Immunotherapeutic strategies in autoimmune uveitis

Gritz, 2004, Incidence and prevalence of uveitis in Northern California; the Northern California Epidemiology of Uveitis Study, Ophthalmology, 111, 491, 10.1016/j.ophtha.2003.06.014 Whitcup, 1997, Immunologic mechanisms of uveitis. New targets for immunomodulation, Arch Ophthalmol, 115, 520, 10.1001/archopht.1997.01100150522013 Selmi, 2014, Diagnosis and classification of autoimmune uveitis, Autoimmun Rev, 13, 591, 10.1016/j.autrev.2014.01.006 Comarmond, 2014, Biotherapies in Behcet's disease, Autoimmun Rev, 13, 762, 10.1016/j.autrev.2014.01.056 Selmi, 2014, Diagnosis and classification of reactive arthritis, Autoimmun Rev, 13, 546, 10.1016/j.autrev.2014.01.005 Jamilloux, 2014, Sarcoidosis and uveitis, Autoimmun Rev, 13, 840, 10.1016/j.autrev.2014.04.001 Sakata, 2014, Diagnosis and classification of Vogt–Koyanagi–Harada disease, Autoimmun Rev, 13, 550, 10.1016/j.autrev.2014.01.023 Greco, 2013, Vogt–Koyanagi–Harada syndrome, Autoimmun Rev, 12, 1033, 10.1016/j.autrev.2013.01.004 Wacker, 1977, Experimental allergic uveitis. Isolation, characterization, and localization of a soluble uveitopathogenic antigen from bovine retina, J Immunol, 119, 1949, 10.4049/jimmunol.119.6.1949 Gery, 1986, Uveoretinitis and pinealitis induced by immunization with interphotoreceptor retinoid-binding protein, Invest Ophthalmol Vis Sci, 27, 1296 Roitt, 1993, The role of autoantigens in the driving of autoimmune diseases, Immunol Ser, 59, 119 Pennesi, 2003, A humanized model of experimental autoimmune uveitis in HLA class II transgenic mice, J Clin Invest, 111, 1171, 10.1172/JCI15155 Medawar, 1961, Immunological tolerance, Nature, 189, 14, 10.1038/189014a0 Caspi, 2006, Ocular autoimmunity: the price of privilege?, Immunol Rev, 213, 23, 10.1111/j.1600-065X.2006.00439.x Ohta, 1999, Effects of experimental ocular inflammation on ocular immune privilege, Invest Ophthalmol Vis Sci, 40, 2010 Hamrah, 2007, Corneal antigen-presenting cells, Chem Immunol Allergy, 92, 58, 10.1159/000099254 Forrester, 2010, Dendritic cell physiology and function in the eye, Immunol Rev, 234, 282, 10.1111/j.0105-2896.2009.00873.x Griffith, 1997, The role of FasL-induced apoptosis in immune privilege, Immunol Today, 18, 240, 10.1016/S0167-5699(97)81663-5 Usui, 2008, Functional expression of B7H1 on retinal pigment epithelial cells, Exp Eye Res, 86, 52, 10.1016/j.exer.2007.09.007 Sugita, 2006, B7+ iris pigment epithelial cells convert T cells into CTLA-4+, B7-expressing CD8+ regulatory T cells, Invest Ophthalmol Vis Sci, 47, 5376, 10.1167/iovs.05-1354 Sugita, 2008, Retinal pigment epithelium-derived CTLA-2alpha induces TGFbeta-producing T regulatory cells, J Immunol, 181, 7525, 10.4049/jimmunol.181.11.7525 Zhou, 2010, Ocular immune privilege, F1000 Biol Rep, 2 Forrester, 2008, Immune privilege or privileged immunity?, Mucosal Immunol, 1, 372, 10.1038/mi.2008.27 Taylor, 1997, Relationships between stress, protein damage, nutrition, and age-related eye diseases, Mol Aspects Med, 18, 305, 10.1016/S0098-2997(95)00049-6 Yoshida, 2000, Participation of pigment epithelium of iris and ciliary body in ocular immune privilege. 2. Generation of TGF-beta-producing regulatory T cells, Invest Ophthalmol Vis Sci, 41, 3862 Zamiri, 2007, Immunosuppressive properties of the pigmented epithelial cells and the subretinal space, Chem Immunol Allergy, 92, 86, 10.1159/000099259 Sugita, 2010, Suppression of bystander T helper 1 cells by iris pigment epithelium-inducing regulatory T cells via negative costimulatory signals, Invest Ophthalmol Vis Sci, 51, 2529, 10.1167/iovs.09-4460 DeVoss, 2006, Spontaneous autoimmunity prevented by thymic expression of a single self-antigen, J Exp Med, 203, 2727, 10.1084/jem.20061864 Biscette, 2007, Uveitis Diagnosis, Management, and Treatment Retinal Physician Rothova, 1992, Uveitis and systemic disease, Br J Ophthalmol, 76, 137, 10.1136/bjo.76.3.137 Heo, 2012, The role of biologic agents in the management of non-infectious uveitis, Expert Opin Biol Ther, 12, 995, 10.1517/14712598.2012.688021 Smith, 2005, A randomized, placebo-controlled, double-masked clinical trial of etanercept for the treatment of uveitis associated with juvenile idiopathic arthritis, Arthritis Rheum, 53, 18, 10.1002/art.20904 Foster, 2003, Efficacy of etanercept in preventing relapse of uveitis controlled by methotrexate, Arch Ophthalmol, 121, 437, 10.1001/archopht.121.4.437 Smith, 2001, Differential efficacy of tumor necrosis factor inhibition in the management of inflammatory eye disease and associated rheumatic disease, Arthritis Rheum, 45, 252, 10.1002/1529-0131(200106)45:3<252::AID-ART257>3.0.CO;2-5 Caspi, 2010, A look at autoimmunity and inflammation in the eye, J Clin Invest, 120, 3073, 10.1172/JCI42440 Gasparin, 2012, Experimental models of autoimmune inflammatory ocular diseases, Arq Bras Oftalmol, 75, 143, 10.1590/S0004-27492012000200016 Caspi, 1988, A new model of autoimmune disease. Experimental autoimmune uveoretinitis induced in mice with two different retinal antigens, J Immunol, 140, 1490, 10.4049/jimmunol.140.5.1490 Wildner, 2013, What causes relapses of autoimmune diseases? The etiological role of autoreactive T cells, Autoimmun Rev, 12, 1070, 10.1016/j.autrev.2013.04.001 Sun, 1997, Genetic susceptibility to experimental autoimmune uveitis involves more than a predisposition to generate a T helper-1-like or a T helper-2-like response, J Immunol, 159, 1004, 10.4049/jimmunol.159.2.1004 Rizzo, 1996, Establishment and characterization of a murine CD4+ T cell line and clone that induce experimental autoimmune uveoretinitis in B10.A mice, J Immunol, 156, 1654, 10.4049/jimmunol.156.4.1654 Jones, 1997, IFN-gamma-deficient mice develop experimental autoimmune uveitis in the context of a deviant effector response, J Immunol, 158, 5997, 10.4049/jimmunol.158.12.5997 Tang, 2007, Autoimmune uveitis elicited with antigen-pulsed dendritic cells has a distinct clinical signature and is driven by unique effector mechanisms: initial encounter with autoantigen defines disease phenotype, J Immunol, 178, 5578, 10.4049/jimmunol.178.9.5578 Amadi-Obi, 2007, TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1, Nat Med, 13, 711, 10.1038/nm1585 Luger, 2008, Either a Th17 or a Th1 effector response can drive autoimmunity: conditions of disease induction affect dominant effector category, J Exp Med, 205, 799, 10.1084/jem.20071258 Vallochi, 2007, The role of cytokines in the regulation of ocular autoimmune inflammation, Cytokine Growth Factor Rev, 18, 135, 10.1016/j.cytogfr.2007.01.012 Horai, 2013, Breakdown of immune privilege and spontaneous autoimmunity in mice expressing a transgenic T cell receptor specific for a retinal autoantigen, J Autoimmun, 44, 21, 10.1016/j.jaut.2013.06.003 Chen, 2013, Comparative analysis of induced vs. spontaneous models of autoimmune uveitis targeting the interphotoreceptor retinoid binding protein, PLoS One, 8, e72161, 10.1371/journal.pone.0072161 Caspi, 1992, Immunogenetic aspects of clinical and experimental uveitis, Reg Immunol, 4, 321 Davey, 2000, The human leukocyte antigen complex and chronic ocular inflammatory disorders, Am J Ophthalmol, 129, 235, 10.1016/S0002-9394(99)00433-X Levinson, 2007, Immunogenetics of ocular inflammatory disease, Tissue Antigens, 69, 105, 10.1111/j.1399-0039.2006.00743.x de Smet, 1990, Cellular immune responses of patients with uveitis to retinal antigens and their fragments, Am J Ophthalmol, 110, 135, 10.1016/S0002-9394(14)76981-8 Szpak, 2001, Spontaneous retinopathy in HLA-A29 transgenic mice, Proc Natl Acad Sci U S A, 98, 2572, 10.1073/pnas.051595998 Rosenbaum, 1980, Endotoxin-induced uveitis in rats as a model for human disease, Nature, 286, 611, 10.1038/286611a0 Broekhuyse, 1992, Experimental autoimmune anterior uveitis (EAAU). II. Dose-dependent induction and adoptive transfer using a melanin-bound antigen of the retinal pigment epithelium, Exp Eye Res, 55, 401, 10.1016/0014-4835(92)90112-6 Bora, 1995, Experimental autoimmune anterior uveitis. Induction with melanin-associated antigen from the iris and ciliary body, Invest Ophthalmol Vis Sci, 36, 1056 Matteson, 1999, Inhibition of experimental melanin protein-induced uveitis (EMIU) by targeting nitric oxide via phosphatidylcholine-specific phospholipase C, J Autoimmun, 13, 197, 10.1006/jaut.1999.0319 Rothlin, 2007, TAM receptors are pleiotropic inhibitors of the innate immune response, Cell, 131, 1124, 10.1016/j.cell.2007.10.034 Lu, 2001, Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family, Science, 293, 306, 10.1126/science.1061663 Ye, 2011, TAM receptor knockout mice are susceptible to retinal autoimmune induction, Invest Ophthalmol Vis Sci, 52, 4239, 10.1167/iovs.10-6700 Saadoun, 2013, Biotherapies in inflammatory ocular disorders: interferons, immunoglobulins, monoclonal antibodies, Autoimmun Rev, 12, 774, 10.1016/j.autrev.2013.02.002 Hoyer, 2008, Interleukin-2 in the development and control of inflammatory disease, Immunol Rev, 226, 19, 10.1111/j.1600-065X.2008.00697.x Banchereau, 2012, From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines, Nat Immunol, 13, 925, 10.1038/ni.2406 Chan, 1987, Immunohistochemical analysis of experimental autoimmune uveoretinitis (EAU) induced by interphotoreceptor retinoid-binding protein (IRBP) in the rat, Immunol Invest, 16, 63, 10.3109/08820138709055713 Roberge, 1989, Selective immunosuppression of activated T cells with the chimeric toxin IL-2-PE40. Inhibition of experimental autoimmune uveoretinitis, J Immunol, 143, 3498, 10.4049/jimmunol.143.11.3498 Higuchi, 1991, Combined anti-interleukin-2 receptor and low-dose cyclosporine therapy in experimental autoimmune uveoretinitis, J Autoimmun, 4, 113, 10.1016/0896-8411(91)90011-Z Guex-Crosier, 1997, Humanized antibodies against the alpha-chain of the IL-2 receptor and against the beta-chain shared by the IL-2 and IL-15 receptors in a monkey uveitis model of autoimmune diseases, J Immunol, 158, 452, 10.4049/jimmunol.158.1.452 Nussenblatt, 1999, Treatment of noninfectious intermediate and posterior uveitis with the humanized anti-Tac mAb: a phase I/II clinical trial, Proc Natl Acad Sci U S A, 96, 7462, 10.1073/pnas.96.13.7462 Nussenblatt, 2003, Humanized anti-interleukin-2 (IL-2) receptor alpha therapy: long-term results in uveitis patients and preliminary safety and activity data for establishing parameters for subcutaneous administration, J Autoimmun, 21, 283, 10.1016/S0896-8411(03)00113-6 Papaliodis, 2003, Treatment of ocular inflammatory disorders with daclizumab, Ophthalmology, 110, 786, 10.1016/S0161-6420(02)01932-2 Yeh, 2008, High-dose humanized anti-IL-2 receptor alpha antibody (daclizumab) for the treatment of active, non-infectious uveitis, J Autoimmun, 31, 91, 10.1016/j.jaut.2008.05.001 Kung, 1979, Monoclonal antibodies defining distinctive human T cell surface antigens, Science, 206, 347, 10.1126/science.314668 Chatenoud, 2003, CD3-specific antibody-induced active tolerance: from bench to bedside, Nat Rev Immunol, 3, 123, 10.1038/nri1000 Ochi, 2006, Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+ CD25−LAP+ T cells, Nat Med, 12, 627, 10.1038/nm1408 Wu, 2008, Nasal anti-CD3 antibody ameliorates lupus by inducing an IL-10-secreting CD4+ CD25− LAP+ regulatory T cell and is associated with down-regulation of IL-17+ CD4+ ICOS+ CXCR5+ follicular helper T cells, J Immunol, 181, 6038, 10.4049/jimmunol.181.9.6038 Herold, 1992, Prevention of autoimmune diabetes with nonactivating anti-CD3 monoclonal antibody, Diabetes, 41, 385, 10.2337/diab.41.3.385 Chatenoud, 1994, Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice, Proc Natl Acad Sci U S A, 91, 123, 10.1073/pnas.91.1.123 Herold, 2005, A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2years after onset of type 1 diabetes, Diabetes, 54, 1763, 10.2337/diabetes.54.6.1763 Utset, 2002, Modified anti-CD3 therapy in psoriatic arthritis: a phase I/II clinical trial, J Rheumatol, 29, 1907 Ke, 2011, Anti-CD3 antibody ameliorates experimental autoimmune uveitis by inducing both IL-10 and TGF-beta dependent regulatory T cells, Clin Immunol, 138, 311, 10.1016/j.clim.2010.12.016 Dean, 2012, Combination therapies in the context of anti-CD3 antibodies for the treatment of autoimmune diseases, Swiss Med Wkly, 142, w13711 Phillips, 2011, Current state of type 1 diabetes immunotherapy: incremental advances, huge leaps, or more of the same?, Clin Dev Immunol, 2011, 432016, 10.1155/2011/432016 Gross, 1992, Identification and distribution of the costimulatory receptor CD28 in the mouse, J Immunol, 149, 380, 10.4049/jimmunol.149.2.380 Greenwald, 2002, CTLA-4 regulates cell cycle progression during a primary immune response, Eur J Immunol, 32, 366, 10.1002/1521-4141(200202)32:2<366::AID-IMMU366>3.0.CO;2-5 Yao, 2011, B7-h2 is a costimulatory ligand for CD28 in human, Immunity, 34, 729, 10.1016/j.immuni.2011.03.014 Greenfield, 1998, CD28/B7 costimulation: a review, Crit Rev Immunol, 18, 389, 10.1615/CritRevImmunol.v18.i5.10 Stebbings, 2007, “Cytokine storm” in the phase I trial of monoclonal antibody TGN1412: better understanding the causes to improve preclinical testing of immunotherapeutics, J Immunol, 179, 3325, 10.4049/jimmunol.179.5.3325 St Clair, 2008, The calm after the cytokine storm: lessons from the TGN1412 trial, J Clin Invest, 118, 1344, 10.1172/JCI35382 Guinan, 1994, Pivotal role of the B7:CD28 pathway in transplantation tolerance and tumor immunity, Blood, 84, 3261, 10.1182/blood.V84.10.3261.3261 Takahashi, 2000, Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4, J Exp Med, 192, 303, 10.1084/jem.192.2.303 Stohl, 2008, Global T cell dysregulation in non-autoimmune-prone mice promotes rapid development of BAFF-independent, systemic lupus erythematosus-like autoimmunity, J Immunol, 181, 833, 10.4049/jimmunol.181.1.833 Pardoll, 2012, The blockade of immune checkpoints in cancer immunotherapy, Nat Rev Cancer, 12, 252, 10.1038/nrc3239 Ramsay, 2013, Immune checkpoint blockade immunotherapy to activate anti-tumour T-cell immunity, Br J Haematol, 162, 313, 10.1111/bjh.12380 Romo-Tena, 2013, CTLA-4 and autoimmunity: new insights into the dual regulator of tolerance, Autoimmun Rev, 12, 1171, 10.1016/j.autrev.2013.07.002 Kremer, 2003, Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig, N Engl J Med, 349, 1907, 10.1056/NEJMoa035075 Rosman, 2013, Biologic therapy for autoimmune diseases: an update, BMC Med, 11, 88, 10.1186/1741-7015-11-88 Bluestone, 2006, CTLA4Ig: bridging the basic immunology with clinical application, Immunity, 24, 233, 10.1016/j.immuni.2006.03.001 Salomon, 2001, Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation, Annu Rev Immunol, 19, 225, 10.1146/annurev.immunol.19.1.225 Moreland, 2002, Costimulatory blockade in patients with rheumatoid arthritis: a pilot, dose-finding, double-blind, placebo-controlled clinical trial evaluating CTLA-4Ig and LEA29Y eighty-five days after the first infusion, Arthritis Rheum, 46, 1470, 10.1002/art.10294 Larsen, 2005, Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties, Am J Transplant, 5, 443, 10.1111/j.1600-6143.2005.00749.x Tesavibul, 1998, Costimulatory molecules in ocular cicatricial pemphigoid, Invest Ophthalmol Vis Sci, 39, 982 Hardy, 1971, Benign mucous membrane pemphigoid, Arch Dermatol, 104, 467, 10.1001/archderm.1971.04000230009002 Fukai, 1999, The role of costimulatory molecules B7-1 and B7-2 in mice with experimental autoimmune uveoretinitis, Graefes Arch Clin Exp Ophthalmol, 237, 928, 10.1007/s004170050388 Silver, 2000, Blockade of costimulation through B7/CD28 inhibits experimental autoimmune uveoretinitis, but does not induce long-term tolerance, J Immunol, 165, 5041, 10.4049/jimmunol.165.9.5041 Verwaerde, 2003, Ocular transfer of retinal glial cells transduced ex vivo with adenovirus expressing viral IL-10 or CTLA4-Ig inhibits experimental autoimmune uveoretinitis, Gene Ther, 10, 1970, 10.1038/sj.gt.3302101 Zulian, 2010, Abatacept for severe anti-tumor necrosis factor alpha refractory juvenile idiopathic arthritis-related uveitis, Arthritis Care Res (Hoboken), 62, 821, 10.1002/acr.20115 Kenawy, 2011, Abatacept: a potential therapy in refractory cases of juvenile idiopathic arthritis-associated uveitis, Graefes Arch Clin Exp Ophthalmol, 249, 297, 10.1007/s00417-010-1523-6 Wu, 2012, Immunotherapies: the blockade of inhibitory signals, Int J Biol Sci, 8, 1420, 10.7150/ijbs.5273 Lipson, 2013, Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody, Clin Cancer Res, 19, 462, 10.1158/1078-0432.CCR-12-2625 Ortler, 2008, B7-H1 restricts neuroantigen-specific T cell responses and confines inflammatory CNS damage: implications for the lesion pathogenesis of multiple sclerosis, Eur J Immunol, 38, 1734, 10.1002/eji.200738071 Reynolds, 2012, Stimulation of the PD-1/PDL-1 T-cell co-inhibitory pathway is effective in treatment of experimental autoimmune glomerulonephritis, Nephrol Dial Transplant, 27, 1343, 10.1093/ndt/gfr529 Wong, 2013, Blockade of programmed death-1 in young (New Zealand Black×New Zealand White)F1 mice promotes the suppressive capacity of CD4+ regulatory T cells protecting from lupus-like disease, J Immunol, 190, 5402, 10.4049/jimmunol.1202382 Sporici, 2001, Costimulation of memory T-cells by ICOS: a potential therapeutic target for autoimmunity?, Clin Immunol, 100, 263, 10.1006/clim.2001.5093 Rottman, 2001, The costimulatory molecule ICOS plays an important role in the immunopathogenesis of EAE, Nat Immunol, 2, 605, 10.1038/89750 Hu, 2009, B7RP-1 blockade ameliorates autoimmunity through regulation of follicular helper T cells, J Immunol, 182, 1421, 10.4049/jimmunol.182.3.1421 Usui, 2006, The role of the ICOS/B7RP-1 T cell costimulatory pathway in murine experimental autoimmune uveoretinitis, Eur J Immunol, 36, 3071, 10.1002/eji.200636138 Hunig, 2007, Manipulation of regulatory T-cell number and function with CD28-specific monoclonal antibodies, Adv Immunol, 95, 111, 10.1016/S0065-2776(07)95004-X Poirier, 2010, Inducing CTLA-4-dependent immune regulation by selective CD28 blockade promotes regulatory T cells in organ transplantation, Sci Transl Med, 2, 17ra10, 10.1126/scitranslmed.3000116 Poirier, 2012, Preclinical efficacy and immunological safety of FR104, an antagonist anti-CD28 monovalent Fab′ antibody, Am J Transplant, 12, 2630, 10.1111/j.1600-6143.2012.04164.x Poirier, 2011, A more selective costimulatory blockade of the CD28-B7 pathway, Transpl Int, 24, 2, 10.1111/j.1432-2277.2010.01176.x Poirier, 2012, CD28-specific immunomodulating antibodies: what can be learned from experimental models?, Am J Transplant, 12, 1682, 10.1111/j.1600-6143.2012.04032.x