B cell repopulation after alemtuzumab induction - Transient increase in transitional B cells and long-term dominance of naïve B cells

American Journal of Transplantation

Volumn 12, Issue 7, 2012, Pages 1784-1792

  Heidt, S ^a   Hester, J ^a   Shankar, S ^a   Friend, P J ^b   Wood, Kathryn J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Campath 1H; Conversion; Depletion; Regulatory B cells; Renal transplant

Indexed keywords

ALEMTUZUMAB; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; RAPAMYCIN; TACROLIMUS;

ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE REPOPULATION; CELL POPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; GRAFT RECIPIENT; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY TRANSPLANTATION; LEUKOPENIA; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL;

ANTIBODIES, MONOCLONAL, HUMANIZED; B-LYMPHOCYTES; CELL DIVISION; FLOW CYTOMETRY; HUMANS; IMMUNOSUPPRESSIVE AGENTS; KIDNEY TRANSPLANTATION;

EID: 84863200586     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/j.1600-6143.2012.04012.x     Document Type: Article

References (40)

1. Terasaki PI, Cai J. Human leukocyte antigen antibodies and chronic rejection: From association to causation. Transplantation 2008; 86: 377-383.
2. Wood KJ, Goto R. Mechanisms of rejection: Current perspectives. Transplantation 2012; 93: 1-10.
3. Kirk AD, Turgeon NA, Iwakoshi NN. B cells and transplantation tolerance. Nat Rev Nephrol 2010; 6: 584-593.
4. Louis S, Braudeau C, Giral M, et al. Contrasting CD25hiCD4+T cells/FOXP3 patterns in chronic rejection and operational drug-free tolerance. Transplantation 2006; 81: 398-407. (Pubitemid 43255726)
5. Sagoo P, Perucha E, Sawitzki B, et al. Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest 2010; 120: 1848-1861.
6. Newell KA, Asare A, Kirk AD, et al. Identification of a B cell signature associated with renal transplant tolerance in humans. J Clin Invest 2010; 120: 1836-1847.
7. Pallier A, Hillion S, Danger R, et al. Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int 2010; 78: 503-513.
8. Heidt S, San Segundo D, Shankar S, et al. Peripheral blood sampling for the detection of allograft rejection: Biomarker identification and validation. Transplantation 2011; 92: 1-9.
9. Liu C, Noorchashm H, Sutter JA, et al. B lymphocyte-directed immunotherapy promotes long-term islet allograft survival in nonhuman primates. Nature Med 2007; 13: 1295-1298. (Pubitemid 350073600)
10. Markmann JF, Fishman JA. Alemtuzumab in kidney-transplant recipients. New Engl J Med 2011; 364: 1968-1969.
11. Knechtle SJ, Pirsch JD, H. Fechner J J, et al. Campath-1H induction plus rapamycin monotherapy for renal transplantation: Results of a pilot study. Am J Transplant 2003; 3: 722-730. (Pubitemid 36745245)
12. Noris M, Casiraghi F, Todeschini M, et al. Regulatory T cells and T cell depletion: Role of immunosuppressive drugs. J Am Soc Nephrol 2007; 18: 1007-1018. (Pubitemid 46434518)
13. Trzonkowski P, Zilvetti M, Friend P, Wood KJ. Recipient memory-like lymphocytes remain unresponsive to graft antigens after CAMPATH-1H induction with reduced maintenance immunosuppression. Transplantation 2006; 82: 1342-1351. (Pubitemid 44834311)
14. Thompson SA, Jones JL, Cox AL, Compston DA, Coles AJ. B-cell reconstitution and BAFF after alemtuzumab (Campath-1H) treatment of multiple sclerosis. J. Clin Immunol 2010; 30: 99-105.
15. Knechtle SJ, Pascual J, Bloom DD, et al. Early and limited use of tacrolimus to avoid rejection in an alemtuzumab and sirolimus regimen for kidney transplantation: Clinical results and immune monitoring. Am J Transplant 2009; 9: 1087-1098.
16. Heidt S, Roelen DL, Eijsink C, van Kooten C, Claas FH, Mulder A. Effects of immunosuppressive drugs on purified human B cells: Evidence supporting the use of MMF and rapamycin. Transplantation 2008; 86: 1292-1300.
17. Klein U, Rajewsky K, Kuppers R. Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J Exp Med 1998; 188: 1679-1689. (Pubitemid 28516113)
18. Bohnhorst JO, Bjorgan MB, Thoen JE, Natvig JB, Thompson KM. Bm1-Bm5 classification of peripheral blood B cells reveals circulating germinal center founder cells in healthy individuals and disturbance in the B cell subpopulations in patients with primary Sjogren's syndrome. J Immunol 2001; 167: 3610-3618. (Pubitemid 32916053)
19. Colonna-Romano G, Bulati M, Aquino A, et al. A double-negative (IgD-CD27-) B cell population is increased in the peripheral blood of elderly people. Mech Ageing Dev 2009; 130: 681-690.
20. Sims GP, Ettinger R, Shirota Y, Yarboro CH, Illei GG, Lipsky PE. Identification and characterization of circulating human transitional B cells. Blood 2005; 105: 4390-4398. (Pubitemid 40720786)
21. Sarantopoulos S, Stevenson KE, Kim HT, et al. Recovery of B-cell homeostasis after rituximab in chronic graft-versus-host disease. Blood 2011; 117: 2275-2283.
22. Blair PA, Norena LY, Flores-Borja F, et al. CD19(+)CD24(hi) CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010; 32: 129-140.
23. Zarkhin V, Lovelace PA, Li L, Hsieh SC, Sarwal MM. Phenotypic evaluation of B-cell subsets after rituximab for treatment of acute renal allograft rejection in pediatric recipients. Transplantation 2011; 91: 1010-1018.
24. Bloom DD, Chang Z, Fechner JH, et al. CD4+ CD25+ FOXP3+ regulatory T cells increase de novo in kidney transplant patients after immunodepletion with Campath-1H. Am J Transplant 2008; 8: 793-802. (Pubitemid 351347746)
25. Pascual J, Bloom D, Torrealba J, et al. Calcineurin inhibitor withdrawal after renal transplantation with alemtuzumab: Clinical outcomes and effect on T-regulatory cells. Am J Transplant 2008; 8: 1529-1536. (Pubitemid 351989487)
26. Trzonkowski P, Zilvetti M, Chapman S, et al. Homeostatic repopulation by CD28-CD8 +T cells in alemtuzumab-depleted kidney transplant recipients treated with reduced immunosuppression. Am J Transplant 2008; 8: 338-347.
27. Le Texier L, Thebault P, Lavault A, et al. Long-term allograft tolerance is characterized by the accumulation of B cells exhibiting an inhibited profile. Am J Transplant 2011; 11: 429-438.
28. Heidt S, Roelen DL, Eijsink C, et al. Calcineurin inhibitors affect B cell antibody responses indirectly by interfering with T cell help. Clin Exp Immunol 2010; 159: 199-207.
29. Anolik JH, Barnard J, Owen T, et al. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum 2007; 56: 3044-3056. (Pubitemid 47502752)
30. Roll P, Dorner T, Tony HP. Anti-CD20 therapy in patients with rheumatoid arthritis: Predictors of response and B cell subset regeneration after repeated treatment. Arthritis Rheum 2008; 58: 1566-1575. (Pubitemid 351847509)
31. Parsons RF, Vivek K, Rostami SY, et al. Acquisition of humoral transplantation tolerance upon de novo emergence of B lymphocytes. J Immunol 2011; 186: 614-620.
32. Calne R, Moffatt SD, Friend PJ, et al. Campath IH allows low-dose cyclosporine monotherapy in 31 cadaveric renal allograft recipients. Transplantation 1999; 68: 1613-1616.
33. Kirk AD, Hale DA, Mannon RB, et al. Results from a human renal allograft tolerance trial evaluating the humanized CD52-specific monoclonal antibody alemtuzumab (CAMPATH-1H). Transplantation 2003; 76: 120-129. (Pubitemid 36877125)
34. Watson CJ, Bradley JA, Friend PJ, et al. Alemtuzumab (CAMPATH 1H) induction therapy in cadaveric kidney transplantation - Efficacy and safety at five years. Am J Transplant 2005; 5: 1347-1353. (Pubitemid 40839424)
35. Ruggenenti P, Perico N, Gotti E, et al. Sirolimus versus cyclosporine therapy increases circulating regulatory T cells, but does not protect renal transplant patients given alemtuzumab induction from chronic allograft injury. Transplantation 2007; 84: 956-964. (Pubitemid 350287376)
36. Hester J, Mills N, Shankar S, Carvalho-Gaspar M, Friend P, Wood KJ. Th17 cells in alemtuzumab-treated patients: The effect of long-term maintenance immunosuppressive therapy. Transplantation 2011; 91: 744-750.
37. Bloom D, Chang Z, Pauly K, et al. BAFF is increased in renal transplant patients following treatment with alemtuzumab. Am J Transplant 2009; 9: 1835-1845.
38. Mackay F, Woodcock SA, Lawton P, et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J Exp Med 1999; 190: 1697-1710. (Pubitemid 30002351)
39. Thien M, Phan TG, Gardam S, et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004; 20: 785-798. (Pubitemid 38757447)
40. Cai J, Terasaki PI, Bloom DD, et al. Correlation between human leukocyte antigen antibody production and serum creatinine in patients receiving sirolimus monotherapy after Campath-1H induction. Transplantation 2004; 78: 919-924. (Pubitemid 39298538)