Resetting the functional capacity of regulatory T cells: A novel immunotherapeutic strategy to promote immune tolerance

Expert Opinion on Biological Therapy

Volumn 5, Issue SUPPL. 1, 2005, Pages

  Chatenoud, Lucienne ^a   Bach, Jean François ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

Autoimmunity; CD3 antibodies; Diabetes; Regulatory T cells

Indexed keywords

CYCLOPHOSPHAMIDE; MONOCLONAL ANTIBODY CD3; OKT 3;

ANTIBODY SPECIFICITY; AUTOIMMUNE DISEASE; CLINICAL TRIAL; EXPERIMENTAL MODEL; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; AUTOIMMUNE DISEASES; CLINICAL TRIALS; DIABETES MELLITUS, TYPE 1; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; HUMANS; IMMUNE TOLERANCE; MICE; MICE, INBRED NOD; MUROMONAB-CD3; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 24144461172     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.5.1.S73     Document Type: Review

References (99)

1. SHEVACH EM: Regulatory T cells in autoimmmunity. Ann. Rev. Immunol. (2000) 18:423-449.
2. + suppressor T cells: more questions than answers. Nat. Rev. Immunol. (2002) 2:389-400.
3. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Ann. Rev. Immunol. (2004) 22:531-562.
4. MASON D, POWRIE F: Control of immune pathology by regulatory T cells. Curr. Opin. Immunol. (1998) 10:649-655.
5. BACH JF, CHATENOUD L: Tolerance to islet autoantigens in Type 1 diabetes. Ann. Rev. Immunol. (2001) 19:131-161.
6. BACH JF: Regulatory T cells under scrutiny. Nat. Rev. Immunol. (2003) 3:189-198.
7. + immunoregulatory T cells that control autoimmune diabetes. Immunity (2000) 12:431-440.
8. COBBOLD SP, ADAMS E, GRACA L, WALDMANN H: Serial analysis of gene expression provides new insights into regulatory T cells. Semin. Immunol. (2003) 15:209-214.
9. BLUESTONE JA, ABBAS AK: Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. (2003) 3:253-257.
10. GERSHON RK, KONDO K: Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology (1970) 18:723-737.
11. GERSHON RK, KONDO K: Infectious immunological tolerance. Immunology (1971) 21:903-914.
12. MOSMANN TR, COFFMAN RL: TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. (1989) 7:145-173.
13. + T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol. Today (1995) 16:34-38.
14. TISCH R, WANG B, SERREZE DV: Induction of glutamic acid decarboxylase 65-specific Th2 cells and suppression of autoimmune diabetes at late stages of disease is epitope dependent. J. Immunol. (1999) 163:1178-1187.
15. LEPAULT F, GAGNERAULT MC: Characterization of peripheral regulatory CD4(+) T cells that prevent diabetes onset in nonobese diabetic mice. J. Immunol. (2000) 164:240-247.
16. BACH JF, CHATENOUD L: Tolerance to islet autoantigens and Type I diabetes. Ann. Rev. Immunol. (2001) 19:131-161.
17. MCCULLAGH P: Curtailment of autoimmunity following parabiosis with a normal partner. Immunology (1990) 71:595-597.
18. KHOURY SJ, HANCOCK WW, WEINER HL: Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with down regulation of inflammatory cytokines and differential upregulation of transforming growth factor beta, IL-4, and prostaglandin E expression in the brain. J. Exp. Med. (1992) 176:1355-1364.
19. DANIEL D, GILL RG, SCHLOOT N, WEGMANN D: Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T cell clones isolated from NOD mice. Eur. J. Immunol. (1995) 25:1056-1062.
20. WEGMANN DR, NORBURY-GLASER M, DANIEL D: Insulin-specific T cells are a predominant component of islet infiltrates in prediabetic NOD mice. Eur. J. Immunol. (1994) 24:1853-1857.
21. DANIEL D, WEGMANN DR: Intranasal administration of insulin peptide B: 9-23 protects NOD mice from diabetes. Ann. NY Acad. Sci. (1996) 778:371-372.
22. ATKINSON MA, MACLAREN NK, LUCHETTA R: Insulitis and diabetes in NOD mice reduced by prophylactic insulin therapy. Diabetes (1990) 39:933-937.
23. FRENCH MB, ALLISON J, CRAM DS et al.: Transgenic expression of mouse proinsulin II prevents diabetes in nonobese diabetic mice. Diabetes (1997) 46:34-39.
24. HONEYMAN MC, CRAM DS, HARRISON LC: Glutamic acid decarboxylase 67-reactive T cells: a marker of insulin-dependent diabetes. J. Exp. Med. (1993) 177:535-540.
25. PANINA-BORDIGNON PR, LANG PM, VAN ENDERT E et al.: Cytotoxic T cells specific for glutamic acid decarboxylase in autoimmune diabetes. J. Exp. Med. (1995) 181:1923-1927.
26. TISCH R, YANG XD, SINGER SM, LIBLAU RS, FUGGER L, MCDEVITT HO: Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature (1993) 366:72-75.
27. TREMBLEAU S, PENNA G, GREGORI S, GATELY MK, ADORINI L: Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur. J. Immunol. (1997) 27:2330-2339.
28. HAWKES CJ, WASMEIER C, CHRISTIE MR, HUTTON JC: Identification of the 37-kDa antigen in IDDM as a tyrosine phosphatase-like protein (phogrin) related to IA-2. Diabetes (1996)45:1187-1192.
29. DOTTA F, DIONISI S, VIGLIETTA V et al.: T cell mediated autoimmunity to the insulinoma-associated protein 2 islet tyrosine phosphatase in Type 1 diabetes mellitus. Eur. J. Endocrinol. (1999) 141:272-278.
30. HAWA M, ROWE R, LAN MS et al.: Value of antibodies to islet protein tyrosine phosphatase-like molecule in predicting Type 1 diabetes. Diabetes (1997) 46:1270-1275.
31. ELIAS D, MARKOVITS D, RESHEF T, VAN DER ZEE R, COHEN IR: Induction and therapy of autoimmune diabetes in the non-obese diabetic (NOD/Lt) mouse by a 65-kDa heat-shock protein. Proc. Natl. Acad. Sci. USA (1990) 87:1576-1580.
32. ELIAS D, COHEN IR: Peptide therapy for diabetes in NOD mice. Lancet (1994) 343:704-706.
33. BIRK OS, DOUEK DC, ELIAS D et al.: A role of hsp60 in autoimmune diabetes: analysis in a transgenic model. Proc. Natl. Acad. Sci. USA (1996) 93:1032-1037.
34. ELIAS D, MEILIN A, ABLAMUNITS V et al.: Hsp60 peptide therapy of NOD mouse diabetes induces a Th2 cytokine burst and downregulates autoimmunity to various beta-cell antigens. Diabetes (1997) 46:758-764.
35. SERREZE DV, CHAPMAN HD, VARNUM DS et al.: B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new 'speed congenic' stock of NOD.Ig mu(null) mice. J. Exp. Med. (1996) 184:2049-2053.
36. AKASHI T, NAGAFUCHI S, ANZAI K et al.: Direct evidence for the contribution of B cells to the progression of insulitis and the development of diabetes in non-obese diabetic mice. Int. Immunol. (1997) 9:1159-1164.
37. NOORCHASHM H, LIEU YK, NOORCHASHM N et al.: I-ag7-mediated antigen presentation by β lymphocytes is critical in overcoming a checkpoint in T cell tolerance to islet beta cells of nonobese diabetic mice. J. Immunol. (1999) 163:743-750.
38. YU LP, REWERS M, GIANANI R et al.: Anti-islet autoantibodies usually develop sequentially rather than simultaneously. J. Clin. Endocrinol. Metab. (1996) 81:4264-4267.
39. BACH JF: Insulin-dependent diabetes mellitus as an autoimmune disease. Endocrine Rev. (1994) 15:516-542.
40. DEBRAY-SACHS MC, CARNAUD C, BOITARD H et al.: Prevention of diabetes in NOD mice treated with antibody to murine IFN gamma. J. Autoimmun. (1991) 4:237-248.
41. WANG Y, HAO L, GILL RG, LAFFERTY KJ: Autoimmune diabetes in NOD mouse is L3T4 T lymphocyte dependent. Diabetes (1987) 36:535-538.
42. RAPOPORT MJ, JARAMILLO A, ZIPRIS D et al.: IL-4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice. J. Exp. Med. (1993) 178:87-99.
43. PENNLINE KJ, ROQUE-GAFFNEY E, MONAHAN M: Recombinant human IL-10 prevents the onset of diabetes in the nonobese diabetic mouse. Clin. Immunol. Immunopathol. (1994) 71:169-175.
44. ZACCONE P, PHILLIPS J, GONGET I et al.: Interleukin-13 prevents autoimmune diabetes in NOD mice. Diabetes (1999) 48:1522-1528.
45. TIAN JD, CLARESALZLER M, HERSCHENFELD A et al.: Modulating autoimmune responses to GAD inhibits disease progression and prolongs islet graft survival in diabetes- prone mice. Nat. Med. (1996) 2:1348-1353.
46. TIAN J, ATKINSON MA, CLARE SALZLER M et al.: Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. J. Exp. Med. (1996) 183:1561-1567.
47. AL-SABBAGH A, MILLER A, SANTOS LM, WEINER HL: Antigen-driven tissue-specific suppression following oral tolerance: orally administered myelin basic protein suppresses proteolipid protein-induced experimental autoimmune encephalomyelitis in the SJL mouse. Eur. J. Immunol. (1994) 24:2104-2109.
48. TIAN J, LEHMANN PH, KAUFMAN DL: Determinant spreading of T helper cell 2 (Th2) responses to pancreatic islet autoantigens. J. Exp. Med. (1997) 186:2039-2043.
49. WANG B, GONZALEZ A, HOGLUND P, KATZ PD, BENOIST C, MATHIS D: Interleukin-4 deficiency does not exacerbate disease in NOD mice. Diabetes (1998) 47:1207-1211.
50. CALCINARO F, GAMBELUNGHE G, LAFFERTY KJ: Protection from autoimmune diabetes by adjuvant therapy in the non-obese diabetic mouse: the role of interleukin-4 and interleukin-10. Immunol. Cell Biol. (1997) 75:467-471.
51. QIN HY, SADELAIN MW, HITCHON C, LAUZON J, SINGH B: Complete Freund s adjuvant-induced T cells prevent the development and adoptive transfer of diabetes in nonobese diabetic mice. J. Immunol. (1993) 150:2072-2080.
52. BOITARD C, YASUNAMI R, DARDENNE M, BACH JF: T cell-mediated inhibition of the transfer of autoimmune diabetes in NOD mice. J. Exp. Med. (1989) 169:1669-1680.
53. HUTCHINGS PR, COOKE A: The transfer of autoimmune diabetes in NOD mice can be inhibited or accelerated by distinct cell populations present in normal splenocytes taken from young males. J. Autoimmun. (1990) 3:175-185.
54. YASUNAMI R, DEBRAY-SACHS M, BACH JF: Ontogeny of regulatory and effector T cells in autoimmune NOD mice. In: Frontiers in Diabetes Research. Lessons from Animal Diabetes III. Shafrir E (Ed.), Smith-Gordon, London. (1990):88-93.
55. LEPAULT F, GAGNERAULT MC, FAVEEUW C, BAZIN H, BOITARD C: Lack of L-selectin expression by cells transferring diabetes in NOD mice: insights into the mechanisms involved in diabetes prevention by Mel-14 antibody treatment. Eur. J. Immunol. (1995) 25:1502-1507.
56. + T cells. J. Exp. Med. (1987) 166:823-832.
57. WICKER LS, MILLER BJ, MULLEN Y: Transfer of autoimmune diabetes mellitus with splenocytes from nonobese diabetic (NOD) mice. Diabetes (1986) 35:855-860.
58. + regulatory T cells in the non-obese diabetic male mouse. Diabetologia (1994) 37:337-343.
59. CHATENOUD L, SALOMON B, BLUESTONE JA: Suppressor T cells-they're back and critical for regulation of autoimmunity! Immunol. Rev. (2001) 182:149-163.
60. ASKENASE PW, HAYDEN BJ, GERSHON RK: Augmentation of delayed-type hypersensitivity by doses of cyclophosphamide which do not affect antibody responses. J. Exp. Med. (1975) 141:697-702.
61. MINAGAWA H, TAKENAKA A, ITOYAMA Y, MORI R: Experimental allergic encephalomyelitis in the Lewis rat. A model of predictable relapse by cyclophosphamide. J. Neurol. Sci. (1987) 78:225-235.
62. MIYAZAKI C, NAKAMURA T, KANEKO K, MORI R, SHIBASAKI H: Reinduction of experimental allergic encephalomyelitis in convalescent Lewis rats with cyclophosphamide. J. Neurol. Sci. (1985) 67:277-284.
63. MCKENNA RM, CARTER BG, SEHON AH: Studies on the mechanism of suppression of experimental allergic encephalomyelitis induced by myelin basic protein-cell conjugates. Cell. Immunol. (1984) 88:251-259.
64. KARDYS E, HASHIM GA: Experimental allergic encephalomyelitis in Lewis rats: immunoregulation of disease by a single amino acid substitution in the disease-inducing determinant. J. Immunol. (1981) 127:862-866.
65. CHARLTON B, BACELJ A, SLATTERY RM, MANDEL TE: Cyclophosphamide-induced diabetes in NOD/WEHI mice. Evidence for suppression in spontaneous autoimmune diabetes mellitus. Diabetes (1989) 38:441-447.
66. YASUNAMI R, BACH JF: Antisuppressor effect of cyclophosphamide on the development of spontaneous diabetes in NOD mice. Eur. J. Immunol. (1988) 18:481-484.
67. MAHIOU J, WALTER U, LEPAULT F, GODEAU F, BACH JF, CHATENOUD L: In vivo blockade of the Fas-Fas ligand pathway inhibits cyclophosphamide-induced diabetes in NOD mice. J. Autoimmun. (2001) 16:431-440.
68. DARDENNE M, LEPAULT F, BENDELAC A, BACH JF: Acceleration of the onset of diabetes in NOD mice by thymectomy at weaning. Eur. J. Immunol. (1989) 19:889-895.
69. HERBELIN A, GOMBERT JM, LEPAULT F, BACH JF, CHATENOUD L: Mature mainstream TCR alpha beta(+)CD4(+) thymocytes expressing L-selectin mediate 'active tolerance' in the nonobese diabetic mouse. J. Immunol. (1998) 161:2620-2628.
70. SAKAGUCHI S: Regulatory T cells: key controllers of immunologic self- tolerance. Cell (2000) 101:455-458.
71. LENSCHOW DJ, HEROLD KC, RHEE L et al.: CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity (1996) 5:285-293.
72. + T cells controlling distinct organ-specific autoimmune diseases. Proc. Natl. Acad. Sci. USA (2003) 100:15806-15811.
73. CLEVERS H, ALARCON B, WILEMAN T, TERHORST TC: The T cell receptor/CD3 complex: a dynamic protein ensemble. Annu. Rev. Immunol. (1998) 6:629-662.
74. DAVIS MM, CHIEN YH: T cell antigen receptors. In: Fundamental Immunology. Paul W (Ed.), Raven Press, New York. (1999):34l-366.
75. KUNG P, GOLDSTEIN G, REINHERZ EL, SCHLOSSMAN SF: Monoclonal antibodies defining distinctive human T cell surface antigens. Science (1988) 206:347-349.
76. COSIMI AB, BURTON RC, COLVIN RB et al.: Treatment of acute renal allograft rejection with OKT3 monoclonal antibody. Transplantation (1981) 32:535-539.
77. DEBURE A, CHKOFF N, CHATENOUD L et al.: One-month prophylactic use of OKT3 in cadaver kidney transplant recipients. Transplantation (1988) 45:546-553.
78. VIGERAL P, CHKOFF N, CHATENOUD L et al.: Prophylactic use of OKT3 monoclonal antibody in cadaver kidney recipients. Utilization of OKT3 as the sole immunosuppressive agent. Transplantation (1986) 41:730-733.
79. LEO O, FOO M, SACHS DH, SAMELSON LE, BLUESTONE JA: Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc. Natl. Acad. Sci. USA (1987) 84:1374-1378.
80. 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) 305:308-314.
81. ORTHO X: A randomized clinical trial of OKT3 monoclonal antibody for acute rejection of cadaveric renal transplants. Ortho Multicenter Transplant Study Group. N. Engl. J. Med. (1985) 313:337-342.
82. CHATENOUD L: CD3-specific antibody-induced active tolerance: from bench to bedside. Nat. Rev. Immunol. (2003) 3:123-132.
83. CHATENOUD L, BAUDRIHAYE MF, CHKOFF N, KREIS H, GOLDSTEIN G, BACH JF: Restriction of the human in vivo immune response against the mouse monoclonal antibody OKT3. J. Immunol. (1986) 137:830-838.
84. CHATENOUD L, FERRAN C, LEGENDRE C et al.: In vivo cell activation following OKT3 administration. Systemic cytokine release and modulation by corticosteroids. Transplantation (1990) 49:697-702.
85. CHATENOUD L, FERRAN C, REUTER A et al.: Systemic reaction to the anti-T-cell monoclonal antibody OKT3 in relation to serum levels of tumour necrosis factor and interferon-gamma. N. Engl. J. Med. (1989) 320:1420-1421.
86. COSIMIAB: Clinical development of orthoclone OKT3. Transplant. Proc. (1987) 19:7-16.
87. ABRAMOWICZ D, SCHANDENE L, GOLDMAN M et al.: Release of tumour necrosis factor, interleukin-2, and gamma-interferon in serum after injection of OKT3 monoclonal antibody in kidney transplant recipients. Transplantation (1989) 47:606-608.
88. EASON JD, COSIMI AB: Biologic immunosuppressive agents. In: Transplantation. Ginns L, Cosimi A, Morris P (Eds), Blackwell Science, Maiden, USA. (1999): 196-224.
89. NICOLLS MR, AVERSA GG, PEARCE NW et al.: Induction of long-term specific tolerance to allografts in rats by therapy with an anti-CD3-like monoclonal antibody. Transplantation (1993) 55:459-468.
90. PLAIN KM, CHEN J, MERTEN S, HE XY, HALL BM: Induction of specific tolerance to allografts in rats by therapy with non-mitogenic, non-depleting anti-CD3 monoclonal antibody: association with TH2 cytokines not anergy. Transplantation (1999) 67:605-613.
91. HAYWARD AR, SHREIBER M: Neonatal injection of CD3 antibody into nonobese diabetic mice reduces the incidence of insulins and diabetes. J. Immunol. (1989) 143:1555-1559.
92. BELGHITH M, BLUESTONE JA, BARRIOT S, MEGRET J, BACH JF, CHATENOUD L: TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat. Med. (2003) 9:1202-1208.
93. CHATENOUD L, THERVET E, PRIMO J, BACH JF: Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc. Natl. Acad. Sci. USA (1994) 91:123-127.
94. CHATENOUD L, PRIMO J, BACH JF: CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice. J. Immunol. (1997) 158:2947-2954.
95. ALEGRE ML, PETERSON LJ, XU D et ai: A non-activating 'humanized' anti-CD3 monoclonal antibody retains immunosuppressive properties in vivo. Transplantation (1994) 57:1537-1543.
96. BOLT S, ROUTLEDGE E, LLOYD I et al.: The generation of a humanized, non-mitogenic CD3 monoclonal antibody which retains in vitro immunosuppressive properties. Eur. J. Immunol. (1993) 23:403-411.
97. FRIEND PJ, HALE G, CHATENOUD L et al.: Phase I study of an engineered aglycosylated humanized CD3 antibody in renal transplant rejection. Transplantation (1999) 68:1632-1637.
98. WOODLE ES, XU D, ZIVIN RA et al.: 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.
99. HEROLD KC, HAGOPIAN W, AUGER JA et al.: Anti-CD3 monoclonal antibody in new-onset Type 1 diabetes mellitus. N. Engl. J. Med. (2002) 346:1692-1698.