Minimal effect of bortezomib in reducing anti-pig antibodies in human leukocyte antigen-sensitized patients: A pilot study

Xenotransplantation

Volumn 20, Issue 6, 2013, Pages 429-437

  Hara, Hidetaka ^a   Bentall, Andrew ^b,d   Long, Cassandra ^a   Fang, Jason ^a   Andreyev, Oleg ^a   Lunz, John ^a   Ezzelarab, Mohamed ^a   Abu Elmagd, Kareem M ^a,e   Shapiro, Ron ^a   Ayares, David ^c   Stegall, Mark ^b   Cooper, David K C ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b MAYO CLINIC   (United States)

^c REVIVICOR INC   (United States)

^d QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^e Transplant Center   (United States)

Author keywords

antibodies, anti Gal; antibodies, anti nonGal; antibodies, anti pig; bortezomib

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; BORTEZOMIB; CD20 ANTIBODY; HLA ANTIGEN; IMMUNOGLOBULIN M ANTIBODY; METHYLPREDNISOLONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; THYMOCYTE ANTIBODY;

ADOLESCENT; ADULT; ALLOTRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY MEDIATED REJECTION; ANTIBODY PRODUCTION; AORTIC ENDOTHELIAL CELL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; HLA SYSTEM; HUMAN; HUMAN CELL; KNOCKOUT GENE; MALE; MULTIPLE MYELOMA; NONHUMAN; ORGAN TRANSPLANTATION; PILOT STUDY; PLASMAPHERESIS; PRIORITY JOURNAL; SWINE; WILD TYPE;

ANTIBODIES, ANTI-GAL; ANTIBODIES, ANTI-NONGAL; ANTIBODIES, ANTI-PIG; BORTEZOMIB;

ADULT; ALLOGRAFTS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIBODIES, HETEROPHILE; BORONIC ACIDS; FEMALE; GALACTOSYLTRANSFERASES; GENE KNOCKOUT TECHNIQUES; HETEROGRAFTS; HLA ANTIGENS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOSUPPRESSIVE AGENTS; MALE; MIDDLE AGED; PILOT PROJECTS; PROTEASOME INHIBITORS; PYRAZINES; SUS SCROFA; YOUNG ADULT;

EID: 84889590218     PISSN: 0908665X     EISSN: 13993089     Source Type: Journal    
DOI: 10.1111/xen.12052     Document Type: Article

References (67)

1. Boothpur R, Torrence S, Brennan DC,. Bortezomib does not reduce ABO-isoagglutinin titers and may not be useful for ABO-incompatible transplant desensitization. Clin Transpl 2009; 23: 491-493.
2. Scott E, Reece D,. What is the benefit of maintenance therapy with lenalidomide or bortezomib after autologous stem cell transplantation in multiple myeloma and what is the risk of developing a secondary primary malignancy? Hematology Am Soc Hematol Educ Program 2011; 2011: 205-207.
3. Neben K, Lokhorst HM, Jauch A, et al. Administration of bortezomib before and after autologous stem cell transplantation improves outcome in multiple myeloma patients with deletion 17p. Blood 2012; 119: 940-948.
4. Anderson KC,. The 39th David A Karnofsky lecture: bench-to-bedside translation of targeted therapies in multiple myeloma. J Clin Oncol 2012; 30: 445-452.
5. Everly MJ, Walsh RC, Alloway RR, Woodle ES,. Proteasome inhibition for antibody-mediated rejection. Curr Opin Organ Transplant 2009; 14: 662-666.
6. Mujtaba T, Dou QP,. Advances in the understanding of mechanisms and therapeutic use of bortezomib. Discov Med 2011; 12: 471-480.
7. Hutter G, Rieken M, Pastore A, et al. The proteasome inhibitor bortezomib targets cell cycle and apoptosis and acts synergistically in a sequence-dependent way with chemotherapeutic agents in mantle cell lymphoma. Ann Hematol 2012; 91: 847-856.
8. Besse B, Planchard D, Veillard AS, et al. Phase 2 study of frontline bortezomib in patients with advanced non-small cell lung cancer. Lung Cancer 2012; 76: 78-83.
9. Everly MJ, Everly MJ, Susskind B, et al. Bortezomib provides effective therapy for antibody- and cell-mediated acute rejection. Transplantation 2008; 86: 1754-1761.
10. Everly MJ,. A summary of bortezomib use in transplantation across 29 centers. Clin Transpl 2009; 23: 323-337.
11. Everly MJ, Terasaki PI, Hopfield J, et al. Protective immunity remains intact after antibody removal by means of proteasome inhibition. Transplantation 2010; 90: 1493-1498.
12. Everly MJ, Terasaki PI,. The state of therapy for removal of alloantibody producing plasma cells in transplantation. Semin Immunol 2012; 24: 143-147.
13. Idica A, Kaneku H, Everly MJ, et al. Elimination of post-transplant donor-specific HLA antibodies with bortezomib. Clin Transpl 2008; 22: 229-239.
14. Island ER, Gonzalez-Pinto IM, Tsai HL, et al. Successful treatment with bortezomib of a refractory humoral rejection of the intestine after multivisceral transplantation. Clin Transpl 2009; 23: 465-469.
15. Lonze BE, Dagher NN, Simpkins CE, et al. The fate of anti-HLA antibody among renal transplantation recipients treated with bortezomib. Clin Transpl 2009; 23: 377-384.
16. Perry DK, Burns JM, Pollinger HS, et al. Proteasome inhibition causes apoptosis of normal human plasma cells preventing alloantibody production. Am J Transplant 2009; 9: 201-209.
17. Wahrmann M, Haidinger M, Drach J, et al. Proteasome inhibition for recipient desensitization? A report of two sensitized kidney transplant candidates subjected to bortezomib treatment. Clin Transpl 2009; 23: 415-420.
18. Wahrmann M, Haidinger M, Körmöczi GF, et al. Effect of the proteasome inhibitor bortezomib on humoral immunity in two presensitized renal transplant candidates. Transplantation 2010; 89: 1385-1390.
19. Flechner SM, Fatica R, Askar M, et al. The role of proteasome inhibition with bortezomib in the treatment of antibody-mediated rejection after kidney-only or kidney-combined organ transplantation. Transplantation 2010; 90: 1486-1492.
20. Shapiro R, Lunz J, Zeevi A, et al. 1.7 year follow-up after bortezomib therapy for refractory antibody mediated rejection. Clin Transpl 2010; 24: 405-407.
21. Trivedi HL, Terasaki PI, Feroz A, et al. Abrogation of anti-HLA antibodies via proteasome. Transplantation 2009; 87: 1555-1561.
22. Trivedi HL, Terasaki PI, Feroz A, et al. Clonal deletion with bortezomib followed by low or no maintenance immunosuppression in renal allograft recipients. Transplantation 2010; 90: 221-222.
23. Trivedi HL, Vanikar AV, Gumber MR, et al. Abrogation of antibodies improves outcome of renal transplantation. Transplant Proc 2012; 44: 241-247.
24. Sberro-Soussan R, Zuber J, Suberbielle-Boissel C, et al. Bortezomib as the sole post-renal transplantation desensitization agent does not decrease donor-specific anti-HLA antibodies. Am J Transplant 2010; 10: 681-686.
25. Sberro-Soussan R, Zuberl J, Suberbielle-Boissel C, Legendre C,. Bortezomib alone fails to decrease donor specific anti-HLA antibodies: even after one year post-treatment. Clin Transpl 2010; 24: 409-414.
26. Diwan TS, Raghavaiah S, Burns JM, et al. The impact of proteasome inhibition on alloantibody-producing plasma cells in vivo. Transplantation 2011; 91: 536-541.
27. Kute VB, Vanikar AV, Trivedi HL, et al. Desensitization protocol for highly sensitized renal transplant patients: a single-center experience. Saudi J Kidney Dis Transpl 2011; 22: 662-669.
28. Mohamed MA, Lorentzen D, Kim J, Djamali A,. Desensitization across the HLA barrier in kidney transplantation. Front Biosci (Schol Ed) 2011; 3: 929-936.
29. Sadaka B, Alloway RR, Woodle ES,. Clinical and investigational use of proteasome inhibitors for transplant rejection. Expert Opin Investig Drugs 2011; 20: 1535-1542.
30. Walsh RC, Everly MJ, Brailey P, et al. Proteasome inhibitor-based primary therapy for antibody-mediated renal allograft rejection. Transplantation 2010; 89: 277-284.
31. Walsh RC, Alloway RR, Girnita AL, Woodle ES,. Proteasome inhibitor-based therapy for antibody-mediated rejection. Kidney Int 2012; 81: 1067-1074.
32. Woodle ES, Alloway RR, Girnita A,. Proteasome inhibitor treatment of antibody-mediated allograft rejection. Curr Opin Organ Transplant 2011; 16: 434-438.
33. Woodle ES, Walsh RC, Alloway RR, Girnita A, Brailey P,. Proteasome inhibitor therapy for antibody-mediated rejection. Pediatr Transplant 2011; 15: 548-556.
34. Guthoff M, Schmid-Horch B, Weisel KC, et al. Proteasome inhibition by bortezomib: effect on HLA-antibody levels and specificity in sensitized patients awaiting renal allograft transplantation. Transpl Immunol 2012; 26: 171-175.
35. Morrow WR, Frazier EA, Mahle WT,. Rapid reduction in donor-specific anti-human leukocyte antigen antibodies and reversal of antibody-mediated rejection with bortezomib in pediatric heart transplant patients. Transplantation 2012; 93: 319-324.
36. Waiser J, Budde K, Schütz M, et al. Comparison between bortezomib and rituximab in the treatment of antibody-mediated renal allograft rejection. Nephrol Dial Transplant 2012; 27: 1246-1251.
37. Schmidt N, Alloway RR, Walsh RC, et al. Prospective evaluation of the toxicity profile of proteasome inhibitor-based therapy in renal transplant candidates and recipients. Transplantation 2012; 94: 352-361.
38. Paterno F, Shiller M, Tillery G, et al. Bortezomib for acute antibody-mediated rejection in liver transplantation. Am J Transplant 2012; 12: 2526-2531.
39. Ezzelarab M, Hara H, Busch J, et al. Antibodies directed to pig non-Gal antigens in naïve and sensitized baboons. Xenotransplantation 2006; 13: 400-407. (Pubitemid 44265708)
40. Hara H, Ezzelarab M, Rood PPM, et al. Allosensitized humans are at no greater risk of humoral rejection of GT-KO pig organs than other humans. Xenotransplantation 2006; 13: 357-365. (Pubitemid 43882179)
41. Rood PPM, Hara H, Busch JL, et al. Incidence and cytotoxicity of antibodies in cynomolgus monkeys directed to nonGal antigens, and their relevance for experimental models. Transpl Int 2006; 19: 158-165.
42. Baumann BC, Stussi G, Huggel K, Rieben R, Seebach JD,. Reactivity of human natural antibodies to endothelial cells from Galalpha (1,3) Gal-deficient pigs. Transplantation 2007; 83: 193-201. (Pubitemid 46185210)
43. Yeh P, Ezzelarab M, Bovin N, et al. Investigation of potential carbohydrate antigen targets for human and baboon antibodies. Xenotransplantation 2010; 17: 197-206.
44. Ezzelarab M, Garcia B, Azimzadeh A, et al. The innate immune response and activation of coagulation in α1,3-galactosyltransferase gene-knockout xenograft recipients. Transplantation 2009; 87: 805-812.
45. Azimzadeh A, Kelishadi S, Ezzelarab M, et al. Early graft failure of GTKO pig organs in baboons is reduced by HCPRP expression (Abstract 499). Am J Transplant 2010; 10: S4.
46. Azimzadeh A, Kelishadi S, Stoddard T, et al. Role of complement regulatory protein expression and CD154 blockade in Gal-independent xenograft rejection (Abstract). Xenotransplantation 2010; 17: 117.
47. McGregor CG, Ricci D, Miyagi N, et al. Human CD55 expression blocks hyperacute rejection and restricts complement activation in gal knockout cardiac xenografts. Transplantation 2012; 93: 686-692.
48. Kozlowski T, Shimizu A, Lambrigts D, et al. Porcine kidney and heart transplantation in baboons undergoing a tolerance induction regimen and antibody adsorption. Transplantation 1999; 67: 18-30. (Pubitemid 29061132)
49. Buhler L, Basker M, Alwayn IPJ, et al. Coagulation and thrombotic disorders associated with pig organ and hematopoietic cell transplantation in nonhuman primates. Transplantation 2000; 70: 1323-1331.
50. Gollackner B, Goh S-K, Qawi I, et al. Acute vascular rejection of xenografts: roles of natural and elicited xenoreactive antibodies in activation of vascular endothelial cells and induction of procoagulant activity. Transplantation 2004; 77: 1735-1741. (Pubitemid 38780542)
51. Houser SL, Kuwaki K, Knosalla C, et al. Thrombotic microangiopathy and graft arteriopathy in pig hearts following transplantation into baboons. Xenotransplantation 2004; 11: 416-425. (Pubitemid 39128211)
52. Kuwaki K, Tseng Y-L, Dor FJMF, et al. Heart transplantation in baboons using α1,3-galactosyltransferase gene-knockout pigs as donors: initial experience. Nat Med 2005; 11: 29-31. (Pubitemid 40215833)
53. Shimizu A, Hisashi Y, Kuwaki K, et al. Thrombotic microangiopathy associated with humoral rejection of cardiac xenografts from α1,3-galactosyltransferase gene-knockout pigs in baboons. Am J Pathol 2008; 172: 1471-1481. (Pubitemid 351793341)
54. Cowan PJ,. Coagulation and the xenograft endothelium. Xenotransplantation 2007; 14: 7-12. (Pubitemid 46051366)
55. Cowan PJ, Roussell JC, d'Apice AJF,. The vascular and coagulation issues in enotransplantation. Curr Opin Organ Transplant 2009; 14: 161-167.
56. Lambrigts D, Van Calster P, Xu Y, et al. Pharmacologic immunosuppressive therapy and extracorporeal immunoadsorption in the suppression of anti-αGal antibody in the baboon. Xenotransplantation 1998; 5: 274-283. (Pubitemid 29015968)
57. Alwayn IPJ, Xu Y, Basker M, et al. Effects of specific anti-B and/or anti-plasma cell immunotherapy on antibody production in baboons: depletion of CD20- and CD22-positive B cells does not result in significantly decreased production of anti-αGal antibody. Xenotransplantation 2001; 8: 157-171. (Pubitemid 32655981)
58. Teranishi K, Treter S, Alwayn IPJ, et al. Assessment of methotrexate as a potential immunosuppressive agent in baboons. J Heart Lung Transplant 2001; 20: 1335-1339. (Pubitemid 34017321)
59. Gollackner B, Ryan D, Knosalla C, et al. An exploratory investigation of the effect of arsenic trioxide on anti-Gal antibody production in baboons. Xenotransplantation 2003; 10: 80-87. (Pubitemid 36908961)
60. Yamamoto S, Cooper DKC,. An investigation of the effect of thalidomide on anti-Gal antibody production in baboons. Xenotransplantation 2003; 10: 470-474. (Pubitemid 37129892)
61. Harper D, Gollackner B, Xu Y, et al. In vitro and in vivo investigation of a novel monoclonal antibody to plasma cells (w5 mAb). Xenotransplantation 2004; 11: 78-90. (Pubitemid 38160269)
62. Kujundzic M, Koren E, Neethling FA, et al. Variability of anti-αGal antibodies in human serum and their relation to serum cytotoxicity against pig cells. Xenotransplantation 1994; 1: 58-65. (Pubitemid 2132342)
63. Buhler L, Pidwell D, Dowling RD, et al. Different responses of human anti-HLA and anti-αGal antibody to long-term intravenous immunoglobulin therapy. Xenotransplantation 1999; 6: 181-186. (Pubitemid 29439063)
64. Galili U, Mandrell RE, Hamadeh RM, Shohet SB, Griffiss JM,. Interaction between human natural anti-alpha-galactosyl immunoglobulin G and bacteria of the human flora. Infect Immun 1988; 56: 1730-1737.
65. Ohdan H, Yang YG, Swenson KG, Thall AD, Sykes M,. In vivo T-cell depletion enhances production of anti-GALalpha1,3GAL natural antibodies in alpha1,3-galactosyltransferase-deficient mice. Transplantation 2000; 69: 910-913. (Pubitemid 30174120)
66. Cretin N, Bracy J, Hanson K, Iacomini J,. The role of T cell help in the production of antibodies specific for Gal alpha 1-3Gal. J Immunol 2002; 168: 1479-1483. (Pubitemid 34094522)
67. Dons EM, Montoya C, Hara H, et al. T cell-based immunosuppressive therapy inhibits the development of natural anti-AB blood type and anti-pig antibodies in infant baboons. Transplantation 2012; 93: 769-776.