The T helper cell response in lyme arthritis: Differential recognition of borrelia burgdorferi outer surface protein a in patients with treatment-resistant or treatment-responsive lyme arthritis

Journal of Experimental Medicine

Volumn 180, Issue 6, 1994, Pages 2069-2078

  Lengl Janlßen, Beate ^a   Strauss, Ann F ^a   Steere, Allen C ^a   Kamradt, Thomas ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; OUTER MEMBRANE PROTEIN;

ADOLESCENT; ADULT; AGED; ANTIGEN RECOGNITION; ARTICLE; BORRELIA BURGDORFERI; CELLULAR IMMUNITY; CHILD; CLINICAL ARTICLE; FEMALE; HELPER CELL; HUMAN; LYME DISEASE; MALE; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ADULT; AGED; ANTIBIOTICS; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI GROUP; CHILD, PRESCHOOL; COMPARATIVE STUDY; DNA PRIMERS; DRUG RESISTANCE; FEMALE; HUMAN; LYME DISEASE; MALE; MIDDLE AGE; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE OF TESTS; RECOMBINANT FUSION PROTEINS; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, P.H.S.; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 0028114190     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.180.6.2069     Document Type: Article

References (63)

1. Steere, A.C. 1989. Lyme disease. N. Engl. J. Med. 321:586.
2. Szczepanski, A., and J.L. Benach. 1991. Lyme borreliosis: host responses to Borrelia burgdorferi. Microbiol. Rev. 55:21.
3. Steere, A.C., A. Gibofsky, M.E. Patarrqyo, R.J. Winchester, J. A. Hardin, and S.E. Malawista. 1979. Chronic Lyme arthritis. Clinical and immunogenetic differentiation from rheumatoid arthritis. Ann. Intern. Med. 90:896.
4. Steere, A.C., R.T. Schoen, and E. Taylor. 1987. The clinical evolution of Lyme arthritis. Ann. Intern. Med. 107:725.
5. Craft, J.E., D.K. Fischer, G.T. Shimamoto, and A.C. Steere. 1986. Antigens of Borrelia burgdorferi recognized during Lyme disease. Appearance of a new immunoglobulin M response and expansion of the immunoglobulin G response late in the ill¬ ness. J. Clin. Invest. 78:934.
6. Sigal, L.H., A.C. Steere, D.H. Freeman, and J.M. Dwyer. 1986. Proliferative responses of mononuclear cells in Lyme disease. Reactivity to Borrelia burgdorferi antigens is greater in joint fluid than in blood. Arthritis Rheum. 29:761.
7. Neumann, A., M. Schlesier, H. Schneider, A. Vogt, and H.H. Peter. 1989. Frequencies of Borrelia burgdorferi reactive T lymphocytes in Lyme arthritis. Rheumatol. Int. 9:237.
8. Yssel, H., M.-C. Shanafelt, C. Soderberg, P.V. Schneider, J. Anzola, and G. Peltz. 1991. Borrelia burgdorferi activates a T helper type 1-like T cell subset in Lyme arthritis.J. Exp. Med. 174:593.
9. Krause, A., G.-R. Burmester, A. Rensing, C. Schoemer, U.E. Schaible, M.M. Simon, P. Herzer, M.D. Kramer, and R. Wal- lich. 1992. Cellular immune reactivity to recombinant OspA and fiagellin from Borrelia burgdorferi in patients with Lyme borreliosis. Complexity of humoral and cellular immune re sponses. J. Clin. Invest. 90:1077.
10. Kalish, R.A., J.L. Leong, and A.C. Steere. 1993. Association of treatment-resistant chronic Lyme arthritis with HLA-DR4 and antibody reactivity to OspA and OspB of Borrelia burgdorferi. Infect. Immun. 61:2774.
11. Steere, A.C., J. Green, R.T. Schoen, E. Taylor, GJ. Hutchinson, D.W. Rahn, and S.E. Malawista. 1985. Successful paren¬ teral penicillin therapy of established Lyme arthritis. N. Engl. J. Mel 312:869.
12. Dattwyler, R.J., J.J. Halperin, D.J. Volkman, and B.J. Luft. 1988. Treatment of late Lyme borreliosis-rand omised com¬ parison of ceftriaxone and penicillin. Lancet. i:1191.
13. Steere, A.C., R.E. Levin, P.J. Molloy, R.A. Kalish, J.H. Abraham III, N.Y. Liu, and C.H. Schmid. 1994. Treatment of Lyme arthritis. Arthritis Rheum. 37:878.
14. Dattwyler, R.J., and J.J. Halperin. 1987. Failure of tetracy¬ cline therapy in early Lyme disease. Arthritis. Rheum. 30:448.
15. Johnston, Y.E., P.H. Durray, A.C. Steere, M. Kashgarian, J. Buza, S.E. Malawista, and P.W. Askenase. 1985. Lyme arthritis: spirochetes found in synovial microangiopathic lesions. Am. f. Pathol. 118:26.
16. Syndman, D.R., D.P. Schenkein, V.P. Berardi, C.C. Lastavica, and K.M. Pariser. 1986. Borrelia burgdorferi in joint fluid in chronic Lyme arthritis. Ann. Intern. Med. 104:796.
17. Steere, A.C., P.H. Duray, and E.C. Butcher. 1988. Spirochetal antigens and lymphoid cell surface markers in Lyme synovitis. Comparison with rheumatoid synovium and tonsillar lymphoid tissue. Arthritis Rheum. 31:487.
18. Norton, J.J., F. Dressier, B.J. Rutledge, P.N. Rys, D.H. Psrsing, and A.C. Steere. 1994. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid in Lyme arthritis. N. Engl. J. Med. 330:229.
19. Bradley, J.F., R.C. Johnson, and J.L. Goodman. 1994. The persistance of spirochetal nucleic acids in active Lyme arthritis. Ann. Intern. Med. 120:487.
20. Steere, A.C., E.D. Dwyer, and R. Winchester. 1990. Associa¬ tion of chronic Lyme arthritis with HL A-DR4 and HLA-DR2 alleles. N. Engl. J. Med. 323:219.
21. Centers for Disease Control. 1990. Clinical criteria for Lyme disease. MMWR (Mork Mortal. Whly. Rep). 39:19.
22. Holoddniy, M., S. Kim, D. Katzenstein, M. Konrad, E. Groves, and T.C. Merigan. 1991.' Inhibition of human immunodeficiency virus gene amplification by heparin. J. Clin. Microbiol. 29:676.
23. Fung, B.P., G.L. McHugh, J.M. Leong, and A.C. Steere. Hu¬ moral immune response to outer-surface protein C (OspC) of Borrelia burgdorferi in Lyme disease: role of the IgM response in the serodiagnosis of early infection. Infect. Immun. 62:3213.
24. Simpson, W.J., M.E. Schrumpf, and T.G. Schwan. 1990. Re¬ activity of human Lyme borreliosis sera with a 39-kilodalton antigen specific to Borrelia burgdorferi. J. Clin. Microbiol. 28:1329.
25. Sadziene, A., D.D. Thomas, V.G. Bundoc, S.C. Holt, and A.G. Barbour. 1991. A flagella-less mutant of Borrelia burgdorferi. Structural, molecular, and in vitro functional characterization. J Clin. Invest. 88:82.
26. Bergström, S., V.G. Bundoc, and A.G. Barbour. 1989. Molec¬ ular analysis of linear plasmid-encoded major surface proteins OspA and OspB, of the lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 3:479.
27. Barbour, A.G., S.L. Tessier, and W.J. Todd. 1983. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal anti¬ body. Infect. Immun. 41:795.
28. Barbour, A.G., S.L. Tessier, and S.F. Hayes. 1984. Variation in a major surface protein of Lyme disease spirochetes. Infect. Immun. 54:94.
29. Wilske, B., V. Prearc-Mursic, S. Jauris, A. Hofmann, I. Pradel, E. Soutschek, E. Schwab, G. Will, and G. Wanner. 1993. Immunological and molecular polymorphisms of OspC, an im¬ munodominant major outer surface protein of Borrelia burg- doferi. Infect. Immun. 61:2182.
30. Volkman, D.J., B.J. Luft, P.D. Gorevic, J. Schultz, and L. Padovano. 1991. Characterization of an immunoreactive 93- kDa core protein of Borrelia burgdorferi with a human IgG monclonal antibody. J. Immunol. 146:3177.
31. Kamradt, T, P.D. Soloway, D.L. Perkins, and M.L. Gefter. 1991. Pertussis toxin prevents the induction of peripheral T cell anergy and enhances the T cell response to an encephalito- genic peptide of myelin basic protein. J. Immunol. 147:3296.
32. Burgdofer, W, A.G. Barbour, S.F. Hayes, J.L. Benach, E. Grun- waldt, and J.P. Davis. 1982. Lyme disease-a tick-borne spirochetosis? Science (Wash. DC). 216:1317.
33. Barbour, A.G., and D. Fish. 1993. The biological and social phenomenon of Lyme disease. Science (Wish. DC). 260:1610.
34. Shanafelt, M.-C., J. Anzola, C. Soderberg, H. Yssel, C.W. lurck, and G. Peltz. 1992. Epitopes on the outer surface protein A of Borrelia burgdorferi recognized by antibodies and T cells of patients with Lyme disease. J. Immunol. 148:218.
35. Lahesmaa, R., M.-C. Shanafelt, A. Allsup, C. Soderberg, J. Anzola, V. Freitas, C. Turck, L. Steinman, and G. Peltz. 1993. Preferential usage of T cell antigen receptor V region segment Vβ5.1 by Borrelia burgdorferi antigen-reactive T cell clones isolated from a patient with Lyme disease. J. Immunol. 150:4125.
36. Yang, L., J.H. Weis, E. Eichwald, C.P. Kolbert, D.H. Persing, and J.J. Weis. 1994. Heritable susceptibility to severe Borrelia burgdorferi-iadnced arthritis is dominant and is associated with persistance of large numbers of spirochetes in tissues. Infect. Immun. 62:492.
37. Persing, D.H., B.J. Rutledge, P.N. Rys, D.S. Podzorski, P.D. Mitchell, K.D. Reed, B. Liu, E. Fikrig, and S.E. Malawista. 1994. Target imbalance: disparity of Borrelia burgdorferi genetic material in synovial fluid from Lyme arthritis patients. J. Infect. Dis. 169:668.
38. Granfors, S., S. Jalkanen, R. von Essen, R. Lahesmaa-Rantala, O. Isomaki, K. Fekkola-Heino, R. Meerilahti-Palo, R. Saario, H. Isomaki, and A. Toivanen. 1989. Yersinia antigens in the synovial-fluid from patients with reactive arthritis. N. Engl. J. Med. 320:216.
39. Miillbacher, A. 1994. The long-term maintainance of cytotoxic T cell memory does not require persistance of antigen. J. Exp. Med. 179:317.
40. Oldstone, M.B. A. 1987. Molecular mimicry and autoimmune disease. Cell. 50:819.
41. Gautam, A.M., C.B. Lock, D.E. Smilek, C.I. Pearson, L.S. Steinman, and H.O. McDevitt. 1994. Minimum structural requirements for peptide presentation by major histocompatibility complex class II molecules. Proc. Natl. Acad. Sci. USA. 91:767.
42. Habicht, G.S., G. Beck, J.L. Benach, J.L. Coleman, and K.D. Leichtling. 1985. Lyme disease spirochetes induce human and murine ILT production. J. Immunol. 134:3147
43. Radolf, J.D., M.V. Norgard, M.E. Brand t, J.D. Isaacs, P.A. Thompson, and B. Beutler. 1991. Lipoproteins of Borrelia burgdorferi and Treponema pallidum activate cachectin/tumor necrosis factor synthesis. Analysis using a CAT reporter construct. J. Immunol. 147:1968.
44. Goverman, J., A. Woods, L. Larson, L.P. Weiner, L. Hood, and D.M. Zaller. 1993. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell. 72:551.
45. Gahring, L.C., and W.O. Weigle. 1990. The regulatory effects of cytokines on the induction of peripheral immunologic tolerance in mice. J. Immunol. 145:1318.
46. Essery, G., M. Feldmann, and J.R. Lamb. 1988. Interleukin-2 can prevent and reverse antigen-induced unresponsiveness in cloned human T lymphocytes. Immunology. 64:413.
47. Gutierrez-Ramos, J.C., I. Moreno de Alboran, and A. Martinez. 1992. In vivo administration of interleukin-2 turns on anergic self-reactive T cells and leads to autoimmune disease. Eur. J. Immunol. 22:2867.
48. Lahesmaa, R., H. Yssel, S. Batsford, R. Luukkainen, T. Mot- tonen, L. Steinman, and G. Peltz. 1992. Yersinia enterocolitica activates a T helper type 1-like subset in reactive arthritis. J. Immunol. 148:3079.
49. Simon, A.K., E. Seipelt, P. Wu, B. Wenzel, J. Braun, and j. Seiper. 1993. Analysis of cytokine profiles in synovial T cell clones from chlamydial reactive arthritis patients: predominance of the Thl subset. Clin. Exp Immunol. 94:122.
50. Schaible, U.E., M.D. Kramer, K. Eichmann, M. Modolell, C. Musetanu, and M.M. Simon. 1990. Monoclonal antibodies specific for the outer surface protein A (OspA) of Borrelia bur dorferi prevent Lyme borreliosis in severe combined immunodeficiency (sdd) mice. Proc Natl. Acad. Sci. USA. 87:3768.
51. Fikrig, E., S.W. Barthold, F.S. Kantor, and R.A. Flavell. 1990. Protection of mice against Lyme disease agent by immunizing with recombinant OspA. Science (Wash. DC). 250:553.
52. Fikrig, E., S.W. Barthold, N. Marcantonio, K. Deponte, F.S. Kantor, and R.A. Flavell. 1992. Roles of OspA, OspB, and flagellin in protective immunity to Lyme borreliosis in laboratory mice. Infect. Immun. 60:657.
53. Simon, M.M., U.E. Schaible, M.D. Kramer, C. Eckerskorn, C. Musetanu, H.K. Müller-Hermelink, and R. Wallich. 1991. Recombinant outer surface protein A from Borrelia burgdorferi induces antibodies protective against spirochetal infection in mice. J. Infect Dis. 164:123.
54. Telford, S.R. Ill, E. Fikrig, S.W. Barthold, L.R.T. Brunet, A. Spielman, and R.A. Flavell. 1993. Protection against antigen- tically variable Borrelia burgdorferi conferred by recombinant vac¬ cines. J. Exp. Med. 178:755.
55. Stover, C.K., G.P. Bansal, M.S. Hanson, J.E. Burlein, S.R. Palaszynski, J.F. Young, S. Koenig, D.B. Young, A. Sadzienne, and A.G. Barbour. 1993. Protective immunity elicited by recom¬ binant Bacille Calmette-Guerin (BCG) expressing outer sur¬ face protein A (OspA) lipoprotein: a cand idate Lyme disease vaccine. J. Exp Med. 178:197.
56. Fikrig, E., S.R. Telford III., S.W. Barthold, F.S. Kantor, A. Spielman, and R.A. Flavell. 1992. Elimination of Borrelia bur dorferi from vector ticks feeding on immunized mice. Proc Natl. Acad. Sci. USA. 89:5418.
57. McIntosh, K., and J.M. Fishaut. 1980. Immunopathologic mechanisms in lower respiratory tract disease of infants due to respiratory syncytial virus. Prog. Med. Virol. 26:94.
58. Zinkernagel, R.M., and P.C. Doherty. 1979. MHC-restricted cytotoxic T-cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction- specificity, function, and responsiveness. Adv. Immunol. 27:51.
59. Alwan, W.H., W.J. Kozlowska, and P.J.M. Openshaw. 1994. Distinct types of lung disease caused by functional subsets of antiviral T cells. J. Exp Med. 179:81.
60. Gerety, S.J., M.K. Rundell, M.C. Dal Canto, and S.D. Miller. 1994. Class II-restricted T cell responses in Theiler’s murine encephalomyelitis virus-induced demyelinating disease VI. Potentiation of demyelination with and characterization of an immunopathologic T cell line specific for an immunodominant VP2 epitope. J. Immunol. 152:919.
61. Ohashi, P.S., S. Oehlen, K. Buerri, H. Pricher, C.T. Ohashi, B. Odermatt, B. Malissen, R.M. Zinkernagel, and H. Hen- gartner. 1991. Ablation of “tolerance” and induction of diabetes by virus infection in viral antigen transgenic mice. Cell. 65:305.
62. Oldstone, M.B.A., M. Nerenberg, P. Southern, J. Price, and H. Lewicki. 1991. Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of anti-self (virus) immune response. Cell. 65:319.
63. Janeway, C.A., Jr., and K. Bottomly. 1994. Signals and signs for lymphocyte responses. Cell. 76:275.