Abstract
Infection of rabbits with Escherichia coli RDEC-1 is a useful model for diarrheal disease caused by mucosally attaching E. coli. Understanding of the protective immunity induced by RDEC-1 infection in rabbits should provide information useful in the design of vaccines for protection against this infection and other mucosally attaching organisms as well. Thus, to define the time course and location of specific immunoglobulin A secretion in relation to bacterial colonization during primary RDEC-1 infection, we infected rabbits with RDEC-1, which express AF/R1 adherence pili, and compared sites of anti-AF/R1 antibody-containing cells in the intestinal mucosa with the sites of luminal colonization and mucosal attachment of RDEC-1. Also, anti-AF/R1 antibodies in intestinal fluids and bile were measured by enzyme-linked immunosorbent assay, and attachment sites of RDEC-1 to the intestinal epithelium were determined by immunohistochemical examination. Anti-AF/R1 pilus antibody-containing cells were most numerous in the proximal intestine (duodenum and jejunum). In contrast, both luminal colonization and attachment of RDEC-1 to epithelial cells were densest in the distal intestine (cecum and colon). Anti-AF/R1 antibodies were present in approximately equal amounts in fluids collected from all levels of the gut after week 1 postinfection. Anti-AF/R1 antibody levels in undiluted bile exceeded those in gut flushes by at least 2 orders of magnitude. Loss of RDEC-1 attachment to epithelial cells preceded resolution of diarrheal illness despite the presence of large numbers of organisms in the intestinal lumen. Our studies indicate that during RDEC-1 infection (i) sites of greatest mucosal anti-AF/R1 antibody secretion are proximal to sites of maximal RDEC-1 luminal colonization and attachment, (ii) bile is a major source of specific antibodies in the intestinal lumen, and (iii) interference with RDEC-1 attachment to epithelial cells may permit resolution of disease.
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- Berendson R., Cheney C. P., Schad P. A., Boedeker E. C. Species-specific binding of purified pili (AF/R1) from the Escherichia coli RDEC-1 to rabbit intestinal mucosa. Gastroenterology. 1983 Oct;85(4):837–845. [PubMed] [Google Scholar]
- Bergmann K. C., Waldman R. H. Stimulation of secretory antibody following oral administration of antigen. Rev Infect Dis. 1988 Sep-Oct;10(5):939–950. doi: 10.1093/clinids/10.5.939. [DOI] [PubMed] [Google Scholar]
- Bienenstock J., Befus A. D. Mucosal immunology. Immunology. 1980 Oct;41(2):249–270. [PMC free article] [PubMed] [Google Scholar]
- Bienenstock J. Gut and bronchus associated lymphoid tissue: an overview. Adv Exp Med Biol. 1982;149:471–477. doi: 10.1007/978-1-4684-9066-4_66. [DOI] [PubMed] [Google Scholar]
- Brown W. R., Burns F. A. Application of peroxidase-labeled antibody methods to identification of immunoglobulin-containing cells in gastrointestinal tissues. J Immunol Methods. 1973 Apr;2(3):303–307. doi: 10.1016/0022-1759(73)90056-2. [DOI] [PubMed] [Google Scholar]
- Brown W. R., Kloppel T. M. The liver and IgA: immunological, cell biological and clinical implications. Hepatology. 1989 May;9(5):763–784. doi: 10.1002/hep.1840090518. [DOI] [PubMed] [Google Scholar]
- Cantey J. R., Blake R. K. Diarrhea due to Escherichia coli in the rabbit: a novel mechanism. J Infect Dis. 1977 Mar;135(3):454–462. doi: 10.1093/infdis/135.3.454. [DOI] [PubMed] [Google Scholar]
- Cantey J. R., Hosterman D. S. Characterization of colonization of the rabbit gastrointestinal tract by Escherichia coli RDEC-1. Infect Immun. 1979 Dec;26(3):1099–1103. doi: 10.1128/iai.26.3.1099-1103.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cantey J. R., Inman L. R., Blake R. K. Production of diarrhea in the rabbit by a mutant of Escherichia coli (RDEC-1) that does not express adherence (AF/R1) pili. J Infect Dis. 1989 Jul;160(1):136–141. doi: 10.1093/infdis/160.1.136. [DOI] [PubMed] [Google Scholar]
- Cantey J. R., Pinson A. G., Blake R. K. Mucosal and systemic immune response to O antigen after colonization and diarrhea due to a Peyer's patch-adherent Escherichia coli (strain RDEC-1). J Infect Dis. 1987 Dec;156(6):1022–1025. doi: 10.1093/infdis/156.6.1022. [DOI] [PubMed] [Google Scholar]
- Cantey J. R. Prevention of bacterial infections of mucosal surfaces by immune secretory IgA. Adv Exp Med Biol. 1978;107:461–470. doi: 10.1007/978-1-4684-3369-2_52. [DOI] [PubMed] [Google Scholar]
- Elson C. O., Ealding W., Lefkowitz J. A lavage technique allowing repeated measurement of IgA antibody in mouse intestinal secretions. J Immunol Methods. 1984 Feb 24;67(1):101–108. doi: 10.1016/0022-1759(84)90089-9. [DOI] [PubMed] [Google Scholar]
- Halstead T. E., Hall J. G. The homing of lymph-borne immunoblasts to the small gut of neonatal rats. Transplantation. 1972 Sep;14(3):339–346. doi: 10.1097/00007890-197209000-00009. [DOI] [PubMed] [Google Scholar]
- Hone D., Hackett J. Vaccination against enteric bacterial diseases. Rev Infect Dis. 1989 Nov-Dec;11(6):853–877. doi: 10.1093/clinids/11.6.853. [DOI] [PubMed] [Google Scholar]
- Husband A. J. Kinetics of extravasation and redistribution of IgA-specific antibody-containing cells in the intestine. J Immunol. 1982 Mar;128(3):1355–1359. [PubMed] [Google Scholar]
- Inman L. R., Cantey J. R. Peyer's patch lymphoid follicle epithelial adherence of a rabbit enteropathogenic Escherichia coli (strain RDEC-1). Role of plasmid-mediated pili in initial adherence. J Clin Invest. 1984 Jul;74(1):90–95. doi: 10.1172/JCI111423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inman L. R., Cantey J. R. Specific adherence of Escherichia coli (strain RDEC-1) to membranous (M) cells of the Peyer's patch in Escherichia coli diarrhea in the rabbit. J Clin Invest. 1983 Jan;71(1):1–8. doi: 10.1172/JCI110737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isaacson R. E. K99 surface antigen of Escherichia coli: purification and partial characterization. Infect Immun. 1977 Jan;15(1):272–279. doi: 10.1128/iai.15.1.272-279.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jerse A. E., Yu J., Tall B. D., Kaper J. B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7839–7843. doi: 10.1073/pnas.87.20.7839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ogra P. L., Karzon D. T. Distribution of poliovirus antibody in serum, nasopharynx and alimentary tract following segmental immunization of lower alimentary tract with poliovaccine. J Immunol. 1969 Jun;102(6):1423–1430. [PubMed] [Google Scholar]
- Parrott D. M., Ferguson A. Selective migration of lymphocytes within the mouse small intestine. Immunology. 1974 Mar;26(3):571–588. [PMC free article] [PubMed] [Google Scholar]
- Pierce N. F., Cray W. C., Jr Determinants of the localization, magnitude, and duration of a specific mucosal IgA plasma cell response in enterically immunized rats. J Immunol. 1982 Mar;128(3):1311–1315. [PubMed] [Google Scholar]
- Tacket C. O., Losonsky G., Link H., Hoang Y., Guesry P., Hilpert H., Levine M. M. Protection by milk immunoglobulin concentrate against oral challenge with enterotoxigenic Escherichia coli. N Engl J Med. 1988 May 12;318(19):1240–1243. doi: 10.1056/NEJM198805123181904. [DOI] [PubMed] [Google Scholar]
- Takeuchi A., Inman L. R., O'Hanley P. D., Cantey J. R., Lushbaugh W. B. Scanning and transmission electron microscopic study of Escherichia coli O15 (RDEC-1) enteric infection in rabbits. Infect Immun. 1978 Feb;19(2):686–694. doi: 10.1128/iai.19.2.686-694.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolf M. K., Andrews G. P., Fritz D. L., Sjogren R. W., Jr, Boedeker E. C. Characterization of the plasmid from Escherichia coli RDEC-1 that mediates expression of adhesin AF/R1 and evidence that AF/R1 pili promote but are not essential for enteropathogenic disease. Infect Immun. 1988 Aug;56(8):1846–1857. doi: 10.1128/iai.56.8.1846-1857.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolf M. K., Boedeker E. C. Cloning of the genes for AF/R1 pili from rabbit enteroadherent Escherichia coli RDEC-1 and DNA sequence of the major structural subunit. Infect Immun. 1990 Apr;58(4):1124–1128. doi: 10.1128/iai.58.4.1124-1128.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]