Mycoplasma superantigen is a CDR3-dependent ligand for the T cell antigen receptor

Journal of Experimental Medicine

Volumn 187, Issue 3, 1998, Pages 319-327

  Hodtsev, Andrew S ^a   Choi, Yongwon ^b   Spanopoulou, Eugenia ^c   Posnett, David N ^d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SUPERANTIGEN; T LYMPHOCYTE ANTIGEN;

ANTIGEN ANTIBODY COMPLEX; ANTIGEN RECOGNITION; ARTICLE; AUTOIMMUNITY; HUMAN; HUMAN CELL; LIGAND BINDING; MAJOR HISTOCOMPATIBILITY COMPLEX; MYCOPLASMA ARTHRITIDIS; PRIORITY JOURNAL; RECEPTOR BINDING; T LYMPHOCYTE;

ANTIGENS, BACTERIAL; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; CLONE CELLS; CLONING, MOLECULAR; HUMANS; LIGANDS; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTAGENESIS; MYCOPLASMA; PEPTIDES; RECEPTORS, ANTIGEN, T-CELL; SEQUENCE ALIGNMENT; SUPERANTIGENS; TRANSFECTION;

EID: 0032472864     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.3.319     Document Type: Article

References (67)

1. Garboczi, D.N., P. Ghosh, U. Ultz, Q.R. Fan, W.E. Biddison, and D.C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature. 384:134-141.
2. Garcia, K.C., M. Degano, R.L. Stanfield, A. Brunmark, M.R. Jackson, P.A. Peterson, L. Teyton, and I.A. Wilson. 1996. An αβ T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science. 274:209-219.
3. Schatz, D.G., M.A. Oettinger, and M.S. Schlissel. 1992. V(D)J recombination: molecular biology and regulation. Annu. Rev. Immunol. 10:359-383.
4. Janeway, C.A., J. Yagi, P.C. Conrad, M.E. Katz, B. Jones, S. Vroegop, and S. Buxser. 1989. T-cell responses to Mls and to bacterial proteins that mimic its behavior. Immunol. Rev. 107: 61-88.
5. Marrack, P., and J. Kappler. 1990. The staphylococcal enterotoxins and their relatives. Science. 248:705-711.
6. Acha-Orbea, H., and H.R. MacDonald. 1995. Superantigens of mouse mammary tumor virus. Annu. Rev. Immunol. 13: 459-486.
7. Choi, Y., J.W. Kappler, and P. Marrack. 1991. A superantigen encoded in the open reading frame of the 3′ long terminal repeat of mouse mammary tumour virus. Nature. 350: 203-207.
8. Lafon, M., M. Lafage, A. Martinez-Arends, R. Ramirez, F. Vuillier, D. Charron, V. Lotteau, and D. Scott-Algara. 1992. Evidence in humans of a viral superantigen. Nature. 338:507-510.
9. + cells in vivo after exposure to the superantigenic lectin Urtica dioica agglutinin. J. Immunol. 54:2600-2611.
10. Golovkina, T., A.V. Chervonsky, J.P. Dudley, and S.R. Ross. 1992. Transgenic mouse mammary tumor virus superantigen expression prevents viral infection. Cell. 69:637-645.
11. Held, W., G.A. Waanders, A.N. Shakhov, L. Scarpellino, H. Acha-Orbea, and H.R. MacDonald. 1993. Superantigen-induced immune stimulation amplifies mouse mammary tumor virus infection and allows virus transmission. Cell. 74: 529-540.
12. Conrad, B., E. Weidmann, G. Trucco, W.A. Rudert, R. Behboo, C. Ricordi, H. Rodriques-Rilo, D. Finegold, and M. Trucco. 1994. Evidence for superantigen involvement in insulin-dependent diabetes mellitus aetiology. Nature. 371:351-355.
13. Conrad, B., R.N. Weissmahr, J. Boni, R. Arcari, J. Schupbach, and B. Mach. 1997. A human endogenous retroviral superantigen as candidate autoimmune gene in type I diabetes. Cell. 90:303-313.
14. Cole, B.C., K.L. Knudtson, A. Oliphant, A.D. Sawitzke, A. Pole, M. Manohar, L.S. Benson, E. Ahmed, and C.L. Atkin. 1996. The sequence of the Mycoplasma arthritidis superantigen, MAM: identification of functional domains and comparison with microbial superantigens and plant lectin mitogens. J. Exp. Med. 183:1105-1110.
15. Cole, B., and C. Atkin. 1991. The Mycoplasma arthritidis T-cell mitogen, MAM: a model superantigen. Immunol. Today. 12: 271-276.
16. Crow, M.K., G. Zagon, Z. Chu, B. Ravina, J.R. Tumang, B.C. Cole, and S.M. Friedman. 1992. Human B cell differentiation induced by microbial superantigens: unselected peripheral blood lymphocytes secrete polyclonal immunoglobulin in response to Mycoplasma arthritides mitogen. Autoimmunity. 14:23-32.
17. Matthes, N., H. Schrezenmeier, J. Hemfeld, S. Fleischer, B. Malissen, H. Kirchner, and B. Fleischer. 1988. Clonal analysis of human cell activation by the Mycoplasma arthritidis mitogen (MAS). Eur. J. Immunol. 18:1733-1737.
18. Bhardwaj, N., A.S. Hodtsev, A. Nisanian, S. Kabak, S.M. Friedman, B.C. Cole, and D.N. Posnett. 1994. Human T-cell responses to Mycoplasma arthritidis-derived superantigen. Infect. Immun. 62:135-144.
19. Atkin, C.L., S. Wei, and B.C. Cole. 1994. The Mycoplasma arthritidis superantigen MAM: purification and identification of an active peptide. Infect. Immun. 62:5367-5375.
20. Genevee, C., A. Diu, J. Nierat, A. Caignard, P.Y. Dietrich, L. Ferradini, S. Roman-Roman, F. Triebel, and T. Hercend. 1992. An experimentally validated panel of subfamily-specific oligonucleotide primers (Vα1-w29/Vβ1-w24) for the study of human T cell receptor variable V gene segment usage by polymerase chain reaction. Eur. J. Immunol. 22:1261-1269.
21. Friedman, S.M., M.K. Crow, J.R. Tumang, M. Tumang, Y. Xu, A.S. Hodtsev, B.C. Cole, and D.N. Posnett. 1991. Characterisation of human T cells reactive with the Mycoplasma arthritidis-derived superantigen (MAM): generation of a monoclonal antibody against Vβ17, the T cell receptor gene product expressed by a large fraction of MAM-reactive human T cells. J. Exp. Med. 174:891-900.
22. Morgenstern, J.P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids. Res. 18:3587-3596.
23. Ho, S.N., H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:51-59.
24. Pear, W.S., G.P. Nolan, M.L. Scott, and D. Baltimore. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA. 90:8392-8396.
25. Choi, Y., A. Herman, D. DiGusto, T. Wade, P. Marrack, and J. Kappler. 1990. Residues of the variable region of the T-cell-receptor β-chain that interact with S. aureus toxin superantigens. Nature. 346:471-473.
26. Saito, H., D.M. Kranz, Y. Takagaki, A.C. Hayday, H. Eisen, and S. Tonegawa. 1984. A third rearranged and expressed gene in a clone of cytotoxic T lymphocytes. Nature. 312:36-40.
27. Kubo, R.T., W. Born, J.W. Kappler, and M. Pigeon. 1989. Characterization of a monoclonal antibody which detects all murine αβ T cell receptors. J. Immunol. 142:2736-2742.
28. Mosmann, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65:55-63.
29. a superantigen-specific T cell responses. J. Exp. Med. 175:1405-1408.
30. Waanders, G.A., A.R. Lussow, and H.R. Macdonald. 1993. Skewed T cell receptor Vα repertoire among superantigen reactive murine T cells. Int. Immunol. 5:55-60.
31. Woodland, D.L., and M.A. Blackman. 1993. How do T-cell receptors, MHC molecules and superantigens get together? Immunol. Today. 14:208-212.
32. Herman, A., G. Croteau, R.P. Sekaly, J. Kappler, and P. Marrack. 1990. HLA-DR alleles differ in their ability to present staphylococcal enterotoxins to T cells. J. Exp. Med. 172:709-718.
33. Thibodeau, J., I. Cloutier, P.M. Lavoie, N. Labrecque, W. Mourad, T. Jardetzky, and R.P. Sekaly. 1994. Subsets of HLA-DR1 molecules defined by SEB and TSST-1 binding. Science. 266:1874-1878.
34. Engel, I., and S.M. Hedrick. 1988. Site-directed mutations in the VDJ junctional region of a T cell receptor β chain cause changes in antigenic peptide recognition. Cell. 54:473-184.
35. Jorgensen, J.L., U. Esser, B. Fazekas de St. Groth, P.A. Reay, and M.M. Davis. 1992. Mapping T-cell receptor-peptide contacts by variant peptide immunization of single-chain transgenics. Nature. 355:224-230.
36. Bentley, G.A., G. Boulot, K. Karjalainen, and R.A. Mariuzza. 1995. Crystal structure of the β chain of a T cell antigen receptor. Science. 267:1984-1987.
37. Chothia, C., D.R. Boswell, and A.M. Lesk. 1988. The outline structure of the T cell αβ receptor. EMBO (Eur. Mol. Biol. Organ.) J. 12:3745-3755.
38. Fields, B.A., E.L. Malchiodi, H. Li, X. Ysern, C.V. Stauffacher, P.M. Schlievert, K. Karjalainen, and R.A. Mariuzza. 1996. Crystal structure of a T-cell receptor β-chain complexed with a superantigen. Nature. 384:188-192.
39. Danska, J.S., A.M. Livingstone, V. Paragas, T. Ishihara, and C.G. Fathman. 1990. The presumptive CDR3 regions of both T cell receptor α and β chains determine T cell specificity for myoglobin peptides. J. Exp. Med. 172:27-33.
40. k determinant. Single conservative amino acid changes in the complementarity-determining region 3 dramatically alter antigen fine specificity. J. Immunol. 157:2291-2298.
41. Bogue, M., S. Candeias, C. Benoist, and D. Mathis. 1991. A special repertoire of a α:β T cells in neonatal mice. EMBO (Eur. Mol. Biol. Organ.) J. 10:3647-3654.
42. Gilfillan, S., A. Dietrich, M. Lemeur, C. Benoist, and D. Mathis. 1993. Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science. 261:1175-1178.
43. Komori, T., A. Okado, V. Stewart, and F. Alt. 1993. Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science. 261:1171-1175.
44. Gilfillan, S., M. Bachmann, S. Trembleau, L. Adorini, U. Kalinke, R. Zinkernagel, C. Benoist, and D. Mathis. 1995. Efficient immune responses in mice lacking N-region diversity. Eur. J. Immunol. 25:3115-3122.
45. Gavin, M.A., and M.J. Bevan. 1995. Increased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity. 3:793-800.
46. Alam, S.M., P.J. Travers, J.L. Wung, W. Nasholds, S. Redpath, S.C. Jameson, and N.R. Gascoigne. 1996. T-cell-receptor affinity and thymocyte positive selection. Nature. 381:616-620.
47. Reich, Z., J.J. Boniface, D.S. Lyons, N. Borochov, E.J. Wachtel, and M.M. Davis. 1997. Ligand-specific oligomerization of T-cell receptor molecules. Nature. 387:617-620.
48. + cells. J. Exp. Med. 174:989-1000.
49. Moss, P.A.H., and J.I. Bell. 1995. Sequence analysis of the human αβ T-cell receptor CDR3 region. Immunogenetics. 42: 10-18.
50. Li, Y., G.R. Sun, J. Tumang, M.K. Crow, and S.M. Friedman. 1994. CDR3 sequence motifs shared by oligoclonal rheumatoid arthritis synovial T cells. Evidence for an antigen-driven response. J. Clin. Invest. 94:2525-2531.
51. Li, Y., G.-R. Sun, Q. Zheng, D.H. Yoo, N. Bhardwaj, D.N. Posnett, M.K. Crow, and S.M. Friedman. 1996. Allelic variants of human TCR BV17S1 defined by restriction fragment length polymorphism, single strand conformation polymorphism and amplification refractory mutation system analyses. Hum. Immunol. 49:8585-8595.
52. + human peripheral blood T lymphocytes. Int. Immunol. 4:643-650.
53. Woodland, D.L., H.P. Smith, S. Surman, P. Le, R. Wen, and M.A. Blackman. 1993. Major histocompatibility complex-specific recognition of Mls-1 is mediated by multiple elements of the T cell receptor. J. Exp. Med. 177:433-442.
54. + T cells in Mls-1a mice. J. Immunol. 155:4171-4178.
55. Musette, P., A. Galelli, P. Truffa-Bachi, W. Peumans, P. Kourilsky, and G. Gachelin. 1996. The Jβ segment of the T cell receptor contributes to the Vβ-specific T cell expansion caused by staphylococcal enterotoxin B and Urtica dioica superantigens. Eur. J. Immunol. 26:618-622.
56. Howell, M.D., J.P. Diveley, K.A. Lundeen, A. Esty, S.T. Winters, D.J. Carlo, and S.W. Brostoff. 1991. Limited T-cell receptor β-chain heterogeneity among interleukin 2 receptor-positive synovial T cells suggests a role for superantigen in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA. 88:10921-10925.
57. Lim, A., A. Toubert, C. Pannetier, M. Dougados, D. Charron, P. Kourilsky, and J. Even. 1996. Spread of clonal T-cell expansions in rheumatoid arthritis patients. Hum. Immunol. 48:77-83.
58. Kouskoff, V., A.-S. Korganow, V. Duchatelle, C. Degott, C. Benoist, and D. Mathis. 1996. Organ-specific disease provoked by systemic autoimmunity. Cell. 87:811-822.
59. Gregersen, P.K., J. Silver, and R.J. Winchester. 1987. The shared epitope hypothesis: an approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis. Rheum. 30:1205-1213.
60. Nepom, G.T., and H. Erlich. 1991. MHC class-II molecules and autoimmunity. Annu. Rev. Immunol. 9:493-525.
61. Weyand, C.M., T.G. McCarthy, and J.J. Goronzy. 1995. Correlation between disease phenotype and genetic heterogeneity in rheumatoid arthritis. J. Clin. Invest. 95:2120-2126.
62. Wucherpfennig, K.W., and J.L. Strominger. 1995. Selective binding of self peptides to disease-associated major histocompatibility complex (MHC) molecules: a mechanism for MHC-linked susceptibility to human autoimmune diseases. J. Exp. Med. 181:1597-601.
63. Arden, B., S.P. Clark, D. Kabelitz, and T.W. Mak. 1995. Human T-cell receptor variable gene segment families. Immunogenetics. 42:455-500.
64. Pullen, A.M., T. Wade, P. Marrack, and J.W. Kappler. 1990. Identification of the region of T cell receptor β chain that interacts with the self-superantigen Mls-1a. Cell. 61:1365-1374.
65. Bellio, M., Y.C. Lone, O. Calle-Martin, B. Malissen, J.P. Abastado, and P. Kourilsky. 1994. The Vβ complementarity determining region 1 of a major histocompatibility complex (MHC) class I-restricted T cell receptor is involved in the recognition of peptide/MHC I and superantigen/MHC II complex. J. Exp. Med. 179:1087-1097.
66. Liao, L., A. Mannescu, A. Molano, C. Ciurli, R.-P. Secaly, J.D. Fraser, A. Popowicz, and D.N. Posnett. 1996. TCR binding differs for a bacterial superantigen (SEE) and a viral superantigen (Mtv-9). J. Exp. Med. 184:1-12.
67. Hong, S.-C., G. Waterbury, and C.A. Janeway. 1996. Different superantigens interact with distinct sites in the Vβ domain of a single T cell receptor. J. Exp. Med. 183:1437-1446.