An altered peptide ligand corresponding to a novel epitope from heat-shock protein 60 induces regulatory T cells and suppresses pathogenic response in an animal model of adjuvant-induced arthritis

References

• Myew-Ling T, Pierre M. The role of T cells in rheumatoid arthritis: New subsets and new targets. Curr Opin Rheumatol. 2007; 19:284–288.
   PubMed Web of Science ®Google Scholar
• Miossec P. Il-17 and Th17 in Rheumatoid Arthritis. In: Quesmiaux V, Ryffel B, Padova F. editors. Th 17 cells: Role in inflammation and autoimmune disease. Basel: Irkhäuser Verlag;2009.
   Google Scholar
• Nistala K, Wedderburn LR. Th17 and regulatory T cells: Rebalancing pro- and anti-inflammatory forces in autoimmune arthritis. Rheumatology. 2009; 48:602–606.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Fox DA. Regulatory T cell defects in rheumatoid arthritis. Arthritis Rheum. 2007; 56:710–713.
   PubMedGoogle Scholar
• Valencia X, Stephens G, Goldbach-Mansky R, Wilson M, Lipsky PE. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood. 2006; 108:253–261.
   PubMed Web of Science ®Google Scholar
• O'Dell JR. Therapeutic strategies for rheumatic arthritis. N Engl J Med. 2004; 350:2591–2602.
   PubMed Web of Science ®Google Scholar
• Olsen NJ, Stein CM. New drugs for rheumatoid arthritis. N Engl J Med. 2004; 350:2167–2179.
   PubMed Web of Science ®Google Scholar
• Kooloos WM, de Jong DJ, Huizinga TWJ, Guchelaar HJ. Potential role of pharmacogenetics in anti-TNF treatment of rheumatoid arthritis and Crohn's disease. Drug Discov Today. 2007; 12:125–131.
   PubMed Web of Science ®Google Scholar
• Welsing PM, Severens JL, Hartman M, van Riel PL, Laan RF. Modeling the 5-years cost effectiveness of treatment strategies including tumor necrosis factor-blocking agents and leflunomide for treating rheumatoid arthritis in the Netherlands. Arthritis Rheum. 2004; 51:964–973.
   PubMed Web of Science ®Google Scholar
• Breedveld FC, Weisman MH, Kavanaugh AF, Cohen SB, Pavelka K, van Vollenhoven R, Sharp J, Perez JL, Spencer-Green GT. The PREMIER study: A multicenter, randomized, double-blind clinical trial of combination therapy with adalimumab plus methotrexate versus methotrexate alone or adalimumab alone in patients with early, aggressive rheumatoid arthritis who had not had previous methotrexate treatment. Arthritis Rheum. 2006; 54:26–37.
   PubMed Web of Science ®Google Scholar
• Nadkarni S, Mauri C, Ehrenstein MR. Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med. 2007; 204 1: 33–39.
   PubMed Web of Science ®Google Scholar
• Cohen IR, Young DB. Autoimmunity, microbial immunity and the immunological homunculus. Immunol Today. 1991; 12:105–110.
   PubMedGoogle Scholar
• Prakken BJ, Roord S, Ronaghy A, Wauben M, Albani S, van Eden W. Heat shock protein 60 and adjuvant arthritis: A model for T cell regulation in human arthritis. Springer Semin Immunopathol. 2003; 25:47–63.
   PubMed Web of Science ®Google Scholar
• Cohen IR, Quintana FJ, Mimran A. T regs in T cell vaccination: Exploring the regulation of regulation. J Clin Invest. 2004; 114:1227–1232.
   PubMed Web of Science ®Google Scholar
• van Eden W, van der Zee R, Prakken B. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat Rev Immunol. 2005; 5:318–330.
   PubMed Web of Science ®Google Scholar
• Alberta GA, van der Zee R, Taams LS, van Eden W. A self-Hsp60 peptide acts as a partial agonist inducing expression of B7-2 on mycobacterial hsp60-specific T cells: A possible mechanism for inhibitory T cell regulation of adjuvant arthritis. Int Immmunol. 2000; 12:1041–1050.
   PubMed Web of Science ®Google Scholar
• Van Eden W, Thole JER, van der Zee R, Noordzij A, Van Embden JDA, Hensen EJ, Cohen IR. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature. 1988; 331:171–173.
   PubMed Web of Science ®Google Scholar
• Zanin-Zhorov A, Cahalon L, Tal G, Margalit R, Lider O, Cohen I. Heat shock protein 60 enhances CD4+CD25+ regulatory T cell function via innate TLR2 signaling. J Clin Invest. 2006; 116:2022–2032.
   PubMed Web of Science ®Google Scholar
• Prakken BJ, Samodal R, Le TD, Giannoni F, Yung GP, Sacavulli J, Amox D, Roord S, de Kleer I, Bonnin D, Lanza P, Berry C, Massa M, Billetta R, Albani S. Epitope specific immunotherapy induces immune deviation of proinflammatory T cells in rheumatoid arthritis. Proc Natl Acad Sci USA. 2004; 101:4228–4233.
   PubMed Web of Science ®Google Scholar
• Koffeman EC, Genovese M, Amox D, Keogh E, Santana E, Matteson EL, Kavanaugh A, Molitor JA, Schiff MH, Posever JO, Bathon JM, Kivitz AJ, Samodal R, Belardi F, Dennehey C, van den Broek T, van Wijk F, Zhang X, Zieseniss P, Le T, Prakken BA, Cutter GC, Albani S. Epitope-specific immunotherapy of rheumatoid arthritis. Clinical responsiveness occurs with immune deviation and relies on the expression of a cluster of molecules associated with T cell tolerance in a double-blind, placebo-controlled, pilot phase II trial. Arthritis Rheumat. 2009; 60:3207–3321.
   PubMed Web of Science ®Google Scholar
• Raz I, Elias D, Avron A, Tamir M, Metzger M, Cohen IR. β-Cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): A randomized, double-blind, phase II trial. Lancet. 2001; 358:1749–1753.
   PubMed Web of Science ®Google Scholar
• Alleva DG, Gaur A, Jin L, Wegmann D, Gottlieb PA, Pahuja A, Johnson EB, Motheral T, Putnam A, Crowe PD, Ling N, Boehme SA, Conlon PJ. Immunological characterization and therapeutic activity of an altered-peptide ligand, NBI-6024, Based on the Immunodominant Type 1 diabetes autoantigen insulin B-Chain (9–23) peptide. Diabetes. 2002; 51:2126–2134.
   PubMed Web of Science ®Google Scholar
• Aruna BV, Sela M, Mozes E. Suppression of myasthenogenic responses of a T cell line by a dual altered peptide ligand by induction of CD4+CD25+ regulatory cells. Proc Natl Acad Sci USA. 2005; 102:10285–10290.
   PubMed Web of Science ®Google Scholar
• Zhao J, Li R, He J, Shi J, Long L, Li Z. Mucosal administration of an altered CII263-272 peptide inhibits collagen-induced arthritis by suppression of Th1/Th17 cells and expansion of regulatory T cells. Rheumatol Int. 2008; 29:9–16.
   PubMed Web of Science ®Google Scholar
• Katsara M, Deraos G, Tselios T, Matsoukas J, Apostolopoulos V. Design of novel cyclic altered peptide ligands of myelin basic protein MBP83-99 that modulate immune responses in SJL/J mice. J Med Chem. 2008; 51:3971–3978.
   PubMed Web of Science ®Google Scholar
• De Magistris M. Antigen analog-major complex histocompatibility complexes act as antagonist of the T cell receptor. Cell. 1992; 68:625–634.
   PubMed Web of Science ®Google Scholar
• Evavold BD. Separation of IL-4 production from Th cell proliferation by an altered T cell ligand. Science. 1991; 252:1308–1310.
   PubMed Web of Science ®Google Scholar
• Paas-Rozner M, Sela M, Mozes E. A dual altered peptide ligand down-regulates myasthenogenic T cell responses by up-regulating CD25- and CTLA-4-expressing CD4+T cells. PANAS. 2003; 100 11: 6676–6681.
   PubMedGoogle Scholar
• Singh H, Raghava GPS. ProPred: Prediction of HLA-DR binding sites. Bioinformatics. 2001; 17:1236–1237.
   PubMed Web of Science ®Google Scholar
• Larche M. Peptide immunotherapy. Immunol Allergy Clin North Am. 2006; 26:321–332.
   PubMed Web of Science ®Google Scholar
• Garrood T, Pitzalis C. Targeting the inflamed synovium: The quest for specificity. Arthritis Rheum. 2006; 54:1055–1060.
   Google Scholar
• Tarzi M, Klunker S, Texier C, Verhoef A, Stapel SO, Akdis CA, Maillere B, Kay AB, Larché M. Induction of interleukin-10 and suppressor of cytokine signalling-3 gene expression following peptide immunotherapy. Clin Exp Allergy. 2006; 36:465–474.
   PubMed Web of Science ®Google Scholar
• Manzo BA, Sundstedt A, Minaee S, Symonds A, Khalid S, Nicolson K, Li S, Wraith DC, Wang P. Persistent antigenic stimulation alters the transcription program in T cells, resulting in antigenic-specific tolerance. Eur J Immunol. 2006; 36:1374–1385.
   Google Scholar
• van Eden W. Stress proteins as targets for anti-inflammatory therapies. Reviews. 2000; 5:115–120.
   Google Scholar
• Anderton SM, Zee R, Prakken B, Noordzij A, van Eden W. Activation of T cells recognizing self 60-kD heat shock protein can protect against experimental arthritis. J Exp Med. 1995; 181:943–952.
   PubMed Web of Science ®Google Scholar
• van Eden W, Tholet JE, Van der Zee R, Noordzij A, Van Embden JD, Hensen EJ, Cohen IR. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature. 1988; 331:171–173.
   PubMed Web of Science ®Google Scholar
• Praken AB, Van Eden W, Rijkers GT, Kuis W, Toebes EA, De Graeff-Meeder ER, van der Zee R, Zegers BJ. Autoreactivity to human heat shock protein 60 predicts disease remission in oligoarticular juvenile rheumatoid arthritis. Arthritis Rheum. 1996; 39:1826–1832.
   Google Scholar
• van Eden W, van der Zee R, Paul AG, Prakken BJ, Wendling U, Anderton SM, Wauben MH. Do heat shock proteins control the balances of T-cells regulation in inflammatory diseases?. Immunol Today. 1998; 19:303–307.
   PubMedGoogle Scholar
• van Eden W, Prakken AB, Albani S. Immunological tolerance in the therapy of rheumatoid arthritis. Discov Med. 2007; 7:46–50.
   Google Scholar
• Roord ST, Zonneveld-Huijssoon E, Le T, Puga G, Koffeman E, Ronaghy A, Ghahramani N, Lanza P, Billetta R, Prakken BJ, Albani S. Modulation of T cell function by combination of epitope specific and low dose anticytokine therapy controls autoimmune arthritis. PLoS ONE. 2006; 87 Suppl 1: 1–9.
   Google Scholar
• Tremoulet AH, Albani S. Novel therapies for rheumatoid arthritis. Expert Opin Investig Drugs. 2006; 15:1427–1441.
   PubMed Web of Science ®Google Scholar
• Hauet-Broere F, Wieten L, Guichelaar T, Berlo S, van der Zee R, van Eden W. Heat shock proteins induce T cell regulation of chronic inflammation. Ann Rheum Dis. 2006; 65:65–68.
   Google Scholar
• Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor Foxp3. Immunity. 2005; 22:329–341.
   PubMed Web of Science ®Google Scholar
• Von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol. 2005; 6:338–344.
   PubMed Web of Science ®Google Scholar
• Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008; 133:775–787.
   PubMed Web of Science ®Google Scholar
• Ulmansky R, Cohen CJ, Szafer F, Moallem E, Fridlender ZG, Kashi Y, Naparstek Y. Resistance to adjuvant arthritis is due to protective antibodies against heat shock protein surface epitopes and the induction of IL-10 secretion. J Immunol. 2002; 168:6463–6469.
   PubMedGoogle Scholar
• Van Eden W, Van der Zee R, Paul AGA, Prakken BJ, Wendling U, Anderton SM, Wauben M. Do heat shock proteins control the balance of T cell regulation in inflammatory diseases?. Immunol Today. 1998; 19:303–307.
   PubMedGoogle Scholar
• Paul AG, van Kooten PJ, van Eden W, van der Zee R. Highly autoproliferative T cells specific for 60-kDa heat shock protein produce IL-4/IL-10 and IFNγ and are protective in adjuvant arthritis. J Immunol. 2000; 165:7270–7277.
   PubMed Web of Science ®Google Scholar
• Choy EH, Panayi GS. Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med. 2001; 344:904–916.
   Google Scholar
• Leipe J, Skapenko A, Lipsky PE, Schulze-Koops H. Regulatory T cells in rheumatoid arthritis. Arthritis Res Ther. 2005; 7:93.
   PubMed Web of Science ®Google Scholar
• Van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber F, Taams LS. CD4+CD25+ regulatory T cells in rheumatoid arthritis: Differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum. 2004; 50:2775–2785.
   PubMed Web of Science ®Google Scholar
• Zrour SH, Boumiza R, Sakly N, Mannai R, Korbaa W, Younes M, Bejia I, Touzi M, Bergaoui N. The impact of pregnancy on rheumatoid arthritis outcome: The role of maternofetal HLA class II disparity. Joint Bone Spine. 2009; 77 1: 36–40.
   Google Scholar
• Borchers AT, Naguwa SM, Keen CL, Gershwin ME. The implications of autoimmunity and pregnancy. J Autoimmun. 2009; 34:287–299.
   Google Scholar