Abstract
Adjuvant-induced arthritis (AIA) is one of many animal models of rheumatoid arthritis, a disease characterized by a T-lymphocyte and macrophage cellular infiltrate. We have characterized the development of this disease model with respect to chemokine expression. Increased levels of two chemokines, RANTES, a T-lymphocyte and monocyte chemo-attractant, and KC a chemoattractant for neutrophils, were found in whole blood and in the joint. Surprisingly, levels of MIP-1alpha, another T-lymphocyte and monocyte chemoattractant, were unchanged throughout the course of the disease in whole blood and only slightly elevated in the joint. RANTES expression plays an important role in the disease since a polyclonal antibody to RANTES greatly ameliorated symptoms in animals induced for AIA and was found to be as efficacious as treatment with indomethacin, a non-steroidal anti inflammatory. Polyclonal antibodies to either MIP-1alpha or KC were ineffective. This is the first report to show the importance of RANTES in the development of AIA.
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- Ackerman N. R., Rooks W. H., 2nd, Shott L., Genant H., Maloney P., West E. Effects of naproxen on connective tissue changes in the adjuvant arthritic rat. Arthritis Rheum. 1979 Dec;22(12):1365–1374. doi: 10.1002/art.1780221208. [DOI] [PubMed] [Google Scholar]
- Bacon K. B., Premack B. A., Gardner P., Schall T. J. Activation of dual T cell signaling pathways by the chemokine RANTES. Science. 1995 Sep 22;269(5231):1727–1730. doi: 10.1126/science.7569902. [DOI] [PubMed] [Google Scholar]
- Brown K. D., Zurawski S. M., Mosmann T. R., Zurawski G. A family of small inducible proteins secreted by leukocytes are members of a new superfamily that includes leukocyte and fibroblast-derived inflammatory agents, growth factors, and indicators of various activation processes. J Immunol. 1989 Jan 15;142(2):679–687. [PubMed] [Google Scholar]
- Cook D. N., Beck M. A., Coffman T. M., Kirby S. L., Sheridan J. F., Pragnell I. B., Smithies O. Requirement of MIP-1 alpha for an inflammatory response to viral infection. Science. 1995 Sep 15;269(5230):1583–1585. doi: 10.1126/science.7667639. [DOI] [PubMed] [Google Scholar]
- Darbonne W. C., Rice G. C., Mohler M. A., Apple T., Hébert C. A., Valente A. J., Baker J. B. Red blood cells are a sink for interleukin 8, a leukocyte chemotaxin. J Clin Invest. 1991 Oct;88(4):1362–1369. doi: 10.1172/JCI115442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edwards S. W., Hallett M. B. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol Today. 1997 Jul;18(7):320–324. doi: 10.1016/s0167-5699(97)01087-6. [DOI] [PubMed] [Google Scholar]
- Firestein G. S., Xu W. D., Townsend K., Broide D., Alvaro-Gracia J., Glasebrook A., Zvaifler N. J. Cytokines in chronic inflammatory arthritis. I. Failure to detect T cell lymphokines (interleukin 2 and interleukin 3) and presence of macrophage colony-stimulating factor (CSF-1) and a novel mast cell growth factor in rheumatoid synovitis. J Exp Med. 1988 Nov 1;168(5):1573–1586. doi: 10.1084/jem.168.5.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Firestein G. S., Zvaifler N. J. How important are T cells in chronic rheumatoid synovitis? Arthritis Rheum. 1990 Jun;33(6):768–773. doi: 10.1002/art.1780330602. [DOI] [PubMed] [Google Scholar]
- Fontana A., Hengartner H., Weber E., Fehr K., Grob P. J., Cohen G. Interleukin 1 activity in the synovial fluid of patients with rheumatoid arthritis. Rheumatol Int. 1982;2(2):49–53. doi: 10.1007/BF00541245. [DOI] [PubMed] [Google Scholar]
- Gong J. H., Ratkay L. G., Waterfield J. D., Clark-Lewis I. An antagonist of monocyte chemoattractant protein 1 (MCP-1) inhibits arthritis in the MRL-lpr mouse model. J Exp Med. 1997 Jul 7;186(1):131–137. doi: 10.1084/jem.186.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horuk R., Martin A. W., Wang Z., Schweitzer L., Gerassimides A., Guo H., Lu Z., Hesselgesser J., Perez H. D., Kim J. Expression of chemokine receptors by subsets of neurons in the central nervous system. J Immunol. 1997 Mar 15;158(6):2882–2890. [PubMed] [Google Scholar]
- Horuk R., Martin A., Hesselgesser J., Hadley T., Lu Z. H., Wang Z. X., Peiper S. C. The Duffy antigen receptor for chemokines: structural analysis and expression in the brain. J Leukoc Biol. 1996 Jan;59(1):29–38. doi: 10.1002/jlb.59.1.29. [DOI] [PubMed] [Google Scholar]
- Horuk R. Molecular properties of the chemokine receptor family. Trends Pharmacol Sci. 1994 May;15(5):159–165. doi: 10.1016/0165-6147(94)90077-9. [DOI] [PubMed] [Google Scholar]
- Houssiau F. A., Devogelaer J. P., Van Damme J., de Deuxchaisnes C. N., Van Snick J. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum. 1988 Jun;31(6):784–788. doi: 10.1002/art.1780310614. [DOI] [PubMed] [Google Scholar]
- Karpus W. J., Lukacs N. W., McRae B. L., Strieter R. M., Kunkel S. L., Miller S. D. An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. J Immunol. 1995 Nov 15;155(10):5003–5010. [PubMed] [Google Scholar]
- Kasama T., Strieter R. M., Lukacs N. W., Lincoln P. M., Burdick M. D., Kunkel S. L. Interleukin-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis. J Clin Invest. 1995 Jun;95(6):2868–2876. doi: 10.1172/JCI117993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Katsikis P. D., Chu C. Q., Brennan F. M., Maini R. N., Feldmann M. Immunoregulatory role of interleukin 10 in rheumatoid arthritis. J Exp Med. 1994 May 1;179(5):1517–1527. doi: 10.1084/jem.179.5.1517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marsh W. L. Present status of the Duffy blood group system. CRC Crit Rev Clin Lab Sci. 1975 Mar;5(4):387–412. doi: 10.3109/10408367509107049. [DOI] [PubMed] [Google Scholar]
- Meade E. A., Smith W. L., DeWitt D. L. Differential inhibition of prostaglandin endoperoxide synthase (cyclooxygenase) isozymes by aspirin and other non-steroidal anti-inflammatory drugs. J Biol Chem. 1993 Mar 25;268(9):6610–6614. [PubMed] [Google Scholar]
- Miossec P., Naviliat M., Dupuy d'Angeac A., Sany J., Banchereau J. Low levels of interleukin-4 and high levels of transforming growth factor beta in rheumatoid synovitis. Arthritis Rheum. 1990 Aug;33(8):1180–1187. doi: 10.1002/art.1780330819. [DOI] [PubMed] [Google Scholar]
- Neote K., DiGregorio D., Mak J. Y., Horuk R., Schall T. J. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 1993 Feb 12;72(3):415–425. doi: 10.1016/0092-8674(93)90118-a. [DOI] [PubMed] [Google Scholar]
- Oliver S. J., Brahn E. Combination therapy in rheumatoid arthritis: the animal model perspective. J Rheumatol Suppl. 1996 Mar;44:56–60. [PubMed] [Google Scholar]
- Oppenheim J. J., Zachariae C. O., Mukaida N., Matsushima K. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu Rev Immunol. 1991;9:617–648. doi: 10.1146/annurev.iy.09.040191.003153. [DOI] [PubMed] [Google Scholar]
- PEARSON C. M. Development of arthritis, periarthritis and periostitis in rats given adjuvants. Proc Soc Exp Biol Med. 1956 Jan;91(1):95–101. doi: 10.3181/00379727-91-22179. [DOI] [PubMed] [Google Scholar]
- Plater-Zyberk C., Hoogewerf A. J., Proudfoot A. E., Power C. A., Wells T. N. Effect of a CC chemokine receptor antagonist on collagen induced arthritis in DBA/1 mice. Immunol Lett. 1997 Jun 1;57(1-3):117–120. doi: 10.1016/s0165-2478(97)00075-8. [DOI] [PubMed] [Google Scholar]
- Rathanaswami P., Hachicha M., Sadick M., Schall T. J., McColl S. R. Expression of the cytokine RANTES in human rheumatoid synovial fibroblasts. Differential regulation of RANTES and interleukin-8 genes by inflammatory cytokines. J Biol Chem. 1993 Mar 15;268(8):5834–5839. [PubMed] [Google Scholar]
- Saxne T., Palladino M. A., Jr, Heinegård D., Talal N., Wollheim F. A. Detection of tumor necrosis factor alpha but not tumor necrosis factor beta in rheumatoid arthritis synovial fluid and serum. Arthritis Rheum. 1988 Aug;31(8):1041–1045. doi: 10.1002/art.1780310816. [DOI] [PubMed] [Google Scholar]
- Schall T. J., Bacon K., Camp R. D., Kaspari J. W., Goeddel D. V. Human macrophage inflammatory protein alpha (MIP-1 alpha) and MIP-1 beta chemokines attract distinct populations of lymphocytes. J Exp Med. 1993 Jun 1;177(6):1821–1826. doi: 10.1084/jem.177.6.1821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schall T. J., Bacon K., Toy K. J., Goeddel D. V. Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature. 1990 Oct 18;347(6294):669–671. doi: 10.1038/347669a0. [DOI] [PubMed] [Google Scholar]
- Schall T. J., Jongstra J., Dyer B. J., Jorgensen J., Clayberger C., Davis M. M., Krensky A. M. A human T cell-specific molecule is a member of a new gene family. J Immunol. 1988 Aug 1;141(3):1018–1025. [PubMed] [Google Scholar]
- Snowden N., Hajeer A., Thomson W., Ollier B. RANTES role in rheumatoid arthritis. Lancet. 1994 Feb 26;343(8896):547–548. doi: 10.1016/s0140-6736(94)91503-2. [DOI] [PubMed] [Google Scholar]
- Stastny P. HLA-D and Ia antigens in rheumatoid arthritis and systemic lupus erythematosus. Arthritis Rheum. 1978 Jun;21(5 Suppl):S139–S143. doi: 10.1002/art.1780210921. [DOI] [PubMed] [Google Scholar]
- Taub D. D., Conlon K., Lloyd A. R., Oppenheim J. J., Kelvin D. J. Preferential migration of activated CD4+ and CD8+ T cells in response to MIP-1 alpha and MIP-1 beta. Science. 1993 Apr 16;260(5106):355–358. doi: 10.1126/science.7682337. [DOI] [PubMed] [Google Scholar]
- Taub D. D., Turcovski-Corrales S. M., Key M. L., Longo D. L., Murphy W. J. Chemokines and T lymphocyte activation: I. Beta chemokines costimulate human T lymphocyte activation in vitro. J Immunol. 1996 Mar 15;156(6):2095–2103. [PubMed] [Google Scholar]
- Waller M. Methods of measurement of rheumatoid factor. Ann N Y Acad Sci. 1969 Dec 10;168(1):5–16. doi: 10.1111/j.1749-6632.1969.tb43090.x. [DOI] [PubMed] [Google Scholar]
- Woodrow J. C., Nichol F. E., Zaphiropoulos G. DR antigens and rheumatoid arthritis: a study of two populations. Br Med J (Clin Res Ed) 1981 Nov 14;283(6302):1287–1288. doi: 10.1136/bmj.283.6302.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xu W. D., Firestein G. S., Taetle R., Kaushansky K., Zvaifler N. J. Cytokines in chronic inflammatory arthritis. II. Granulocyte-macrophage colony-stimulating factor in rheumatoid synovial effusions. J Clin Invest. 1989 Mar;83(3):876–882. doi: 10.1172/JCI113971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshimura T., Robinson E. A., Tanaka S., Appella E., Kuratsu J., Leonard E. J. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J Exp Med. 1989 Apr 1;169(4):1449–1459. doi: 10.1084/jem.169.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zipfel P. F., Balke J., Irving S. G., Kelly K., Siebenlist U. Mitogenic activation of human T cells induces two closely related genes which share structural similarities with a new family of secreted factors. J Immunol. 1989 Mar 1;142(5):1582–1590. [PubMed] [Google Scholar]