Anti-CD28 Antibody-Initiated Cytokine Storm in Canines

Transplantation Direct

Volumn 1, Issue 2, 2015, Pages E7-

  Rosinski, Steven L ^a,b   Storb, Rainer ^a,b   Strong, Roland K ^a   Sale, George E ^a   Stone, Diane M ^a   Gewe, Mesfin M ^a   Friend, Della J ^a   Abrams, V Kraig ^a   Randolph Habecker, Julie ^a   Graves, Scott S ^a,b  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85014325995     PISSN: None     EISSN: 23738731     Source Type: Journal    
DOI: 10.1097/TXD.0000000000000516     Document Type: Article

References (47)

1. Storb R, Yu C, Zaucha JM, et al. Stable mixed hematopoietic chimerism in dogs given donor antigen, CTLA4Ig, and 100 cGy total body irradiation before and pharmacologic immunosuppression after marrow transplant. Blood. 1999;94:2523.
2. Yu C, Linsley P, Seidel K, et al. Cytotoxic T lymphocyte antigen 4-immunoglobulin fusion protein combined with methotrexate/ cyclosporine as graft-versus-host disease prevention in a canine dog leukocyte antigen-nonidentical marrow transplant model. Transplantation. 2000;69:450.
3. Miller WP, Srinivasan S, Panoskaltsis-Mortari A, et al. GVHD after haploidentical transplantation: a novel, MHC-defined rhesus macaque model identifies CD28- CD8+ T cells as a reservoir of breakthrough T-cell proliferation during costimulation blockade and sirolimus-based immunosuppression. Blood. 2010;116:5403.
4. Daikh D, Wofsy D, Imboden JB. The CD28-B7 costimulatory pathway and its role in autoimmune disease (Review). J Leukoc Biol. 1997;62:156.
5. Buch MH, Vital EM, Emery P. Abatacept in the treatment of rheumatoid arthritis (Review). Arthritis Res Ther. 2008;10(Suppl. 1):S5.
6. Turka LA, Linsley PS, Lin H, et al. T-cell activation by the CD28 ligand B7 is required for cardiac allograft rejection in vivo. Proc Natl Acad Sci U S A. 1992;89:11102.
7. Pearson TC, Alexander DZ, Winn KJ, Linsley PS, Lowry RP, Larsen CP. Transplantation tolerance induced by CTLA4-Ig. Transplantation. 1994;57:1701.
8. Kean LS, Adams AB, Strobert E, et al. Induction of chimerism in rhesus macaques through stem cell transplant and costimulation blockade-based immunosuppression. Am J Transplant. 2007;7:320.
9. Yu XZ, Bidwell SJ, Martin PJ, Anasetti C. CD28-specific antibody prevents graft-versus-host disease in mice. J Immunol. 2000;164:4564.
10. Poirier N, Blancho G, Vanhove B. CD28-specific immunomodulating antibodies: what can be learned from experimental models? Am J Transplant. 2012;12:1682.
11. Luhder F, Huang Y, Dennehy KM, et al. Topological requirements and signaling properties of T cell-activating, anti-CD28 antibody superagonists. J Exp Med. 2003;197:955.
12. Dennehy KM, Elias F, Zeder-Lutz G, et al. Cutting edge: monovalency of CD28 maintains the antigen dependence of T cell costimulatory responses. J Immunol. 2006;176:5725.
13. Dennehy KM, Elias F, Na SY, Fischer KD, Hunig T, Luhder F. Mitogenic CD28 signals require the exchange factor Vav1 to enhance TCR signaling at the SLP-76-Vav-Itk signalosome. J Immunol. 2007;178:1363.
14. Singh M, Basu S, Camell C, et al. Selective expansion of memory CD4(+) T cells by mitogenic human CD28 generates inflammatory cytokines and regulatory T cells. Eur J Immunol. 2008;38:1522.
15. Sanchez-Lockhart M, Kim M, Miller J. Cutting edge: a role for inside-out signaling in TCR regulation of CD28 ligand binding. J Immunol. 2011; 187:5515.
16. Beyersdorf N, Ding X, Blank G, Dennehy KM, Kerkau T, Hunig T. Protection from graft-versus-host disease with a novel B7 binding site-specific mouse anti-mouse CD28 monoclonal antibody. Blood. 2008; 112:4328.
17. Beyersdorf N, Hanke T, Kerkau T, Hunig T. Superagonistic anti-CD28 antibodies: potent activators of regulatory T cells for the therapy of autoimmune diseases (Review).Ann Rheum Dis. 2005;64Suppl 4:iv91–iv95.
18. Urakami H, Ostanin DV, Hunig T, Grisham MB. Combination of donor-specific blood transfusion with anti-CD28 antibody synergizes to prolong graft survival in rat liver transplantation. Transplant Proc. 2006; 38:3244.
19. Azuma H, Isaka Y, Li X, et al. Superagonistic CD28 antibody induces donor-specific tolerance in rat renal allografts. Am J Transplant. 2008; 8:2004.
20. Kitazawa Y, Fujino M, Sakai T, et al. Foxp3-expressing regulatory T cells expanded with CD28 superagonist antibody can prevent rat cardiac allograft rejection. J Heart Lung Transplant. 2008;27:362.
21. Beyersdorf N, Ding X, Hunig T, Kerkau T. Superagonistic CD28 stimulation of allogeneic T cells protects from acute graft-versus-host disease. Blood. 2009;114:4575.
22. Kitazawa Y, Fujino M, Li XK, et al. Superagonist CD28 antibody preferentially expanded Foxp3-expressing nTreg cells and prevented graft-versus-host diseases. Cell Transplant. 2009;18:627.
23. 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;355:1018.
24. Eastwood D, Findlay L, Poole S, et al. Monoclonal antibody TGN1412 trial failure explained by species differences in CD28 expression on CD4+ effector memory T-cells. Br J Pharmacol. 2010;161:512.
25. Pallardy M, Hunig T. Primate testing of TGN1412: right target, wrong cell. Br J Pharmacol. 2010;161:509.
26. Eastwood D, Bird C, Dilger P, et al. Severity of the TGN1412 trial disaster cytokine storm correlated with IL-2 release. Br J Clin Pharmacol. 2013;76:299.
27. Findlay L, Eastwood D, Stebbings R, et al. Improved in vitro methods to predict the in vivo toxicity in man of therapeutic monoclonal antibodies including TGN1412. J Immunol Methods. 2010;352:1.
28. Findlay L, Sharp G, Fox B, et al. Endothelial cells co-stimulate peripheral blood mononuclear cell responses to monoclonal antibody TGN1412 in culture. Cytokine. 2011;55:141.
29. Stebbings R, Findlay L, Edwards C, et al. “Cytokine storm” in the phase I trial of monoclonal antibody TGN1412: better understanding the causes to improve preclinical testing of immunotherapeutics. J Immunol. 2007; 179:3325.
30. Stebbings R, Eastwood D, Poole S, Thorpe R. After TGN1412: recent developments in cytokine release assays. J Immunotoxicol. 2013;10:75.
31. Mary C, Coulon F, Poirier N, et al. Antagonist properties of monoclonal antibodies targeting human CD28: role of valency and the heavy-chain constant domain. mAbs. 2013;5:47.
32. Graves SS, Stone DM, Loretz C, et al. Antagonistic and agonistic anticanine CD28 monoclonal antibodies: tools for allogeneic transplantation. Transplantation. 2011;91:833.
33. Storb R, Raff RF, Appelbaum FR, et al. FK506 and methotrexate prevent graft-versus-host disease in dogs given 9.2 Gy total body irradiation and marrow grafts from unrelated DLA-nonidentical donors. Transplantation. 1993;56:800.
34. Thomas ED. Transplantation of hematopoietic progenitor cells with emphasis on the results in children. Turkish J Pediatr. 1995;37:31.
35. Yu C, Storb R, Deeg HJ, et al. Tacrolimus (FK506) and methotrexate regimens to prevent graft-versus-host disease after unrelated dog leukocyte antigen (DLA) nonidentical marrow transplantation. Bone Marrow Transplant. 1996;17:649.
36. Wagner JL, Burnett RC, DeRose SA, Francisco LV, Storb R, Ostrander EA. Histocompatibility testing of dog families with highly polymorphic microsatellite markers. Transplantation. 1996;62:876.
37. Wagner JL, Works JD, Storb R. DLA-DRB1 and DLA-DQB1 histocompatibility typing by PCR-SSCP and sequencing (Brief Communication). Tissue Antigens. 1998;52:397.
38. Lee WS, Suzuki Y, Graves SS, et al. Canine bone marrow-derived mesenchymal stromal cells suppress alloreactive lymphocyte proliferation in vitro but fail to enhance engraftment in canine bone marrow transplantation. Biol Blood Marrow Transplant. 2011;17:465.
39. Romer PS, Berr S, Avota E, et al. Preculture of PBMCs at high cell density increases sensitivity of T-cell responses, revealing cytokine release by CD28 superagonist TGN1412. Blood. 2011;118:6772.
40. Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372:774.
41. Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28:235.
42. Stamper CC, Zhang Y, Tobin JF, et al. Crystal structure of the B7-1/ CTLA-4 complex that inhibits human immune responses [erratum appears in Nature 2001 May 31;411(6837):617]. Nature. 2001; 410:608.
43. Evans EJ, Esnouf RM, Manso-Sancho R, et al. Crystal structure of a soluble CD28-Fab complex. Nat Immunol. 2005;6:271.
44. Poirier N, Mary C, Dilek N, et al. Preclinical efficacy and immunological safety of FR104, an antagonist anti-CD28 monovalent Fab' antibody. Am J Transplant. 2012;12:2630.
45. Poirier N, Blancho G, Vanhove B. Alternatives to calcineurin inhibition in renal transplantation: belatacept, the first co-stimulation blocker (Review). Immunotherapy. 2010;2:625.
46. Lee DW, Gardner R, Porter DL, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014;124:188.
47. Kopf M, Bachmann MF, Marsland BJ. Averting inflammation by targeting the cytokine environment (Review). Nat Rev Drug Discov. 2010;9:703.