Treatment of new onset type 1 diabetes with teplizumab: successes and pitfalls in development

Bibliography

• CDC. National diabetes fact sheet: national estimates and general information on diabetes and prediabetes in the United States. Center for Disease Control and Prevention, USA; 2011
   Google Scholar
• Eisenbarth GS. Type I diabetes mellitus. A chronic autoimmune disease. N Engl J Med 1986;314(21):1360-8
   PubMed Web of Science ®Google Scholar
• Herold KC, Vignali DA, Cooke A, Bluestone JA. Type 1 diabetes: translating mechanistic observations into effective clinical outcomes. Nat Rev Immunol 2013;13(4):243-56
   PubMed Web of Science ®Google Scholar
• Chatenoud L. Immune therapy for type 1 diabetes mellitus-what is unique about anti-CD3 antibodies? Nature reviews Endocrinol 2010;6(3):149-57
   PubMed Web of Science ®Google Scholar
• Bougneres PF, Landais P, Boisson C, et al. Limited duration of remission of insulin dependency in children with recent overt type I diabetes treated with low-dose cyclosporin. Diabetes 1990;39(10):1264-72
   PubMed Web of Science ®Google Scholar
• Parving HH, Tarnow L, Nielsen FS, et al. Cyclosporine nephrotoxicity in type 1 diabetic patients. A 7-year follow-up study. Diabetes Care 1999;22(3):478-83
   PubMed Web of Science ®Google Scholar
• Silverstein J, Maclaren N, Riley W, et al. Immunosuppression with azathioprine and prednisone in recent-onset insulin-dependent diabetes mellitus. N Engl J Med 1988;319(10):599-604
   PubMed Web of Science ®Google Scholar
• Eisenbarth GS, Srikanta S, Jackson R, et al. Anti-thymocyte globulin and prednisone immunotherapy of recent onset type 1 diabetes mellitus. Diabetes Res 1985;2(6):271-6
   PubMedGoogle Scholar
• Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H, et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N Engl J Med 2009;361(22):2143-52
   PubMed Web of Science ®Google Scholar
• Orban T, Bundy B, Becker DJ, et al. Co-stimulation modulation with abatacept in patients with recent-onset type 1 diabetes: a randomised, double-blind, placebo-controlled trial. Lancet 2011;378(9789):412-19
   PubMed Web of Science ®Google Scholar
• Rigby MR, DiMeglio LA, Rendell MS, et al. Targeting of memory T cells with alefacept in new-onset type 1 diabetes (T1DAL study): 12 month results of a randomised, double-blind, placebo-controlled phase 2 trial. Lancet Diabetes Endocrinol 2013;1(4):284-94
   PubMed Web of Science ®Google Scholar
• Pescovitz MD, Greenbaum CJ, Bundy B, et al. B-lymphocyte depletion with rituximab and beta-cell function: two-year results. Diabetes Care. 2013. [ Epub ahead of print]
   Google Scholar
• Moran A, Bundy B, Becker DJ, et al. Interleukin-1 antagonism in type 1 diabetes of recent onset: two multicentre, randomised, double-blind, placebo-controlled trials. Lancet 2013;381(9881):1905-15
   PubMed Web of Science ®Google Scholar
• Agardh CD, Lynch KF, Palmer M, et al.65 vaccination: 5 years of follow-up in a randomised dose-escalating study in adult-onset autoimmune diabetes. Diabetologia 2009;52(7):1363-8
   PubMed Web of Science ®Google Scholar
• Mastrandrea L, Yu J, Behrens T, et al. Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care 2009;32(7):1244-9
   PubMed Web of Science ®Google Scholar
• Roep BO, Solvason N, Gottlieb PA, et al. Plasmid-encoded proinsulin preserves C-peptide while specifically reducing proinsulin-specific CD8(+) T cells in type 1 diabetes. Sci Transl Med 2013;5(191):191ra82
   PubMedGoogle Scholar
• Chatenoud L, Primo J, Bach JF. CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice. J Immunol 1997;158(6):2947-54
   PubMed Web of Science ®Google Scholar
• You S, Leforban B, Garcia C, et al. Adaptive TGF-beta-dependent regulatory T cells control autoimmune diabetes and are a privileged target of anti-CD3 antibody treatment. Proc Natl Acad Sci USA 2007;104(15):6335-40
   PubMed Web of Science ®Google Scholar
• You S, Slehoffer G, Barriot S, et al. Unique role of CD4+CD62L+ regulatory T cells in the control of autoimmune diabetes in T cell receptor transgenic mice. Proc Natl Acad Sci USA 2004;101(Suppl 2):14580-5
   PubMedGoogle Scholar
• Belghith M, Bluestone JA, Barriot S, et al. F-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 2003;9(9):1202-8
   PubMed Web of Science ®Google Scholar
• You S, Zuber J, Kuhn C, et al. Induction of allograft tolerance by monoclonal CD3 antibodies: a matter of timing. Am J Transplant 2012;12(11):2909-19
   PubMed Web of Science ®Google Scholar
• Penaranda C, Tang Q, Bluestone JA. Anti-CD3 therapy promotes tolerance by selectively depleting pathogenic cells while preserving regulatory T cells. J Immunol 2011;187(4):2015-22
   PubMed Web of Science ®Google Scholar
• Goto R, You S, Zaitsu M, et al. Delayed anti-CD3 therapy results in depletion of alloreactive T cells and the dominance of foxp3(+) CD4(+) graft infiltrating cells. Am J Transplant 2013;13(7):1655-64
   PubMed Web of Science ®Google Scholar
• Esplugues E, Huber S, Gagliani N, et al. Control of TH17 cells occurs in the small intestine. Nature 2011;475(7357):514-18
   PubMed Web of Science ®Google Scholar
• Waldron-Lynch F, Henegariu O, Deng S, et al. Teplizumab induces human gut-tropic regulatory cells in humanized mice and patients. Sci Transl Med 2012;4(118):118ra12
   PubMed Web of Science ®Google Scholar
• Cosimi AB, Colvin RB, Burton RC, et al. Use of monoclonal antibodies to T-cell subsets for immunologic monitoring and treatment in recipients of renal allografts. N Engl J Med 1981;305(6):308-14
   PubMed Web of Science ®Google Scholar
• Hooks MA, Wade CS, Millikan WJ Jr. Muromonab CD-3: a review of its pharmacology, pharmacokinetics, and clinical use in transplantation. Pharmacotherapy 1991;11(1):26-37
   PubMed Web of Science ®Google Scholar
• Chatenoud L, Baudrihaye MF, Chkoff N, et al. Restriction of the human in vivo immune response against the mouse monoclonal antibody OKT3. J Immunol 1986;137(3):830-8
   PubMed Web of Science ®Google Scholar
• Chatenoud L, Ferran C, Legendre C, et al. In vivo cell activation following OKT3 administration. Systemic cytokine release and modulation by corticosteroids. Transplantation 1990;49(4):697-702
   PubMed Web of Science ®Google Scholar
• Smith KG, Austyn JM, Hariri G, et al. T cell activation by anti-T3 antibodies: comparison of IgG1 and IgG2b switch variants and direct evidence for accessory function of macrophage Fc receptors. Eur J Immunol 1986;16(5):478-86
   PubMed Web of Science ®Google Scholar
• Parren PW, Warmerdam PA, Boeije LC, et al. Characterization of IgG FcR-mediated proliferation of human T cells induced by mouse and human anti-CD3 monoclonal antibodies. Identification of a functional polymorphism to human IgG2 anti-CD3. J Immunol 1992;148(3):695-701
   PubMed Web of Science ®Google Scholar
• Vallhonrat H, Williams WW, Cosimi AB, et al. In vivo generation of C4d, Bb, iC3b, and SC5b-9 after OKT3 administration in kidney and lung transplant recipients. Transplantation 1999;67(2):253-8
   PubMed Web of Science ®Google Scholar
• Woodle ES, Thistlethwaite JR, Ghobrial IA, et al.3 F(ab’)2 fragments--retention of the immunosuppressive properties of whole antibody with marked reduction in T cell activation and lymphokine release. Transplantation 1991;52(2):354-60
   PubMed Web of Science ®Google Scholar
• Cole MS, Stellrecht KE, Shi JD, et al. HuM291, a humanized anti-CD3 antibody, is immunosuppressive to T cells while exhibiting reduced mitogenicity in vitro. Transplantation 1999;68(4):563-71
   PubMed Web of Science ®Google Scholar
• Xu D, Alegre ML, Varga SS, et al. In vitro characterization of five humanized OKT3 effector function variant antibodies. Cell Immunol 2000;200(1):16-26
   PubMed Web of Science ®Google Scholar
• Daifotis AG, Koenig S, Chatenoud L, Herold KC. Anti-CD3 clinical trials in type 1 diabetes mellitus. Clin Immunol 2013;149(3):268-78
   PubMed Web of Science ®Google Scholar
• Hagopian W, Ferry RJ, Jr. Sherry N, et al. Teplizumab preserves C-peptide in recent-onset type 1 diabetes: 2-year results from the randomized, placebo-controlled Protege trial. Diabetes 2013;62(11):3901-8
   Google Scholar
• Woodle ES, Bluestone JA, Zivin RA, et al. Humanized, nonmitogenic OKT3 antibody, huOKT3 gamma(Ala-Ala): initial clinical experience. Transplant Proc 1998;30(4):1369-70
   PubMed Web of Science ®Google Scholar
• Utset TO, Auger JA, Peace D, et al. Modified anti-CD3 therapy in psoriatic arthritis: a phase I/II clinical trial. J Rheumatol 2002;29(9):1907-13
   PubMed Web of Science ®Google Scholar
• Herold KC, Hagopian W, Auger JA, et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N Engl J Med 2002;346(22):1692-8
   PubMed Web of Science ®Google Scholar
• Herold KC, Gitelman SE, Masharani U, et al. A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 2005;54(6):1763-9
   PubMed Web of Science ®Google Scholar
• Herold KC, Gitelman S, Greenbaum C, et al. Treatment of patients with new onset Type 1 diabetes with a single course of anti-CD3 mAb Teplizumab preserves insulin production for up to 5 years. Clin Immunol 2009;132(2):166-73
   PubMed Web of Science ®Google Scholar
• Keymeulen B, Vandemeulebroucke E, Ziegler AG, et al. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N Engl J Med 2005;352(25):2598-608
   PubMed Web of Science ®Google Scholar
• Keymeulen B, Walter M, Mathieu C, et al. Four-year metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset type 1 diabetic patients depends on their age and baseline residual beta cell mass. Diabetologia 2010;53(4):614-23
   PubMed Web of Science ®Google Scholar
• Sherry N, Hagopian W, Ludvigsson J, et al. Teplizumab for treatment of type 1 diabetes (Protege study): 1-year results from a randomised, placebo-controlled trial. Lancet 2011;378(9790):487-97
   PubMed Web of Science ®Google Scholar
• Herold KC, Gitelman SE, Ehlers MR, et al. Teplizumab (anti-CD3 mAb) treatment preserves C-peptide responses in patients with new-onset type 1 diabetes in a randomized controlled trial: metabolic and immunologic features at baseline identify a subgroup of responders. Diabetes 2013;62(11):3766-74
   Google Scholar
• Herold KC, Gitelman SE, Willi SM, et al. Teplizumab treatment may improve C-peptide responses in participants with type 1 diabetes after the new-onset period: a randomised controlled trial. Diabetologia 2013;56(2):391-400
   PubMed Web of Science ®Google Scholar
• Sherry NA, Kushner JA, Glandt M, et al. Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes 2006;55(12):3238-45
   PubMed Web of Science ®Google Scholar
• Lebastchi J, Deng S, Lebastchi AH, et al. Immune therapy and beta-cell death in type 1 diabetes. Diabetes 2013;62(5):1676-80
   PubMed Web of Science ®Google Scholar
• Bisikirska B, Colgan J, Luban J, et al.R stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8+CD25+ Tregs. J Clin Invest 2005;115(10):2904-13
   PubMed Web of Science ®Google Scholar
• Ablamunits V, Bisikirska B, Herold KC. Acquisition of regulatory function by human CD8(+) T cells treated with anti-CD3 antibody requires TNF. Eur J Immunol 2010;40(10):2891-901
   PubMed Web of Science ®Google Scholar
• Ablamunits V, Henegariu O, Preston-Hurlburt P, Herold KC. NKG2A is a marker for acquisition of regulatory function by human CD8+ T cells activated with anti-CD3 antibody. Eur J Immunol 2011;41(7):1832-42
   PubMed Web of Science ®Google Scholar
• Ablamunits V, Bisikirska BC, Herold KC. Human regulatory CD8 T cells. Ann NY Acad Sci 2008;1150:234-8
   PubMed Web of Science ®Google Scholar
• Ablamunits V, Henegariu O, Hansen JB, et al. Synergistic reversal of type 1 diabetes in NOD mice with anti-CD3 and interleukin-1 blockade: evidence of improved immune regulation. Diabetes 2012;61(1):145-54
   PubMedGoogle Scholar
• Takiishi T, Korf H, Van Belle TL, et al. Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. J Clin Invest 2012;122(5):1717-25
   PubMed Web of Science ®Google Scholar
• Sherry NA, Chen W, Kushner JA, et al. Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 monoclonal antibody by enhancing recovery of beta-cells. Endocrinology 2007;148(11):5136-44
   PubMed Web of Science ®Google Scholar
• Bresson D, Togher L, Rodrigo E, et al. Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J Clin Invest 2006;116(5):1371-81
   PubMed Web of Science ®Google Scholar
• Palmer JP, Fleming GA, Greenbaum CJ, et al. C-peptide is the appropriate outcome measure for type 1 diabetes clinical trials to preserve beta-cell function: report of an ADA workshop, 21-22 October 2001. Diabetes 2004;53(1):250-64
   PubMedGoogle Scholar
• Steffes MW, Sibley S, Jackson M. Thomas W. beta-Cell function and the development of diabetes-related complications in the diabetes control and complications trial. Diabetes Care 2003;26(3):832-6
   PubMed Web of Science ®Google Scholar
• Stiller CR, Dupre J, Gent M, et al. Effects of cyclosporine immunosuppression in insulin-dependent diabetes mellitus of recent onset. Science 1984;223(4643):1362-7
   PubMed Web of Science ®Google Scholar
• Greenbaum CJ, Beam CA, Boulware D, et al. Fall in C-peptide during first 2 years from diagnosis: evidence of at least two distinct phases from composite Type 1 Diabetes TrialNet data. Diabetes 2012;61(8):2066-73
   PubMed Web of Science ®Google Scholar
• McClymont SA, Putnam AL, Lee MR, et al. Plasticity of human regulatory T cells in healthy subjects and patients with type 1 diabetes. J Immunol 2011;186(7):3918-26
   PubMed Web of Science ®Google Scholar
• Andris F, Van Mechelen M, De Mattia F, et al. Induction of T cell unresponsiveness by anti-CD3 antibodies occurs independently of co-stimulatory functions. Eur J Immunol 1996;26(5):1187-95
   PubMed Web of Science ®Google Scholar
• Andris F, Denanglaire S, de Mattia F, et al. Naive T cells are resistant to anergy induction by anti-CD3 antibodies. J Immunol 2004;173(5):3201-8
   PubMed Web of Science ®Google Scholar