Abstract
Diminished systemic immune reaction after ingestion of antigen has been reported in several animal models. Conversely, it has been reported recently that oral immunization may lead to the production of secretory antibodies. To determine whether these events could occur concurrently, CBA/J mice were immunized intragastrically with varying doses of ovalbumin (OVA) and Streptococcus mutans. After 7 d, the animals were challenged systemically with antigen in complete adjuvant and 8 d later serum and saliva taken, and the draining lymph nodes assayed for a proliferative response. Intragastric doses of 1 mg OVA or 10(9) S. mutans led to significant suppression of the proliferative response, and intragastric doses of 10 mg OVA or 2.5 X 10(9) S. mutans led to the production of detectable salivary antibodies using hemagglutination. Serum antibodies were not detected after intragastric administration of OVA or S. mutans. Suppression of the proliferative response could be detected from 2-60 d after intragastric administration of OVA, and 2-21 d after S. mutans. Prior intragastric immunization with heterologous antigens did not suppress the response to OVA or S. mutans. Transfer of 40 X 10(6) mesenteric lymph node cells from mice given 20 mg OVA or 10(9) S. mutans led to suppression of the proliferative response in syngeneic recipients. Salivary antibodies wer removed by absorption with anti-IgA, but not anti-IgG or IgM, indicating that they were of the IgA class. It appears that intragastric administration of soluble or particulate antigens in mice may lead to the concurrent induction of salivary antibodies and systemic suppression.
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Selected References
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- Alkan S. S. Antigen-induced proliferation assay for mouse T lymphocytes. Response to a monovalent antigen. Eur J Immunol. 1978 Feb;8(2):112–118. doi: 10.1002/eji.1830080208. [DOI] [PubMed] [Google Scholar]
- André C., Heremans J. F., Vaerman J. P., Cambiaso C. L. A mechanism for the induction of immunological tolerance by antigen feeding: antigen-antibody complexes. J Exp Med. 1975 Dec 1;142(6):1509–1519. doi: 10.1084/jem.142.6.1509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Asherson G. L., Zembala M., Perera M. A., Mayhew B., Thomas W. R. Production of immunity and unresponsiveness in the mouse by feeding contact sensitizing agents and the role of suppressor cells in the peyer's patches, mesenteric lymph nodes and other lymphoid tissues. Cell Immunol. 1977 Sep;33(1):145–155. doi: 10.1016/0008-8749(77)90142-3. [DOI] [PubMed] [Google Scholar]
- Basten A., Miller J. F., Johnson P. T cell-dependent suppression of an anti-hapten antibody response. Transplant Rev. 1975;26:130–169. doi: 10.1111/j.1600-065x.1975.tb00178.x. [DOI] [PubMed] [Google Scholar]
- Bockman D. E., Cooper M. D. Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer's patches. An electron microscopic study. Am J Anat. 1973 Apr;136(4):455–477. doi: 10.1002/aja.1001360406. [DOI] [PubMed] [Google Scholar]
- Challacombe S. J., Lehner T. Salivary antibody responses in rhesus monkeys immunized with Streptococcus mutans by the oral, submucosal or subcutaneous routes. Arch Oral Biol. 1979;24(12):917–925. doi: 10.1016/0003-9969(79)90217-6. [DOI] [PubMed] [Google Scholar]
- Craig S. W., Cebra J. J. Peyer's patches: an enriched source of precursors for IgA-producing immunocytes in the rabbit. J Exp Med. 1971 Jul 1;134(1):188–200. doi: 10.1084/jem.134.1.188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elson C. J., Taylor R. B. The suppressive effect of carrier priming on the response to a hapten-carrier conjugate. Eur J Immunol. 1974 Oct;4(10):682–687. doi: 10.1002/eji.1830041009. [DOI] [PubMed] [Google Scholar]
- Elson C. O., Heck J. A., Strober W. T-cell regulation of murine IgA synthesis. J Exp Med. 1979 Mar 1;149(3):632–643. doi: 10.1084/jem.149.3.632. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guy-Grand D., Griscelli C., Vassalli P. The gut-associated lymphoid system: nature and properties of the large dividing cells. Eur J Immunol. 1974 Jun;4(6):435–443. doi: 10.1002/eji.1830040610. [DOI] [PubMed] [Google Scholar]
- Husband A. J., Gowans J. L. The origin and antigen-dependent distribution of IgA-containing cells in the intestine. J Exp Med. 1978 Nov 1;148(5):1146–1160. doi: 10.1084/jem.148.5.1146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishizaka K., Adachi T. Generation of specific helper cells and suppressor cells in vitro for the IgE and IgG antibody responses. J Immunol. 1976 Jul;117(1):40–47. [PubMed] [Google Scholar]
- Joel D. D., Laissue J. A., LeFevre M. E. Distribution and fate of ingested carbon particles in mice. J Reticuloendothel Soc. 1978 Nov;24(5):477–487. [PubMed] [Google Scholar]
- Julius M. H., Simpson E., Herzenberg L. A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. doi: 10.1002/eji.1830031011. [DOI] [PubMed] [Google Scholar]
- Kagnoff M. F. Effects of antigen-feeding on intestinal and systemic immune responses. III. Antigen-specific serum-mediated suppression of humoral antibody responses after antigen feeding. Cell Immunol. 1978 Sep 15;40(1):186–203. doi: 10.1016/0008-8749(78)90326-x. [DOI] [PubMed] [Google Scholar]
- Lowney E. D. Immunologic unresponsiveness to a contact sensitizer in man. J Invest Dermatol. 1968 Dec;51(6):411–417. [PubMed] [Google Scholar]
- Mattingly J. A., Waksman B. H. Immunologic suppression after oral administration of antigen. I. Specific suppressor cells formed in rat Peyer's patches after oral administration of sheep erythrocytes and their systemic migration. J Immunol. 1978 Nov;121(5):1878–1883. [PubMed] [Google Scholar]
- Mestecky J., McGhee J. R., Arnold R. R., Michalek S. M., Prince S. J., Babb J. L. Selective induction of an immune response in human external secretions by ingestion of bacterial antigen. J Clin Invest. 1978 Mar;61(3):731–737. doi: 10.1172/JCI108986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michalek S. M., McGhee J. R., Babb J. L. Effective immunity to dental caries: dose-dependent studies of secretory immunity by oral administration of Streptococcus mutans to rats. Infect Immun. 1978 Jan;19(1):217–224. doi: 10.1128/iai.19.1.217-224.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moorhead J. W. Tolerance and contact sensitivity to DNFB in mice. VI. Inhibition of afferent sensitivity by suppressor T cells in adoptive tolerance. J Immunol. 1976 Sep;117(3):802–806. [PubMed] [Google Scholar]
- Muirhead D. Y., Cudkowicz G. Subpopulations of splenic T cells regulating an anti-hapten antibody response. II. Distinct functions of, and sequential requirement for, helper and amplifier cells. J Immunol. 1978 Jul;121(1):130–137. [PubMed] [Google Scholar]
- Ngan J., Kind L. S. Suppressor T cells for IgE and IgG in Peyer's patches of mice made tolerant by the oral administration of ovalbumin. J Immunol. 1978 Mar;120(3):861–865. [PubMed] [Google Scholar]
- Parks D. E., Shaller D. A., Weigle W. O. Induction and mode of action of suppressor cells generated against human gamma globulin. II. Effects of colchicine. J Exp Med. 1979 May 1;149(5):1168–1182. doi: 10.1084/jem.149.5.1168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pierce N. F., Koster F. T. Priming and suppression of the intestinal immune response to cholera toxoid/toxin by parenteral toxoid in rats. J Immunol. 1980 Jan;124(1):307–311. [PubMed] [Google Scholar]
- Richman L. K., Chiller J. M., Brown W. R., Hanson D. G., Vaz N. M. Enterically induced immunologic tolerance. I. Induction of suppressor T lymphoyctes by intragastric administration of soluble proteins. J Immunol. 1978 Dec;121(6):2429–2434. [PubMed] [Google Scholar]
- Sewell H. F., Gell P. G., Basu M. K. Immune responsiveness and oral immunization. Int Arch Allergy Appl Immunol. 1979;58(4):414–425. doi: 10.1159/000232221. [DOI] [PubMed] [Google Scholar]
- Swarbrick E. T., Stokes C. R., Soothill J. F. Absorption of antigens after oral immunisation and the simultaneous induction of specific systemic tolerance. Gut. 1979 Feb;20(2):121–125. doi: 10.1136/gut.20.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tomasi T. B., Jr Oral tolerance. Transplantation. 1980 May;29(5):353–356. doi: 10.1097/00007890-198005000-00001. [DOI] [PubMed] [Google Scholar]
- Vaz N. M., Maia L. C., Hanson D. G., Lynch J. M. Inhibition of homocytotropic antibody responses in adult inbred mice by previous feeding of the specific antigen. J Allergy Clin Immunol. 1977 Aug;60(2):110–115. doi: 10.1016/0091-6749(77)90035-5. [DOI] [PubMed] [Google Scholar]
- Walker W. A., Isselbacher K. J. Intestinal antibodies. N Engl J Med. 1977 Oct 6;297(14):767–773. doi: 10.1056/NEJM197710062971407. [DOI] [PubMed] [Google Scholar]