Skip to main content
NCBI home page
Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1994 Aug;97(2):204–211. doi: 10.1111/j.1365-2249.1994.tb06069.x

Accelerated onset of collagen-induced arthritis by remote inflammation.

L A Joosten 1, M M Helsen 1, W B van den Berg 1
PMCID: PMC1534682  PMID: 8050168

Abstract

Collagen-induced arthritis (CIA) in DBA-1 lac/J mice often has a low incidence, with gradual disease expression occurring over a broad time span (between days 35 and 70). The exact mechanisms underlying spontaneous expression are still poorly understood, although it is evident that some inflammatory cytokines like IL-1, tumour necrosis factor-alpha (TNF-alpha) and transforming growth factor-beta (TGF-beta) are potent accelerators. We have investigated whether we could trigger collagen type II-driven inflammation by: (i) enhancing anti-collagen type II (CII) antibodies, or (ii) a non-related inflammatory process. Male DBA-1 lac/J mice were immunized with 100 micrograms bovine type II collagen in Freund's complete adjuvant (FCA), resulting in a low disease expression at day 28. Addition of anti-CII antibodies slightly enhanced the expression of CIA. Zymosan (3 mg), given intraperitoneally, induced consistent expression of CIA after 1 week, whereas a retarded onset was noted with higher dosages. Local injection of a low dose of Zymosan (60 micrograms) in the knee joint, clearly potentiated the expression of CIA at that particular site. Higher concentrations not only elicited prolonged CIA expression at the injection site, but also induced marked CIA in the draining ankle joint. In contrast, intra-articular injection of Zymosan in nonimmunized DBAs or methylated bovine serum albumin (mBSA)/FCA-immunized controls only induced transient joint inflammation. The nature of the highly erosive CIA was confirmed histologically, and could easily be discriminated from the reversible changes induced with Zymosan. Our data indicate that latent autoimmune reactions may come to expression at the moment of non-specific inflammation, even at a remote site.

Full text

PDF
204

Images in this article

206Fig. 2
on p.206

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brahn E., Trentham D. E. Experimental synovitis induced by collagen-specific T cell lines. Cell Immunol. 1989 Feb;118(2):491–503. doi: 10.1016/0008-8749(89)90396-1. [DOI] [PubMed] [Google Scholar]
  2. Cooper W. O., Fava R. A., Gates C. A., Cremer M. A., Townes A. S. Acceleration of onset of collagen-induced arthritis by intra-articular injection of tumour necrosis factor or transforming growth factor-beta. Clin Exp Immunol. 1992 Aug;89(2):244–250. doi: 10.1111/j.1365-2249.1992.tb06939.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Echtenacher B., Falk W., Männel D. N., Krammer P. H. Requirement of endogenous tumor necrosis factor/cachectin for recovery from experimental peritonitis. J Immunol. 1990 Dec 1;145(11):3762–3766. [PubMed] [Google Scholar]
  5. Hansson I., Holmdahl R., Mattsson R. Constant darkness enhances autoimmunity to type II collagen and exaggerates development of collagen-induced arthritis in DBA/1 mice. J Neuroimmunol. 1990 Apr;27(1):79–84. doi: 10.1016/0165-5728(90)90139-e. [DOI] [PubMed] [Google Scholar]
  6. Hansson I., Holmdahl R., Mattsson R. The pineal hormone melatonin exaggerates development of collagen-induced arthritis in mice. J Neuroimmunol. 1992 Jul;39(1-2):23–30. doi: 10.1016/0165-5728(92)90171-g. [DOI] [PubMed] [Google Scholar]
  7. Hart B. A., Bakker N. P., Jonker M., Bontrop R. E. Resistance to collagen-induced arthritis in rats and rhesus monkeys after immunization with attenuated type II collagen. Eur J Immunol. 1993 Jul;23(7):1588–1594. doi: 10.1002/eji.1830230729. [DOI] [PubMed] [Google Scholar]
  8. Holmdahl R., Jansson L., Larsson A., Jonsson R. Arthritis in DBA/1 mice induced with passively transferred type II collagen immune serum. Immunohistopathology and serum levels of anti-type II collagen auto-antibodies. Scand J Immunol. 1990 Feb;31(2):147–157. doi: 10.1111/j.1365-3083.1990.tb02754.x. [DOI] [PubMed] [Google Scholar]
  9. Hom J. T., Bendele A. M., Carlson D. G. In vivo administration with IL-1 accelerates the development of collagen-induced arthritis in mice. J Immunol. 1988 Aug 1;141(3):834–841. [PubMed] [Google Scholar]
  10. Jacobs M. J., van den Hoek A. E., van de Putte L. B., van den Berg W. B. Aberrant tolerance induction with cationic antigens. Scand J Immunol. 1993 Jan;37(1):97–103. doi: 10.1111/j.1365-3083.1993.tb01670.x. [DOI] [PubMed] [Google Scholar]
  11. Johns L. D., Flanders K. C., Ranges G. E., Sriram S. Successful treatment of experimental allergic encephalomyelitis with transforming growth factor-beta 1. J Immunol. 1991 Sep 15;147(6):1792–1796. [PubMed] [Google Scholar]
  12. Killar L. M., Dunn C. J. Interleukin-1 potentiates the development of collagen-induced arthritis in mice. Clin Sci (Lond) 1989 May;76(5):535–538. doi: 10.1042/cs0760535. [DOI] [PubMed] [Google Scholar]
  13. Louis R., Bury T., Corhay J. L., Radermecker M. F. Potentiation of histamine release from human leucocytes by PAF. Agents Actions. 1994 Mar;41(1-2):5–10. doi: 10.1007/BF01986385. [DOI] [PubMed] [Google Scholar]
  14. Santambrogio L., Hochwald G. M., Leu C. H., Thorbecke G. J. Antagonistic effects of endogenous and exogenous TGF-beta and TNF on auto-immune diseases in mice. Immunopharmacol Immunotoxicol. 1993 Aug;15(4):461–478. doi: 10.3109/08923979309035240. [DOI] [PubMed] [Google Scholar]
  15. Staite N. D., Richard K. A., Aspar D. G., Franz K. A., Galinet L. A., Dunn C. J. Induction of an acute erosive monarticular arthritis in mice by interleukin-1 and methylated bovine serum albumin. Arthritis Rheum. 1990 Feb;33(2):253–260. doi: 10.1002/art.1780330215. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Thorbecke G. J., Shah R., Leu C. H., Kuruvilla A. P., Hardison A. M., Palladino M. A. Involvement of endogenous tumor necrosis factor alpha and transforming growth factor beta during induction of collagen type II arthritis in mice. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7375–7379. doi: 10.1073/pnas.89.16.7375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. van Beuningen H. M., van der Kraan P. M., Arntz O. J., van den Berg W. B. Protection from interleukin 1 induced destruction of articular cartilage by transforming growth factor beta: studies in anatomically intact cartilage in vitro and in vivo. Ann Rheum Dis. 1993 Mar;52(3):185–191. doi: 10.1136/ard.52.3.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. van den Berg W. B., Joosten L. A., Helsen M., van de Loo F. A. Amelioration of established murine collagen-induced arthritis with anti-IL-1 treatment. Clin Exp Immunol. 1994 Feb;95(2):237–243. doi: 10.1111/j.1365-2249.1994.tb06517.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. van den Berg W. B., Kruijsen M. W., van de Putte L. B., van Beusekom H. J., van der Sluis-van der Pol M., Zwarts W. A. Antigen-induced and zymosan-induced arthritis in mice: studies on in vivo cartilage proteoglycan synthesis and chondrocyte death. Br J Exp Pathol. 1981 Jun;62(3):308–316. [PMC free article] [PubMed] [Google Scholar]
  23. van den Berg W. B., van de Putte L. B., Zwarts W. A., Joosten L. A. Electrical charge of the antigen determines intraarticular antigen handling and chronicity of arthritis in mice. J Clin Invest. 1984 Nov;74(5):1850–1859. doi: 10.1172/JCI111604. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Clinical and Experimental Immunology are provided here courtesy of British Society for Immunology

RESOURCES