bioserotypes of Escherichia coli. Infect Immun. 1985 Sep;49(3):528–532. doi: 10.1128/iai.49.3.528-532.1985. [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]
- Sunthadvanich R., Chiewsilp D., Seriwatana J., Sakazaki R., Echeverria P. Nationwide surveillance program to identify diarrhea-causing Escherichia coli in children in Thailand. J Clin Microbiol. 1990 Mar;28(3):469–472. doi: 10.1128/jcm.28.3.469-472.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tzipori S., Gibson R., Montanaro J. Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infect Immun. 1989 Apr;57(4):1142–1150. doi: 10.1128/iai.57.4.1142-1150.1989. [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., Fujita K., Yokota T. Adherence characteristics to human small intestinal mucosa of Escherichia coli isolated from patients with diarrhea or urinary tract infections. J Infect Dis. 1990 Oct;162(4):896–908. doi: 10.1093/infdis/162.4.896. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Fujita K., Yokota T. Piliated Vibrio parahaemolyticus adherent to human ureteral mucosa. J Infect Dis. 1990 Feb;161(2):361–362. doi: 10.1093/infdis/161.2.361. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Kamano T., Uchimura M., Iwanaga M., Yokota T. Vibrio cholerae O1 adherence to villi and lymphoid follicle epithelium: in vitro model using formalin-treated human small intestine and correlation between adherence and cell-associated hemagglutinin levels. Infect Immun. 1988 Dec;56(12):3241–3250. doi: 10.1128/iai.56.12.3241-3250.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto T., Yokota T. Adherence targets of Vibrio parahaemolyticus in human small intestines. Infect Immun. 1989 Aug;57(8):2410–2419. doi: 10.1128/iai.57.8.2410-2419.1989. [DOI] [PMC free article] [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. Vibrio cholerae O1 adherence to human small intestinal M cells in vitro. J Infect Dis. 1989 Jul;160(1):168–169. doi: 10.1093/infdis/160.1.168. [DOI] [PubMed] [Google Scholar]
- Yamamoto T., Yokota T. Vibrio cholerae non-O1: production of cell-associated hemagglutinins and in vitro adherence to mucus coat and epithelial surfaces of the villi and lymphoid follicles of human small intestines treated with formalin. J Clin Microbiol. 1988 Oct;26(10):2018–2024. doi: 10.1128/jcm.26.10.2018-2024.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Harven E., Leung R., Christensen H. A novel approach for scanning electron microscopy of colloidal gold-labeled cell surfaces. J Cell Biol. 1984 Jul;99(1 Pt 1):53–57. doi: 10.1083/jcb.99.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]