Induction of circulating myelin basic protein and proteolipid protein- specific transforming growth factor-β1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients

Journal of Clinical Investigation

Volumn 98, Issue 1, 1996, Pages 70-77

  Fukaura, Hikoaki ^a   Kent, Sally C ^a   Pietrusewicz, Matthew J ^a   Khoury, Samia J ^a   Weiner, Howard L ^a   Hafler, David A ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Center for Neurologic Diseases   (United States)

Author keywords

autoantigen; demyelination; oral tolerance; regulatory cytokines

Indexed keywords

AUTOANTIGEN; GAMMA INTERFERON; INTERLEUKIN 4; MYELIN; MYELIN BASIC PROTEIN; MYLORAL; PROTEOLIPID PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DEMYELINATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 0030035509     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118779     Document Type: Article

References (36)

1. McFarlin, D.E., and H.F. McFarland. 1982. Multiple sclerosis. N. Engl. J. Med. 307:1183-1188.
2. Hafler, D.A., and H.L. Weiner. 1995. Immunologic mechanisms and therapy in multiple sclerosis. Immunol. Reviews. 144:75-107.
3. Zamvil, S., P. Nelson, J. Trotter, D. Mitchell, R. Knobler, R. Fritz, and L. Steinman. 1985. T cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination. Nature (Lond.). 317:355-358.
4. Tuohy, V.K., R.A. Sobel, and M.B. Lees. 1988. Myelin proteolipid protein-induced experimental allergic encephalomyelitis. Variations of disease expression in different strains of mice. J. Immunol. 140:1868-1873.
5. Linington, C., T. Berger, L. Perry, S. Weerth, D. Hinze-Selch, Y. Zhang, H.C. Lu, H. Lassmann, and H. Wekerle. 1993. T cells specific for the myelin oligodendrocyte glycoprotein mediate an unusual autoimmune inflammatory response in the central nervous system. Eur. J. Immunol. 23:1364-1372.
6. Khoury, S.J., W.W. Hancock, and H.L. Weiner. 1992. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of transforming growth factor-β, interleukin-4, and prostaglandin E expression in the brain. J. Exp. Med. 176:1355-1364.
7. Chase, M.W. 1946. Inhibition of experimental drug allergy by prior feeding of the sensitizing agent. Proc. Soc. Exp. Biol. Med. 61:257-259.
8. Mowat, A.M. 1987. The regulation of immune responses to dietary protein antigens. Immunol. Today. 8:93-98.
9. Higgins, P.J., and H.L. Weiner. 1988. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein and its fragments. J. Immunol. 140:440-445.
10. Bitar, D.M., and C.C. Whitacre. 1988. Suppression of experimental autoimmune encephalomyelitis by the oral administration of myelin basic protein. Cell. Immunol. 112:364-370.
11. Thompson, H.S., and N.A. Staines. 1986. Gastric administration of type II collagen delays the onset and severity of collagen-induced arthritis in rats. Clin. Exp. Immunol. 64:581-586.
12. Nagler-Anderson, C., L.A. Bober, M.E. Robinson, G.W. Siskind, and G.J. Thorbecke. 1986. Suppression of type II collagen-induced arthritis by intragastric administration of soluble type II collagen. Proc. Natl. Acad. Sci. USA. 83:7443-7446.
13. Zhang, Z.J., C.S.Y. Lee, O. Lider, and H.L. Weiner. 1990. Suppression of adjuvant arthritis in Lewis rats by oral administration of type II collagen. J. Immunol. 145:2489-2493.
14. Nussenblatt, R.B., R.R. Caspi, R. Mahdi, C.-C. Chan, F. Roberge, O. Lider, and H.L. Weiner. 1990. Inhibition of S-antigen induced experimental autoimmune uveoretinitis by oral induction of tolerance with S-antigen. J Immunol. 144:1689-1695.
15. Zhang, Z.J., L. Davidson, G. Eisenbarth, and H.L. Weiner. 1991. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc. Natl. Acad. Sci. USA. 88:10252-10256.
16. Chen, Y., J.-I. Inobe, R. Marks, P. Gonnella, V.K. Kuchroo, and H.L. Weiner. 1995. Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature (Lond.). 376:177-180.
17. Whitacre, C.C., I.E. Gienapp, C.G. Orosz, and D.M. Bitar. 1991. Oral tolerance in experimental autoimmune encephalomyelitis. III. Evidence for clonal anergy. J. Immunol. 147:2155-2163.
18. Friedman, A., and H.L. Weiner. 1994. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc. Natl. Acad. Sci. USA. 91:6688-6692.
19. Miller, A., O. Lider, and H.L. Weiner. 1991. Antigen-driven bystander suppression following oral administration of antigens. J. Exp. Med. 174:791-798.
20. Chen, Y., V.K. Kuchroo, J.-I. Inobe, D.A. Hafler, and H.L. Weiner. 1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science (Wash. DC). 265:1237-1240.
21. Chen, Y., J.-I. Inobe, V.K. Kuchroo, J.L. Baron, C.A. Janeway, Jr., and H.L. Weiner. 1996. Oral tolerance in myelin basic protein T-cell receptor transgenic mice: suppression of autoimmune encephalomyelitis and dose-dependent induction of regulatory cells. Proc. Natl. Acad. Sci. USA. 93:388-391.
22. Weiner, H.L., G.A. Mackin, M. Matsui, E.J. Orav, S.J. Khoury, D.M. Dawson, and D.A. Hafler. 1993. Double-blind pilot trial of oral tolerization with myelin antigens in multiple sclerosis. Science (Wash. DC). 259:1321-1324.
23. Trentham, D.E., R.A. Dynesius-Trentham, E.J. Orav, D. Combitchi, C. Lorenzo, K.L. Sewall, D.A. Hafler, and H.L. Weiner. 1993. Effects of oral administration of type II collagen on rheumatoid arthritis. Science (Wash. DC). 261:1727-1730.
24. Hohol, M.J., S.J. Khoury, S.L. Cook, E.J. Orav, D.A. Hafler, and H.L. Weiner. 1996. Three year open protocol continuation study of oral tolerization with myelin antigens in multiple sclerosis and design of a phase III pivotal trial. Annu. NY Acad. Sci. 778:243-250.
25. Chou, F.C.-H., C.-H.J. Chou, R. Shapira, and R.F. Kibler. 1976. Basis of microheterogeneity of myelin basic protein. J. Biol. Chem. 251:2671-2679.
26. Bizzozero, O.A., G. Zuniga, and M.B. Lees. 1991. Fatty acid composition of human myelin proteolipid protein in peroxisomal disorders. J. Neurochem. 56:872-878.
27. Miller, A., O. Lider, A.B. Roberts, M.B. Sporn, and H.L. Weiner. 1992. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor β after antigen-specific triggering. Proc. Natl. Acad. Sci. USA. 89:421-425.
28. Lehman, D.A., F.D. Lee, and R.L. Coffman. 1990. Mechanism for transforming growth factor β and IL-2 enhancement of IgA expression in lipopolysaccharide-stimulated B cell cultures. J. Immunol. 144:952-959.
29. Wahl, S.M., N. McCarthy-Francis, and S.E. Mergenhagen. 1989. Inflammatory and immunomodulatory roles of TGFβ. Immunol. Today. 10:258-261.
30. Weiner, H.L., A. Friedman, A. Miller, S.J. Khoury, A. Al-Sabbagh, L. Santos, M. Sayegh, R.B. Nussenblatt, D.E. Trentham, and D.A. Hafler. 1994. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune disease by oral administration of autoantigens. Annu. Rev. Immunol. 12:809-837.
31. Husby, S., J. Mestecky, Z. Moldoveanu, S. Holland, and C.O. Elson. 1994. Oral tolerance in humans: T cell but not B cell tolerance after antigen feeding. J. Immunol. 152:4663-4670.
32. Salk, R.J.S. 1983. A study of myelin basic protein as a therapeutic probe in patients with multiple sclerosis. In Multiple Sclerosis. J.F. Hallpike, C.W.M. Adams, and W.W. Tourtellotte, editors. Chapman and Hall, London. 621-630.
33. Kojima, K., T. Berger, H. Lassman, D. Hinze-Seich, Y. Zhang, J. Gehrmann, K. Reske, H. Wekerle, and C. Linington. 1994. Experimental autoimmune panencephalitis and uvoretinitis transferred to the Lewis rat by T lymphocytes specific for the S100-beta molecule, a calcium binding protein of astroglia. J. Exp. Med. 180:817-829.
34. Lehmann, P.V., T. Forsthuber, A. Miller, and E.E. Sercarz. 1992. Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature (Lond.). 358:155-157.
35. Zhang, J., S. Markovic-Plese, B. Lacet, J. Raus, H.L. Weiner, and D.A. Hafler. 1994. Increased frequency of interleukin-2 responsive T cells specific for myelin basic protein and proteolipid protein in peripheral blood and cerebrospinal fluid of patients with multiple sclerosis. J. Exp. Med. 179:973-984.
36. Mosmann, T.R., and S. Sad. 1996. The expanding universe of T cell subsets: Th1, Th2 and more. Immunol. Today. 17:138-146.