Manipulating T cell-mediated pathology: Targets and functions of monoclonal antibody immunotherapy

Clinical Immunology

Volumn 148, Issue 1, 2013, Pages 136-147

  Martin, Aaron ^a   Tisch, Roland M ^a   Getts, Daniel R ^b,c  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Tolera Therapeutics Inc   (United States)

Author keywords

Activation induced cell death; Anti thymocyte globulin; Antibody dependent cellular cytotoxicity; Lymphocyte immune globulin; T cell receptor

Indexed keywords

COMPLEMENT; MONOCLONAL ANTIBODY; T LYMPHOCYTE RECEPTOR;

B LYMPHOCYTE; CELL DEATH; CLONAL ANERGY; CYTOTOXICITY; EFFECTOR CELL; HUMAN; IMMUNOTHERAPY; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; AUTOIMMUNITY; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTES;

EID: 84878962832     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2013.04.011     Document Type: Review

References (129)

1. Boitard C., Sempe P., Bach J.F. Anti-TcR antibodies in autoimmune diseases. Immunol. Ser. 1993, 59:167-173.
2. Goldschmidt T.J., Holmdahl R. Therapeutic effects of monoclonal antibodies to alpha beta TCR but not to CD4 on collagen-induced arthritis in the rat. Cell. Immunol. 1994, 154:240-248.
3. Lavasani S., Dzhambazov B., Andersson M. Monoclonal antibody against T-cell receptor alphabeta induces self-tolerance in chronic experimental autoimmune encephalomyelitis. Scand. J. Immunol. 2007, 65:39-47.
4. Howard L.M., Kohm A.P., Castaneda C.L., Miller S.D. Therapeutic blockade of TCR signal transduction and co-stimulation in autoimmune disease. Curr. Drug Targets Inflamm. Allergy 2005, 4:205-216.
5. Kohm A.P., Williams J.S., Bickford A.L., McMahon J.S., Chatenoud L., Bach J.F., Bluestone J.A., Miller S.D. Treatment with nonmitogenic anti-CD3 monoclonal antibody induces CD4+ T cell unresponsiveness and functional reversal of established experimental autoimmune encephalomyelitis. J. Immunol. 2005, 174:4525-4534.
6. Timm M.M., Kimlinger T.K., Haug J.L., Kline M.P., Greipp P.R., Rajkumar S.V., Kumar S.K. Thymoglobulin targets multiple plasma cell antigens and has in vitro and in vivo activity in multiple myeloma. Leukemia 2006, 20:1863-1869.
7. Gilson C.R., Milas Z., Gangappa S., Hollenbaugh D., Pearson T.C., Ford M.L., Larsen C.P. Anti-CD40 monoclonal antibody synergizes with CTLA4-Ig in promoting long-term graft survival in murine models of transplantation. J. Immunol. 2009, 183:1625-1635.
8. Larsen C.P., Grinyo J., Medina-Pestana J., Vanrenterghem Y., Vincenti F., Breshahan B., Campistol J.M., Florman S., Rial Mdel C., Kamar N., Block A., Di Russo G., Lin C.S., Garg P., Charpentier B. Belatacept-based regimens versus a cyclosporine A-based regimen in kidney transplant recipients: 2-year results from the BENEFIT and BENEFIT-EXT studies. Transplantation 2010, 90:1528-1535.
9. Pearson T.C., Alexander D.Z., Hendrix R., Elwood E.T., Linsley P.S., Winn K.J., Larsen C.P. CTLA4-Ig plus bone marrow induces long-term allograft survival and donor specific unresponsiveness in the murine model. Evidence for hematopoietic chimerism. Transplantation 1996, 61:997-1004.
10. Ruderman E.M., Pope R.M. The evolving clinical profile of abatacept (CTLA4-Ig): a novel co-stimulatory modulator for the treatment of rheumatoid arthritis. Arthritis Res. Ther. 2005, 7(Suppl. 2):S21-S25.
11. Ruderman E.M., Pope R.M. Drug insight: abatacept for the treatment of rheumatoid arthritis. Nature clinical practice. Rheumatology 2006, 2:654-660.
12. Moreau T., Coles A., Wing M., Thorpe J., Miller D., Moseley I., Issacs J., Hale G., Clayton D., Scolding N., Waldmann H., Compston A. CAMPATH-IH in multiple sclerosis. Mult. Scler. 1996, 1:357-365.
13. Coles A.J., Fox E., Vladic A., Gazda S.K., Brinar V., Selmaj K.W., Bass A.D., Wynn D.R., Margolin D.H., Lake S.L., Moran S., Palmer J., Smith M.S., Compston D.A. Alemtuzumab versus interferon beta-1a in early relapsing-remitting multiple sclerosis: post-hoc and subset analyses of clinical efficacy outcomes. Lancet Neurol. 2011, 10:338-348.
14. McFarland H.F., Jacobson S. Natalizumab and immune cells. Arch. Neurol. 2006, 63:1366-1367.
15. Salvana E.M., Salata R.A. Infectious complications associated with monoclonal antibodies and related small molecules. Clin. Microbiol. Rev. 2009, 22:274-290. (Table of Contents).
16. Getts D.R., Getts M.T., McCarthy D.P., Chastain E.M., Miller S.D. Have we overestimated the benefit of human(ized) antibodies?. MAbs 2010, 2:682-694.
17. Getts D.R., Shankar S., Chastain E.M., Martin A., Getts M.T., Wood K., Miller S.D. Current landscape for T-cell targeting in autoimmunity and transplantation. Immunotherapy 2011, 3:853-870.
18. Weiss A. The right team at the right time to go for a home run: tyrosine kinase activation by the TCR. Nat. Immunol. 2010, 11:101-104.
19. Guy C.S., Vignali K.M., Temirov J., Bettini M.L., Overacre A.E., Smeltzer M., Zhang H., Huppa J.B., Tsai Y.H., Lobry C., Xie J., Dempsey P.J., Crawford H.C., Aifantis I., Davis M.M., Vignali D.A. Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat. Immunol. 2013, 14:262-270.
20. Artyomov M.N., Lis M., Devadas S., Davis M.M., Chakraborty A.K. CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16916-16921.
21. Zamoyska R. CD4 and CD8: modulators of T-cell receptor recognition of antigen and of immune responses?. Curr. Opin. Immunol. 1998, 10:82-87.
22. Bockenstedt L.K., Goldsmith M.A., Dustin M., Olive D., Springer T.A., Weiss A. The CD2 ligand LFA-3 activates T cells but depends on the expression and function of the antigen receptor. J. Immunol. 1988, 141:1904-1911.
23. Wilde M.I., Goa K.L. Muromonab CD3: a reappraisal of its pharmacology and use as prophylaxis of solid organ transplant rejection. Drugs 1996, 51:865-894.
24. Xu D., Alegre M.L., Varga S.S., Rothermel A.L., Collins A.M., Pulito V.L., Hanna L.S., Dolan K.P., Parren P.W., Bluestone J.A., Jolliffe L.K., Zivin R.A. In vitro characterization of five humanized OKT3 effector function variant antibodies. Cell. Immunol. 2000, 200:16-26.
25. Alegre M.L., Collins A.M., Pulito V.L., Brosius R.A., Olson W.C., Zivin R.A., Knowles R., Thistlethwaite J.R., Jolliffe L.K., Bluestone J.A. Effect of a single amino acid mutation on the activating and immunosuppressive properties of a "humanized" OKT3 monoclonal antibody. J. Immunol. 1992, 148:3461-3468.
26. Herold K.C., Hagopian W., Auger J.A., Poumian-Ruiz E., Taylor L., Donaldson D., Gitelman S.E., Harlan D.M., Xu D., Zivin R.A., Bluestone J.A. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 2002, 346:1692-1698.
27. Herold K.C., Rubenstein A.H. Immunosuppression for insulin-dependent diabetes. N. Engl. J. Med. 1988, 318:701-703.
28. Keymeulen B., Vandemeulebroucke E., Ziegler A.G., Mathieu C., Kaufman L., Hale G., Gorus F., Goldman M., Walter M., Candon S., Schandene L., Crenier L., De Block C., Seigneurin J.M., De Pauw P., Pierard D., Weets I., Rebello P., Bird P., Berrie E., Frewin M., Waldmann H., Bach J.F., Pipeleers D., Chatenoud L. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 2005, 352:2598-2608.
29. Malcolm S.L., Smith E.L., Bourne T., Shaw S. A humanised mouse model of cytokine release: comparison of CD3-specific antibody fragments. J. Immunol. Methods 2012, 384:33-42.
30. Kjer-Nielsen L., Dunstone M.A., Kostenko L., Ely L.K., Beddoe T., Mifsud N.A., Purcell A.W., Brooks A.G., McCluskey J., Rossjohn J. Crystal structure of the human T cell receptor CD3 epsilon gamma heterodimer complexed to the therapeutic mAb OKT3. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7675-7680.
31. Waid T.H., Lucas B.A., Thompson J.S., Brown S.A., Munch L., Prebeck R.J., Jezek D. Treatment of acute cellular rejection with T10B9.1A-31 or OKT3 in renal allograft recipients. Transplantation 1992, 53:80-86.
32. Waid T.H., Lucas B.A., Amlot P., Janossy G., Yacoub M., Cammisuli S., Jezek D., Rhoades J., Brown S., Thompson J.S. T10B9.1A-31 anti-T-cell monoclonal antibody: preclinical studies and clinical treatment of solid organ allograft rejection. Am. J. Kidney Dis. 1989, 14:61-70.
33. Zlabinger G.J., Pohanka E., Stuhlmeier K.M., Eher R., Schmaldienst S., Watschinger B., Steiner G., Kovarik J. Can treatment with the monoclonal antibody BMA031 induce cytokine release?. Transplant. Proc. 1992, 24:271-272.
34. Borst J., van Dongen J.J., de Vries E., Comans-Bitter W.M., van Tol M.J., Vossen J.M., Kurrle R. BMA031, a monoclonal antibody suited to identify the T-cell receptor alpha beta/CD3 complex on viable human T lymphocytes in normal and disease states. Hum. Immunol. 1990, 29:175-188.
35. Matsutake T., Sasaki T., Ogino T., Kaku M., Nakayama E. Prevention of mortality by in vivo depletion of alpha beta T cells in murine lethal listeriosis and involvement of gamma delta T cells in bacterial elimination. Immunobiology 1995, 193:71-83.
36. Waldor M.K., Sriram S., Hardy R., Herzenberg L.A., Lanier L., Lim M., Steinman L. Reversal of experimental allergic encephalomyelitis with monoclonal antibody to a T-cell subset marker. Science 1985, 227:415-417.
37. Wang Y., Hao L., Gill R.G., Lafferty K.J. Autoimmune diabetes in NOD mouse is L3T4 T-lymphocyte dependent. Diabetes 1987, 36:535-538.
38. Butler L., Simmons B., Zimmerman J., Deriso P., Phadke K., Hom J. Regulation of cellular and humoral immune responses to collagen type I or collagen type II. Immunology 1988, 63:611-617.
39. Stull S.J., Kyriakos M., Sharp G.C., Braley-Mullen H. Prevention and reversal of experimental autoimmune thyroiditis (EAT) in mice by administration of anti-L3T4 monoclonal antibody at different stages of disease development. Cell. Immunol. 1988, 117:188-198.
40. Wofsy D., Ledbetter J.A., Hendler P.L., Seaman W.E. Treatment of murine lupus with monoclonal anti-T cell antibody. J. Immunol. 1985, 134:852-857.
41. Wang B., Gonzalez A., Benoist C., Mathis D. The role of CD8+ T cells in the initiation of insulin-dependent diabetes mellitus. Eur. J. Immunol. 1996, 26:1762-1769.
42. Koyasu S., Lawton T., Novick D., Recny M.A., Siliciano R.F., Wallner B.P., Reinherz E.L. Role of interaction of CD2 molecules with lymphocyte function-associated antigen 3 in T-cell recognition of nominal antigen. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2603-2607.
43. Jung S., Toyka K., Hartung H.P. Suppression of experimental autoimmune encephalomyelitis in Lewis rats by antibodies against CD2. Eur. J. Immunol. 1995, 25:1391-1398.
44. Barlow A.K., Like A.A. Anti-CD2 monoclonal antibodies prevent spontaneous and adoptive transfer of diabetes in the BB/Wor rat. Am. J. Pathol. 1992, 141:1043-1051.
45. Hoffmann J.C., Herklotz C., Zeidler H., Bayer B., Rosenthal H., Westermann J. Initiation and perpetuation of rat adjuvant arthritis is inhibited by the anti-CD2 monoclonal antibody (mAb) OX34. Ann. Rheum. Dis. 1997, 56:716-722.
46. Giardina S.L., Schroff R.W., Kipps T.J., Woodhouse C.S., Abrams P.G., Rager H.C., Morgan A.C., Foon K.A. The generation of monoclonal anti-idiotype antibodies to human B cell-derived leukemias and lymphomas. J. Immunol. 1985, 135:653-658.
47. Levitt L., Kipps T.J., Engleman E.G., Greenberg P.L. Human bone marrow and peripheral blood T lymphocyte depletion: efficacy and effects of both T cells and monocytes on growth of hematopoietic progenitors. Blood 1985, 65:663-679.
48. Jefferis R. Isotype and glycoform selection for antibody therapeutics. Arch. Biochem. Biophys. 2012, 526:159-166.
49. Investigators C.T., Coles A.J., Compston D.A., Selmaj K.W., Lake S.L., Moran S., Margolin D.H., Norris K., Tandon P.K. Alemtuzumab vs. interferon beta-1a in early multiple sclerosis. N. Engl. J. Med. 2008, 359:1786-1801.
50. Coles A., Deans J., Compston A. Campath-1H treatment of multiple sclerosis: lessons from the bedside for the bench. Clin. Neurol. Neurosurg. 2004, 106:270-274.
51. Dyer M.J., Hale G., Hayhoe F.G., Waldmann H. Effects of CAMPATH-1 antibodies in vivo in patients with lymphoid malignancies: influence of antibody isotype. Blood 1989, 73:1431-1439.
52. Neff K.S., Richards S.M., Williams J.M., Garman R.D., Ruzek M.C. Murine antithymocyte globulin T-cell depletion is mediated predominantly by macrophages, but the Fas/FasL pathway selectively targets regulatory T cells. Transplantation 2011, 92:523-528.
53. van de Linde P., Tysma O.M., Medema J.P., Hale G., Waldmann H., Roelen D.L., Roep B.O. Mechanisms of antibody immunotherapy on clonal islet reactive T cells. Hum. Immunol. 2006, 67:264-273.
54. van de Griend R.J., Bolhuis R.L., Stoter G., Roozemond R.C. Regulation of cytolytic activity in CD3- and CD3+ killer cell clones by monoclonal antibodies (anti-CD16, anti-CD2, anti-CD3) depends on subclass specificity of target cell IgG-FcR. J. Immunol. 1987, 138:3137-3144.
55. Ravetch J.V., Clynes R.A. Divergent roles for Fc receptors and complement in vivo. Annu. Rev. Immunol. 1998, 16:421-432.
56. Waldor M.K., Mitchell D., Kipps T.J., Herzenberg L.A., Steinman L. Importance of immunoglobulin isotype in therapy of experimental autoimmune encephalomyelitis with monoclonal anti-CD4 antibody. J. Immunol. 1987, 139:3660-3664.
57. Alters S.E., Steinman L., Oi V.T. Comparison of rat and rat-mouse chimeric anti-murine CD4 antibodies in vitro. Chimeric antibodies lyse low-density CD4+ cells. J. Immunol. 1989, 142:2018-2023.
58. Alters S.E., Sakai K., Steinman L., Oi V.T. Mechanisms of anti-CD4-mediated depletion and immunotherapy. A study using a set of chimeric anti-CD4 antibodies. J. Immunol. 1990, 144:4587-4592.
59. Rashid A., Auchincloss H., Sharon J. Comparison of GK1.5 and chimeric rat/mouse GK1.5 anti-CD4 antibodies for prolongation of skin allograft survival and suppression of alloantibody production in mice. J. Immunol. 1992, 148:1382-1388.
60. Bruggemann M., Teale C., Clark M., Bindon C., Waldmann H. A matched set of rat/mouse chimeric antibodies. Identification and biological properties of rat H chain constant regions mu, gamma 1, gamma 2a, gamma 2b, gamma 2c, epsilon, and alpha. J. Immunol. 1989, 142:3145-3150.
61. Pluschke G., Bordmann G., Daoudaki M.E., Lambris J.D., Achtman M., Neibert M. Isolation of rat IgM to IgG hybridoma isotype switch variants and analysis of the efficiency of rat Ig in complement activation. Eur. J. Immunol. 1989, 19:131-135.
62. Yi Z., Diz R., Martin A.J., Morillon Y.M., Kline D.E., Li L., Wang B., Tisch R. Long-term remission of diabetes in NOD mice is induced by nondepleting anti-CD4 and anti-CD8 antibodies. Diabetes 2012, 61:2871-2880.
63. Wasserman H.A., Evavold B.D. Induction of anergy by antibody blockade of TCR in myelin oligodendrocyte glycoprotein-specific cells. J. Immunol. 2008, 180:7259-7264.
64. Shearman C.W., Pollock D., White G., Hehir K., Moore G.P., Kanzy E.J., Kurrle R. Construction, expression and characterization of humanized antibodies directed against the human alpha/beta T cell receptor. J. Immunol. 1991, 147:4366-4373.
65. Boyd P.N., Lines A.C., Patel A.K. The effect of the removal of sialic acid, galactose and total carbohydrate on the functional activity of Campath-1H. Mol. Immunol. 1995, 32:1311-1318.
66. Lifely M.R., Hale C., Boyce S., Keen M.J., Phillips J. Glycosylation and biological activity of CAMPATH-1H expressed in different cell lines and grown under different culture conditions. Glycobiology 1995, 5:813-822.
67. Shi Y.F., Sahai B.M., Green D.R. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature 1989, 339:625-626.
68. Hildeman D.A., Zhu Y., Mitchell T.C., Kappler J., Marrack P. Molecular mechanisms of activated T cell death in vivo. Curr. Opin. Immunol. 2002, 14:354-359.
69. von Rossum A., Krall R., Escalante N.K., Choy J.C. Inflammatory cytokines determine the susceptibility of human CD8 T cells to Fas-mediated activation-induced cell death through modulation of FasL and c-FLIP(S) expression. J. Biol. Chem. 2011, 286:21137-21144.
70. Kohm A.P., McMahon J.S., Podojil J.R., Begolka W.S., DeGutes M., Kasprowicz D.J., Ziegler S.F., Miller S.D. Cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells. J. Immunol. 2006, 176:3301-3305.
71. Cosimi A.B., Burton R.C., Colvin R.B., Goldstein G., Delmonico F.L., LaQuaglia M.P., Tolkoff-Rubin N., Rubin R.H., Herrin J.T., Russell P.S. Treatment of acute renal allograft rejection with OKT3 monoclonal antibody. Transplantation 1981, 32:535-539.
72. Hale G., Rebello P., Al Bakir I., Bolam E., Wiczling P., Jusko W.J., Vandemeulebroucke E., Keymeulen B., Mathieu C., Ziegler A.G., Chatenoud L., Waldmann H. Pharmacokinetics and antibody responses to the CD3 antibody otelixizumab used in the treatment of type 1 diabetes. J. Clin. Pharmacol. 2010, 50:1238-1248.
73. Page E.K., Dar W.A., Knechtle S.J. Biologics in organ transplantation. Transpl. Int. 2012, 25:707-719.
74. Norman D.J. Mechanisms of action and overview of OKT3. Ther. Drug Monit. 1995, 17:615-620.
75. Chatenoud L., Bluestone J.A. CD3-specific antibodies: a portal to the treatment of autoimmunity. Nat. Rev. Immunol. 2007, 7:622-632.
76. Carriere D., Arcier J.M., Derocq J.M., Fontaine C., Richer G. Antigenic modulation induced by four monoclonal antibodies adsorbed on gold particles (specificity anti-CD4, anti-CD5, anti-CD7, and anti-150-kDa antigen): relationship between modulation and cytotoxic activity of immunotoxins. Exp. Cell Res. 1989, 182:114-128.
77. Roelants G., Forni L., Pernis B. Blocking and redistribution ("capping") of antigen receptors on T and B lymphocytes by anti-immunoglobulin antibody. J. Exp. Med. 1973, 137:1060-1077.
78. Elson C.J., Singh J., Taylor R.B. The effect of capping by anti-immunoglobulin antibody on the expression of cell surface immunoglobulin and on lymphocyte activation. Scand. J. Immunol. 1973, 2:143-149.
79. Rahimi N., Golde T.E., Meyer R.D. Identification of ligand-induced proteolytic cleavage and ectodomain shedding of VEGFR-1/FLT1 in leukemic cancer cells. Cancer Res. 2009, 69:2607-2614.
80. Petrelli A., Circosta P., Granziero L., Mazzone M., Pisacane A., Fenoglio S., Comoglio P.M., Giordano S. Ab-induced ectodomain shedding mediates hepatocyte growth factor receptor down-regulation and hampers biological activity. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5090-5095.
81. McMahan C.J., Fink P.J. RAG reexpression and DNA recombination at T cell receptor loci in peripheral CD4+ T cells. Immunity 1998, 9:637-647.
82. Ali M., Weinreich M., Balcaitis S., Cooper C.J., Fink P.J. Differential regulation of peripheral CD4+ T cell tolerance induced by deletion and TCR revision. J. Immunol. 2003, 171:6290-6296.
83. Cooper C.J., Orr M.T., McMahan C.J., Fink P.J. T cell receptor revision does not solely target recent thymic emigrants. J. Immunol. 2003, 171:226-233.
84. Fink P.J., McMahan C.J. Lymphocytes rearrange, edit and revise their antigen receptors to be useful yet safe. Immunol. Today 2000, 21:561-566.
85. Lantelme E., Orlando L., Porcedda P., Turinetto V., De Marchi M., Amoroso A., Mantovani S., Giachino C. An in vitro model of T cell receptor revision in mature human CD8+ T cells. Mol. Immunol. 2008, 45:328-337.
86. Hale J.S., Fink P.J. T-cell receptor revision: friend or foe?. Immunology 2010, 129:467-473.
87. Mueller D.L. Mechanisms maintaining peripheral tolerance. Nat. Immunol. 2010, 11:21-27.
88. Getts D.R., Martin A.J., McCarthy D.P., Terry R.L., Hunter Z.N., Yap W.T., Getts M.T., Pleiss M., Luo X., King N.J., Shea L.D., Miller S.D. Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat. Biotechnol. 2012, 30:1217-1224.
89. Brusko T.M., Putnam A.L., Bluestone J.A. Human regulatory T cells: role in autoimmune disease and therapeutic opportunities. Immunol. Rev. 2008, 223:371-390.
90. Minamimura K., Gao W., Maki T. CD4+ regulatory T cells are spared from deletion by antilymphocyte serum, a polyclonal anti-T cell antibody. J. Immunol. 2006, 176:4125-4132.
91. Noris M., Casiraghi F., Todeschini M., Cravedi P., Cugini D., Monteferrante G., Aiello S., Cassis L., Gotti E., Gaspari F., Cattaneo D., Perico N., Remuzzi G. Regulatory T cells and T cell depletion: role of immunosuppressive drugs. J. Am. Soc. Nephrol. 2007, 18:1007-1018.
92. Lopez M., Clarkson M.R., Albin M., Sayegh M.H., Najafian N. A novel mechanism of action for anti-thymocyte globulin: induction of CD4+CD25+Foxp3+ regulatory T cells. J. Am. Soc. Nephrol. 2006, 17:2844-2853.
93. Smith J.A., Tso J.Y., Clark M.R., Cole M.S., Bluestone J.A. Nonmitogenic anti-CD3 monoclonal antibodies deliver a partial T cell receptor signal and induce clonal anergy. J. Exp. Med. 1997, 185:1413-1422.
94. Smith J.A., Tang Q., Bluestone J.A. Partial TCR signals delivered by FcR-nonbinding anti-CD3 monoclonal antibodies differentially regulate individual Th subsets. J. Immunol. 1998, 160:4841-4849.
95. Wojciechowski D., Vincenti F. Belatacept for prevention of acute rejection in adult patients who have had a kidney transplant: an update. Biol. Targets Ther. 2012, 6:385-393.
96. Opelz G. Efficacy of rejection prophylaxis with OKT3 in renal transplantation. Collaborative Transplant Study. Transplantation 1995, 60:1220-1224.
97. Ferran C., Bluestone J., Bach J.F., Chatenoud L. In vivo T lymphocyte activation induced in mice following the injection of anti-CD3 monoclonal antibody. Transplant. Proc. 1990, 22:1922-1923.
98. Keymeulen B., Candon S., Fafi-Kremer S., Ziegler A., Leruez-Ville M., Mathieu C., Vandemeulebroucke E., Walter M., Crenier L., Thervet E., Legendre C., Pierard D., Hale G., Waldmann H., Bach J.F., Seigneurin J.M., Pipeleers D., Chatenoud L. Transient Epstein-Barr virus reactivation in CD3 monoclonal antibody-treated patients. Blood 2010, 115:1145-1155.
99. Herold K.C., Gitelman S.E., Willi S.M., Gottlieb P.A., Waldron-Lynch F., Devine L., Sherr J., Rosenthal S.M., Adi S., Jalaludin M.Y., Michels A.W., Dziura J., Bluestone J.A. Teplizumab treatment may improve C-peptide responses in participants with type 1 diabetes after the new-onset period: a randomised controlled trial. Diabetologia 2013, 56:391-400.
100. Sempe P., Bedossa P., Richard M.F., Villa M.C., Bach J.F., Boitard C. Anti-alpha/beta T cell receptor monoclonal antibody provides an efficient therapy for autoimmune diabetes in nonobese diabetic (NOD) mice. Eur. J. Immunol. 1991, 21:1163-1169.
101. Lee L.F., Logronio K., Tu G.H., Zhai W., Ni I., Mei L., Dilley J., Yu J., Rajpal A., Brown C., Appah C., Chin S.M., Han B., Affolter T., Lin J.C. Anti-IL-7 receptor-alpha reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12674-12679.
102. Coles A.J. Alemtuzumab therapy for multiple sclerosis. Neurotherapeutics 2013, 10:29-33.
103. Coles A.J., Fox E., Vladic A., Gazda S.K., Brinar V., Selmaj K.W., Skoromets A., Stolyarov I., Bass A., Sullivan H., Margolin D.H., Lake S.L., Moran S., Palmer J., Smith M.S., Compston D.A. Alemtuzumab more effective than interferon beta-1a at 5-year follow-up of CAMMS223 clinical trial. Neurology 2012, 78:1069-1078.
104. Kohm A.P., Turley D.M., Miller S.D. Targeting the TCR: T-cell receptor and peptide-specific tolerance-based strategies for restoring self-tolerance in CNS autoimmune disease. Int. Rev. Immunol. 2005, 24:361-392.
105. Cho B.A., Sim J.H., Park J.A., Kim H.W., Yoo W.H., Lee S.H., Lee D.S., Kang J.S., Hwang Y.I., Lee W.J., Kang I., Lee E.B., Kim H.R. Characterization of effector memory CD8+ T cells in the synovial fluid of rheumatoid arthritis. J. Clin. Immunol. 2012, 32:709-720.
106. Macedo C., Walters J.T., Orkis E.A., Isse K., Elinoff B.D., Fedorek S.P., McMichael J.M., Chalasani G., Randhawa P., Demetris A.J., Zeevi A., Tan H., Shapiro R., Landsittel D., Lakkis F.G., Metes D. Long-term effects of alemtuzumab on regulatory and memory T-cell subsets in kidney transplantation. Transplantation 2012, 93:813-821.
107. Khan M.A., Nicolls M.R. Complement-mediated microvascular injury leads to chronic rejection. Adv. Exp. Med. Biol. 2013, 734a:233-246.
108. Fehr T., Gaspert A. Antibody-mediated kidney allograft rejection: therapeutic options and their experimental rationale. Transpl. Int. 2012, 25:623-632.
109. Koga T., Ichinose K., Mizui M., Crispin J.C., Tsokos G.C. Calcium/calmodulin-dependent protein kinase IV suppresses IL-2 production and regulatory T cell activity in lupus. J. Immunol. 2012, 189:3490-3496.
110. Moulton V.R., Lo M.S., Tsokos G.C. Methods and protocols to study T cell signaling abnormalities in human systemic lupus erythematosus. Methods Mol. Biol. 2012, 900:25-60.
111. Utset T.O., Auger J.A., Peace D., Zivin R.A., Xu D., Jolliffe L., Alegre M.L., Bluestone J.A., Clark M.R. Modified anti-CD3 therapy in psoriatic arthritis: a phase I/II clinical trial. J. Rheumatol. 2002, 29:1907-1913.
112. Waldron-Lynch F., Henegariu O., Deng S., Preston-Hurlburt P., Tooley J., Flavell R., Herold K.C. Teplizumab induces human gut-tropic regulatory cells in humanized mice and patients. Sci. Transl. Med. 2012, 4:118ra112.
113. Woodle E.S., Xu D., Zivin R.A., Auger J., Charette J., O'Laughlin R., Peace D., Jollife L.K., Haverty T., Bluestone J.A., Thistlethwaite J.R. Phase I trial of a humanized, Fc receptor nonbinding OKT3 antibody, huOKT3gamma1(Ala-Ala) in the treatment of acute renal allograft rejection. Transplantation 1999, 68:608-616.
114. Ablamunits V., Bisikirska B., Herold K.C. Acquisition of regulatory function by human CD8(+) T cells treated with anti-CD3 antibody requires TNF. Eur. J. Immunol. 2010, 40:2891-2901.
115. Sandborn W.J., Colombel J.F., Frankel M., Hommes D., Lowder J.N., Mayer L., Plevy S., Stokkers P., Travis S., Van Assche G., Baumgart D.C., Targan S.R. Anti-CD3 antibody visilizumab is not effective in patients with intravenous corticosteroid-refractory ulcerative colitis. Gut 2010, 59:1485-1492.
116. Baumgart D.C., Targan S.R., Dignass A.U., Mayer L., van Assche G., Hommes D.W., Hanauer S.B., Mahadevan U., Reinisch W., Plevy S.E., Salzberg B.A., Buchman A.L., Mechkov G.M., Krastev Z.A., Lowder J.N., Frankel M.B., Sandborn W.J. Prospective randomized open-label multicenter phase I/II dose escalation trial of visilizumab (HuM291) in severe steroid-refractory ulcerative colitis. Inflamm. Bowel Dis. 2010, 16:620-629.
117. Midtvedt K., Fauchald P., Lien B., Hartmann A., Albrechtsen D., Bjerkely B.L., Leivestad T., Brekke I.B. Individualized T cell monitored administration of ATG versus OKT3 in steroid-resistant kidney graft rejection. Clin. Transplant. 2003, 17:69-74.
118. Kimball J.A., Norman D.J., Shield C.F., Schroeder T.J., Lisi P., Garovoy M., O'Connell J.B., Stuart F., McDiarmid S.V., Wall W. The OKT3 Antibody Response Study: a multicentre study of human anti-mouse antibody (HAMA) production following OKT3 use in solid organ transplantation. Transpl. Immunol. 1995, 3:212-221.
119. Brown S., Lucas B., Waid T., McKeown W., Tsuchida M., Thompson J. T10B9 action: the effect of anti-T-cell antibody mitogenicity and graft rejection on the first dose cytokine response. Transplant. Proc. 1997, 29:315-316.
120. Brown S.A., Lucas B.A., Waid T.H., McKeown J.W., Barve S., Jackson L.R., Thompson J.S. T10B9 (MEDI-500) mediated immunosuppression: studies on the mechanism of action. Clin. Transplant. 1996, 10:607-613.
121. Knight R.J., Kurrle R., McClain J., Racenberg J., Baghdahsarian V., Kerman R., Lewis R., van Buren C.T., Kahan B.D. Clinical evaluation of induction immunosuppression with a murine IgG2b monoclonal antibody (BMA 031) directed toward the human alpha/beta-T cell receptor. Transplantation 1994, 57:1581-1588.
122. Rider D.A., Havenith C.E., de Ridder R., Schuurman J., Favre C., Cooper J.C., Walker S., Baadsgaard O., Marschner S., vandeWinkel J.G., Cambier J., Parren P.W., Alexander D.R. A human CD4 monoclonal antibody for the treatment of T-cell lymphoma combines inhibition of T-cell signaling by a dual mechanism with potent Fc-dependent effector activity. Cancer Res. 2007, 67:9945-9953.
123. Villadsen L.S., Skov L., Dam T.N., Dagnaes-Hansen F., Rygaard J., Schuurman J., Parren P.W., van de Winkel J.G., Baadsgaard O. In situ depletion of CD4+ T cells in human skin by Zanolimumab. Arch. Dermatol. Res. 2007, 298:449-455.
124. Lopez E., Racadot E., Bataillard M., Berger E., Rumbach L. Interferon gamma, IL2, IL4, IL10 and TNFalpha secretions in multiple sclerosis patients treated with an anti-CD4 monoclonal antibody. Autoimmunity 1999, 29:87-92.
125. Nizet Y., Chentoufi A.A., de la Parra B., Lewalle P., Rouas R., Cornet A., Besse T., Mourad M., Malaise J., Squifflet J.P., Bazin H., Latinne D. The experimental (in vitro) and clinical (in vivo) immunosuppressive effects of a rat IgG2b anti-human CD2 mAb, LO-CD2a/BTI-322. Transplantation 2000, 69:1420-1428.
126. Nizet Y., Chentoufi A.A., Havaux X., Kinet I., Cormont F., Bazin H., Latinne D. Apoptosis of human naive NK cells mediated by a rat IgG2b anti CD2 mAb through a fractricidal ADCC reaction. Immunol. Lett. 1999, 68:229-235.
127. Latinne D., De La Parra B., Nizet Y., Cornet A., Giovino-Barry V., Monroy R.L., White-Scharf M.E., Bazin H. An anti-CD2 mAb induces immunosuppression and hyporesponsiveness of CD2+ human T cells in vitro. Int. Immunol. 1996, 8:1113-1119.
128. Lundin J., Kimby E., Bjorkholm M., Broliden P.A., Celsing F., Hjalmar V., Mollgard L., Rebello P., Hale G., Waldmann H., Mellstedt H., Osterborg A. Phase II trial of subcutaneous anti-CD52 monoclonal antibody alemtuzumab (Campath-1H) as first-line treatment for patients with B-cell chronic lymphocytic leukemia (B-CLL). Blood 2002, 100:768-773.
129. Wiendl H., Kieseier B. Multiple sclerosis: reprogramming the immune repertoire with alemtuzumab in MS. Nat. Rev. Neurol. 2013, 9:125-126.