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Superantigen-Mediated Lethal Shock: The Functional State of Ligand-Reactive T Cells

  • K. Heeg
  • T. Miethke
  • H. Wagner
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 216)

Abstract

A group of bacterial and viral proteins has been termed superantigens (SAg) because of their unique mechanisms to interact with antigen-presenting cells (APC) and T lymphocytes (Herman et al. 1991a; Marrack and Kappler 1990; Herrmann and MacDonald 1991; Acha-Orbea et al. 1993). SAg are comprised of bacterial exoproducts including the staphylococcal enterotoxins, proteins encoded by viral genomes, and retroviral products such as those of open reading frame region encoded SAg of mouse mammary tumor viruses (Table 1 ; Mac-Donald et al. 1988; Marrack et al. 1991,1993; Janeway et al. 1989; Acha-Orbea et al. 1993). All SAg share the distinctive ability to bind to MHC class II molecules as intact molecules, thus bypassing rate-limiting steps during normal antigen processing, including antigen uptake, antigen degradation, and internal binding as peptide fragment to the antigen-presenting groove of class II MHC molecules of APC (Carlsson et al. 1988; Mollick et al. 1989; Fleischer and Schrezenmeier 1988; Torres et al. 1993; Thibodeau et al. 1994; Mottershead et al, 1995). SAg bind directly to regions of the class II molecule that are outside the physiological MHC haplotype-restricted antigen-binding groove (Fig. 1; Dellabona et al. 1990; Herman et al. 1991b; Jardetzky et al. 1994). The SAg binding region seems to be conserved within various MHC haplotypes of mammalian species since SAg bind to murine and rat as well as to human class II molecules (Herrmann and MacDonald 1991; Fraser 1989).

Keywords

Mouse Mammary Tumor Virus Staphylococcal Enterotoxin Clonal Deletion Cell Shock Lethal Shock 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Acha-Orbea H, Held W, Waanders GA, Shakhov AN, Scarpellino L, Lees RK, MacDonald HR (1993) Exogenous and endogenous mouse mammary tumor virus superantigens. Immunol Rev 131: 5–25.PubMedCrossRefGoogle Scholar
  2. Arnold B, Schönrich G, Hämmerling GJ (1993) Multiple levels of peripheral tolerance. Immunol Today 14: 12–14.PubMedCrossRefGoogle Scholar
  3. Aroeira LS, Williams O, Lozano EG, Martinez AC (1994) Age-dependent changes in the response to staphylococcal enterotoxin B. Int Immunol 6: 1555–1560.PubMedCrossRefGoogle Scholar
  4. Avery, AC, Markowitz, JS, Grusby MJ, Glimcher LH, Cantor H (1994) Activation of T cells by superantigen in class ll-negative mice. J Immunol 153: 4853–4861.PubMedGoogle Scholar
  5. Bandeira A, Mengel J, Burlen-Defranoux O, Coutinho A (1993) Proliferative T cell anergy to Mls-1a does not correlate with in vivo tolerance. Int Immunol 3: 923–931.CrossRefGoogle Scholar
  6. Baschieri S, Lees RK, Lussow AR, MacDonald HR (1993) Clonal anergy to staphylococcal enterotoxin B in vivo: selective effects on T cell subsets and lymphokines. Eur J Immunol 23: 2661–2666.PubMedCrossRefGoogle Scholar
  7. Bean AG, Freiberg RA, Andrade S, Menon S, Zlotnik A (1993) Interleukin 10 protects mice against staphylococcal enterotoxin B-induced lethal shock. Infect Immun 61: 4937–4939.PubMedGoogle Scholar
  8. Bhardwaj N, Young JW, Nisanian AJ, Baggers J, Steinman RM (1993) Small amounts of superantigen, when presented on dendritic cells, are sufficient to initiate T cell responses. J Exp Med 178: 633–642.PubMedCrossRefGoogle Scholar
  9. Bretscher P, Cohn M (1970) A theory of self-nonself discrimination. Science 169: 1042–1049.PubMedCrossRefGoogle Scholar
  10. Cantor H, Crump AL, Raman VK, Liu H, Markowitz JS, Grusby MJ, Glimcher LH (1993) Immunoregulatory effects of superantigens: interactions of staphylococcal enterotoxins with host MHC and non-MHC products. Immunol Rev 131: 27–42.PubMedCrossRefGoogle Scholar
  11. Carlsson R, Fischer H, Sjögren HO (1988) Binding of staphylococcal enterotoxin A to accessory cells is a requirement for its ability to activate human T cells. J Immunol 140: 2484–2488.PubMedGoogle Scholar
  12. Chatila T, Geha RS (1993) Signal transduction by microbial superantigens via MHC class II molecules. Immunol Rev 131: 43–59.PubMedCrossRefGoogle Scholar
  13. Chen ZW, Kou ZC, Shen L, Regan JD, Lord CI, Halloran M, Lee-Parritz D, Fultz PN, Letvin NL (1994) An acutely lethal simian immunodeficiency virus stimulates expansion of Vβ7-and Vβ14-expressing T lymphocytes. Proc Natl. Acad Sci USA 91: 7501–7505.PubMedCrossRefGoogle Scholar
  14. Choi YW, Herman A, DiGiusto D, Wade T, Marrack P, Kappler JW (1990) Residues of the variable region of the T-cell-receptor beta-chain that interact with S. aureus toxin superantigens. Nature 346: 471–473.PubMedCrossRefGoogle Scholar
  15. Cunha FQ, Assreuy J, Moss DW, Rees D, Leal LMC, Moncada S, Carrier M, O’Donnel CA, Liew FY (1994) Differential induction of nitric oxide synthase in various organs of the mouse during endotoxaemia: role of TNF-α and IL-1-β. Immunology 81: 211–215.PubMedGoogle Scholar
  16. D’Andrea A, Aste Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G (1993) Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041–1048.PubMedCrossRefGoogle Scholar
  17. Dadaglio G, Garcia S, Montagnier L, Gougeon ML (1994) Selective anergy of V beta 8(+) T cells in human immunodeficiency virus-infected individuals. J Exp Med 179: 413–424.PubMedCrossRefGoogle Scholar
  18. Daynes RA, Araneo BA, (1989) Contrasting effects of glucocorticoids on the capacity of T cells to produce the growth factors interleukin 2 and interleukin 4. Eur J Immunol 19: 2319–2325.PubMedCrossRefGoogle Scholar
  19. Dellabona P, Peccoud J, Kappler JW, Marrack P, Benoist C, Mathis D (1990) Superantigens interact with MHC class II molecules outside of the antigen groove. Cell 62: 1115–1121.PubMedCrossRefGoogle Scholar
  20. Ding L, Linsley PS, Huang LY, Germain RN, Shevach EM (1993) IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol 151:1224–1234.PubMedGoogle Scholar
  21. Enk AH, Angeloni VL, Udey MC, Katz SI (1993) Inhibition of Langerhans cell antigen-presenting function by IL-10. J Immunol 151: 2390–2398.PubMedGoogle Scholar
  22. Fleischer B, Schrezenmeier H (1988) T cell stimulation by staphylococcal enterotoxins. Clonally variable response and requirement for major histocompatibility complex class II molecules on accessory or target cells. J Exp Med 167: 1697–1707.PubMedCrossRefGoogle Scholar
  23. Fraser JD (1989) High-affinity binding of staphylococcal enterotoxins A and B to HLA-DR. Nature 339:221–223.PubMedCrossRefGoogle Scholar
  24. Freudenberg MA, Galanos C (1990) Bacterial lipopolysaccharides: structure, metabolism and mechanisms of action. Int Rev Immunol 6: 207–221.PubMedCrossRefGoogle Scholar
  25. Galanos C, Freudenberg MA, Reutter W (1979) Galactosamine-induced sensitization of the lethal effects of endotoxln. Proc Natl Acad Sci USA 76: 5939–5943.PubMedCrossRefGoogle Scholar
  26. Gaus H, Miethke T, Wagner H, Heeg K (1994) Superantigen-induced anergy of Vβ8+ CD4+ T cells induces functional but nonproliferative T cells in vivo. Immunology 83: 333–340.PubMedGoogle Scholar
  27. Glauser MP, Zanetti G, Baumgartner JD, Cohen J (1991) Septic shock: pathogenesis. Lancet 338:732–736.PubMedCrossRefGoogle Scholar
  28. Gonzalo JA, Moreno de Alboran I, Ales Martinez JE, Martinez C, Kroemer G (1992) Expansion and clonal deletion of peripheral T cells induced by bacterial superantigen is independent of the interleukin-2 pathway. Eur J Immunol 22: 1007–1011.PubMedCrossRefGoogle Scholar
  29. Gonzalo JA, Gonzalez-Garcia A, Kalland T, Hedlund G, Martinez AC, Kroemer G (1993a) Linomide, a novel immunomodulator that prevents death in four models of septic shock. Eur J Immunol 23:2372–2374.PubMedCrossRefGoogle Scholar
  30. Gonzalo JA, Gonzalez-Garcia A, Martinez C, Kroemer G (1993b) Glucocorticoid-mediated control of the activation and clonal deletion of peripheral T cells in vivo. J Exp Med 177: 1239–1246.PubMedCrossRefGoogle Scholar
  31. Grossman D, Cook RG, Sparrow JT, Mollick JA, Rich RR (1990) Dissociation of the stimulatory activities of staphylococcal enterotoxins for T cells and monocytes. J Exp Med 172: 1831–1841.PubMedCrossRefGoogle Scholar
  32. Hamad ARA, Herman A, Marrack P, Kappler JW (1994) Monoclonal antibodies defining functional sites on the toxin superantigen staphylococcal enterotoxin BJ Exp Med 180: 615–621.CrossRefGoogle Scholar
  33. Hayball JD, Robinson JH, O’Hehir RE, Verhoef A, Lamb JR, Lake RA (1994) Identification of two binding sites in staphylococcal enterotoxin B that confer specificity for TCR Vβ gene products. Int Immunol 6: 199–211.PubMedCrossRefGoogle Scholar
  34. Hämmerling GJ, Schönrich G, Momburg F, Auphan N, Malissen M, Malissen B, Schmitt-Verhulst AM, Arnold B (1991) Non-deletional mechanisms of peripheral and central tolerance: studies with transgenic mice with tissue-specific expression of a foreign MHC class I antigen. Immunol Rev 122:47–67.PubMedCrossRefGoogle Scholar
  35. Heeg K, Wagner H (1995) Induction of responsiveness in superantigen-induced anergic T cells: role of ligand density and costimulatory signals. J Immunol 155: 83–92.PubMedGoogle Scholar
  36. Heeg K, Bendings S, Miethke T, Wagner H (1993) Induction of unresponsiveness to the superantigen staphylococcal enterotoxin B: cyclosporin A resisitant split unresponsiveness unfolds in vivo without preceding clonal expansion. Int Immunol 5: 929–937.PubMedCrossRefGoogle Scholar
  37. Heeg K, Gaus H, Griese D, Bendigs S, Miethke T, Wagner H (1995) Superantigen-reactive T cells that display an anergic phenotype in vitro appear functional in vivo. Int Immunol 7: 105–114.PubMedCrossRefGoogle Scholar
  38. Herman A, Kappler JW, Marrack P, and Pullen AM (1991a) Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu Rev Immunol 9: 745–772.PubMedCrossRefGoogle Scholar
  39. Herman A, Labrecque N, Thibodeau J, Marrack P, Kappler JW, Sekaly RP (1991b) Identification of the staphylococcal enterotoxin A superantigen binding site in the beta 1 domain of the human histocompatibility antigen HLA-DR. Proc Natl Acad Sci USA 88: 9954–9958.PubMedCrossRefGoogle Scholar
  40. Herrmann T and MacDonald HR (1991) T cell recognition of superantigens. Curr Top Microbiol Immunol 174: 21–38.PubMedGoogle Scholar
  41. Herrmann T, Baschieri S, Lees RK, MacDonald HR (1992) In vivo responses of CD4+ and CD8+ cells to bacterial superantigens. Eur J Immunol 22: 1935–1938.PubMedCrossRefGoogle Scholar
  42. Huang L, Crispe IN (1993) Superantigen-driven peripheral deletion of T cells. Apoptosis occurs in cells that have lost the alpha/beta T cell receptor. J Immunol 151: 1844–1851.PubMedGoogle Scholar
  43. Irwin MJ, Hudson KR, Fraser JD, Gascoigne NRJ (1992) Enterotoxin residues determining T-cell receptor V beta binding specificity. Nature 359: 841–843.PubMedCrossRefGoogle Scholar
  44. Irwin MJ, Hudson KR, Ames KT, Fraser JD, Gascoigne NRJ (1993) T-cell receptor β-chain binding to enterotoxin superantigens. Immunol Rev 131: 61–78.PubMedCrossRefGoogle Scholar
  45. Janeway CA, Yagi J, Conrad PJ, Katz ME, Jones B, Vroegop S, Buxser S, (1989) T-cell responses to MIs and to bacterial proteins that mimic its behavior. Immunol Rev 107: 61–88.PubMedCrossRefGoogle Scholar
  46. Jardetzky TS, Brown JH, Gorga JC, Stern LJ, Urban RG, Chi Y, Stauffacher C, Strominger JL, Wiley DC (1994) Three-dimensional structure of a human class II histocompatibility molecule complexed with superantigen. Nature 368: 711–718.PubMedCrossRefGoogle Scholar
  47. Jiang H, Ware R, Stall A, Flaherty L, Chess L, Pernis B (1995) Murine CD8+ T cells that specifically delete autologous CD4+ T cells expressing Vβ8 TCR: a role of the Qa-1 molecule. Immunity 2:185–194.PubMedCrossRefGoogle Scholar
  48. Kappler JW, Kotzin BL, Herron L, Gelfand EW, Bigler RD, Boylston A, Carrel S, Posnett DN, Choi YW, Marrack P (1989) V beta-specific stimulation of human T cells by staphylococcal toxins. Science 244:811–813.PubMedCrossRefGoogle Scholar
  49. Kappler JW, White J, Kozono H, Clements J, Marrack P (1994) Binding of a soluble aβ T-cell receptor to superantigen/major histocompatibility complex lignands. Proc Natl Acad Sci USA 91: 8462–8466.PubMedCrossRefGoogle Scholar
  50. Kawabe Y, Ochi A (1990) Selective anergy of V beta 8+, CD4+ T cells in Staphylococcus enterotoxin B-primed mice. J Exp Med 172: 1065–1070.PubMedCrossRefGoogle Scholar
  51. Kawabe Y, Ochi A (1991) Programmed cell death and extrathymic reduction of Vbeta8+ CD4+ T cells in mice tolerant to Staphylococcus aureux enterotoxin B. Nature 349: 245–248.PubMedCrossRefGoogle Scholar
  52. Kotzin BL, Leung DYM, Kappler JW, Marrack P (1994) Superantigens and their potential role in human disease. Adv Immunol 54: 99–166.CrossRefGoogle Scholar
  53. Lafferty KJ, Woolnough J (1977) The origin and mechanism of the allograft reaction. Immunol Rev 35:231–262.PubMedCrossRefGoogle Scholar
  54. Lehmann V, Freudenberg MA, Galanos C (1987) Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine-treated mice. J Exp Med 165: 657–663.PubMedCrossRefGoogle Scholar
  55. Lewis DE, Ng Tang DS, Adu-Oppong A, Schober W, Rodgers JR (1994) Anergy and apoptosis in CD8+ T cells from HIV-infected persons. J Immunol 153: 412–420.PubMedGoogle Scholar
  56. Lussow AR, MacDonald HR (1994) Differential effect of superantigen-induced “anergy” on priming and effector stages of a T cell-dependent antibody response. Eur J Immunol 24: 445–449.PubMedCrossRefGoogle Scholar
  57. Lussow AR, Crompton T, Karapetian O, MacDonald HR (1993) Peripheral clonal deletion of superantigen-reactive T cells is enhanced by cortisone. Eur J Immunol 23: 578–581.PubMedCrossRefGoogle Scholar
  58. MacDonald HR, Schneider R, Lees RK, Howe RC, Acha-Orbea H, Festenstein H, Zinkernagel RM, Hengartner H (1988) T-cell receptor V beta use predicts reactivity and tolerance to Mlsa-encoded antigens. Nature 332: 40–45.PubMedCrossRefGoogle Scholar
  59. MacDonald HR, Baschieri S, Lees RK (1991) Clonal expansion precedes anergy and death of V beta 8+ peripheral T cells responding to staphylococcal enterotoxin B in vivo. Eur J Immunol 21:1963–1966.PubMedCrossRefGoogle Scholar
  60. Marrack P, Kappler JW (1990) The staphylococcal enterotoxins and their relatives. Science 248: 705–711.PubMedCrossRefGoogle Scholar
  61. Marrack P, Blackman MA, Kushnir E, Kappler JW (1990) The toxicity of staphylococcal enterotoxin B in mice is mediated by T cells. J Exp Med 171: 455–464.PubMedCrossRefGoogle Scholar
  62. Marrack P, Kushnir E, Kappler JW (1991) A maternally inherited superantigen encoded by a mammary tumor virus. Nature 349: 524–526.PubMedCrossRefGoogle Scholar
  63. Marrack P, Winslow GM, Choi YW, Scherer MT, Pullen AM, White J, Kappler JW (1993) The bacterial and mouse mammary tumor virus superantigens; two different families of proteins with the same functions. Immunol Rev 131: 79–92.PubMedCrossRefGoogle Scholar
  64. Matsui K, Boniface JJ, Reay PA, Schild H, Fazekas de St Groth B, Davis MM (1991) Low affinity interaction of peptide-MHC complexes with T cell receptors. Science 254: 1788–1791.PubMedCrossRefGoogle Scholar
  65. Miethke T, Gaus H, Wahl C, Heeg K, Wagner H (1992a) T-cell-dependent shock induced by a bacterial superantigen. Chem Immunol 55: 172–184.PubMedCrossRefGoogle Scholar
  66. Miethke T, Wahl C, Heeg K, Echtenacher B, Krammer PH, Wagner H (1992b) T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B: critical role of tumor necrosis factor. J Exp Med 175: 91–98.PubMedCrossRefGoogle Scholar
  67. Miethke T, Duschek K, Wahl C, Heeg K, Wagner H (1993a) Pathogenesis of the toxic shock syndrome: T cell mediated lethal shock caused by the superantigen TSST-1. Eur J Immunol 23: 1494–1500.PubMedCrossRefGoogle Scholar
  68. Miethke T, Wahl C, Heeg K, Wagner H (1993b) Acquired resistance to superantigen-induced T cell shock. J Immunol 150: 3776–3784.PubMedGoogle Scholar
  69. Miethke T, Wahl C, Holzmann B, Heeg K, Wagner H (1993c) Bacterial superantigens induce rapid and TCR Vβ-selective downregulation of L-selectin (gp90-Mel14) in vivo. J Immunol 151: 6777–6782.PubMedGoogle Scholar
  70. Miethke T, Wahl C, Regele D, Gaus H, Heeg K, Wagner H (1993d) Superantigen mediated shock: a cytokine release syndrome. Immunobiology 189: 270–284.PubMedCrossRefGoogle Scholar
  71. Miethke T, Wahl C, Gaus H, Heeg K, Wagner H (1994) Exogenous superantigens acutely trigger distinct levels of peripheral T cell tolerance/immunosuppression: dose-response relationship. Eur J Immunol 24: 1893–1902.PubMedCrossRefGoogle Scholar
  72. Miethke T, Wahl C, Heeg K, Wagner H (1995) Bacterial superantigens induce T cell unresponsiveness in B cell deficient mice. Eur J Immunol 25: 3187–3190.PubMedCrossRefGoogle Scholar
  73. Migita K, Ochi A (1993) The fate of anergic T cells in vivo J Immunol 150: 763–770.PubMedGoogle Scholar
  74. Mollick JA, Cook RG, Rich RR (1989) Class II MHC molecules are specific receptors for staphylococcus enterotoxin A. Science 244: 817–820.PubMedCrossRefGoogle Scholar
  75. Mottershead DG, Hsu PN, Urban RG, Strominger JL, Huber BT (1995) Direct binding of the Mtv7 superantigen (Mls-1) to soluble MHC class II molecules. Immunity 2: 149–154.PubMedCrossRefGoogle Scholar
  76. Nathan C, Xie Q (1994) Nitric oxide synthases: Roles, tolls, and controls. Cell 78: 915–918.PubMedCrossRefGoogle Scholar
  77. O’Hehir RE, Lamb JR (1990) Induction of specific clonal anergy in human T lymphocytes by Staphylococcus aureus enterotoxins. Proc Natl Sei USA 87: 8884–8888.CrossRefGoogle Scholar
  78. Otten GR, Germain RN (1991) Split anergy in a CD8+ T cell: receptor-dependent cytolysis in the absence of interleukin-2 production. Science 251: 1228–1231.PubMedCrossRefGoogle Scholar
  79. Paliard X, West SG, Lafferty JA, Clements JR, Kappler JW, Marrack P, Kotzin BL (1991) Evidence for the effects of a superantigen in rheumatoid arthritis. Science 253: 325–329.PubMedCrossRefGoogle Scholar
  80. Pantaleo G, Demarest JF, Soudeyns H, Graziosi C, Denis F, Adelsberger JW, Borrow P, Saag MS, Shaw GM, Sekaly RP, Fauci AS (1994) Major expansion of CD8+ T cells with a predominant Vß usage during the primary immune response to HIV. Nature 370: 463–467.PubMedCrossRefGoogle Scholar
  81. Pietra BA, de Inocenico J, Giannini EH, Hirsch R (1994) TCR Vß family repertoire and T cell activation markers in Kawasaki disease. J Immunol 153: 1881–1888.PubMedGoogle Scholar
  82. Rellahan BL, Jones LA, Kruisbeek AM, Fry AM, Matis LA (1990) In vivo induction of anergy in peripheral V beta 8+ T cells by staphylococcal enterotoxin B. J Exp Med 172: 1091–1100.PubMedCrossRefGoogle Scholar
  83. Rietschel ET, Brade H (1992) Bacterial endotoxins. Sei Am 267: 54–61.Google Scholar
  84. Röcken M, Urban JF, Shevach EM (1992) Infection breaks T-cell tolerance. Nature 359: 79–82.PubMedCrossRefGoogle Scholar
  85. Schönrieh G, Momburg F, Malissen M, Schmitt-Verhulst AM, Malissen B, Hämmerling GJ, Arnold B (1992) Distinct mechanisms of extrathymic T cell tolerance due to differential expression of self antigen. Int Immunol 4: 581–590.CrossRefGoogle Scholar
  86. Seth A, Stern LJ, Ottenhoff THM, Engel I, Owen MJ, Lamb JR, Klausner RD, Wiley DC (1994) Binary and ternary complexes between T cell receptor class II MHC and superantigen in vitro. Nature 369: 324–327.PubMedCrossRefGoogle Scholar
  87. Stiles BG, Bavari S, Krakauer T, Ulrich RG (1993) Toxicity of staphylococcal enterotoxins potentiated by lipopolysaccharide: major histocompatibility complex class II molecule dependency and cytokine release. Infect Immun 61: 5333–5338.PubMedGoogle Scholar
  88. Thibodeau J, Labrecque N, Denis F, Huber BT, Sekaly RP (1994) Binding sites for bacterial and endogenous retroviral superantigens can be dissociated on major histocompatibility complex class II molecules. J Exp Med 179: 1029–1034.PubMedCrossRefGoogle Scholar
  89. Torres BA, Griggs ND, Johnson HM (1993) Bacterial and retroviral superantigens share a common binding region on class II molecules. Nature 364: 152–154.PubMedCrossRefGoogle Scholar
  90. Vanier LE, Prud’homme GJ (1992) Cyclosporin A markedly enhances superantigen-induced peripheral T cell deletion and inhibits anergy induction. J Exp Med 176: 37–46.PubMedCrossRefGoogle Scholar
  91. Vella AT, McCormack JE, Linsley PS, Kappler JW, Marrack P (1995) Lipoplysaccharide interferes with the induction of peripheral T cell death. Immunity 2: 261–270.PubMedCrossRefGoogle Scholar
  92. Wahl C, Miethke T, Heeg K, Wagner H (1993) Clonal deletion as direct consequence of an in vivo T cell response to bacterial superantigen. Eur J Immunol 23: 1197–1200.PubMedCrossRefGoogle Scholar
  93. Weber S, Traunecker A, Oliveri F, Gerhard W, Karjalainen K (1992) Specific low-affinity recognition of major histocompatibility complex plus peptide by soluble T-cell receptor. Nature 356: 793–796.PubMedCrossRefGoogle Scholar
  94. White J, Herman A, Pullen AM, Kubo RT, Kappler JW, Marrack P (1989) The V beta-specific superantigen staphylococcal enterotoxin B: stimulation of mature T cells and clonal deletion in neonatal mice. Cell 56: 27–35.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • K. Heeg
    • 1
  • T. Miethke
    • 1
  • H. Wagner
    • 1
  1. 1.Institut für Medizinische Mikrobiologie und HygieneTechnische Universität MünchenMünchenGermany

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