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. 1987 Apr;79(4):1160–1171. doi: 10.1172/JCI112933

Thymus-dependent and -independent regulation of Ia antigen expression in situ by cells in the synovium of rats with streptococcal cell wall-induced arthritis. Differences in site and intensity of expression in euthymic, athymic, and cyclosporin A-treated LEW and F344 rats.

R L Wilder, J B Allen, C Hansen
PMCID: PMC424298  PMID: 3494045

Abstract

Euthymic LEW rats, when injected with streptococcal cell walls, exhibited rapid onset development of acute exudative arthritis coincident with enhanced synovial expression of Ia antigen. By 21 d after injection, the expression of Ia was markedly increased compared with basal conditions and paralleled the severity of the later developing proliferative and erosive disease. Immunodeficient athymic and cyclosporin A-treated LEW rats developed only the early phase arthritis, which was again paralleled by synovial Ia expression. Chronic expression of high levels of Ia antigen was not observed. Histocompatible F344 rats, both athymic and euthymic, developed minimal, if any, clinically significant arthritis and did not exhibit the enhanced Ia expression demonstrated in the LEW rats. Our results indicate that enhanced synovial Ia expression parallels clinical disease severity and varies by rat strain, and that the rapid onset enhanced synovial Ia expression is thymus independent, whereas the markedly enhanced chronic phase Ia expression is thymus dependent.

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Selected References

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  1. Allen J. B., Calandra G. B., Wilder R. L. Cutaneous inflammatory reactions to group A streptococcal cell wall fragments in Fisher and Lewis inbred rats. Infect Immun. 1983 Nov;42(2):796–801. doi: 10.1128/iai.42.2.796-801.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen J. B., Malone D. G., Wahl S. M., Calandra G. B., Wilder R. L. Role of the thymus in streptococcal cell wall-induced arthritis and hepatic granuloma formation. Comparative studies of pathology and cell wall distribution in athymic and euthymic rats. J Clin Invest. 1985 Sep;76(3):1042–1056. doi: 10.1172/JCI112057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Amento E. P., Bhan A. K., McCullagh K. G., Krane S. M. Influences of gamma interferon on synovial fibroblast-like cells. Ia induction and inhibition of collagen synthesis. J Clin Invest. 1985 Aug;76(2):837–848. doi: 10.1172/JCI112041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Anderle S. K., Allen J. B., Wilder R. L., Eisenberg R. A., Cromartie W. J., Schwab J. H. Measurement of streptococcal cell wall in tissues of rats resistant or susceptible to cell wall-induced chronic erosive arthritis. Infect Immun. 1985 Sep;49(3):836–837. doi: 10.1128/iai.49.3.836-837.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Behbehani K., Beller D. I., Unanue E. R. The effects of beryllium and other adjuvants on Ia expression by macrophages. J Immunol. 1985 Apr;134(4):2047–2049. [PubMed] [Google Scholar]
  6. Beraud E., Reshef T., Vandenbark A. A., Offner H., Friz R., Chou C. H., Bernard D., Cohen I. R. Experimental autoimmune encephalomyelitis mediated by T lymphocyte lines: genotype of antigen-presenting cells influences immunodominant epitope of basic protein. J Immunol. 1986 Jan;136(2):511–515. [PubMed] [Google Scholar]
  7. Caspi R. R., Roberge F. G., McAllister C. G., el-Saied M., Kuwabara T., Gery I., Hanna E., Nussenblatt R. B. T cell lines mediating experimental autoimmune uveoretinitis (EAU) in the rat. J Immunol. 1986 Feb 1;136(3):928–933. [PubMed] [Google Scholar]
  8. Cavender D. E., Haskard D. O., Joseph B., Ziff M. Interleukin 1 increases the binding of human B and T lymphocytes to endothelial cell monolayers. J Immunol. 1986 Jan;136(1):203–207. [PubMed] [Google Scholar]
  9. Clark R. L., Cuttino J. T., Jr, Anderle S. K., Cromartie W. J., Schwab J. H. Radiologic analysis of arthritis in rats after systemic injection of streptococcal cell walls. Arthritis Rheum. 1979 Jan;22(1):25–35. doi: 10.1002/art.1780220105. [DOI] [PubMed] [Google Scholar]
  10. Cromartie W. J., Craddock J. G., Schwab J. H., Anderle S. K., Yang C. H. Arthritis in rats after systemic injection of streptococcal cells or cell walls. J Exp Med. 1977 Dec 1;146(6):1585–1602. doi: 10.1084/jem.146.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DISCHE Z., SHETTLES L. B. A specific color reaction of methylpentoses and a spectrophotometric micromethod for their determination. J Biol Chem. 1948 Sep;175(2):595–603. [PubMed] [Google Scholar]
  12. Dallman M. J., Thomas M. L., Green J. R. MRC OX-19: a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol. 1984 Mar;14(3):260–267. doi: 10.1002/eji.1830140311. [DOI] [PubMed] [Google Scholar]
  13. Decker J. L., Malone D. G., Haraoui B., Wahl S. M., Schrieber L., Klippel J. H., Steinberg A. D., Wilder R. L. NIH conference. Rheumatoid arthritis: evolving concepts of pathogenesis and treatment. Ann Intern Med. 1984 Dec;101(6):810–824. doi: 10.7326/0003-4819-101-6-810. [DOI] [PubMed] [Google Scholar]
  14. Griffiths M. M., Eichwald E. J., Martin J. H., Smith C. B., DeWitt C. W. Immunogenetic control of experimental type II collagen-induced arthritis. I. Susceptibility and resistance among inbred strains of rats. Arthritis Rheum. 1981 Jun;24(6):781–789. doi: 10.1002/art.1780240605. [DOI] [PubMed] [Google Scholar]
  15. Haraoui B., Wilder R. L., Allen J. B., Sporn M. B., Helfgott R. K., Brinckerhoff C. E. Dose-dependent suppression by the synthetic retinoid, 4-hydroxyphenyl retinamide, of streptococcal cell wall-induced arthritis in rats. Int J Immunopharmacol. 1985;7(6):903–916. doi: 10.1016/0192-0561(85)90054-2. [DOI] [PubMed] [Google Scholar]
  16. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  17. Hsu S. M., Ree H. J. Self-sandwich method. An improved immunoperoxidase technic for the detection of small amounts of antigens. Am J Clin Pathol. 1980 Jul;74(1):32–40. doi: 10.1093/ajcp/74.1.32. [DOI] [PubMed] [Google Scholar]
  18. Iguchi T., Ziff M. Electron microscopic study of rheumatoid synovial vasculature. Intimate relationship between tall endothelium and lymphoid aggregation. J Clin Invest. 1986 Feb;77(2):355–361. doi: 10.1172/JCI112312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kunkel S. L., Chensue S. W., Plewa M., Higashi G. I. Macrophage function in the Schistosoma mansoni egg-induced pulmonary granuloma. Role of arachidonic acid metabolites in macrophage Ia antigen expression. Am J Pathol. 1984 Feb;114(2):240–249. [PMC free article] [PubMed] [Google Scholar]
  20. Kunkel S. L., Fantone J. C., Ward P. A., Zurier R. B. Modulation of inflammatory reactions by prostaglandins. Prog Lipid Res. 1981;20:633–640. doi: 10.1016/0163-7827(81)90118-1. [DOI] [PubMed] [Google Scholar]
  21. Lehman T. J., Allen J. B., Plotz P. H., Wilder R. L. Lactobacillus casei cell wall-induced arthritis in rats: cell wall fragment distribution and persistence in chronic arthritis-susceptible LEW/N and -resistant F344/N rats. Arthritis Rheum. 1984 Aug;27(8):939–942. doi: 10.1002/art.1780270815. [DOI] [PubMed] [Google Scholar]
  22. Lehman T. J., Allen J. B., Plotz P. H., Wilder R. L. Polyarthritis in rats following the systemic injection of Lactobacillus casei cell walls in aqueous suspension. Arthritis Rheum. 1983 Oct;26(10):1259–1265. doi: 10.1002/art.1780261013. [DOI] [PubMed] [Google Scholar]
  23. Malone D. G., Wahl S. M., Tsokos M., Cattell H., Decker J. L., Wilder R. L. Immune function in severe, active rheumatoid arthritis. A relationship between peripheral blood mononuclear cell proliferation to soluble antigens and synovial tissue immunohistologic characteristics. J Clin Invest. 1984 Oct;74(4):1173–1185. doi: 10.1172/JCI111526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McMaster W. R., Williams A. F. Identification of Ia glycoproteins in rat thymus and purification from rat spleen. Eur J Immunol. 1979 Jun;9(6):426–433. doi: 10.1002/eji.1830090603. [DOI] [PubMed] [Google Scholar]
  25. Miossec P., Yu C. L., Ziff M. Lymphocyte chemotactic activity of human interleukin 1. J Immunol. 1984 Oct;133(4):2007–2011. [PubMed] [Google Scholar]
  26. Ridge S. C., Zabriske J. B., Oronsky A. L., Kerwar S. S. Streptococcal cell wall arthritis: studies with nude (athymic) inbred Lewis rats. Cell Immunol. 1985 Nov;96(1):231–234. doi: 10.1016/0008-8749(85)90354-5. [DOI] [PubMed] [Google Scholar]
  27. Rosenthale M. E. A comparative study of the Lewis and Sprague Dawley rat in adjuvant arthritis. Arch Int Pharmacodyn Ther. 1970 Nov;188(1):14–22. [PubMed] [Google Scholar]
  28. Scher M. G., Beller D. I., Unanue E. R. Demonstration of a soluble mediator that induces exudates rich in Ia-positive macrophages. J Exp Med. 1980 Dec 1;152(6):1684–1698. doi: 10.1084/jem.152.6.1684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwab J. H., Allen J. B., Anderle S. K., Dalldorf F., Eisenberg R., Cromartie W. J. Relationship of complement to experimental arthritis induced in rats with streptococcal cell walls. Immunology. 1982 May;46(1):83–88. [PMC free article] [PubMed] [Google Scholar]
  30. Skoskiewicz M. J., Colvin R. B., Schneeberger E. E., Russell P. S. Widespread and selective induction of major histocompatibility complex-determined antigens in vivo by gamma interferon. J Exp Med. 1985 Nov 1;162(5):1645–1664. doi: 10.1084/jem.162.5.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Snyder D. S., Beller D. I., Unanue E. R. Prostaglandins modulate macrophage Ia expression. Nature. 1982 Sep 9;299(5879):163–165. doi: 10.1038/299163a0. [DOI] [PubMed] [Google Scholar]
  32. Sobel R. A., Blanchette B. W., Bhan A. K., Colvin R. B. The immunopathology of experimental allergic encephalomyelitis. II. Endothelial cell Ia increases prior to inflammatory cell infiltration. J Immunol. 1984 May;132(5):2402–2407. [PubMed] [Google Scholar]
  33. Sobel R. A., Colvin R. B. The immunopathology of experimental allergic encephalomyelitis (EAE). III. Differential in situ expression of strain 13 Ia on endothelial and inflammatory cells of (strain 2 x strain 13)F1 guinea pigs with EAE. J Immunol. 1985 Apr;134(4):2333–2337. [PubMed] [Google Scholar]
  34. Steeg P. S., Johnson H. M., Oppenheim J. J. Regulation of murine macrophage Ia antigen expression by an immune interferon-like lymphokine: inhibitory effect of endotoxin. J Immunol. 1982 Dec;129(6):2402–2406. [PubMed] [Google Scholar]
  35. Steeg P. S., Moore R. N., Oppenheim J. J. Regulation of murine macrophage Ia-antigen expression by products of activated spleen cells. J Exp Med. 1980 Dec 1;152(6):1734–1744. doi: 10.1084/jem.152.6.1734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stern D. M., Bank I., Nawroth P. P., Cassimeris J., Kisiel W., Fenton J. W., 2nd, Dinarello C., Chess L., Jaffe E. A. Self-regulation of procoagulant events on the endothelial cell surface. J Exp Med. 1985 Oct 1;162(4):1223–1235. doi: 10.1084/jem.162.4.1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vos J. G., Kreeftenberg J. G., Kruijt B. C., Kruizinga W., Steerenberg P. The athymic nude rat. II. Immunological characteristics. Clin Immunol Immunopathol. 1980 Feb;15(2):229–237. doi: 10.1016/0090-1229(80)90033-1. [DOI] [PubMed] [Google Scholar]
  38. Wilder R. L., Allen J. B. Regulation of susceptibility to bacterial cell wall-induced arthritis in rats. Arthritis Rheum. 1985 Nov;28(11):1318–1319. doi: 10.1002/art.1780281124. [DOI] [PubMed] [Google Scholar]
  39. Wilder R. L., Allen J. B., Wahl L. M., Calandra G. B., Wahl S. M. The pathogenesis of group A streptococcal cell wall-induced polyarthritis in the rat. Comparative studies in arthritis resistant and susceptible inbred rat strains. Arthritis Rheum. 1983 Dec;26(12):1442–1451. doi: 10.1002/art.1780261205. [DOI] [PubMed] [Google Scholar]
  40. Wilder R. L., Calandra G. B., Garvin A. J., Wright K. D., Hansen C. T. Strain and sex variation in the susceptibility to streptococcal cell wall-induced polyarthritis in the rat. Arthritis Rheum. 1982 Sep;25(9):1064–1072. doi: 10.1002/art.1780250906. [DOI] [PubMed] [Google Scholar]
  41. Yocum D. E., Allen J. B., Wahl S. M., Calandra G. B., Wilder R. L. Inhibition by cyclosporin A of streptococcal cell wall-induced arthritis and hepatic granulomas in rats. Arthritis Rheum. 1986 Feb;29(2):262–273. doi: 10.1002/art.1780290215. [DOI] [PubMed] [Google Scholar]

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