Split tolerance in a novel transgenic model of autoimmune myasthenia gravis

Journal of Immunology

Volumn 169, Issue 11, 2002, Pages 6570-6579

  Stacy, Sue ^a   Gelb, Bruce E ^a   Koop, Barbara A ^c,e   Windle, Jolene J ^c,f   Wall, Katherine A ^d   Krolick, Keith A ^a   Infante, Anthony J ^b   Kraig, Ellen ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b University of Texas Health Science Center   (United States)

^c University of Texas Health Science Center at San Antonio   (United States)

^d MEDICAL COLLEGE OF OHIO   (United States)

^e UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^f VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CHOLINERGIC RECEPTOR ANTIBODY; CHOLINERGIC RECEPTOR; COMPLEMENTARY DNA; EPITOPE; PROTEIN SUBUNIT;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; MOUSE; MUSCLE WEAKNESS; MYASTHENIA GRAVIS; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TORPEDO CALIFORNICA; TRANSGENIC MOUSE; ANIMAL; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; NUCLEOTIDE SEQUENCE; TORPEDO;

ANIMALS; AUTOANTIGENS; B-LYMPHOCYTES; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA, COMPLEMENTARY; HUMANS; IMMUNE TOLERANCE; IMMUNIZATION; IMMUNODOMINANT EPITOPES; MICE; MICE, TRANSGENIC; MYASTHENIA GRAVIS, AUTOIMMUNE, EXPERIMENTAL; PROTEIN SUBUNITS; RECEPTORS, CHOLINERGIC; T-LYMPHOCYTES; TORPEDO;

EID: 0036884943     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.11.6570     Document Type: Article

References (62)

1. Brostoff, J., G. K. Scadding, D. Male, and I. M. Roit. 1991. Autoimmune diseases: a general introduction. In Clinical Immunology. Gower Medical Publishing, New York, p. 4.1.
2. Lindstrom, J., D. Shelton, and Y. Fujii. 1988. Myasthenia gravis. Adv. Immunol. 42:233.
3. Compston, D. A., A. Vincent, J. Newsom-Davis, and J. R. Batchelor. 1980. Clinical, pathological. HLA antigen and immunological evidence for disease heterogeneity in myasthenia gravis. Brain 103:579.
4. Christadoss, P., J. M. Lindstrom, R. W. Melvold, and N. Talal. 1985. Mutation at I-A β chain prevents experimental autoimmune myasthenia gravis. Immunogenetics 21:33.
5. Graus, Y. M., and M. H. De Baets. 1993. Myasthenia gravis: an autoimmune response against the acetylcholine receptor. Immunol. Res. 12:78.
6. Atassi, M. Z. 1994. Molecular recognition of acetylcholine receptor: recognition by α-neurotoxins and by immune and autoimmune responses and manipulation of the responses. Adv. Neuroimmunol. 4:403.
7. b binding, self-nonself discrimination, and TCR antagonism. J. Immunol. 152:4526.
8. Wang, Z-Y. D. K. Okita, J. F. Howard, Jr., and B. M. Conti-Fine. 1997. Th1 epitope repertoire on the α subunit of human muscle acetylcholine receptor in myasthenia gravis. Neurology 48:1643.
9. + T-epitope repertoire on the human acetylcholine receptor α subunit in severe myasthenia gravis: a study with synthetic peptides. Neurology 42:1092.
10. Hawke, S., H. Matsuo, M. Nicolle, G. Malcherek, A. Melms, and N. Willcox. 1996. Autoimmune T cells in myasthenia gravis: heterogeneity and potential for specific immunotargeting. Immunol. Today 17:307.
11. Beeson, D., A. P. Bond, L. Corlett, S. J. Curnow, M. E. Hill, L. W. Jacobson, C. MacLennan, A. Meager, A. M. Moody, P. Moss, et al. 1998. Thymus, thymoma, and specific T cells in myasthenia gravis. Ann. NY Acad. Sci. 841:371.
12. Infante, A. J., P. D. Infante, C. E. Jackson, R. J. Barohn, J. Tami, E. Iturriaga, S. Talib, E. Kraig, K. Z. Clarkin, and K. A. Krolick. 1996. Evidence against chronic antigen-specific T lymphocyte activation in myasthenia gravis. J. Neurosci. Res. 45:492.
13. Hill, M., D. Beeson, P. Moss, L. Jacobson, A. Bond, L. Corlett, J. Newsom-Davis, A. Vincent, and N. Willcox. 1999. Early-onset myasthenia gravis: a recurring T-cell epitope in the adult-specific acetylcholine receptor epsilon subunit presented by the susceptibility allele HLA-DR52a. Ann. Neurol. 45:224.
14. Conti-Fine, B. M., D. Navaneetham, P. I. Karachunski, R. Raju, B. Diethelm-Okita, D. Okita, J. F. Howard, and Z. Y. Wang. 1998. T cell recognition of the acetylcholine receptor in myasthenia gravis. Ann. NY Acad. Sci. 841:283.
15. Infante, A. J., and E. Kraig. 1999. Myasthenia gravis and its animal model: T cell receptor expression in an antibody mediated autoimmune disease. Int. Rev. Immunol. 18:83.
16. Deitiker, P., T. Ashizawa, and M. Z. Atassi. 2000. Antigen mimicry in autoimmune disease: can immune responses to microbial antigens that mimic acetylcholine receptor act as initial triggers of myasthenia gravis? Hum. Immunol. 61:255.
17. Gebhardt, B. M. 2000. Evidence for antigenic cross-reactivity between herpes virus and the acetylcholine receptor. J. Neuroimmunol. 105:145.
18. Schwimmbeck, P. L., T. Dyrberg, D. B. Drachman, and M. B. Oldstone. 1989. Molecular mimicry and myasthenia gravis: an autoantigenic site of the acetylcholine receptor α-subunit that has biologic activity and reacts immunochemically with herpes simplex virus. J. Clin. Invest. 84:1174.
19. Berman, P. W., and J. Patrick. 1980. Experimental myasthenia gravis: a murine system. J. Exp. Med. 151:204.
20. Drachman, D. B., K. R. McIntosh, and B. Yang. 1998. Factors that determine the severity of experimental myasthenia gravis. Ann. NY Acad. Sci. 841:262.
21. Oshima, M., A. R. Pachner, and M. Z. Atassi. 1994. Profile of the regions of acetylcholine receptor α chain recognized by T-lymphocytes and by antibodies in EAMG-susceptible and non-susceptible mouse strains after different periods of immunization with the receptor. Mol. Immunol. 31:833.
22. Bellone, M., N. Ostlie, S. Lei, and B. M. Conti-Tronconi. 1991. Experimental myasthenia gravis in congenic mice: sequence mapping and H-2 restriction of T helper epitopes on the α subunits of Torpedo californica and murine acetylcholine receptors. Eur. J. Immunol. 21:2303.
23. Infante. A. J., P. A. Thompson, K. A. Krolick, and K. A. Wall. 1991. Determinant selection in murine experimental autoimmune myasthenia gravis: effect of the bm12 mutation on T cell recognition of acetylcholine receptor epitopes. J. Immunol. 146:2977.
24. Infante, A. J., H. Levcovitz, V. Gordon, K. A. Wall, P. A. Thompson, and K. A. Krolick. 1992. Preferential use of a T cell receptor Vβ gene by acetylcholine receptor reactive T cells from myasthenia gravis-susceptible mice. J. Immunol. 148:3385.
25. Kraig, E., J. L. Pierce, K. Z. Clarkin, N. E. Standifer, P. Currier, K. A. Wall, and A. J. Infante. 1996. Restricted T cell receptor repertoire for acetylcholine receptor in murine myasthenia gravis. J. Neuroimmunol. 71:87.
26. Yang, B., K. R. McIntosh, and D. B. Drachman. 1998. How subtle differences in MHC class II affect the severity of experimental myasthenia gravis. Clin. Immunol. Immunopathol. 86:45.
27. Malmstrom, V., J. Backlund, L. Jansson, J. Kihlberg, and R. Holmdahl. 2000. T cells that are naturally tolerant to cartilage-derived type II collagen are involved in the development of collagen-induced arthritis. Arthritis Res. 2:315.
28. Antonia, S. J., T. Geiger, J. Miller, and R. A. Flavell. 1995. Mechanisms of immune tolerance induction through the thymic expression of a peripheral tissue-specific protein. Int. Immunol. 7:715.
29. Steinhoff, U., K. J. Maloy, C. Burkhart, A. J. Clark, T. Rulicke, H. Hengartner, and R. M. Zinkernagel. 1999. Variable immune response against a developmentally regulated self-antigen. J. Autoimmun. 12:27.
30. Salmon, A. M., C. Bruand, A. Cardona, J. P. Changeux, and S. Berrih-Aknin. 1998. An acetylcholine receptor α subunit promoter confers intrathymic expression in transgenic mice: implications for tolerance of a transgenic self-antigen and for autoreactivity in myasthenia gravis. J. Clin. Invest. 101:2340.
31. Akkaraju, S., W. Y. Ho, D. Leong, K. Canaan, M. M. Davis, and C. C. Goodnow. 1997. A range of CD4 T cell tolerance: partial inactivation to organ-specific antigen allows nondestructive thyroiditis or insulitis. Immunity 7:255.
32. Ridgway, W. M., M. Fasso, and C. G. Fathman. 1999. A new look at MHC and autoimmune disease. Science 284:749.
33. Howes, K. A., N. Ransom, D. S. Papermaster, J. G. Lasudry, D. M. Albert, and J. J. Windle. 1994. Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes Dev. 8:1300.
34. Claudio, T., H. L. Paulson, D. Hartman, S. Sine, and F. J. Sigworth. 1988. Establishing a stable expression system for studies of acetylcholine receptors. Curr. Top. Membr. Transport 33:219.
35. Sanes, J. R., Y. R. Johnson, P. T. Kotzbauer, J. Mudd, T. Hanley, J. C. Martinou, and J. P. Merlie. 1991. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development 113:1181.
36. Klarsfeld, A., P. Daubas, B. Bourachot, and J. P. Changeux. 1987. A 5′-flanking region of the chicken acetylcholine receptor α-subunit gene confers tissue specificity and developmental control of expression in transfected cells. Mol. Cell. Biol. 7:951.
37. Hogan, B., T. Beddington, F. Costantini, and E. Lacy. 1994. Production of transgenic mice. In Manipulating the Mouse Embryo. Cold Spring Harbor Lab. Press. Cold Spring Harbor, NY, p. 217.
38. Kronenberg, M., E. Kraig, G. Siu, J. A. Kapp, J. Kappler, P. Marrack, C. W. Pierce, and L. Hood. 1983. Three T cell hybridomas do not contain detectable heavy chain variable gene transcripts. J. Exp. Med. 158:210.
39. Kawasaki, E. S. 1990. Amplification of RNA. In PCR Protocols. M. A. Innis, D. H. Gelfrand, J. J. Sninsky, and T. J. White, eds. Academic, San Diego, CA, p. 21.
40. Olsberg, C. A., L. C. Maxwell, T. M. Mikiten, and K. A. Krolick. 1987. Analysis of contractile properties of muscles from rats immunized with purified acetylcholine receptor. J. Neuroimmunol. 14:253.
41. van Kimmenade, A., M. W. Bond, J. H. Schumacher, C. Laquoi, and R. A. Kastelein. 1988. Expression, renaturation and purification of recombinant human interleukin 4 from Escherichia coli. Eur. J. Biochem. 173:109.
42. Schrattenholz A., S. Pfeiffer, V. Pejovic, R. Rudolph, J. Godovac-Zimmermann, and A. Maelicke. 1998. Expression and renaturation of the N-terminal extracellular domain of Torpedo nicotinic acetylcholine receptor α-subunit. J. Biol. Chem. 273:32393.
43. Sitaraman, S., D. W. Metzger, R. J. Belloto, Jr., A. J. Infante, and K. A. Wall. 2000. Interleukin-12 enhances clinical experimental autoimmune myasthenia gravis in susceptible but not resistant mice. J. Neuroimmunol. 107:73.
44. Lefkovits, I., and H. Waldmann. 1999. Limiting Dilution Analysis of Cells in the Immune System, with LDA software developed by P. Rovensky, J. Rubes, and T. Beran. Oxford Univ. Press, New York, p. 123.
45. Zoda, T. E., and K. A. Krolick. 1993. Antigen presentation and T cell specificity repertoire in determining responsiveness to an epitope important in experimental autoimmune myasthenia gravis. J. Neuroimmunol. 43:131.
46. Mohan, S., R. J. Barohn, C. E. Jackson, and K. A. Krolick. 1994. Evaluation of myosin-reactive antibodies from a panel of myasthenia gravis patients. Clin. Immunol. Immunopathol. 70:266.
47. Lindstrom, J., J. Merlie, and G. Yogeeswaran. 1979. Biochemical properties of acetylcholine receptor subunits from Torpedo californica. Biochemistry 18:4465.
48. Christadoss, P., M. Shenoy, M. Oshima, and M. Z. Atassi. 1994. Suppression of experimental autoimmune myasthenia gravis by epitope-specific neonatal tolerance. Adv. Exp. Med. Biol. 347:65.
49. Loutrari, H., S. J. Tzartos, and T. Claudio. 1992. Use of Torpedo-mouse hybrid acetylcholine receptors reveals immunodominance of the α subunit in myasthenia gravis antisera. Eur. J. Immunol. 22:2949.
50. Vanderlugt, C. L., K. L. Neville, K. M. Nikcevich, T. N. Eagar, J. A. Bluestone, and S. D. Miller. 2000. Pathologic role and temporal appearance of newly emerging autoepitopes in relapsing experimental autoimmune encephalomyelitis. J. Immunol. 164:670.
51. Moiola, L., F. Galbiati, G. Martino, S. Amadio, E. Brambilla, G. Comi, A. Vincent, L. M. Grimaldi, and L. Adorini. 1998. IL-12 is involved in the induction of experimental autoimmune myasthenia gravis, an antibody-mediated disease. Eur. J. Immunol. 28:2487.
52. MacLennan, C. A., D. Beeson, N. Willcox, A. Vincent, and J. Newsom-Davis. 1998. Muscle nicotinic acetylcholine receptor mRNA expression in hyperplastic and neoplastic myasthenia gravis thymus. Ann. NY Acad. Sci. 841:407.
53. Navaneetham, D., A. S. Penn, J. F. J. Howard, and B. M. Conti-Fine. 2001. Human thymuses express incomplete sets of muscle acetylcholine receptor subunit transcripts that seldom include the δ subunit. Muscle Nerve 24:203.
54. Wakkach, A., T. Guyon, C. Bruand, S. Tzartos, S. Cohen-Kaminsky, and S. Berrih-Aknin. 1996. Expression of acetylcholine receptor genes in human thymic epithelial cells: implications for myasthenia gravis. J. Immunol. 157:3752.
55. Zoda, T. E., K. Brandon, and K. A. Krolick. 1995. Neonatal tolerance to an immunodominant T cell reactivity does not confer resistance to EAMG induction in Lewis rats. J. Neuroimmunol. 57:35.
56. Thompson, P. A., R. McAtee, A. J. Infante, P. Currier, W. Beninati, and K. A. Krolick. 1994. Vβ-specific immunotoxin selectively kills acetylcholine receptor-reactive T lymphocytes from mice with experimental autoimmune myasthenia gravis. Int. Immunol. 6:1807.
57. Yeh, T. M., and K. A. Krolick. 1987. Influence of T cell specificity on the heterogeneity and disease-causing capability of antibody against the acetylcholine receptor. J. Neuroimmunol. 17:17.
58. Drachman, D. B., R. N. Adams, L. F. Josifek, and S. G. Self. 1982. Functional activities of autoantibodies to acetylcholine receptors and the clinical severity of myasthenia gravis. N. Engl. J. Med. 307:769.
59. Stegall, T., and K. A. Krolick. 2000. A monoclonal Lewis rat myocyte line that responds to interferon-γ: responsiveness with the potential to influence subsequent interactions with the immune system. Clin. Immunol. 94:125.
60. Curnow, J., L. Corlett, N. Willcox, and A. Vincent. 2001. Presentation by myoblasts of an epitope from endogenous acetylcholine receptor indicates a potential role in the spreading of the immune response. J. Neuroimmunol. 115:127.
61. Balasa, B., and N. Sarvetnick. 2000. Is pathogenic humoral autoimmunity a Th1 response? Lessons from (for) myasthenia gravis. Immunol. Today 21:19.
62. Falcone, M., B. Yeung, L. Tucker, E. Rodriquez, T. Krahl, and N. Sarvetnick. 2001. IL-4 triggers autoimmune diabetes by increasing self-antigen presentation within the pancreatic islets. Clin. Immunol. 98:190.