The state of therapy for removal of alloantibody producing plasma cells in transplantation

Seminars in Immunology

Volumn 24, Issue 2, 2012, Pages 143-147

  Everly, Matthew J ^a   Terasaki, Paul I ^b  

^a One Lambda Inc   (United States)

^b Terasaki Foundation   (United States)

Author keywords

Alloantibodies; Belimumab; Blys; Bortezomib; HLA; Plasma cell; Proteasome; Transplantation

Indexed keywords

ALLOANTIBODY; BORTEZOMIB; IMMUNOGLOBULIN; RITUXIMAB;

ACUTE GRAFT REJECTION; ANTIBODY PRODUCTION; CELL TRANSPLANTATION; DRUG EFFECT; GRAFT FAILURE; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; NONHUMAN; PLASMA CELL; PLASMAPHERESIS; REVIEW; TREATMENT OUTCOME;

ANIMALS; BORONIC ACIDS; GRAFT REJECTION; HUMANS; ISOANTIBODIES; KIDNEY TRANSPLANTATION; MICE; PLASMA CELLS; PROTEASE INHIBITORS; PYRAZINES; TREATMENT OUTCOME;

EID: 84859266862     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2011.08.014     Document Type: Review

References (88)

1. Kinukawa T., Kato M., Terasaki P.I., Ozawa M. Retrospective antibody analysis of thirty patients with kidney graft failure. Clinical Transplants 2006, 291-303.
2. Lee P.C., Terasaki P.I., Takemoto S.K., Lee P.H., Hung C.J., Chen Y.L., et al. All chronic rejection failures of kidney transplants were preceded by the development of HLA antibodies. Transplantation 2002, 74(8):1192-1194.
3. Mizutani K., Terasaki P.I., Shih R.N., Pei R., Ozawa M., Lee J. Frequency of MIC antibody in rejected renal transplant patients without HLA antibody. Human Immunology 2006, 67(3):223-229.
4. Worthington J.E., Martin S., Al-Husseini D.M., Dyer P.A., Johnson R.W. Posttransplantation production of donor HLA-specific antibodies as a predictor of renal transplant outcome. Transplantation 2003, 75(7):1034-1040.
5. Lachmann N., Terasaki P.I., Budde K., Liefeldt L., Kahl A., Reinke P., et al. Anti-human leukocyte antigen and donor-specific antibodies detected by luminex posttransplant serve as biomarkers for chronic rejection of renal allografts. Transplantation 2009, 87(10):1505-1513.
6. Lachmann N., Terasaki P.I., Schonemann C. Donor-specific HLA antibodies in chronic renal allograft rejection: a prospective trial with a four-year follow-up. Clinical Transplants 2006, 171-199.
7. Mizutani K., Shibata L., Ozawa M., Esquenazi V., Rosen A., Miller J., et al. Detection of HLA and MICA antibodies before kidney graft failure. Clinical Transplants 2006, 255-264.
8. Ozawa M., Rebellato L.M., Terasaki P.I., Tong A., Briley K.P., Catrou P., et al. Longitudinal testing of 266 renal allograft patients for HLA and MICA antibodies: Greenville experience. Clinical Transplants 2006, 265-290.
9. Ozawa M., Terasaki P.I., Castro R., Alberu J., Morales-Buenrostro L., Alvarez I., et al. 14th international HLA and Immunogenetics workshop prospective chronic rejection project: a three-year follow-up analysis. Clinical Transplants 2007, 255-260.
10. van den Berg-Loonen E.M., Terasaki P., Kohanof S., Christiaans M.H. Longitudinal testing of seventy-six renal allograft patients for HLA antibodies: Maastricht experience. Clinical Transplants 2006, 305-322.
11. Cai J., Terasaki P.I. Humoral theory of transplantation: mechanism, prevention, and treatment. Human Immunology 2005, 66(4):334-342.
12. Everly M.J., Terasaki P.I. Monitoring and treating posttransplant human leukocyte antigen antibodies. Human Immunology 2009, 70(8):655-659.
13. Terasaki P.I. Humoral theory of transplantation. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2003, 3(6):665-673.
14. Terasaki P.I., Cai J. Humoral theory of transplantation: further evidence. Current Opinion in Immunology 2005, 17(5):541-545.
15. Terasaki P.I., Cai J. Human leukocyte antigen antibodies and chronic rejection: from association to causation. Transplantation 2008, 86(3):377-383.
16. Hachem R.R., Yusen R.D., Meyers B.F., Aloush A.A., Mohanakumar T., Patterson G.A., et al. Anti-human leukocyte antigen antibodies and preemptive antibody-directed therapy after lung transplantation. The Journal of Heart and Lung Transplantation: The Official Publication of the International Society for Heart Transplantation 2010, 29(9):973-980. PMCID: 2926224.
17. Jordan S.C., Pescovitz M.D. Presensitization: the problem and its management. Clinical Journal of the American Society of Nephrology 2006, 1(3):421-432.
18. Dean P.G., Gloor J.M., Stegall M.D. Conquering absolute contraindications to transplantation: positive-crossmatch and ABO-incompatible kidney transplantation. Surgery 2005, 137(3):269-273.
19. Jordan S.C., Tyan D., Stablein D., McIntosh M., Rose S., Vo A., et al. Evaluation of intravenous immunoglobulin as an agent to lower allosensitization and improve transplantation in highly sensitized adult patients with end-stage renal disease: report of the NIH IG02 trial. Journal of the American Society of Nephrology 2004, 15(12):3256-3262.
20. Montgomery R.A., Zachary A.A., Racusen L.C., Leffell M.S., King K.E., Burdick J., et al. Plasmapheresis and intravenous immune globulin provides effective rescue therapy for refractory humoral rejection and allows kidneys to be successfully transplanted into cross-match-positive recipients. Transplantation 2000, 70(6):887-895.
21. Gloor J.M., Sethi S., Stegall M.D., Park W.D., Moore S.B., DeGoey S., et al. Transplant glomerulopathy: subclinical incidence and association with alloantibody. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2007, 7(9):2124-2132.
22. Zarkhin V., Li L., Kambham N., Sigdel T., Salvatierra O., Sarwal M.M. A randomized, prospective trial of rituximab for acute rejection in pediatric renal transplantation. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2008, 8(12):2607-2617.
23. Everly M.J., Everly J.J., Arend L.J., Brailey P., Susskind B., Govil A., et al. Reducing de novo donor-specific antibody levels during acute rejection diminishes renal allograft loss. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2009, 9(5):1063-1071.
24. Everly M.J., Rebellato L.M., Ozawa M., Briley K.P., Catrou P.G., Haisch C.E., et al. Beyond histology: lowering human leukocyte antigen antibody to improve renal allograft survival in acute rejection. Transplantation 2010, 89(8):962-967.
25. Lefaucheur C., Nochy D., Andrade J., Verine J., Gautreau C., Charron D., et al. Comparison of combination Plasmapheresis/IVIg/anti-CD20 versus high-dose IVIg in the treatment of antibody-mediated rejection. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2009, 9(5):1099-1107.
26. Everly M.J., Everly J.J., Susskind B., Brailey P., Arend L.J., Alloway R.R., et al. Bortezomib provides effective therapy for antibody- and cell-mediated acute rejection. Transplantation 2008, 86(12):1754-1761.
27. Zarkhin V., Kambham N., Li L., Kwok S., Hsieh S.C., Salvatierra O., et al. Characterization of intra-graft B cells during renal allograft rejection. Kidney International 2008, 74(5):664-673.
28. Radbruch A., Muehlinghaus G., Luger E.O., Inamine A., Smith K.G., Dorner T., et al. Competence and competition: the challenge of becoming a long-lived plasma cell. Nature Reviews Immunology 2006, 6(10):741-750.
29. Perry D.K., Burns J.M., Pollinger H.S., Amiot B.P., Gloor J.M., Gores G.J., et al. Proteasome inhibition causes apoptosis of normal human plasma cells preventing alloantibody production. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2009, 9(1):201-209.
30. Blink E.J., Light A., Kallies A., Nutt S.L., Hodgkin P.D., Tarlinton D.M. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. The Journal of Experimental Medicine 2005, 201(4):545-554.
31. Odendahl M., Mei H., Hoyer B.F., Jacobi A.M., Hansen A., Muehlinghaus G., et al. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 2005, 105(4):1614-1621.
32. Meister S., Schubert U., Neubert K., Herrmann K., Burger R., Gramatzki M., et al. Extensive immunoglobulin production sensitizes myeloma cells for proteasome inhibition. Cancer Research 2007, 67(4):1783-1792.
33. Gass J.N., Gunn K.E., Sriburi R., Brewer J.W., Stressed-out B cells? Plasma-cell differentiation and the unfolded protein response. Trends in Immunology 2004, 25(1):17-24.
34. Kim R., Emi M., Tanabe K., Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006, 11(1):5-13.
35. Everly M.J., Terasaki P.I., Hopfield J., Trivedi H.L., Kaneku H. Protective immunity remains intact after antibody removal by means of proteasome inhibition. Transplantation 2010, 90(12):1493-1498.
36. Luo H., Wu Y., Qi S., Wan X., Chen H., Wu J. A proteasome inhibitor effectively prevents mouse heart allograft rejection. Transplantation 2001, 72(2):196-202.
37. Wu Y., Han B., Luo H., Shi G., Wu J. Dipeptide boronic acid, a novel proteasome inhibitor, prevents islet-allograft rejection. Transplantation 2004, 78(3):360-366.
38. Wu J. On the role of proteasomes in cell biology and proteasome inhibition as a novel frontier in the development of immunosuppressants. American Journal of Transplantation: Official Journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2002, 2(10):904-912.
39. Everly M.J., Everly J.J., Susskind B., Brailey P., Arend L.J., Alloway R.R., et al. Proteasome inhibition reduces donor-specific antibody levels. Transplantation Proceedings 2009, 41(1):105-107.
40. Trivedi H.L., Terasaki P.I., Feroz A., Everly M.J., Vanikar A.V., Shankar V., et al. Abrogation of anti-HLA antibodies via proteasome inhibition. Transplantation 2009, 87(10):1555-1561.
41. Everly M.J., Terasaki P.I., Trivedi H.L., Kaneku H., Idica A. DSA monitoring may improve donor specific HLA-antibody relapse and refratoriness following proteasome inhibition. American Journal of Transplantion 2010, 10(Suppl. 4):467.
42. Neumann J., Tarrasconi H., Bortolotto A., Machuca T., Canabarro R., Sporleder H., et al. Acute humoral rejection in a lung recipient: reversion with bortezomib. Transplantation 2010, 89(1):125-126.
43. Neumann J., Schio S., Tarrasconi H., Bortolotto A., Costa C., Machuca T., et al. Bortezomib in lung transplantation: a promising start. Clinical Transplants 2009, 421-424.
44. Al Meshari K. Bortezomib for the treatment of de novo HLA antibody-related antibody mediated rejection. Clinical Transplants 2009, 385-386.
45. Boothpur R., Torrence S., Brennan D.C. Bortezomib does not reduce ABO-isoagglutinin titers and may not be useful for ABO-incompatible transplant desensitization. Clinical Transplants 2009, 491-493.
46. Cooper J.E., Wiseman A.C., Chan L. Bortezomib use in chronic antibody-mediated allograft dysfunction: a report of three cases. Clinical Transplants 2009, 455-459.
47. Djamali A., Muth B.L., Torrealba J., Bloom D., Miller K.M., Lorentzen D., et al. Bortezomib as a rescue therapy for hyperacute and multi-drug resistant mixed acute rejection after kidney transplantation. Clinical Transplants 2009, 485-490.
48. Eckman P.M., Thorsgard M., Maurer D., Kim Y., Alloway R.R., Woodle E.S. Bortezomib for refractory antibody-mediated cardiac allograft rejection. Clinical Transplants 2009, 475-478.
49. Govil A., Walsh R.C., Tevar A., Alloway R., Roy-Chaudhury P., Mogilishetty G., et al. Bortezomib-based treatment of antibody mediated rejection in pancreas allograft recipients. Clinical Transplants 2009, 443-453.
50. Hamawi K., Heilman R.L., Mazur M.J., Chakkera H.A., Mulligan D.C., Moss A.A., et al. Use of bortezomib for treatment of antibody medicated rejection in kidney transplant recipients-case report. Clinical Transplants 2009, 407-414.
51. Hardinger K.L., Alford K., Murillo D. Bortezomib for acute humoral rejection in two repeat transplant recipients. Clinical Transplants 2009, 479-483.
52. Hartono C., Lubetzky M., Aull M.J., Saal S., Figueiro J., Kapur S., et al. Use of bortezomib for prevention and treatment of rejection in sensitized patients. Clinical Transplants 2009, 499-503.
53. Heidt S., Roelen D.L., Vergunst M., Doxiadis I.I., Claas F.H., Mulder A. Bortezomib affects the function of human B cells: possible implications for desensitization protocols. Clinical Transplants 2009, 387-392.
54. Island E.R., Gonzalez-Pinto I.M., Tsai H.L., Ruiz P., Tryphonopoulos P., Gonzalez M.L., et al. Successful treatment with bortezomib of a refractory humoral rejection of the intestine after multivisceral transplantation. Clinical Transplants 2009, 465-469.
55. Kumar V., Elkins S., Gaston R.S., Prendergast M.B., Reddy V., Cook W.J., et al. Bortezomib successfully reduces monoclonal serum free light chain levels in a patient with recurrent myeloma and cast nephropathy in the renal transplant. Clinical Transplants 2009, 439-441.
56. Lachmann N., Schutz M., Budde K., Schonemann C., Waiser J. Antihumoral rejection therapy by proteasome inhibitor bortezomib: a case series. Clinical Transplants 2009, 351-358.
57. Lee I., Constantinescu S., Gillespie A., Swami A., Birkenbach M., Leech S., et al. Bortezomib as therapy for mixed humoral and cellular rejection: should it be first line?. Clinical Transplants 2009, 425-429.
58. Leyva S., Marino-Vazquez L.A., Reyes-Loaeza J.A., Vega O., Uribe-Uribe N., Alberu J., et al. Bortezomib for antibody mediated rejection treatment: experience at the Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran in Mexico City. Clinical Transplants 2009, 369-376.
59. Mai H.L., Cesbron A., Brouard S., Blanchol G., Cantarovich D., Dantal J., et al. Bortezomib in the treatment of antibody-mediated rejection-a report of 3 cases. Clinical Transplants 2009, 361-368.
60. Patel J.K., Everly M.J., Kittleson M., Kobashigawa J.A. Use of bortezomib as adjunctive therapy for densensitization in combined heart and kidney transplantation-a case report. Clinical Transplants 2009, 347-349.
61. Pavlakis M. Case presentations on two patients who received bortezomib for antibody mediated rejection at BIDMC. Clinical Transplants 2009, 343-345.
62. Raghavan R., Jeroudi A., Achkar K., Suki W., Gaber A.O., Knight R., et al. Bortezomib in kidney transplant desensitization: a case report. Clinical Transplants 2009, 339-342.
63. Sberro-Soussan R., Zuber J., Suberbielle-Boissel C., Legendre C. Bortezomib alone fails to decrease donor specific anti-HLA antibodies: 4 case reports. Clinical Transplants 2009, 433-438.
64. Shapiro R., Basu A., Zeevi A., Lunz J., Mapara M., Randhawa P., et al. Bortezomib rescue in refractory acute humoral rejection-report of a case. Clinical Transplants 2009, 431-432.
65. Stuckey L.J., Kamoun M., Wadhwa A., Samaniego M., Bartos C., Berry J., et al. Acute rejection in a highly sensitized lung transplant recipient with pre-formed donor-directed anti-HLA class II antibodies: role of bortezomib therapy. Clinical Transplants 2009, 471-474.
66. Wahrmann M., Haidinger M., Drach J., Geyeregger R., Kikic Z., Raab R., et al. Proteasome inhibition for recipient desensitization? A report of two sensitized kidney transplant candidates subjected to bortezomib treatment. Clinical Transplants 2009, 415-420.
67. Weston M., Rolfe M., Haddad T., Lopez-Cepero M. Desensitization protocol using bortezomib for highly sensitized patients awaiting heart or lung transplants. Clinical Transplants 2009, 393-399.
68. Wong W., Lee R.A., Saidman S.L., Smith R.N., Zorn E. Bortezomib in kidney transplant recipients with antibody mediated rejection: three case reports. Clinical Transplants 2009, 401-405.
69. Zhu L., Lin Z., Xiang Y., Liu S., Chen G. Successful desensitization in a crossmatch positive living-related kidney transplant recipient using a bortezomib-based protocol. Clinical Transplants 2009, 359-360.
70. Everly M.J. A summary of bortezomib use in transplantation across 29 centers. Clinical Transplants 2009, 323-337.
71. Marino-Vazquez L.A., Leyva S., Alberu J., Morales-Buenrostro L. Bortezomib for desensitization of patients on a waiting list for deseased donor kideny transplant: experience in Mexico City. Clinical Transplants 2010, 363-367.
72. Leyva S., Marino-Vazquez L.A., Alberu J., Morales-Buenrostro L. Bortezomib for acute humoral rejection treatment at the Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran in Mexico City: an update. Clinical Transplants 2010, 369-382.
73. Al Meshari K., Elgamal H., Alzayer F., Altalhi M. Bortezomib as adjuvant to conventional therapy in the treatment of antibody mediated rejection (AMR): the full spectrum. Clinical Transplants 2010, 383-390.
74. Schwaiger E., Regele H., Wahrmann M., Werzowa J., Haidbauer B., Schmidt A., et al. Bortezomib for the treatment of chronic antibody-mediated kidney allograft rejection: a case report. Clinical Transplants 2010, 391-396.
75. Lee I., Constantinescu S., Gillespie A., Rao S., Silva P., Birkenbach M., et al. Targeting alloantibody production with bortezomib: does it make more sense?. Clinical Transplants 2010, 397-403.
76. Shapiro R., Lunz J., Zeevi A., Basu A., Mapara M., Randhawa P., et al. 1.7 year follow-up after bortezomib therapy for refractory antibody mediated rejection. Clinical Transplants 2010, 405-407.
77. Sberro-Soussan R., Zuber J., Suberbielle-Boissel C., Legendre C. Bortezomib alone fails to decrease donor specific anti-HLA antibodies: even after one year post-treatment. Clinical Transplants 2010, 409-414.
78. Cooper J.E., Wiseman A.C., Chan L. Bortezomib use in chronic antibody-mediated allograft dysfunction: updates and additional cases. Clinical Transplants 2010, 415-420.
79. Manitpisitkul W., Wilson N.S., Philosophe B., Cooper M., Drachenberg C., KuKuruga D., et al. Rescue therapy for acute antibody mediated rejection with proteasome inhibitor after kidney transplantation. Clinical Transplants 2010, 421-428.
80. Hardinger K.L., Alford K., Murillo D. Bortezomib as a rescue therapy for antibody mediated rejection: a single-center experience. Clinical Transplants 2010, 429-436.
81. Lubetzky M., Aull M.J., Walker J., Leeser D., Kapur S., Hartono C., et al. Reduction in proteinuria with bortezomib based therapy for antibody mediated rejection. Clinical Transplants 2010, 437-440.
82. Everly M.J. An update on antibody reduction and rejection reversal following bortezomib use: a report of 52 cases across 10 centers. Clinical Transplants 2010, 353-362.
83. Schmidt N., Alloway R., Sadaka B., Wall G., Shields A.R., Woodle E. Intermediate-term global toxicity analysis of proteasome inhibitor-based antihumoral therapy. American Journal of Transplantation 2011, 11(S2):192.
84. Raghavaiah S.R., Daiwan T.S., Burns J.M., Gloor J.M., Gandhi M.J., Winters J.L., et al. Depletion of alloantibody-secreting plasma cells by proteasome inhibition improves desensitization. American Journal of Transplantation 2010, 10(Suppl. 4):44.
85. Walsh R.C., Rike Shields A., Wall G.E., Brailey P., Girnita A., Cardi M., et al. A prospective, staged trial of proteasome inhibitor-based therapy for reduction of HLA sensitization in kidney transplant candidates. American Journal of Transplantation 2010, 10(Suppl. 4):44.
86. Kuhn D.J., Chen Q., Voorhees P.M., Strader J.S., Shenk K.D., Sun C.M., et al. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 2007, 110(9):3281-3290. PMCID: 2200918.
87. Siegel D.S.D., Martin T., Wang M., Vij R., Jakubowiak A.J., Jagannath S., et al. Results of PX 171 003 A1, an open label, single arm phase 2 (Ph 2) study of carfilzomib (CFZ) in patients (pts) with relapsed and refractory multiple myeloma (MM). Blood 2010, 116(21):433.
88. Navarra S.V., Guzman R.M., Gallacher A.E., Hall S., Levy R.A., Jimenez R.E., et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011, 377(9767):721-731.