IL-35 inhibits acute graft-versus-host disease in a mouse model

Ferrara, 2009, Graft-versus-host disease, Lancet, 373, 1550, 10.1016/S0140-6736(09)60237-3 Antin, 1992, Cytokine dysregulation and acute graft-versus-host disease, Blood, 80, 2964, 10.1182/blood.V80.12.2964.2964 Vignali, 2012, IL-12 family cytokines: immunological playmakers, Nat. Immunol., 13, 722, 10.1038/ni.2366 Devergne, 1996, A novel interleukin-12 p40-related protein induced by latent Epstein–Barr virus infection in B lymphocytes, J. Virol., 70, 1143, 10.1128/JVI.70.2.1143-1153.1996 Collison, 2007, The inhibitory cytokine IL-35 contributes to regulatory T-cell function, Nature, 450, 566, 10.1038/nature06306 Niedbala, 2007, IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells, Eur. J. Immunol., 37, 3021, 10.1002/eji.200737810 Whitehead, 2012, IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease, J. Allergy Clin. Immunol., 129, 207, 10.1016/j.jaci.2011.08.009 Wirtz, 2011, Interleukin-35 mediates mucosal immune responses that protect against T-cell-dependent colitis, Gastroenterology, 141, 1875, 10.1053/j.gastro.2011.07.040 Zhang, 2015, Reduced IL-35 levels are associated with increased platelet aggregation and activation in patients with acute graft-versus-host disease after allogeneic hematopoietic stem cell transplantation, Ann. Hematol., 94, 837, 10.1007/s00277-014-2278-7 Vezina, 1975, Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle, J. Antibiot. (Tokyo), 28, 721, 10.7164/antibiotics.28.721 Couriel, 2005, Sirolimus in combination with tacrolimus and corticosteroids for the treatment of resistant chronic graft-versus-host disease, Br. J. Haematol., 130, 409, 10.1111/j.1365-2141.2005.05616.x Antin, 2003, Sirolimus, tacrolimus, and low-dose methotrexate for graft-versus-host disease prophylaxis in mismatched related donor or unrelated donor transplantation, Blood, 102, 1601, 10.1182/blood-2003-02-0489 Kahan, 2001, Rapamycin: clinical results and future opportunities, Transplantation, 72, 1181, 10.1097/00007890-200110150-00001 Battaglia, 2005, Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells, Blood, 105, 4743, 10.1182/blood-2004-10-3932 Wang, 2012, Rapamycin combined with allogenic immature dendritic cells selectively expands CD4+CD25+Foxp3+ regulatory T cells in rats, Hepatobiliary Pancreat. Dis. Int., 11, 203, 10.1016/S1499-3872(12)60149-0 Zeiser, 2006, Inhibition of CD4+CD25+ regulatory T-cell function by calcineurin-dependent interleukin-2 production, Blood, 108, 390, 10.1182/blood-2006-01-0329 Kuroiwa, 2001, Hepatocyte growth factor ameliorates acute graft-versus-host disease and promotes hematopoietic function, J. Clin. Invest., 107, 1365, 10.1172/JCI11808 Kuroiwa, 2006, Hepatocyte growth factor prevents lupus nephritis in a murine lupus model of chronic graft-versus-host disease, Arthritis Res. Ther., 8, R123, 10.1186/ar2012 Bouazzaoui, 2011, Steroid treatment alters adhesion molecule and chemokine expression in experimental acute graft-vs.-host disease of the intestinal tract, Exp. Hematol., 39, 238, 10.1016/j.exphem.2010.11.006 Imado, 2004, Hepatocyte growth factor preserves graft-versus-leukemia effect and T-cell reconstitution after marrow transplantation, Blood, 104, 1542, 10.1182/blood-2003-12-4309 Zeiser, 2008, Differential impact of mammalian target of rapamycin inhibition on CD4+CD25+Foxp3+ regulatory T cells compared with conventional CD4+ T cells, Blood, 111, 453, 10.1182/blood-2007-06-094482 Phung, 2007, Endothelial Akt signaling is rate-limiting for rapamycin inhibition of mouse mammary tumor progression, Cancer Res., 67, 5070, 10.1158/0008-5472.CAN-06-3341 Gavrieli, 1992, Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation, J. Cell Biol., 119, 493, 10.1083/jcb.119.3.493 Xu, 2013, Tryptophan metabolite analog, N-(3,4-dimethoxycinnamonyl) anthranilic acid, ameliorates acute graft-versus-host disease through regulating T cell proliferation and polarization, Int. Immunopharmacol., 17, 601, 10.1016/j.intimp.2013.08.004 Cooke, 1996, An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin, Blood, 88, 3230, 10.1182/blood.V88.8.3230.bloodjournal8883230 Hill, 1997, Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines, Blood, 90, 3204, 10.1182/blood.V90.8.3204 Stuber, 1998, Involvement of OX40–OX40L interactions in the intestinal manifestations of the murine acute graft-versus-host disease, Gastroenterology, 115, 1205, 10.1016/S0016-5085(98)70092-7 Krenger, 2000, Thymic atrophy in murine acute graft-versus-host disease is effected by impaired cell cycle progression of host pro-T and pre-T cells, Blood, 96, 347, 10.1182/blood.V96.1.347 Ghayur, 1988, Complete sequential regeneration of graft-vs.-host-induced severely dysplastic thymuses. Implications for the pathogenesis of chronic graft-vs.-host disease, Am. J. Pathol., 133, 39 Collison, 2012, The composition and signaling of the IL-35 receptor are unconventional, Nat. Immunol., 13, 290, 10.1038/ni.2227 Devergne, 1997, Epstein–Barr virus-induced gene 3 and the p35 subunit of interleukin 12 form a novel heterodimeric hematopoietin, Proc. Natl. Acad. Sci. U. S. A., 94, 12,041, 10.1073/pnas.94.22.12041 Collison, 2010, IL-35-mediated induction of a potent regulatory T cell population, Nat. Immunol., 11, 1093, 10.1038/ni.1952 Tirotta, 2013, Epstein–Barr virus-induced gene 3 negatively regulates neuroinflammation and T cell activation following coronavirus-induced encephalomyelitis, J. Neuroimmunol., 254, 110, 10.1016/j.jneuroim.2012.10.005 Liu, 2012, Increased Th17 and regulatory T cell responses in EBV-induced gene 3-deficient mice lead to marginally enhanced development of autoimmune encephalomyelitis, J. Immunol., 188, 3099, 10.4049/jimmunol.1100106 Thiolat, 2014, Interleukin-35 gene therapy exacerbates experimental rheumatoid arthritis in mice, Cytokine, 69, 87, 10.1016/j.cyto.2014.05.015 Bardel, 2008, Human CD4+ CD25+ Foxp3+ regulatory T cells do not constitutively express IL-35, J. Immunol., 181, 6898, 10.4049/jimmunol.181.10.6898 Allan, 2008, Inducible reprogramming of human T cells into Treg cells by a conditionally active form of FOXP3, Eur. J. Immunol., 38, 3282, 10.1002/eji.200838373 Kuo, 2011, Interleukin-35 enhances Lyme arthritis in Borrelia-vaccinated and -infected mice, Clin. Vaccine Immunol., 18, 1125, 10.1128/CVI.00052-11 Collison, 2009, Regulatory T cell suppression is potentiated by target T cells in a cell contact, IL-35- and IL-10-dependent manner, J. Immunol., 182, 6121, 10.4049/jimmunol.0803646 Edinger, 2003, CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation, Nat. Med., 9, 1144, 10.1038/nm915 Taylor, 2002, The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality, Blood, 99, 3493, 10.1182/blood.V99.10.3493 Jurado, 2007, Sirolimus as part of immunosuppressive therapy for refractory chronic graft-versus-host disease, Biol. Blood Marrow Transplant., 13, 701, 10.1016/j.bbmt.2007.02.003 Cutler, 2014, Tacrolimus/sirolimus vs tacrolimus/methotrexate as GVHD prophylaxis after matched, related donor allogeneic HCT, Blood, 124, 1372, 10.1182/blood-2014-04-567164 Battaglia, 2006, Rapamycin promotes expansion of functional CD4+CD25+FOXP3+ regulatory T cells of both healthy subjects and type 1 diabetic patients, J. Immunol., 177, 8338, 10.4049/jimmunol.177.12.8338 Qian, 2013, Advances in the treatment of acute graft-versus-host disease, J. Cell. Mol. Med., 17, 966, 10.1111/jcmm.12093 Dalton, 1993, Multiple defects of immune cell function in mice with disrupted interferon-gamma genes, Science, 259, 1739, 10.1126/science.8456300 Ferrara, 1999, Pathophysiologic mechanisms of acute graft-vs.-host disease, Biol. Blood Marrow Transplant., 5, 347, 10.1016/S1083-8791(99)70011-X Murphy, 1998, Differential effects of the absence of interferon-gamma and IL-4 in acute graft-versus-host disease after allogeneic bone marrow transplantation in mice, J. Clin. Invest., 102, 1742, 10.1172/JCI3906 Welniak, 2000, Opposing roles of interferon-gamma on CD4+ T cell-mediated graft-versus-host disease: effects of conditioning, Biol. Blood Marrow Transplant., 6, 604, 10.1016/S1083-8791(00)70025-5 Koenecke, 2012, IFN-gamma production by allogeneic Foxp3+ regulatory T cells is essential for preventing experimental graft-versus-host disease, J. Immunol., 189, 2890, 10.4049/jimmunol.1200413 Zhao, 2011, IL-17-producing T cells contribute to acute graft-versus-host disease in patients undergoing unmanipulated blood and marrow transplantation, Eur. J. Immunol., 41, 514, 10.1002/eji.201040793 Reddy, 2003, Immunobiology of acute graft-versus-host disease, Blood Rev., 17, 187, 10.1016/S0268-960X(03)00009-2 Ferrara, 2005, Acute graft versus host disease: pathophysiology, risk factors, and prevention strategies, Clin. Adv. Hematol. Oncol., 3, 415 van den Brink, 2000, Graft-versus-host-disease-associated thymic damage results in the appearance of T cell clones with anti-host reactivity, Transplantation, 69, 446, 10.1097/00007890-200002150-00026 Rossi, 2002, Keratinocyte growth factor preserves normal thymopoiesis and thymic microenvironment during experimental graft-versus-host disease, Blood, 100, 682, 10.1182/blood.V100.2.682 Weinberg, 2001, Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation, Blood, 97, 1458, 10.1182/blood.V97.5.1458 Wang, 2014, Interleukin-35 induces regulatory B cells that suppress autoimmune disease, Nat. Med., 20, 633, 10.1038/nm.3554