Stress proteins are used by the immune system for cognate interactions with anti-inflammatory regulatory T cells

FEBS Letters

Volumn 587, Issue 13, 2013, Pages 1951-1958

  Van Eden, Willem ^a   Van Herwijnen, Martijn ^a   Wagenaar, Josée ^a   Van Kooten, Peter ^a   Broere, Femke ^a   Van Der Zee, Ruurd ^a  

^a Department of Infectious Diseases and Immunology   (Netherlands)

Author keywords

HSP Stress protein HSP60 HSP70 Treg Inflammation Autoimmunity

Indexed keywords

ANTIGEN; CD79B ANTIGEN; CHAPERONIN 60; EPITOPE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HLA DQ8 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SELF ANTIGEN; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ARTHRITIS; CD4+ CD25+ FOXP3+ T LYMPHOCYTE; CELL INTERACTION; HUMAN; IMMUNOCOMPETENT CELL; IN VIVO STUDY; LYMPHOCYTE DEPLETION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; ARTHRITIS; EPITOPES; HEAT-SHOCK PROTEINS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES, REGULATORY;

MURINAE; MUS; MUS MUSCULUS;

EID: 84878914156     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.05.024     Document Type: Review

References (76)

1. K. Golab, D. Leveson-Gower, X.J. Wang, J. Grzanka, N. Marek-Trzonkowska, A. Krzystyniak, P. Trzonkowski, and P. Witkowski Challenges in cryopreservation of regulatory T cells (Tregs) for clinical therapeutic applications Int. Immunopharmacol. 2013 http://dx.doi.org/10.1016/j.intimp.2013.02.001. [Epub ahead of print]
2. N. Marek-Trzonkowska, M. Mysliwiec, A. Dobyszuk, M. Grabowska, I. Techmanska, J. Juscinska, M.A. Wujtewicz, P. Witkowski, W. Mlynarski, A. Balcerska, J. Mysliwska, and P. Trzonkowski Administration of CD4+CD25highCD127- regulatory T cells preserves beta-cell function in type 1 diabetes in children Diabetes Care 35 2012 1817 1820
3. M.R. Ehrenstein, J.G. Evans, A. Singh, S. Moore, G. Warnes, D.A. Isenberg, and C. Mauri Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy J. Exp. Med. 200 2004 277 285
4. F. Flores-Borja, E.C. Jury, C. Mauri, and M.R. Ehrenstein Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis Proc. Natl. Acad. Sci. USA 105 2008 19396 19401
5. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda Pillars article: immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases J. Immunol. 186 2011 3808 3821 J. Immunol. 1995
6. J.D. Fontenot, and A.Y. Rudensky A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3 Nat. Immunol. 6 2005 331 337
7. D. Haribhai, J.B. Williams, S. Jia, D. Nickerson, E.G. Schmitt, B. Edwards, J. Ziegelbauer, M. Yassai, S.H. Li, L.M. Relland, P.M. Wise, A. Chen, Y.Q. Zheng, P.M. Simpson, J. Gorski, N.H. Salzman, M.J. Hessner, T.A. Chatila, and C.B. Williams A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity Immunity 35 2011 109 122
8. C.S. Hsieh, Y. Zheng, Y. Liang, J.D. Fontenot, and A.Y. Rudensky An intersection between the self-reactive regulatory and nonregulatory T cell receptor repertoires Nat. Immunol. 7 2006 401 410
9. P. McGuirk, C. McCann, and K.H. Mills Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis J. Exp. Med. 195 2002 221 231
10. D.A. Vignali, L.W. Collison, and C.J. Workman How regulatory T cells work Nat. Rev. Immunol. 8 2008 523 532
11. L.W. Collison, C.J. Workman, T.T. Kuo, K. Boyd, Y. Wang, K.M. Vignali, R. Cross, D. Sehy, R.S. Blumberg, and D.A. Vignali The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 450 2007 566 569
12. W.J. Grossman, J.W. Verbsky, W. Barchet, M. Colonna, J.P. Atkinson, and T.J. Ley Human T regulatory cells can use the perforin pathway to cause autologous target cell death Immunity 21 2004 589 601
13. A.M. Thornton, and E.M. Shevach CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production J. Exp. Med. 188 1998 287 296
14. C. Oderup, L. Cederbom, A. Makowska, C.M. Cilio, and F. Ivars Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression Immunology 118 2006 240 249
15. C.T. Huang, C.J. Workman, D. Flies, X. Pan, A.L. Marson, G. Zhou, E.L. Hipkiss, S. Ravi, J. Kowalski, H.I. Levitsky, J.D. Powell, D.M. Pardoll, C.G. Drake, and D.A. Vignali Role of LAG-3 in regulatory T cells Immunity 21 2004 503 513
16. A.M. Thornton, and E.M. Shevach Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific J. Immunol. 164 2000 183 190
17. T. Koga, A. Wand-Wurttenberger, J. DeBruyn, M.E. Munk, B. Schoel, and S.H. Kaufmann T cells against a bacterial heat shock protein recognize stressed macrophages Science 245 1989 1112 1115
18. J.R. Newcomb, and P. Cresswell Characterization of endogenous peptides bound to purified HLA-DR molecules and their absence from invariant chain-associated alpha beta dimers J. Immunol. 150 1993 499 507
19. V.L. Crotzer, and J.S. Blum Autophagy and intracellular surveillance: modulating MHC class II antigen presentation with stress Proc. Natl. Acad. Sci. USA 102 2005 7779 7780
20. B. Levine, N. Mizushima, and H.W. Virgin Autophagy in immunity and inflammation Nature 469 2011 323 335
21. S. Kaushik, and A.M. Cuervo Chaperone-mediated autophagy: a unique way to enter the lysosome world Trends Cell Biol. 22 2012 407 417
22. J. Dengjel, O. Schoor, R. Fischer, M. Reich, M. Kraus, M. Muller, K. Kreymborg, F. Altenberend, J. Brandenburg, H. Kalbacher, R. Brock, C. Driessen, H.G. Rammensee, and S. Stevanovic Autophagy promotes MHC class II presentation of peptides from intracellular source proteins Proc. Natl. Acad. Sci. USA 102 2005 7922 7927
23. M.J. van Herwijnen, L. Wieten, R. van der Zee, P.J. van Kooten, J.P. Wagenaar-Hilbers, A. Hoek, I. den Braber, S.M. Anderton, M. Singh, H.D. Meiring, C.A. van Els, W. van Eden, and F. Broere Regulatory T cells that recognize a ubiquitous stress-inducible self-antigen are long-lived suppressors of autoimmune arthritis Proc. Natl. Acad. Sci. USA 109 2012 14134 14139
24. C. Paludan, D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Munz Endogenous MHC class II processing of a viral nuclear antigen after autophagy Science 307 2005 593 596
25. M. Gannage, and C. Munz Autophagy in MHC class II presentation of endogenous antigens Curr. Top. Microbiol. Immunol. 335 2009 123 140
26. A. Kuma, M. Hatano, M. Matsui, A. Yamamoto, H. Nakaya, T. Yoshimori, Y. Ohsumi, T. Tokuhisa, and N. Mizushima The role of autophagy during the early neonatal starvation period Nature 432 2004 1032 1036
27. D. Schmid, and C. Munz Innate and adaptive immunity through autophagy Immunity 27 2007 11 21
28. C. Munz Autophagy and antigen presentation Cell. Microbiol. 8 2006 891 898
29. A.B. Strawbridge, and J.S. Blum Autophagy in MHC class II antigen processing Curr. Opin. Immunol. 19 2007 87 92
30. C.M. Costantino, E. Spooner, H.L. Ploegh, and D.A. Hafler Class II MHC self-antigen presentation in human B and T lymphocytes PLoS ONE 7 2012 e29805
31. I.R. Cohen, F.J. Quintana, and A. Mimran Tregs in T cell vaccination: exploring the regulation of regulation J. Clin. Invest. 114 2004 1227 1232
32. F.J. Quintana, A. Mimran, P. Carmi, F. Mor, and I.R. Cohen HSP60 as a target of anti-ergotypic regulatory T cells PLoS ONE 3 2008 e4026
33. B.S. Polla, and S. Kantengwa Heat shock proteins and inflammation Curr. Top. Microbiol. Immunol. 167 1991 93 105
34. C.J. Boog, E.R. de Graeff-Meeder, M.A. Lucassen, R. van der Zee, M.M. Voorhorst-Ogink, P.J. van Kooten, H.J. Geuze, and W. van Eden Two monoclonal antibodies generated against human hsp60 show reactivity with synovial membranes of patients with juvenile chronic arthritis J. Exp. Med. 175 1992 1805 1810
35. T.W. Fawcett, S.L. Sylvester, K.D. Sarge, R.I. Morimoto, and N.J. Holbrook Effects of neurohormonal stress and aging on the activation of mammalian heat shock factor 1 J. Biol. Chem. 269 1994 32272 32278
36. R. Njemini, M.V. Abeele, C. Demanet, M. Lambert, S. Vandebosch, and T. Mets Age-related decrease in the inducibility of heat-shock protein 70 in human peripheral blood mononuclear cells J. Clin. Immunol. 22 2002 195 205
37. J. Debler, U. Schiemann, U. Seybold, T. Mussack, N. Landauer, R. Ladurner, and M. Gross Heat-shock protein HSP70-2 genotypes in patients with Crohn's disease: a more severe clinical course with intestinal complications in presence of the PstI-polymorphism Eur. J. Med. Res. 8 2003 120 124
38. J. Clarimon, J. Bertranpetit, M. Boada, L. Tarraga, and D. Comas HSP70-2 (HSPA1B) is associated with noncognitive symptoms in late-onset Alzheimer's disease J. Geriatr. Psychiatry Neurol. 16 2003 146 150
39. A. Balog, Z. Gyulai, L.G. Boros, G. Farkas, T. Takacs, J. Lonovics, and Y. Mandi Polymorphism of the TNF-alpha, HSP70-2, and CD14 genes increases susceptibility to severe acute pancreatitis Pancreas 30 2005 e46 50
40. K. Bogunia-Kubik, and A. Lange HSP70-hom gene polymorphism in allogeneic hematopoietic stem-cell transplant recipients correlates with the development of acute graft-versus-host disease Transplantation 79 2005 815 820
41. K. Bellmann, L. Hui, J. Radons, V. Burkart, and H. Kolb Low stress response enhances vulnerability of islet cells in diabetes-prone BB rats Diabetes 46 1997 232 236
42. V. Burkart, L. Germaschewski, N.C. Schloot, K. Bellmann, and H. Kolb Deficient heat shock protein 70 response to stress in leukocytes at onset of type 1 diabetes Biochem. Biophys. Res. Commun. 369 2008 421 425
43. L. Wieten, R. van der Zee, R. Spiering, J. Wagenaar-Hilbers, P. van Kooten, F. Broere, and W. van Eden A novel heat-shock protein coinducer boosts stress protein Hsp70 to activate T cell regulation of inflammation in autoimmune arthritis Arthritis Rheum. 62 2010 1026 1035
44. G.H. van Puijvelde, T. van Es, E.J. van Wanrooij, K.L. Habets, P. de Vos, R. van der Zee, W. van Eden, T.J. van Berkel, and J. Kuiper Induction of oral tolerance to HSP60 or an HSP60-peptide activates T cell regulation and reduces atherosclerosis Arterioscler. Thromb. Vasc. Biol. 27 2007 2677 2683
45. G. Wick, M. Knoflach, and Q. Xu Autoimmune and inflammatory mechanisms in atherosclerosis Annu. Rev. Immunol. 22 2004 361 403
46. G.K. Hansson Vaccination against atherosclerosis: science or fiction? Circulation 106 2002 1599 1601
47. A.G. van Halteren, B. Mosselman, B.O. Roep, W. van Eden, A. Cooke, G. Kraal, and M.H. Wauben T cell reactivity to heat shock protein 60 in diabetes-susceptible and genetically protected nonobese diabetic mice is associated with a protective cytokine profile J. Immunol. 165 2000 5544 5551
48. R. Maron, G. Sukhova, A.M. Faria, E. Hoffmann, F. Mach, P. Libby, and H.L. Weiner Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice Circulation 106 2002 1708 1715
49. R.Y. Chandawarkar, M.S. Wagh, J.T. Kovalchin, and P. Srivastava Immune modulation with high-dose heat-shock protein gp96: therapy of murine autoimmune diabetes and encephalomyelitis Int. Immunol. 16 2004 615 624
50. S. Aldridge Toll-like receptor blocker slows beta cell death in type 1 diabetes Nat. Biotechnol. 30 2012 124-124c
51. O.S. Birk, D.C. Douek, D. Elias, K. Takacs, H. Dewchand, S.L. Gur, M.D. Walker, R. van der Zee, I.R. Cohen, and D.M. Altmann A role of Hsp60 in autoimmune diabetes: analysis in a transgenic model Proc. Natl. Acad. Sci. USA 93 1996 1032 1037
52. D. Elias, T. Reshef, O.S. Birk, R. van der Zee, M.D. Walker, and I.R. Cohen Vaccination against autoimmune mouse diabetes with a T-cell epitope of the human 65-kDa heat shock protein Proc. Natl. Acad. Sci. USA 88 1991 3088 3091
53. I. Raz, D. Elias, A. Avron, M. Tamir, M. Metzger, and I.R. Cohen Beta-cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial Lancet 358 2001 1749 1753
54. I. Alvarez, J. Collado, X. Daura, N. Colome, M. Rodriguez-Garcia, T. Gallart, F. Canals, and D. Jaraquemada The rheumatoid arthritis-associated allele HLA-DR10 (DRB1â̂ - 1001) shares part of its repertoire with HLA-DR1 (DRB1â̂ - 0101) and HLADR4 (DRBâ̂ - 0401) Arthritis Rheum. 58 2008 1630 1639
55. C.A. Nelson, R.W. Roof, D.W. McCourt, and E.R. Unanue Identification of the naturally processed form of hen egg white lysozyme bound to the murine major histocompatibility complex class II molecule I-Ak Proc. Natl. Acad. Sci. U. S. A. 89 1992 7380 7383
56. A.R. Dongre, S. Kovats, P. deRoos, A.L. McCormack, T. Nakagawa, V. Paharkova-Vatchkova, J. Eng, H. Caldwell, J.R. Yates 3rd, and A.Y. Rudensky In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses Eur. J. Immunol. 31 2001 1485 1494
57. R.M. Chicz, R.G. Urban, J.C. Gorga, D.A. Vignali, W.S. Lane, and J.L. Strominger Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles J. Exp. Med. 178 1993 27 47
58. D. Stepniak, M. Wiesner, A.H. de Ru, A.K. Moustakas, J.W. Drijfhout, G.K. Papadopoulos, P.A. van Veelen, and F. Koning Large-scale characterization of natural ligands explains the unique gluten-binding properties of HLA-DQ2 J. Immunol. 180 2008 3268 3278
59. A. Suri, J.J. Walters, M.L. Gross, and E.R. Unanue Natural peptides selected by diabetogenic DQ8 and murine IA(g7) molecules show common sequence specificity J. Clin. Invest. 115 2005 2268 2276
60. C.T. Spencer, S.M. Dragovic, S.B. Conant, J.J. Gray, M. Zheng, P. Samir, X. Niu, M. Moutaftsi, L. Van Kaer, A. Sette, A.J. Link, and S. Joyce Sculpting MHC class II?restricted self and non-self peptidome by the class I Ag-processing machinery and its impact on Th-cell responses Eur. J. Immunol. 2013
61. C.M. Costantino, E. Spooner, H.L. Ploegh, and D.A. Hafler Class II MHC self-antigen presentation in human B and T lymphocytes PLoS One 7 2012 e29805
62. F.A. Verreck, A. van de Poel, J.W. Drijfhout, R. Amons, J.E. Coligan, and F. Konig Natural peptides isolated from Gly86/Val86-containing variants of HLA-DR1, -DR11, -DR13, and -DR52 Immunogenetics 43 1996 392 397
63. O. Chornoguz, A. Gapeev, M.C. O'Neill, and S. Ostrand-Rosenberg Major histocompatibility complex class II+ invariant chain negative breast cancer cells present unique peptides that activate tumor-specific T cells from breast cancer patients Mol. Cell. Proteomics 11 2012 1457 1467
64. S. Sharif, B.A. Mallard, and B.N. Wilkie Characterization of naturally processed and presented peptides associated with bovine major histocompatibility complex (BoLA) class II DR molecules Anim. Genet. 34 2003 116 123
65. A. Muntasell, M. Carrascal, I. Alvarez, L. Serradell, P. van Veelen, F.A. Verreck, F. Koning, J. Abian, and D. Jaraquemada Dissection of the HLA-DR4 peptide repertoire in endocrine epithelial cells: strong influence of invariant chain and HLADM expression on the nature of ligands J. Immunol. 173 2004 1085 1093
66. J. Dengjel, O. Schoor, R. Fischer, M. Reich, M. Kraus, M. Muller, K. Kreymborg, F. Altenberend, J. Brandenburg, H. Kalbacher, R. Brock, C. Driessen, H.G. Rammensee, and S. Stevanovic Autophagy promotes MHC class II presentation of peptides from intracellular source proteins Proc. Natl. Acad. Sci. U. S. A. 102 2005 7922 7927
67. T. Halder, G. Pawelec, A.F. Kirkin, J. Zeuthen, H.E. Meyer, L. Kun, and H. Kalbacher Isolation of novel HLA-DR restricted potential tumor-associated antigens from the melanoma cell line FM3 Cancer Res. 57 1997 3238 3244
68. C.B. Sanjeevi, T.P. Lybrand, S. Stevanovic, and H.G. Rammensee Molecular modeling of eluted peptides from DQ6 molecules (DQB1â̂ - 0602 and DQB1â̂ - 0604) negatively and positively associated with type 1 diabetes Ann. N. Y. Acad. Sci. 958 2002 317 320
69. P. Marrack, L. Ignatowicz, J.W. Kappler, J. Boymel, and J.H. Freed Comparison of peptides bound to spleen and thymus class II J. Exp. Med. 178 1993 2173 2183
70. J.H. Freed, A. Marrs, J. VanderWall, P.L. Cohen, and R.A. Eisenberg MHC class II-bound self peptides from autoimmune MRL/lpr mice reveal potential T cell epitopes for autoantibody production in murine systemic lupus erythematosus J. Immunol. 164 2000 4697 4705
71. B. Reizis, F. Mor, M. Eisenstein, H. Schild, S. Stefanovic, H.G. Rammensee, and I.R. Cohen The peptide binding specificity of the MHC class II I-A molecule of the Lewis rat, RT1.BI Int. Immunol. 8 1996 1825 1832
72. T. Friede, V. Gnau, G. Jung, W. Keilholz, S. Stevanovic, and H.G. Rammensee Natural ligand motifs of closely related HLA-DR4 molecules predict features of rheumatoid arthritis associated peptides Biochim. Biophys. Acta 1316 1996 85 101
73. J.D. Lippolis, F.M. White, J.A. Marto, C.J. Luckey, T.N. Bullock, J. Shabanowitz, D.F. Hunt, and V.H. Engelhard Analysis of MHC class II antigen processing by quantitation of peptides that constitute nested sets J. Immunol. 169 2002 5089 5097
74. R.J. Seward, E.E. Drouin, A.C. Steere, and C.E. Costello Peptides presented by HLA-DR molecules in synovia of patients with rheumatoid arthritis or antibiotic-refractory Lyme arthritis Molecular & Cellular Proteomics 10 2011
75. H. Nishikawa, T. Kato, I. Tawara, K. Saito, H. Ikeda, K. Kuribayashi, P.M. Allen, R.D. Schreiber, S. Sakaguchi, L.J. Old, and H. Shiku Definition of target antigens for naturally occurring CD4(+) CD25(+) regulatory T cells J. Exp. Med. 201 2005 681 686
76. U. Wendling, L. Paul, R. van der Zee, B. Prakken, M. Singh, and W. van Eden A conserved mycobacterial heat shock protein (hsp) 70 sequence prevents adjuvant arthritis upon nasal administration and induces IL-10-producing T cells that cross-react with the mammalian self-hsp70 homologue J. Immunol. 164 2000 2711 2717