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The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1992 Apr 1;175(4):933–937. doi: 10.1084/jem.175.4.933

Resistance to collagen-induced arthritis in a nonhuman primate species maps to the major histocompatibility complex class I region

PMCID: PMC2119185  PMID: 1552289

Abstract

Type II collagen-induced arthritis (CIA) is an experimentally inducible autoimmune disorder that is, just like several forms of human arthritis, influenced by a genetic background. Immunization of young rhesus monkeys (Macaca mulatta) with type II collagen (CII) induced CIA in about 70% of the animals. One major histocompatibility complex (MHC) class I allele was present only in young animals resistant to CIA and absent in arthritic animals. This strong association suggests that the MHC class I allele itself, or a closely linked gene, determines resistance to CIA. The mechanism controlling the resistance to CIA becomes less efficient in aged animals since older rhesus monkeys, which were positive for the resistance marker, developed a mild form of arthritis. At the cellular level it is demonstrated that resistance to CIA is reflected by a low responsiveness of T cells to CII. This association between a specified MHC class I allele and resistance to an autoimmune disease points at the importance of the MHC class I region in the regulation of the immune response to an autoantigen.

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Selected References

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  1. Bakker N. P., van Erck M. G., Botman C. A., Jonker M., 't Hart B. A. Collagen-induced arthritis in an outbred group of rhesus monkeys comprising responder and nonresponder animals. Relationship between the course of arthritis and collagen-specific immunity. Arthritis Rheum. 1991 May;34(5):616–624. doi: 10.1002/art.1780340514. [DOI] [PubMed] [Google Scholar]
  2. Bakker N. P., van Erck M. G., Zurcher C., Faaber P., Lemmens A., Hazenberg M., Bontrop R. E., Jonker M. Experimental immune mediated arthritis in rhesus monkeys. A model for human rheumatoid arthritis? Rheumatol Int. 1990;10(1):21–29. doi: 10.1007/BF02274777. [DOI] [PubMed] [Google Scholar]
  3. Banerji J., Sands J., Strominger J. L., Spies T. A gene pair from the human major histocompatibility complex encodes large proline-rich proteins with multiple repeated motifs and a single ubiquitin-like domain. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2374–2378. doi: 10.1073/pnas.87.6.2374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buus S., Sette A., Colon S. M., Miles C., Grey H. M. The relation between major histocompatibility complex (MHC) restriction and the capacity of Ia to bind immunogenic peptides. Science. 1987 Mar 13;235(4794):1353–1358. doi: 10.1126/science.2435001. [DOI] [PubMed] [Google Scholar]
  5. Caffrey M. F., James D. C. Human lymphocyte antigen association in ankylosing spondylitis. Nature. 1973 Mar 9;242(5393):121–121. doi: 10.1038/242121a0. [DOI] [PubMed] [Google Scholar]
  6. Ciccone E., Colonna M., Viale O., Pende D., Di Donato C., Reinharz D., Amoroso A., Jeannet M., Guardiola J., Moretta A. Susceptibility or resistance to lysis by alloreactive natural killer cells is governed by a gene in the human major histocompatibility complex between BF and HLA-B. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9794–9797. doi: 10.1073/pnas.87.24.9794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gregersen P. K., Silver J., Winchester R. J. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987 Nov;30(11):1205–1213. doi: 10.1002/art.1780301102. [DOI] [PubMed] [Google Scholar]
  8. Hammer R. E., Maika S. D., Richardson J. A., Tang J. P., Taurog J. D. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell. 1990 Nov 30;63(5):1099–1112. doi: 10.1016/0092-8674(90)90512-d. [DOI] [PubMed] [Google Scholar]
  9. Harley J. B., Reichlin M., Arnett F. C., Alexander E. L., Bias W. B., Provost T. T. Gene interaction at HLA-DQ enhances autoantibody production in primary Sjögren's syndrome. Science. 1986 May 30;232(4754):1145–1147. doi: 10.1126/science.3458307. [DOI] [PubMed] [Google Scholar]
  10. Hill A. V., Allsopp C. E., Kwiatkowski D., Anstey N. M., Twumasi P., Rowe P. A., Bennett S., Brewster D., McMichael A. J., Greenwood B. M. Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991 Aug 15;352(6336):595–600. doi: 10.1038/352595a0. [DOI] [PubMed] [Google Scholar]
  11. Holmdahl R., Andersson M., Goldschmidt T. J., Gustafsson K., Jansson L., Mo J. A. Type II collagen autoimmunity in animals and provocations leading to arthritis. Immunol Rev. 1990 Dec;118:193–232. doi: 10.1111/j.1600-065x.1990.tb00817.x. [DOI] [PubMed] [Google Scholar]
  12. Holmdahl R., Karlsson M., Andersson M. E., Rask L., Andersson L. Localization of a critical restriction site on the I-A beta chain that determines susceptibility to collagen-induced arthritis in mice. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9475–9479. doi: 10.1073/pnas.86.23.9475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Klein J., Bontrop R. E., Dawkins R. L., Erlich H. A., Gyllensten U. B., Heise E. R., Jones P. P., Parham P., Wakeland E. K., Watkins D. I. Nomenclature for the major histocompatibility complexes of different species: a proposal. Immunogenetics. 1990;31(4):217–219. doi: 10.1007/BF00204890. [DOI] [PubMed] [Google Scholar]
  14. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature. 1985 Apr 11;314(6011):537–539. doi: 10.1038/314537a0. [DOI] [PubMed] [Google Scholar]
  15. Lawlor D. A., Warren E., Ward F. E., Parham P. Comparison of class I MHC alleles in humans and apes. Immunol Rev. 1990 Feb;113:147–185. doi: 10.1111/j.1600-065x.1990.tb00040.x. [DOI] [PubMed] [Google Scholar]
  16. Mayer W. E., Jonker M., Klein D., Ivanyi P., van Seventer G., Klein J. Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J. 1988 Sep;7(9):2765–2774. doi: 10.1002/j.1460-2075.1988.tb03131.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moore M. W., Carbone F. R., Bevan M. J. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell. 1988 Sep 9;54(6):777–785. doi: 10.1016/s0092-8674(88)91043-4. [DOI] [PubMed] [Google Scholar]
  18. Sargent C. A., Dunham I., Trowsdale J., Campbell R. D. Human major histocompatibility complex contains genes for the major heat shock protein HSP70. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1968–1972. doi: 10.1073/pnas.86.6.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schlosstein L., Terasaki P. I., Bluestone R., Pearson C. M. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med. 1973 Apr 5;288(14):704–706. doi: 10.1056/NEJM197304052881403. [DOI] [PubMed] [Google Scholar]
  20. Schreuder G. M., Tilanus M. G., Bontrop R. E., Bruining G. J., Giphart M. J., van Rood J. J., de Vries R. R. HLA-DO polymorphism associated with resistance to type I diabetes detected with monoclonal antibodies, isoelectric point differences, and restriction fragment length polymorphism. J Exp Med. 1986 Sep 1;164(3):938–943. doi: 10.1084/jem.164.3.938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sollid L. M., Markussen G., Ek J., Gjerde H., Vartdal F., Thorsby E. Evidence for a primary association of celiac disease to a particular HLA-DQ alpha/beta heterodimer. J Exp Med. 1989 Jan 1;169(1):345–350. doi: 10.1084/jem.169.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Spies T., Bresnahan M., Strominger J. L. Human major histocompatibility complex contains a minimum of 19 genes between the complement cluster and HLA-B. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8955–8958. doi: 10.1073/pnas.86.22.8955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Todd J. A., Bell J. I., McDevitt H. O. HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature. 1987 Oct 15;329(6140):599–604. doi: 10.1038/329599a0. [DOI] [PubMed] [Google Scholar]
  24. Townsend A. R., Rothbard J., Gotch F. M., Bahadur G., Wraith D., McMichael A. J. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell. 1986 Mar 28;44(6):959–968. doi: 10.1016/0092-8674(86)90019-x. [DOI] [PubMed] [Google Scholar]
  25. de Vries R. R., Meera Khan P., Bernini L. F., van Loghem E., van Rood J. J. Genetic control of survival in epidemics. J Immunogenet. 1979 Aug;6(4):271–287. doi: 10.1111/j.1744-313x.1979.tb00684.x. [DOI] [PubMed] [Google Scholar]
  26. van Vreeswijk W., Roger J. H., D'Amaro J., Balner H. The major histocompatibility complex of rhesus monkeys, RhL--A. VII. Identification of five new serologically defined antigens. Tissue Antigens. 1977 Jan;9(1):17–30. doi: 10.1111/j.1399-0039.1977.tb01075.x. [DOI] [PubMed] [Google Scholar]

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