Best Practice & Research Clinical Rheumatology
Volume 24, Issue 4 , Pages 463-477 , August 2010

Co-stimulation and T cells as therapeutic targets

  • Alison M. Gizinski

      Affiliations

    • Division of Rheumatology, Department of Internal Medicine and Rheumatic Disease Core Center, University of Michigan, 1500 East Medical Center Drive, 3918Taubman Center, SPC 5358, Ann Arbor, Michigan 48109, USA
    • Tel.: +1 734 936 5560; Fax: +1 734 763 1253.
    • ,
  • David A. Fox

      Affiliations

    • Division of Rheumatology, Department of Internal Medicine and Rheumatic Disease Core Center, University of Michigan, 1500 East Medical Center Drive, 3918Taubman Center, SPC 5358, Ann Arbor, Michigan 48109, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 734 936 5560; Fax: +1 734 763 1253.
    web address
    • ,
  • Sujata Sarkar

      Affiliations

    • Section of Rheumatology, Department of Medicine, University of Arizona, 1501 North Campbell Avenue, Rm 6310, Tucson, Arizona 85724, USA
    • Tel.: +1 520 626 5727; Fax: +1 520 626 9366.

References 

  1. Linsley PS, Brady W, Grosmaire L, et al. Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J Exp Med. 1991;173(3):721–730
  2. Linsley PS, Greene JL, Brady W, et al. Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4 receptors. Immunity. 1994;1(9):793–801
  3. Peach RJ, Bajorath J, Brady W, et al. Complementarity determining region 1 (CDR1)- and CDR3-analogous regions in CTLA-4 and CD28 determine the binding to B7-1. J Exp Med. 1994;180(6):2049–2058
  4. Greene JL, Leytze GM, Emswiler J, et al. Covalent dimerization of CD28/CTLA-4 and oligomerization of CD80/CD86 regulate T cell costimulatory interactions. J Biol Chem. 1996;271(43):26762–26771
  5. Orabona C, Grohmann U, Belladonna ML, et al. CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nat Immunol. 2004;5(11):1134–1142
  6. Walunas TL, Lenschow DJ, Bakker CY, et al. CTLA-4 can function as a negative regulator of T cell activation. Immunity. 1994;1(5):405–413
  7. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med. 1995;182(2):459–465
  8. London CA, Lodge MP, Abbas AK. Functional responses and costimulator dependence of memory CD4 + T cells. J Immunol. 2000;164(1):265–272
  9. Ndejembi MP, Teijaro JR, Patke DS, et al. Control of memory CD4 T cell recall by the CD28/B7 costimulatory pathway. J Immunol. 2006;177(11):7698–7706
  10. Suntharalingam G, Perry MR, Ward S, et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med. 2006;355(10):1018–1028
  11. Webb LM, Walmsley MJ, Feldmann M. Prevention and amelioration of collagen-induced arthritis by blockade of the CD28 co-stimulatory pathway: requirement for both B7-1 and B7-2. Eur J Immunol. 1996;26(10):2320–2328
  12. Moreland LW, Alten R, Van den Bosch F, et al. 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. 2002;46(6):1470–1479
  13. Kremer JM, Westhovens R, Leon M, et al. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med. 2003;349(20):1907–1915
  14. Kremer JM, Dougados M, Emery P, et al. Treatment of rheumatoid arthritis with the selective costimulation modulator abatacept: twelve-month results of a phase iib, double-blind, randomized, placebo-controlled trial. Arthritis Rheum. 2005;52(8):2263–2271
  15. Westhovens R, Kremer JM, Moreland LW, et al. Safety and efficacy of the selective costimulation modulator abatacept in patients with rheumatoid arthritis receiving background methotrexate: a 5-year extended phase IIB study. J Rheumatol. 2009;36(4):736–742
  16. Genovese MC, Becker JC, Schiff M, et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med. 2005;353(11):1114–1123
  17. Genovese MC, Schiff M, Luggen M, et al. Efficacy and safety of the selective co-stimulation modulator abatacept following 2 years of treatment in patients with rheumatoid arthritis and an inadequate response to anti-tumour necrosis factor therapy. Ann Rheum Dis. 2008;67(4):547–554
  18. Schiff M, Keiserman M, Codding C, et al. Efficacy and safety of abatacept or infliximab vs placebo in ATTEST: a phase III, multi-centre, randomised, double-blind, placebo-controlled study in patients with rheumatoid arthritis and an inadequate response to methotrexate. Ann Rheum Dis. 2008;67(8):1096–1103
  19. Kremer JM, Genant HK, Moreland LW, et al. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann Intern Med. 2006;144(12):865–876
  20. Westhovens R, Robles M, Ximenes AC, et al. Clinical efficacy and safety of abatacept in methotrexate-naive patients with early rheumatoid arthritis and poor prognostic factors. Ann Rheum Dis. 2009;
  21. Weinblatt M, Combe B, Covucci A, et al. Safety of the selective costimulation modulator abatacept in rheumatoid arthritis patients receiving background biologic and nonbiologic disease-modifying antirheumatic drugs: A one-year randomized, placebo-controlled study. Arthritis Rheum. 2006;54(9):2807–2816
  22. Weinblatt M, Schiff M, Goldman A, et al. Selective costimulation modulation using abatacept in patients with active rheumatoid arthritis while receiving etanercept: a randomised clinical trial. Ann Rheum Dis. 2007;66(2):228–234
  23. Weisman MH, Durez P, Hallegua D, et al. Reduction of inflammatory biomarker response by abatacept in treatment of rheumatoid arthritis. J Rheumatol. 2006;33(11):2162–2166
  24. Buch MH, Boyle DL, Rosengren S, et al. Mode of action of abatacept in rheumatoid arthritis patients having failed tumour necrosis factor blockade: a histological, gene expression and dynamic magnetic resonance imaging pilot study. Ann Rheum Dis. 2009;68(7):1220–1227
  25. Larsen CP, Pearson TC, Adams AB, et al. Rational development of LEA29Y (belatacept), a high-affinity variant of CTLA4-Ig with potent immunosuppressive properties. Am J Transplant. 2005;5(3):443–453
  26. Latek R, Fleener C, Lamian V, et al. Assessment of belatacept-mediated costimulation blockade through evaluation of CD80/86-receptor saturation. Transplantation. 2009;87(6):926–933
  27. Vincenti F, Larsen C, Durrbach A, et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med. 2005;353(8):770–781
  28. Walker LS, Gulbranson-Judge A, Flynn S, et al. Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J Exp Med. 1999;190(8):1115–1122
  29. Ohshima Y, Tanaka Y, Tozawa H, et al. Expression and function of OX40 ligand on human dendritic cells. J Immunol. 1997;159(8):3838–3848
  30. Murata K, Ishii N, Takano H, et al. Impairment of antigen-presenting cell function in mice lacking expression of OX40 ligand. J Exp Med. 2000;191(2):365–374
  31. Saijo S, Asano M, Horai R, et al. Suppression of auto-immune arthritis in interleukin-1-deficient mice in which T cell activation is impaired due to low levels of CD40 ligand and OX40 expression on T cells. Arthritis Rheum. 2002;46(2):533–544
  32. Yoshioka T, Nakajima A, Akiba H, et al. Contribution of OX40/OX40 ligand interaction to the pathogenesis of rheumatoid arthritis. Eur J Immunol. 2000;30(10):2815–2823
  33. Boot EP, Koning GA, Storm G, et al. CD134 as target for specific drug delivery to auto-aggressive CD4 + T cells in adjuvant arthritis. Arthritis Res Ther. 2005;7(3):R604–R615
  34. Brugnoni D, Bettinardi A, Malacarne F, et al. CD134/OX40 expression by synovial fluid CD4 + T lymphocytes in chronic synovitis. Br J Rheumatol. 1998;37(5):584–585
  35. Giacomelli R, Passacantando A, Perricone R, et al. T lymphocytes in the synovial fluid of patients with active rheumatoid arthritis display CD134-OX40 surface antigen. Clin Exp Rheumatol. 2001;19(3):317–320
  36. Passacantando A, Parzanese I, Rascente M, et al. Synovial fluid OX40T lymphocytes of patients with rheumatoid arthritis display a Th2/Th0 polarization. Int J Immunopathol Pharmacol. 2006;19(3):499–505
  37. Imura A, Hori T, Imada K, et al. The human OX40/gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells. J Exp Med. 1996;183(5):2185–2195
  38. Stuber E, Neurath M, Calderhead D, et al. Cross-linking of OX40 ligand, a member of the TNF/NGF cytokine family, induces proliferation and differentiation in murine splenic B cells. Immunity. 1995;2(5):507–521
  39. Stuber E, Strober W. The T cell-B cell interaction via OX40-OX40L is necessary for the T cell-dependent humoral immune response. J Exp Med. 1996;183(3):979–989
  40. Nurieva RI, Treuting P, Duong J, et al. Inducible costimulator is essential for collagen-induced arthritis. J Clin Invest. 2003;111(5):701–706
  41. Iwai H, Kozono Y, Hirose S, et al. Amelioration of collagen-induced arthritis by blockade of inducible costimulator-B7 homologous protein costimulation. J Immunol. 2002;169(8):4332–4339
  42. Okamoto T, Saito S, Yamanaka H, et al. Expression and function of the co-stimulator H4/ICOS on activated T cells of patients with rheumatoid arthritis. J Rheumatol. 2003;30(6):1157–1163
  43. Ruth JH, Rottman JB, Kingsbury GA, et al. ICOS and B7 costimulatory molecule expression identifies activated cellular subsets in rheumatoid arthritis. Cytometry A. 2007;71(5):317–326
  44. Wang C, Lin GH, McPherson AJ, et al. Immune regulation by 4-1BB and 4-1BBL: complexities and challenges. Immunol Rev. 2009;229(1):192–215
  45. Foell JL, Diez-Mendiondo BI, Diez OH, et al. Engagement of the CD137 (4-1BB) costimulatory molecule inhibits and reverses the autoimmune process in collagen-induced arthritis and establishes lasting disease resistance. Immunology. 2004;113(1):89–98
  46. Seo SK, Choi JH, Kim YH, et al. 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nat Med. 2004;10(10):1088–1094
  47. Jung HW, Choi SW, Choi JI, et al. Serum concentrations of soluble 4-1BB and 4-1BB ligand correlated with the disease severity in rheumatoid arthritis. Exp Mol Med. 2004;36(1):13–22
  48. Michel J, Langstein J, Hofstadter F, et al. A soluble form of CD137 (ILA/4-1BB), a member of the TNF receptor family, is released by activated lymphocytes and is detectable in sera of patients with rheumatoid arthritis. Eur J Immunol. 1998;28(1):290–295
  49. Zola H. Leukocyte and stromal cell molecules: the CD markers. Hoboken, N.J: Wiley-Liss; 2007;
  50. Mason D. In: Leucocyte typing VII: white cell differentiation antigens: proceedings of the Seventh International Workshop and Conference held in Harrogate, United Kingdom. Oxford:: Oxford University Press; 2002;
  51. Isaacs JD, Burrows N, Wing M, et al. Humanized anti-CD4 monoclonal antibody therapy of autoimmune and inflammatory disease. Clin Exp Immunol. 1997;110(2):158–166
  52. Choy EH, Connolly DJ, Rapson N, et al. Pharmacokinetic, pharmacodynamic and clinical effects of a humanized IgG1 anti-CD4 monoclonal antibody in the peripheral blood and synovial fluid of rheumatoid arthritis patients. Rheumatology (Oxford). 2000;39(10):1139–1146
  53. Choy EH, Panayi GS, Emery P, et al. Repeat-cycle study of high-dose intravenous 4162W94 anti-CD4 humanized monoclonal antibody in rheumatoid arthritis. A randomized placebo-controlled trial. Rheumatology (Oxford). 2002;41(10):1142–1148
  54. Moreland LW, Bucy RP, Tilden A, et al. Use of a chimeric monoclonal anti-CD4 antibody in patients with refractory rheumatoid arthritis. Arthritis Rheum. 1993;36(3):307–318
  55. Plater-Zyberk C, Taylor PC, Blaylock MG, et al. Anti-CD5 therapy decreases severity of established disease in collagen type II-induced arthritis in DBA/1 mice. Clin Exp Immunol. 1994;98(3):442–447
  56. Strand V, Lipsky PE, Cannon GW, et al. Effects of administration of an anti-CD5 plus immunoconjugate in rheumatoid arthritis. Results of two phase II studies. The CD5 Plus Rheumatoid Arthritis Investigators Group. Arthritis Rheum. 1993;36(5):620–630
  57. Fox DA. Biological therapies: a novel approach to the treatment of autoimzmune disease. Am J Med. 1995;99(1):82–88
  58. Olsen NJ, Brooks RH, Cush JJ, et al. A double-blind, placebo-controlled study of anti-CD5 immunoconjugate in patients with rheumatoid arthritis. The Xoma RA Investigator Group. Arthritis Rheum. 1996;39(7):1102–1108
  59. Janeway CA. Immunobiology: the immune system in health and disease. 5th ed.. New York: Garland; 2001;
  60. Boumpas DT, Furie R, Manzi S, et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum. 2003;48(3):719–727
  61. Bhat P, Radhakrishnan J. B lymphocytes and lupus nephritis: new insights into pathogenesis and targeted therapies. Kidney Int. 2008;73(3):261–268
  62. Kalunian KC, Davis JC, Merrill JT, et al. Treatment of systemic lupus erythematosus by inhibition of T cell costimulation with anti-CD154: a randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2002;46(12):3251–3258
  63. Polman CH, O'Connor PW, Havrdova E, et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med. 2006;354(9):899–910
  64. Kleinschmidt-DeMasters BK, Tyler KL. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N Engl J Med. 2005;353(4):369–374
  65. Langer-Gould A, Atlas SW, Green AJ, et al. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N Engl J Med. 2005;353(4):375–381
  66. Van Assche G, Van Ranst M, Sciot R, et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N Engl J Med. 2005;353(4):362–368
  67. Gray JX, Haino M, Roth MJ, et al. CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J Immunol. 1996;157(12):5438–5447
  68. Hamann J, Wishaupt JO, van Lier RA, et al. Expression of the activation antigen CD97 and its ligand CD55 in rheumatoid synovial tissue. Arthritis Rheum. 1999;42(4):650–658
  69. Kop EN, Kwakkenbos MJ, Teske GJ, et al. Identification of the epidermal growth factor-TM7 receptor EMR2 and its ligand dermatan sulfate in rheumatoid synovial tissue. Arthritis Rheum. 2005;52(2):442–450
  70. Kop EN, Adriaansen J, Smeets TJ, et al. CD97 neutralisation increases resistance to collagen-induced arthritis in mice. Arthritis Res Ther. 2006;8(5):R155
  71. Strand V, Kimberly R, Isaacs JD. Biologic therapies in rheumatology: lessons learned, future directions. Nat Rev Drug Discov. 2007;6(1):75–92
  72. Brett S, Baxter G, Cooper H, et al. Repopulation of blood lymphocyte sub-populations in rheumatoid arthritis patients treated with the depleting humanized monoclonal antibody, CAMPATH-1H. Immunology. 1996;88(1):13–19
  73. Isaacs JD, Manna VK, Rapson N, et al. CAMPATH-1H in rheumatoid arthritis–an intravenous dose-ranging study. Br J Rheumatol. 1996;35(3):231–240
  74. Weinblatt ME, Maddison PJ, Bulpitt KJ, et al. CAMPATH-1H, a humanized monoclonal antibody, in refractory rheumatoid arthritis. An intravenous dose-escalation study. Arthritis Rheum. 1995;38(11):1589–1594
  75. Oelke K, Lu Q, Richardson D, et al. Overexpression of CD70 and overstimulation of IgG synthesis by lupus T cells and T cells treated with DNA methylation inhibitors. Arthritis Rheum. 2004;50(6):1850–1860
  76. Lu Q, Wu A, Richardson BC. Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J Immunol. 2005;174(10):6212–6219
  77. Lee WW, Yang ZZ, Li G, et al. Unchecked CD70 expression on T cells lowers threshold for T cell activation in rheumatoid arthritis. J Immunol. 2007;179(4):2609–2615
  78. Oflazoglu E, Boursalian TE, Zeng W, et al. Blocking of CD27-CD70 pathway by anti-CD70 antibody ameliorates joint disease in murine collagen-induced arthritis. J Immunol. 2009;183(6):3770–3777
  79. McEarchern JA, Smith LM, McDonagh CF, et al. Preclinical characterization of SGN-70, a humanized antibody directed against CD70. Clin Cancer Res. 2008;14(23):7763–7772

PII: S1521-6942(09)00160-0

doi: 10.1016/j.berh.2009.12.015

Best Practice & Research Clinical Rheumatology
Volume 24, Issue 4 , Pages 463-477 , August 2010

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