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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Oct;83(19):7443–7446. doi: 10.1073/pnas.83.19.7443

Suppression of type II collagen-induced arthritis by intragastric administration of soluble type II collagen.

C Nagler-Anderson, L A Bober, M E Robinson, G W Siskind, G J Thorbecke
PMCID: PMC386734  PMID: 3463976

Abstract

Although oral administration of protein antigens may lead to specific immunologic unresponsiveness, this method of immunoregulation has not been applied to models of autoimmune disease. Type II collagen-induced arthritis is an animal model of polyarthritis induced in susceptible mice and rats by immunization with type II collagen, a major component of cartilage. Intragastric administration of soluble type II collagen, prior to immunization with type II collagen in adjuvant, suppresses the incidence of collagen-induced arthritis. Administration of denatured type II collagen has no observable effect on the incidence or severity of the disease. The overall magnitude of the antibody response is not significantly reduced in collagen-fed mice as compared to controls. While the isotype distribution of the anti-collagen antibodies is similar in the two groups, there is a tendency toward reduced IgG2 responses in the collagen-fed mice.

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Selected References

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  1. Bhogal B. S., Karkhanis Y. D., Bell M. K., Sanchez P., Zemcik B., Siskind G. W., Thorbecke G. J. Production of auto-anti-idiotypic antibody during the normal immune response. XII. Enhanced auto-anti-idiotypic antibody production as a mechanism for apparent B-cell tolerance in rabbits after feeding antigen. Cell Immunol. 1986 Aug;101(1):93–104. doi: 10.1016/0008-8749(86)90189-9. [DOI] [PubMed] [Google Scholar]
  2. Brahn E., Trentham D. E. Antigen-specific suppression of collagen arthritis by adoptive transfer of spleen cells. Clin Immunol Immunopathol. 1984 Apr;31(1):124–131. doi: 10.1016/0090-1229(84)90197-1. [DOI] [PubMed] [Google Scholar]
  3. Challacombe S. J., Tomasi T. B., Jr Systemic tolerance and secretory immunity after oral immunization. J Exp Med. 1980 Dec 1;152(6):1459–1472. doi: 10.1084/jem.152.6.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Courtenay J. S., Dallman M. J., Dayan A. D., Martin A., Mosedale B. Immunisation against heterologous type II collagen induces arthritis in mice. Nature. 1980 Feb 14;283(5748):666–668. doi: 10.1038/283666a0. [DOI] [PubMed] [Google Scholar]
  5. Cremer M. A., Hernandez A. D., Townes A. S., Stuart J. M., Kang A. H. Collagen-induced arthritis in rats: antigen-specific suppression of arthritis and immunity by intravenously injected native type II collagen. J Immunol. 1983 Dec;131(6):2995–3000. [PubMed] [Google Scholar]
  6. Dallman M., Fathman C. G. Type II collagen-reactive T cell clones from mice with collagen-induced arthritis. J Immunol. 1985 Aug;135(2):1113–1118. [PubMed] [Google Scholar]
  7. Engvall E., Perlmann P. Enzyme-linked immunosorbent assay, Elisa. 3. Quantitation of specific antibodies by enzyme-labeled anti-immunoglobulin in antigen-coated tubes. J Immunol. 1972 Jul;109(1):129–135. [PubMed] [Google Scholar]
  8. Gautam S. C., Battisto J. R. Orally induced tolerance generates an efferently acting suppressor T cell and an acceptor T cell that together down-regulate contact sensitivity. J Immunol. 1985 Nov;135(5):2975–2983. [PubMed] [Google Scholar]
  9. Hahn E., Nowack H., GOTZE D., Timpl R. H-2-linked genetic control of antibody response to soluble calf skin collagen in mice. Eur J Immunol. 1975 Apr;5(4):288–291. doi: 10.1002/eji.1830050415. [DOI] [PubMed] [Google Scholar]
  10. Jackson S., Mestecky J. Oral-parenteral immunization leads to the appearance of IgG auto-anti-idiotypic cells in mucosal tissues. Cell Immunol. 1981 May 15;60(2):498–502. doi: 10.1016/0008-8749(81)90290-2. [DOI] [PubMed] [Google Scholar]
  11. Kerwar S. S., Englert M. E., McReynolds R. A., Landes M. J., Lloyd J. M., Oronsky A. L., Wilson F. J. Type II collagen-induced arthritis. Studies with purified anticollagen immunoglobulin. Arthritis Rheum. 1983 Sep;26(9):1120–1131. doi: 10.1002/art.1780260910. [DOI] [PubMed] [Google Scholar]
  12. Klinman N. R., Pickard A. R., Sigal N. H., Gearhart P. J., Metcalf E. S., Pierce S. K. Assessing B cell diversification by antigen receptor and precursor cell analysis. Ann Immunol (Paris) 1976 Jun-Jul;127(3-4):489–502. [PubMed] [Google Scholar]
  13. Kresina T. F., Moskowitz R. W. Adoptive transfer of suppression of arthritis in the mouse model of collagen-induced arthritis. Evidence for a type II collagen-specific suppressor T cell. J Clin Invest. 1985 Jun;75(6):1990–1998. doi: 10.1172/JCI111917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lafont S., André C., André F., Gillon J., Fargier M. C. Abrogation by subsequent feeding of antibody response including IgE, in parenterally immunized mice. J Exp Med. 1982 May 1;155(5):1573–1578. doi: 10.1084/jem.155.5.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Miller E. J., Rhodes R. K. Preparation and characterization of the different types of collagen. Methods Enzymol. 1982;82(Pt A):33–64. doi: 10.1016/0076-6879(82)82059-4. [DOI] [PubMed] [Google Scholar]
  17. Miller S. D., Hanson D. G. Inhibition of specific immune responses by feeding protein antigens. IV. Evidence for tolerance and specific active suppression of cell-mediated immune responses to ovalbumin. J Immunol. 1979 Nov;123(5):2344–2350. [PubMed] [Google Scholar]
  18. NUSSENZWEIG R. S., MERRYMAN C., BENACERRAF B. ELECTROPHORETIC SEPARATION AND PROPERTIES OF MOUSE ANTIHAPTEN ANTIBODIES INVOLVED IN PASSIVE CUTANEOUS ANAPHYLAXIS AND PASSIVE HEMOLYSIS. J Exp Med. 1964 Aug 1;120:315–328. doi: 10.1084/jem.120.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Nowack H., Hahn E., Timpl R. Specificity of the antibody response in inbred mice to bovine type I and type II collagen. Immunology. 1975 Oct;29(4):621–628. [PMC free article] [PubMed] [Google Scholar]
  21. Phadke K., Fouts R., Parrish J. E. Collagen-induced and adjuvant-induced arthritis in rats. Post-immunization treatment with collagen to suppress or abrogate the arthritic response. Arthritis Rheum. 1984 Jul;27(7):797–806. doi: 10.1002/art.1780270711. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Richman L. K., Graeff A. S., Yarchoan R., Strober W. Simultaneous induction of antigen-specific IgA helper T cells and IgG suppressor T cells in the murine Peyer's patch after protein feeding. J Immunol. 1981 Jun;126(6):2079–2083. [PubMed] [Google Scholar]
  24. Schoen R. T., Greene M. I., Trentham D. E. Antigen-specific suppression of type II collagen-induced arthritis by collagen-coupled spleen cells. J Immunol. 1982 Feb;128(2):717–719. [PubMed] [Google Scholar]
  25. Solinger A. M., Bhatnagar R., Stobo J. D. Cellular, molecular, and genetic characteristics of T cell reactivity to collagen in man. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3877–3881. doi: 10.1073/pnas.78.6.3877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stuart J. M., Dixon F. J. Serum transfer of collagen-induced arthritis in mice. J Exp Med. 1983 Aug 1;158(2):378–392. doi: 10.1084/jem.158.2.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stuart J. M., Tomoda K., Yoo T. J., Townes A. S., Kang A. H. Serum transfer of collagen-induced arthritis. II. Identification and localization of autoantibody to type II collagen in donor and recipient rats. Arthritis Rheum. 1983 Oct;26(10):1237–1244. doi: 10.1002/art.1780261011. [DOI] [PubMed] [Google Scholar]
  28. Stuart J. M., Townes A. S., Kang A. H. Nature and specificity of the immune response to collagen in type II collagen-induced arthritis in mice. J Clin Invest. 1982 Mar;69(3):673–683. doi: 10.1172/JCI110495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Terato K., Hasty K. A., Cremer M. A., Stuart J. M., Townes A. S., Kang A. H. Collagen-induced arthritis in mice. Localization of an arthritogenic determinant to a fragment of the type II collagen molecule. J Exp Med. 1985 Aug 1;162(2):637–646. doi: 10.1084/jem.162.2.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thomas H. C., Parrott M. V. The induction of tolerance to a soluble protein antigen by oral administration. Immunology. 1974 Oct;27(4):631–639. [PMC free article] [PubMed] [Google Scholar]
  32. Titus R. G., Chiller J. M. Orally induced tolerance. Definition at the cellular level. Int Arch Allergy Appl Immunol. 1981;65(3):323–338. [PubMed] [Google Scholar]
  33. Tomasi T. B., Jr Oral tolerance. Transplantation. 1980 May;29(5):353–356. doi: 10.1097/00007890-198005000-00001. [DOI] [PubMed] [Google Scholar]
  34. Trentham D. E., Townes A. S., Kang A. H. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med. 1977 Sep 1;146(3):857–868. doi: 10.1084/jem.146.3.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Watson W. C., Townes A. S. Genetic susceptibility to murine collagen II autoimmune arthritis. Proposed relationship to the IgG2 autoantibody subclass response, complement C5, major histocompatibility complex (MHC) and non-MHC loci. J Exp Med. 1985 Dec 1;162(6):1878–1891. doi: 10.1084/jem.162.6.1878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wood F. D., Pearson C. M., Tanaka A. Capacity of mycobacterial wax D and its subfractions to induce adjuvant arthritis in rats. Int Arch Allergy Appl Immunol. 1969;35(5):456–467. doi: 10.1159/000230198. [DOI] [PubMed] [Google Scholar]
  37. Wooley P. H., Luthra H. S., Krco C. J., Stuart J. M., David C. S. Type II collagen-induced arthritis in mice. II. Passive transfer and suppression by intravenous injection of anti-type II collagen antibody or free native type II collagen. Arthritis Rheum. 1984 Sep;27(9):1010–1017. doi: 10.1002/art.1780270907. [DOI] [PubMed] [Google Scholar]
  38. Wooley P. H., Luthra H. S., Stuart J. M., David C. S. Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med. 1981 Sep 1;154(3):688–700. doi: 10.1084/jem.154.3.688. [DOI] [PMC free article] [PubMed] [Google Scholar]

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