Combination and Adjuvant Therapies to Facilitate the Efficacy of Costimulatory Blockade

Immunotherapy in Transplantation: Principles and Practice

Volumn , Issue , 2012, Pages 407-428

  Srinivasan, Swetha K ^a   Triemer, Helen L ^a   Kirk, Allan D ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Antibodies; Biologics; Costimulation; Fusion proteins; Immunosuppression; Transplantation

Indexed keywords

EID: 84885773095     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444355628.ch28     Document Type: Chapter

References (115)

1. Meier-Kriesche HU, Schold JD, Srinivas TR, Kaplan B. Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. Am J Transplant 2004; 4 (3): 378-383.
2. Barocci S, Valente U, Fontana I et al. Long-term outcome on kidney retransplantation: a review of 100 cases from a single center. Transplant Proc 2009; 41 (4): 1156-1158.
3. Bach FH, Sachs DH. Current concepts: immunology. Transplantation immunology. N Engl J Med 1987; 317 (8): 489-492.
4. Lafferty KJ, Cunningham AJ. A new analysis of allogeneic interactions. Aust J Exp Biol Med Sci 1975; 53 (1): 27-42.
5. Bretscher P, Cohn M. A theory of self-nonself discrimination. Science 1970; 169 (950): 1042-1049.
6. Jenkins MK, Schwartz RH. Antigen presentation by chemically modified splenocytes induces antigenspecific T cell unresponsiveness in vitro and in vivo. J Exp Med 1987; 165 (2): 302-319.
7. Janeway CA, Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989; 54 (Pt 1): 1-13.
8. Schwartz RH. A cell culture model for T lymphocyte clonal anergy. Science 1990; 248 (4961): 1349-1356.
9. Martin PJ, Ledbetter JA, Morishita Y et al. A 44 kilodalton cell surface homodimer regulates interleukin 2 production by activated human T lymphocytes. J Immunol 1986; 136 (9): 3282-3287.
10. Hara T, Fu SM, Hansen JA. Human T cell activation. II. A new activation pathway used by a major T cell population via a disulfide-bonded dimer of a 44 kilodalton polypeptide (9.3 antigen). J Exp Med 1985; 161 (6): 1513-1524.
11. Lenschow DJ, Zeng Y, Thistlethwaite JR et al. Longterm survival of xenogeneic pancreatic islet grafts induced by CTLA4lg. Science 1992; 257 (5071): 789-792.
12. Harlan DM, Kirk AD. The future of organ and tissue transplantation: can T-cell costimulatory pathway modifiers revolutionize the prevention of graft rejection? JAMA 1999; 282 (11): 1076-1082.
13. Brunet JF, Denizot F, Luciani MF et al. A new member of the immunoglobulin superfamily-CTLA-4. Nature 1987; 328 (6127): 267-270.
14. Paulie S, Ehlin-Henriksson B, Mellstedt H et al. A p50 surface antigen restricted to human urinary bladder carcinomas and B lymphocytes. Cancer Immunol Immunother 1985; 20 (1): 23-28.
15. Clark EA, Shu G, Ledbetter JA. Role of the Bp35 cell surface polypeptide in human B-cell activation. Proc Natl Acad Sci U S A 1985; 82 (6): 1766-1770.
16. Larsen CP, Pearson TC. The CD40 pathway in allograft rejection, acceptance, and tolerance. Curr Opin Immunol 1997; 9 (5): 641-647.
17. Larsen CP, Knechtle SJ, Adams A et al. A new look at blockade of T-cell costimulation: a therapeutic strategy for long-term maintenance immunosuppression. Am J Transplant 2006; 6 (5 Pt 1): 876-883.
18. Van Essen D, Kikutani H, Gray D. CD40 ligand-transduced co-stimulation of T cells in the development of helper function. Nature 1995; 378 (6557): 620-623.
19. Armitage RJ, Fanslow WC, Strockbine L et al. Molecular and biological characterization of a murine ligand for CD40. Nature 1992; 357 (6373): 80-82.
20. Noelle RJ, Roy M, Shepherd DM et al. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc Natl Acad Sci U S A 1992; 89 (14): 6550-6554.
21. Armitage RJ, Sato TA, Macduff BM et al. Identification of a source of biologically active CD40 ligand. Eur J Immunol 1992; 22 (8): 2071-2076.
22. Johnson-Leger C, Christenson JR, Holman M, Klaus GG. Evidence for a critical role for IL-2 in CD40- mediated activation of naive B cells by primary CD4 T cells. J Immunol 1998; 161 (9): 4618-4626.
23. Kirk AD, Blair PJ, Tadaki DK et al. The role of CD154 in organ transplant rejection and acceptance. Philos Trans R Soc Lond B Biol Sci 2001; 356 (1409): 691-702.
24. Henn V, Slupsky JR, Grafe M et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998; 391 (6667): 591-594.
25. Xu H, Zhang X, Mannon RB, Kirk AD. Platelet-derived or soluble CD154 induces vascularized allograft rejection independent of cell-bound CD154. J Clin Invest 2006; 116 (3): 769-774.
26. Parker DC, Greiner DL, Phillips NE et al. Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand. Proc Natl Acad Sci U S A 1995; 92 (21): 9560-9564.
27. Larsen CP, Elwood ET, Alexander DZ et al. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 1996; 381 (6581): 434-438.
28. Kirk AD, Burkly LC, Batty DS et al. Treatment with humanized monoclonal antibody against CD154 prevents acute renal allograft rejection in nonhuman primates. Nat Med 1999; 5 (6): 686-693.
29. Kirk AD, Harlan DM, Armstrong NN et al. CTLA4-Ig and anti-CD40 ligand prevent renal allograft rejection in primates. Proc Natl Acad Sci U S A 1997; 94 (16): 8789-8794.
30. Sayegh MH, Turka LA. The role of T-cell costimulatory activation pathways in transplant rejection. N Engl J Med 1998; 338 (25): 1813-1821.
31. Davignon D, Martz E, Reynolds T et al. Lymphocyte function-associated antigen 1 (LFA-1): a surface antigen distinct from Lyt-2,3 that participates in T lymphocyte-mediated killing. Proc Natl Acad Sci U S A 1981; 78 (7): 4535-4539.
32. Van Seventer GA, Shimizu Y, Horgan KJ, Shaw S. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J Immunol 1990; 144 (12): 4579-4586.
33. Ford ML, Larsen CP. Translating costimulation blockade to the clinic: lessons learned from three pathways. Immunol Rev 2009; 229 (1): 294-306.
34. Johnson JG, Jenkins MK. Accessory cell-derived signals required for T cell activation. Immunol Res 1993; 12 (1): 48-64.
35. Owens T. A role for adhesion molecules in contactdependent T help for B cells. Eur J Immunol 1991; 21 (4): 979-983.
36. Van Seventer GA, Bonvini E, Yamada H et al. Costimulation of T cell receptor/CD3-mediated activation of resting human CD4 + T cells by leukocyte function- associated antigen-1 ligand intercellular cell adhesion molecule-1 involves prolonged inositol phospholipid hydrolysis and sustained increase of intracellular Ca 2+ levels. J Immunol 1992; 149 (12): 3872-3880.
37. Zuckerman LA, Pullen L, Miller J. Functional consequences of costimulation by ICAM-1 on IL-2 gene expression and T cell activation. J Immunol 1998; 160 (7): 3259-3268.
38. Sanchez-Madrid F, Krensky AM, Ware CF et al. Three distinct antigens associated with human T-lymphocytemediated cytolysis: LFA-1, LFA-2, and LFA-3. Proc Natl Acad Sci U S A 1982; 79 (23): 7489-7493.
39. Wilkins AL, Yang W, Yang JJ. Structural biology of the cell adhesion protein CD2: from molecular recognition to protein folding and design. Curr Protein Pept Sci 2003; 4 (5): 367-373.
40. Latchman Y, Reiser H. Enhanced murine CD4 + T cell responses induced by the CD2 ligand CD48. Eur J Immunol 1998; 28 (12): 4325-4331.
41. Bachmann MF, Barner M, Kopf M. CD2 sets quantitative thresholds in T cell activation. J Exp Med 1999; 190 (10): 1383-1392.
42. Aruffo A, Hollenbaugh D. Therapeutic intervention with inhibitors of co-stimulatory pathways in autoimmune disease. Curr Opin Immunol 2001; 13 (6): 683-686.
43. Semnani RT, Nutman TB, Hochman P et al. Costimulation by purified intercellular adhesion molecule 1 and lymphocyte function-associated antigen 3 induces distinct proliferation, cytokine and cell surface antigen profiles in human "naive" and "memory" CD4 + T cells. J Exp Med 1994; 180 (6): 2125-2135.
44. Köhler G, Milstein C. Derivation of specific antibodyproducing tissue culture and tumor lines by cell fusion. Eur J Immunol 1976; 6 (7): 511-519.
45. Reichert JM, Valge-Archer VE. Development trends for monoclonal antibody cancer therapeutics. Nat Rev Drug Discov 2007; 6 (5): 349-356.
46. Bluestone JA, St Clair EW, Turka LA. CTLA4Ig: bridging the basic immunology with clinical application. Immunity 2006; 24 (3): 233-238.
47. Weaver TA, Charafeddine AH, Kirk AD. Costimulation blockade: towards clinical application. Front Biosci 2008; 13: 2120-2139.
48. Kirk AD, Tadaki DK, Celniker A et al. Induction therapy with monoclonal antibodies specific for CD80 and CD86 delays the onset of acute renal allograft rejection in non-human primates. Transplantation 2001; 72 (3): 377-384.
49. 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.
50. Crameri A, Raillard SA, Bermudez E, Stemmer WP. DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 1998; 391 (6664): 288-291.
51. Lazetic S, Leong SR, Chang JC et al. Chimeric co-stimulatory molecules that selectively act through CD28 or CTLA-4 on human T cells. J Biol Chem 2002; 277 (41): 38660-38668.
52. Stebbings R, Poole S, Thorpe R. Safety of biologics, lessons learnt from TGN1412. Curr Opin Biotechnol 2009; 20 (6): 673-677.
53. 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.
54. Weber J. Ipilimumab: controversies in its development, utility and autoimmune adverse events. Cancer Immunol Immunother 2009; 58: 823-830.
55. 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.
56. Imai A, Suzuki T, Sugitani A et al. A novel fully human anti-CD40 monoclonal antibody, 4D11, for kidney transplantation in cynomolgus monkeys. Transplantation 2007; 84 (8): 1020-1028.
57. Aoyagi T, Yamashita K, Suzuki T et al. A human anti-CD40 monoclonal antibody, 4D11, for kidney transplantation in cynomolgus monkeys: induction and maintenance therapy. Am J Transplant 2009; 9 (8): 1732-1741.
58. Robak T. Novel monoclonal antibodies for the treatment of chronic lymphocytic leukemia. Curr Cancer Drug Targets 2008; 8 (2): 156-171.
59. Adams AB, Shirasugi N, Jones TR et al. Development of a chimeric anti-CD40 monoclonal antibody that synergizes with LEA29Y to prolong islet allograft survival. J Immunol 2005; 174 (1): 542-550.
60. Ellis CN, Krueger GG. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N Engl J Med 2001; 345 (4): 248-255.
61. Weaver TA, Charafeddine AH, Agarwal A et al. Alefacept promotes co-stimulation blockade based allograft survival in nonhuman primates. Nat Med 2009; 15 (7): 746-749.
62. Pearson TC, Alexander DZ, Corbascio M et al. Analysis of the B7 costimulatory pathway in allograft rejection. Transplantation 1997; 63 (10): 1463-1469.
63. Pearson TC, Alexander DZ, Winn KJ et al. Transplantation tolerance induced by CTLA4-Ig. Transplantation 1994; 57 (12): 1701-1706.
64. Goeb V, Buch MH, Vital EM, Emery P. Costimulation blockade in rheumatic diseases: where we are? Curr Opin Rheumatol 2009; 21 (3): 244-250.
65. Kean LS, Hamby K, Koehn B et al. NK cells mediate costimulation blockade-resistant rejection of allogeneic stem cells during nonmyeloablative transplantation. Am J Transplant 2006; 6 (2): 292-304.
66. Zhai Y, Meng L, Gao F et al. Allograft rejection by primed/memory CD8 + T cells is CD154 blockade resistant: thera peutic implications for sensitized transplant recipients. J Immunol 2002; 169 (8): 4667-4673.
67. Page AJ, Ford ML, Kirk AD. Memory T-cell-specific therapeutics in organ transplantation. Curr Opin Organ Transplant 2009; 14 (6): 643-649.
68. Blair PJ, Riley JL, Harlan DM et al. CD40 ligand (CD154) triggers a short-term CD4 + T cell activation response that results in secretion of immunomodulatory cytokines and apoptosis. J Exp Med 2000; 191 (4): 651-660.
69. Durie FH, Foy TM, Masters SR et al. The role of CD40 in the regulation of humoral and cell-mediated immunity. Immunol Today 1994; 15 (9): 406-411.
70. Andre P, Prasad KS, Denis CV et al. CD40L stabilizes arterial thrombi by a beta3 integrin-dependent mechanism. Nat Med 2002; 8 (3): 247-252.
71. Nicolls MR, Gill RG. LFA-1 (CD11a) as a therapeutic target. Am J Transplant 2006; 6 (1): 27-36.
72. Vincenti F, Mendez R, Pescovitz M et al. A Phase I/II randomized open-label multicenter trial of efalizumab, a humanized anti-CD11a, anti-LFA-1 in renal transplantation. Am J Transplant 2007; 7 (7): 1770-1777.
73. Chamian F, Lowes MA, Lin SL et al. Alefacept reduces infiltrating T cells, activated dendritic cells, nd inflammatory genes in psoriasis vulgaris. Proc Natl Acad Sci U S A 2005; 102 (6): 2075-2080.
74. Dhanireddy KK, Bruno DA, Weaver TA et al. Portal venous donor-specific transfusion in conjunction with sirolimus prolongs renal allograft survival in nonhuman primates. Am J Transplant 2009; 9 (1): 124-131.
75. Kaplon RJ, Hochman PS, Michler RE et al. Short course single agent therapy with an LFA-3-IgG1 fusion protein prolongs primate cardiac allograft survival. Transplantation 1996; 61 (3): 356-363.
76. Rang HP. The receptor concept: pharmacology's big idea. Br J Pharmacol 2006; 147 (Suppl 1): S9-S16.
77. Kenakin T. Efficacy in drug receptor theory: outdated concept or under-valued tool? Trends Pharmacol Sci 1999; 20 (10): 400-405.
78. Perez N, Karumuthil-Melethil S, Li R et al. Preferential costimulation by CD80 results in IL-10-dependent TGF-beta1 + -adaptive regulatory T cell generation. J Immunol 2008; 180 (10): 6566-6576.
79. Latek R, Fleener C, Lamian V et al. Assessment of belatacept-mediated costimulation blockade throu evaluation of CD80/86-receptor saturation. Transplantation 2009; 87 (6): 926-933.
80. Gilson CR, Milas Z, Gangappa S et al. Anti-CD40 monoclonal antibody synergizes with CTLA4-Ig in promoting long-term graft survival in murine models of transplantation. J Immunol 2009; 183 (3): 1625-1635.
81. 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.
82. Vincenti F, Kirk AD. What's next in the pipeline. Am J Transplant 2008; 8 (10): 1972-1981.
83. Vincenti F, Larsen C, Durrbach A et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med 2005; 353 (8): 770-781.
84. Xu H, Elster EA, Blair PJ et al. Effects of combined treatment with CD25- and CD154-specific monoclonal antibodies in non-human primate allotransplantation. Am J Transplant 2003; 3 (11): 1350-1354.
85. Jones TR, Ha J, Williams MA et al. The role of the IL-2 pathway in costimulation blockade-resistant rejection of allografts. J Immunol 2002; 168 (3): 1123-1130.
86. Emamaullee JA, Merani S, Larsen CP, Shapiro AM. Belatacept and basiliximab diminish human antiporcine xenoreactivity and synergize to inhibit alloimmunity. Transplantation 2008; 85 (1): 118-124.
87. Bluestone JA, Liu W, Yabu JM et al. The effect of costimulatory and interleukin 2 receptor blockade on regulatory T cells in renal transplantation. Am J Transplant 2008; 8 (10): 2086-2096.
88. Li Y, Li XC, Zheng XX et al. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat Med 1999; 5 (11): 1298-1302.
89. Pearl JP, Parris J, Hale DA et al. Immunocompetent T-cells with a memory-like phenotype are the dominant cell type following antibody-mediated T-cell depletion. Am J Transplant 2005; 5 (3): 465-474.
90. Vincenti F, Chapentier B, Vanrenterghem Y et al. A Phase III study of belatacept-based immunosuppression regimens versus cyclosporine in renal transplant recipients (BENEFIT Study). Am J Transplant 2010; 10: 535-546.
91. Adams AB, Pearson TC, Larsen CP. Heterologous immunity: an overlooked barrier to tolerance. Immunol Rev 2003; 196: 147-160.
92. Kirk AD. 4D11: the second mouse? Am J Transplant 2009; 9 (8): 1701-1702.
93. Cho CS, Burkly LC, Fechner JH, Jr, et al. Successful conversion from conventional immunosuppression to anti-CD154 monoclonal antibody costimulatory molecule blockade in rhesus renal allograft recipients. Transplantation 2001; 72 (4): 587-597.
94. Wells AD, Li XC, Li Y et al. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat Med 1999; 5 (11): 1303-1307.
95. Preston EH, Xu H, Dhanireddy KK et al. IDEC-131 (anti-CD154), sirolimus and donor-specific transfusion facilitate operational tolerance in non-human primates. Am J Transplant 2005; 5 (5): 1032-1041.
96. Montgomery SP, Mog SR, Xu H et al. Efficacy and toxicity of a protocol using sirolimus, tacrolimus and daclizumab in a nonhuman primate renal allotransplant model. Am J Transplant 2002; 2 (4): 381-385.
97. Clinicaltrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US); 2000. Available from: http://clinicaltrials.gov (accessed 2 March 2010).
98. Wu Z, Bensinger SJ, Zhang J et al. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 2004; 10 (1): 87-92.
99. Preville X, Flacher M, LeMauff B et al. Mechanisms involved in antithymocyte globulin immunosuppressive activity in a nonhuman primate model. Transplantation 2001; 71 (3): 460-468.
100. Kirk AD, Mannon RB, Kleiner DE et al. Results from a human renal allograft tolerance trial valuating T-cell depletion with alemtuzumab combined with deoxyspergualin. Transplantation 2005; 80 (8): 1051-1059.
101. Knechtle SJ, Kirk AD, Fechner JH, Jr, et al. Inducing unresponsiveness by the use of anti-CD3 immunotoxin, CTLA4-Ig, and anti-CD40 ligand. Transplant Proc 1999; 31 (3B Suppl): 27S-28S.
102. Wu G, Pfeiffer S, Schroder C et al. Co-stimulation blockade targeting CD154 and CD28/B7 modulates the induced antibody response after a pig-to-baboon cardiac xenograft. Xenotransplantation 2005; 12 (3): 197-208.
103. Montgomery SP, Xu H, Tadaki DK et al. Combination induction therapy with monoclonal antibodies specific for CD80, CD86, and CD154 in nonhuman primate renal transplantation. Transplantation 2002; 74 (10): 1365-1369.
104. Li ZL, Tian PX, Xue WJ, Wu J. Co-expression of sCD40LIg and CTLA4Ig mediated by adenovirus prolonged mouse skin allograft survival. J Zhejiang Univ Sci B 2006; 7 (6): 436-444.
105. Zhu P, Chen YF, Chen XP et al. Mechanisms of survival prolongation of murine cardiac allografts using the treatment of CTLA4-Ig and MR1. Transplant Proc 2008; 40 (5): 1618-1624.
106. Rigby MR, Trexler AM, Pearson TC, Larsen CP. CD28/CD154 blockade prevents autoimmune diabetes by inducing nondeletional tolerance after effector t-cell inhibition and regulatory T-cell expansion. Diabetes 2008; 57 (10): 2672-2683.
107. Yin D, Ma L, Shen J et al. CTLA-41 g in combination with anti-CD40L prolongs xenograft survival and inhibits anti-gal ab production in GT-Ko mice. Am J Transplant 2002; 2 (1): 41-47.
108. Cardona K, Korbutt GS, Milas Z et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med 2006; 12 (3): 304-306.
109. Pierson RN, 3rd, Crowe JE, Jr, Pfeiffer S et al. CD40- ligand in primate cardiac allograft and viral immunity. Immunol Res 2001; 23 (2-3): 253-262.
110. Barrett TB, Shu G, Clark EA. CD40 signaling activates CD11a/CD18 (LFA-1)-mediated adhesion in B cells. J Immunol 1991; 146 (6): 1722-1729.
111. Blazar BR, Taylor PA, Panoskaltsis-Mortari A et al. Coblockade of the LFA1:ICAM and CD28/CTLA4:B7 pathways is a highly effective means of preventing acute lethal graft-versus-host disease induced by fully major histocompatibility complex-disparate donor grafts. Blood 1995; 85 (9): 2607-2618.
112. Wang Y, Gao D, Lunsford KE et al. Targeting LFA-1 synergizes with CD40/CD40L blockade for suppression of both CD4-dependent and CD8- dependent rejection. Am J Transplant 2003; 3 (10): 1251-1258.
113. Corbascio M, Mahanty H, Osterholm C et al. Antilymphocyte function-associated antigen-1 monoclonal antibody inhibits CD40 ligandindependent immune responses and prevents chronic vasculopathy in CD40 ligand-deficient mice. Transplantation 2002; 74 (1): 35-41.
114. Badell IR, Thompson P, Turner A et al. Combination CD28/LFA-1 blockade promotes alloislet survival in nonhuman primates. Presented at the American Transplant Congress, San Diego, CA, 30 April-4 May, 2010.
115. Durbach A, Pestana JM, Pearson T et al. A phase III study of belatacept versus cyclosporine in kidney transplants from extended criteria donors (BENEFITEXT Study). Am J Transplant 2010; 10: 547-557.