Anti-HLA-DR-triggered monocytes mediate in vitro T cell anergy

International Immunology

Volumn 20, Issue 4, 2008, Pages 601-613

  Kriegel, Martin A ^a,b   Adam klages, Sabine ^c   Gabler, Christoph ^a,d   Blank, Norbert ^a,e   Schiller, Martin ^a,e   Scheidig, Christina ^a   Kalden, Joachim R ^a   Lorenz, Hanns Martin ^a,e  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Caspase; CD45; Cell cycle; ERK; p21cip; p27kip

Indexed keywords

CASPASE 3; CASPASE 8; CD28 ANTIGEN; CD3 ANTIGEN; CD45 ANTIGEN; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; HLA DR ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; MONOKINE; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL FUNCTION; CELL SEPARATION; CLONAL ANERGY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE RELEASE; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; MONOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ANTIBODIES, MONOCLONAL; ANTIGEN-ANTIBODY REACTIONS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; CLONAL ANERGY; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HLA-DR ANTIGENS; HUMANS; LEUKOCYTES, MONONUCLEAR; PHOSPHORYLATION; REFERENCE VALUES; T-LYMPHOCYTES;

EID: 41149086312     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxn019     Document Type: Article

References (72)

1. Sprent, J. and Kishimoto, H. 2001. The thymus and central tolerance. Phil. Trans. R. Soc. B. 356:609.
2. Walker, L. S. and Abbas, A. K. 2002. The enemy within: Keeping self-reactive T cells at bay in the periphery. Nat. Rev. Immunol. 2:11.
3. Bouneaud, C., Kourilsky, P. and Bousso, P. 2000. Impact of negative selection on the T cell repertoire reactive to a self-peptide: A large fraction of T cell clones escapes clonal deletion. Immunity. 13:829.
4. Schwartz, R. H. 2003. T cell anergy. Annu. Rev. immunol. 21:305.
5. Lechler, R., Chai, J. G., Marelli-Berg, F, Lombardi, G. and Shevach, E. M. 2001. T-cell anergy and peripheral T-cell tolerance. Phil. Trans. R. Soc. B. 356:625.
6. Appleman, L. J., Tzachanis, D., Grader-Beck, T., van Puijenbroek, A. A. and Boussiotis, V. A. 2001. Helper T cell anergy: From biochemistry to cancer pathophysiology and therapeutics. J. Mol. Med. 78:673.
7. Mueller, D. L. 2004. E3 ubiquitin ligases as T cell anergy factors. Nat. Immunol. 5:883.
8. Mueller, D. L. 2006. Linking diacylglycerol kinase to T cell anergy. Nat. Immunol. 7:1132.
9. Maloy, K. J. and Powrie, F. 2001. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2:816.
10. Macian, F, Garcia-Cozar, F, Im, S. H., Horton, H. F, Byrne, M. C. and Rao, A. 2002. Transcriptional mechanisms underlying lymphocyte tolerance. Cell. 109:719.
11. Salmena, L., Lemmers, B., Hakem, A. et al. 2003. Essential role for caspase 8 in T-cell homeostasis and T-cell-mediated immunity. Genes Dev. 17:883.
12. Chun, H. J., Zheng, L., Ahmad, M. et al. 2002. Pleiotropic defects in lymphocyte activation caused by caspase-8 mutations lead to human immunodeficiency. Nature. 419:395.
13. Alam, A., Cohen, L. Y., Aouad, S. and Sekaly, R. P. 1999. Early activation of caspases during T lymphocyte stimulation results in selective substrate cleavage in nonapoptotic cells. J. Exp. Med. 190:1879.
14. Kennédy, N. J., Kataoka, T., Tschopp, J. and Budd, R. C. 1999. Caspase activation is required for T cell proliferation. J. Exp. Med. 190:1891.
15. Falk, M., Ussat, S., Reiling, N., Wesch, D., Kabelitz, D. and Adam-Klages, S. 2004. Caspase inhibition blocks human T cell proliferation by suppressing appropriate regulation of IL-2, CD25, and cell cycle-associated proteins. J Immunol. 173:5077.
16. Adam-Klages, S., Adam, D., Janssen, O. and Kabelitz, D. 2005. Death receptors and caspases: Role in lymphocyte proliferation, cell death, and autoimmunity. Immunol. Res. 33:149.
17. Rowell, E. A., Walsh, M. C. and Wells, A. D. 2005. Opposing roles for the cyclin-dependent kinase inhibitor p27kip1 in the control of CD4+ T cell proliferation and effector function. J. Immunol. 174:3359.
18. Glennie, S., Soeiro, I., Dyson, P. J., Lam, E. W. and Dazzi, F. 2005. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 105:2821.
19. Wells, A. D., Walsh, M. C., Bluestone, J. A. and Turka, L. A. 2001. Signaling through CD28 and CTLA-4 controls two distinct forms of T cell anergy. J. Clin. Invest. 108:895.
20. Jackson, S. K., DeLoose, A. and Gilbert, K. M. 2001. Induction of anergy in Th1 cells associated with increased levels of cyclin-dependent kinase inhibitors p21Cip1 and p27Kip1. J. Immunol. 166:952.
21. Boussiotis, V. A., Freeman, G. J., Taylor, P. A. et al. 2000. p27kip1 functions as an anergy factor inhibiting interleukin 2 transcription and clonal expansion of alloreactive human and mouse helper T lymphocytes. Nat Med. 6:290.
22. Waiczies, S., Prozorovski, T., Infante-Duarte, C. et al. 2005. Atorvastatin induces T cell anergy via phosphorylation of ERK1. J. Immunol. 174:5630.
23. Greenwald, R. J., Boussiotis, V. A., Lorsbach, R. B., Abbas, A. K. and Sharpe, A. H. 2001. CTLA-4 regulates induction of anergy in vivo. Immunity. 14:145.
24. Li, L., Iwamoto, Y., Berezovskaya, A. and Boussiotis, V. A. 2006. A pathway regulated by cell cycle inhibitor p27(Kip1) and checkpoint inhibitor Smad3 is involved in the induction of T cell tolerance. Nat. Immunol. 7:1157.
25. Verdoodt, B., Blazek, T., Rauch, P. et al. 2003. The cyclin-dependent kinase inhibitors p27Kip1 and p21Cip1 are not essential in T cell anergy. Eur. J. Immunol. 33:3154.
26. Powell, J. D., Bruniquel, D. and Schwartz, R. H. 2001. TCR engagement in the absence of cell cycle progression leads to T cell anergy independent of p27(Kip1). Eur. J. Immunol. 31:3737.
27. Goerdt, S. and Orfanos, C. E. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10:137.
28. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23.
29. Morelli, A. E. and Thomson, A. W. 2003. Dendritic cells: Regulators of alloimmunity and opportunities for tolerance induction. Immunol. Rev. 196:125.
30. Beyth, S., Borovsky, Z., Mevorach, D. et al. 2005. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 105:2214.
31. Kubo, T., Hatton, R. D., Oliver, J., Liu, X., Elson, C. O. and Weaver, C. T. 2004. Regulatory T cell suppression and anergy are differentially regulated by proinflammatory cytokines produced by TLR-activated dendritic cells. J. Immunol. 173:7249.
32. Hoves, S., Krause, S. W., Schutz, C. et al. 2006. Monocyte-derived human macrophages mediate anergy in allogeneic T cells and induce regulatory T cells. J. Immunol. 177:2691.
33. Germain, R. N. and Margulies, D. H. 1993. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11:403.
34. Theofilopoulos, A. N., Dummer, W. and Kono, D. H. 2001. T cell homeostasis and systemic autoimmunity. J. Clin. Invest. 108:335.
35. Stefanova, I., Dorfman, J. R. and Germain, R. N. 2002. Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature. 420:429.
36. Bouillon, M., El Fakhry, Y., Girouard, J., Khalil, H., Thibodeau, J. and Mourad, W. 2003. Lipid raft-dependent and -independent signaling through HLA-DR molecules. J. Biol. Chem. 278:7099.
37. Matsuoka, T., Tabata, H. and Matsushita, S. 2001. Monocytes are differentially activated through HLA-DR, -DQ, and -DP molecules via mitogen-activated protein kinases. J. Immunol. 166:2202.
38. Rich, T., Lawler, S. E., Lord, J. M., Blancheteau, V. M., Charron, D. J. and Mooney, N. A. 1997. HLA class II-induced translocation of PKC alpha and PKC beta II isoforms is abrogated following truncation of DR beta cytoplasmic domains. J. Immunol. 159:3792.
39. Lang, P., Stolpa, J. C., Freiberg, B. A. et al. 2001. TCR-induced transmembrane signaling by peptide/MHC class II via associated lg-alpha/ beta dimers. Science. 291:1537.
40. Bertho, N., Drenou, B., Laupeze, B. et al. 2000. HLA-DR-mediated apoptosis susceptibility discriminates differentiation stages of dendritic/monocytic APC. J. Immunol. 164:2379.
41. Catlett, I. M., Xie, P., Hostager, B. S. and Bishop, G. A. 2001. Signaling through MHC class II molecules blocks CD95-induced apoptosis. J. Immunol. 166:6019.
42. Nagy, Z. A.. Hubner, B., Lohning, C. et al. 2002. Fully human, HLA-DR-specific monoclonal antibodies efficiently induce programmed death of malignant lymphoid cells. Nat. Med. 8:8.
43. Drenou, B., Blancheteau, V., Burgess, D. H., Fauchet, R., Charron, D. J. and Mooney, N. A. 1999. A caspase-indepen dent pathway of MHC class II antigen-mediated apoptosis of human B lymphocytes. J. Immunol. 163:4115.
44. Drenou, B., Amiot, L., Setterblad, N. et al. 2005. MHC class II signaling function is regulated during maturation of plasmacytoid dendritic cells. J. Leukoc. Biol. 77:560.
45. Bertho, N., Blancheteau, V. M., Setterblad, N. et al. 2002. MHC class II-mediated apoptosis of mature dendritic cells proceeds by activation of the protein kinase C-delta isoenzyme. Int. Immunol. 14:935.
46. Palacios, R., Martinez-Maza, O. and Guy, K. 1983. Monoclonal antibodies against HLA-DR antigens replace T helper cells in activation of B lymphocytes. Proc. Natl. Acad. Sci. USA. 80:3456.
47. Ruggiero, G., Manzo, C., Fontana, S. et al. 1987. Inhibition by anti-HLA class II monoclonal antibodies of monocyte-dependent T cell proliferation induced by monoclonal antibody OKT3. Eur. J. Immunol. 17:1585.
48. Racioppi, L., Moscarella, A., Ruggiero, G. et al. 1990. Inhibition by anti-HLA class II monoclonal antibodies of monoclonal antibody OKT3-induced T cell proliferation. Studies at the mRNA level. J. Immunol. 145:3635.
49. Ruggiero, G., Racioppi, L., Manzo, C. et al. 1991. HLA class II molecules on monocytes regulate T cell proliferation through physical interaction in the CD3 activation pathway. Eur. J. Immunol. 21:29.
50. Blank, N., Kriegel, M., Hieronymus, T. et al. 2001. CD45 tyrosine phosphatase controls common gamma-chain cytokine-mediated STAT and extracellular signal-related kinase phosphorylation in activated human lymphoblasts: Inhibition of proliferation without induction of apoptosis. J. Immunol. 166:6034.
51. Gaipi, U. S., Kuenkele, S., Voll, R. E. et al. 2001. Complement binding is an early feature of necrotic and a rather late event during apoptotic cell death. Cell Death Differ 8:327.
52. Kriegel, M. A., Lohmann, T., Gabler, C., Blank, N., Kalden, J. R. and Lorenz, H. M. 2004. Defective suppressor function of human CD4+ CD25+ regulatory T cells in autoimmune polyglandular syndrome type II. J. Exp. Med. 199:1285.
53. Kriegel, M. A., Tretter, T., Blank, N. et al. 2006. Interleukin-4 supports interleukin-12-induced proliferation and interferon-gamma secretion in human activated lymphoblasts and T helper type 1 cells. Immunology. 119:43.
54. Luschen, S., Ussat, S., Scherer, G., Kabelitz, D. and Adam-Klages, S. 2000. Sensitization to death receptor cytotoxicity by inhibition of fas-associated death domain protein (FADD)/caspase signaling. Requirement of cell cycle progression. J. Biol. Chem. 275:24670.
55. Malakhov, M. P., Kim, K. I., Malakhova, O. A., Jacobs, B. S., Borden, E. C. and Zhang, D. E. 2003. High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction. J. Biol. Chem. 278:16608.
56. Avice, M. N., Rubio, M., Sergerie, M., Delespesse, G. and Sarfati, M. 2001. Role of CD47 in the induction of human naive T cell anergy. J. Immunol. 167:2459.
57. Holling, T. M., van der Stoep, N., Quinten, E. and van den Elsen, P. J. 2002. Activated human T cells accomplish MHC class II expression through T cell-specific occupation of class II transactivator promoter III. J. Immunol. 168:763.
58. Ting, J. P. and Trowsdale, J. 2002. Genetic control of MHC class II expression. Cell. 109:S21.
59. Kudo, H., Matsuoka, T., Mitsuya, H., Nishimura, Y. and Matsushita, S. 2002. Cross-linking HLA-DR molecules on Th1 cells induces anergy in association with increased level of cyclin-dependent kinase inhibitor p27(Kip1). Immunol. Lett. 81:149.
60. Mantovani, A., Sozzani, S., Locati, M., Allavena, P. and Sica, A. 2002. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23:549.
61. Tzachanis, D., Berezovskaya, A., Nadler, L. M. and Boussiotis, V. A. 2002. Blockade of B7/CD28 in mixed lymphocyte reaction cultures results in the generation of alternatively activated macrophages, which suppress T-cell responses. Blood. 99:1465.
62. Boussiotis, V. A., Barber, D. L., Nakarai, T. et al. 1994. Prevention of T cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science. 266:1039.
63. Harding, F. A., McArthur, J. G., Gross, J. A., Raulet, D. H. and Allison, J. P. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature. 356:607.
64. Beverly, B., Kang, S. M.., Lenardo, M. J. and Schwartz, R. H. 1992. Reversal of in vitro T cell clonal anergy by IL-2 stimulation. Int. Immunol. 4:661.
65. Powell, J. D., Lerner, C. G. and Schwartz, R. H. 1999. Inhibition of cell cycle progression by rapamycin induces T cell clonal anergy even in the presence of costimulation. J. Immunol. 162:2775.
66. Laudanski, K., Miller-Graziano, C., Xiao, W. et al. 2006. Cell-specific expression and pathway analyses reveal alterations in trauma-related human T cell and monocyte pathways. Proc. Natl Acad. Sci. USA. 103:15564.
67. Cammarota, G., Scheirle, A., Takacs, B. et al. 1992. Identification of a CD4 binding site on the beta 2 domain of HLA-DR molecules. Nature. 356:799.
68. Searles, R. P., Savage, S. M., Brozek, C. M., Marnell, L. L. and Hoffman, C. L. 1988. Network regulation in rheumatoid arthritis. Studies of DR+ T cells, anti-DR, antiidiotypic antibodies, and clinical disease activity. Arthritis Rheum. 31:834.
69. Sany, J., Clot, J., Bonneau, M. and Andary, M. 1982. Immunomodulating effect of human placenta-eluted gamma globulins in rheumatoid arthritis. Arthritis Rheum. 25:17.
70. Moynier, M., Cosso, B., Brochier, J. and Clot, J. 1987. Identification of class II HLA alloantibodies in placenta-eluted gamma globulins used for treating rheumatoid arthritis. Arthritis Rheum. 30:375.
71. Taams, L. S., van Eden, W. and Wauben, M. H. 1999. Dose-dependent induction of distinct anergic phenotypes: Multiple levels of T cell anergy. J. Immunol. 162:1974.
72. Kurtz, J., Shaffer, J., Lie, A., Anosova, N., Benichou, G. and Sykes, M. 2004. Mechanisms of early peripheral CD4 T cell tolerance induction by anti-CD154 monoclonal antibody and allogeneic bone marrow transplantation: Evidence for anergy and deletion, but not regulatory cells. Blood. 103:4336.