CD24hiCD27+ and plasmablast-like regulatory B cells in human chronic graft-versus-host disease

Blood

Volumn 125, Issue 11, 2015, Pages 1830-1839

  De Masson, Adèle ^a,b,c   Bouaziz, Jean David ^a,b,c   Le Buanec, Hélène ^a,b   Robin, Marie ^c   O'Meara, Alix ^c   Parquet, Nathalie ^c   Rybojad, Michel ^c   Hau, Estelle ^a,b   Monfort, Jean Benoît ^a,b   Branchtein, Mylène ^a,b   Michonneau, David ^c   Dessirier, Valérie ^a,b   De Fontbrune, Flore Sicre ^c   Bergeron, Anne ^c   Itzykson, Raphaël ^c   Dhédin, Nathalie ^c   Bengoufa, Djaouida ^c   De Latour, Régis Peffault ^a,b,c   Xhaard, Aliénor ^c   Bagot, Martine ^a,b,c   Bensussan, Armand ^a,b   Socié, Gérard ^a,b,c   more..

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SAINT LOUIS HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; CORTICOSTEROID; CYCLOSPORIN; EVEROLIMUS; IMATINIB; INTERLEUKIN 10; METHOTREXATE; MITOGEN ACTIVATED PROTEIN KINASE; MYCOPHENOLATE MOFETIL; PREDNISONE; RAPAMYCIN; STAT3 PROTEIN; TACROLIMUS; CD24 PROTEIN, HUMAN; CD38 PROTEIN, HUMAN; IL10 PROTEIN, HUMAN; MEMBRANE PROTEIN; STAT3 PROTEIN, HUMAN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ADULT; AGED; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CHRONIC GRAFT VERSUS HOST DISEASE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; CORTICOSTEROID THERAPY; CYTOKINE PRODUCTION; DISEASE SEVERITY; FEMALE; GRAFT RECIPIENT; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; MYELOPROLIFERATIVE DISORDER; NONHODGKIN LYMPHOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMABLAST; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; CHRONIC DISEASE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; METABOLISM; MOUSE; PATHOLOGY; PLASMA CELL; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADULT; AGED; ANIMALS; ANTIGENS, CD24; ANTIGENS, CD27; ANTIGENS, CD38; B-LYMPHOCYTES, REGULATORY; CELL DIFFERENTIATION; CHRONIC DISEASE; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTERLEUKIN-10; MALE; MAP KINASE SIGNALING SYSTEM; MEMBRANE GLYCOPROTEINS; MICE; MIDDLE AGED; PLASMA CELLS; PROSPECTIVE STUDIES; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; YOUNG ADULT;

EID: 84928536031     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-09-599159     Document Type: Article

References (61)

1. Socié G, Ritz J. Current issues in chronic graft-versus-host disease. Blood. 2014;124(3):374-384.
2. Di Ianni M, Falzetti F, Carotti A, et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood. 2011;117(14):3921-3928.
3. Brunstein CG, Miller JS, Cao Q, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood. 2011;117(3): 1061-1070.
4. Koreth J, Matsuoka K, Kim HT, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med. 2011;365(22):2055-2066.
5. Matsuoka K, Koreth J, Kim HT, Bascug G, McDonough S, Kawano Y, et al. Low-dose interleukin-2 therapy restores regulatory T cell homeostasis in patients with chronic graft-versus-host disease. Sci Transl Med. 2013;5(179): 179ra43.
6. Bouaziz J-D, Calbo S, Maho-Vaillant M, et al. IL-10 produced by activated human B cells regulates CD4(+) T-cell activation in vitro. Eur J Immunol. 2010;40(10):2686-2691.
7. Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530-541.
8. Socié G. Chronic GVHD: B cells come of age. Blood. 2011;117(7):2086-2087.
9. Shimabukuro-Vornhagen A, Hallek MJ, Storb RF, von Bergwelt-Baildon MS. The role of B cells in the pathogenesis of graft-versus-host disease. Blood. 2009;114(24):4919-4927.
10. Allen JL, Tata PV, Fore MS, et al. Increased BCR responsiveness in B cells from patients with chronic GVHD. Blood. 2014;123(13):2108-2115.
11. Sarantopoulos S, Stevenson KE, Kim HT, et al. Altered B-cell homeostasis and excess BAFF in human chronic graft-versus-host disease. Blood. 2009;113(16):3865-3874.
12. Sarantopoulos S, Stevenson KE, Kim HT, et al. Recovery of B-cell homeostasis after rituximab in chronic graft-versus-host disease. Blood. 2011; 117(7):2275-2283.
13. Allen JL, Fore MS, Wooten J, et al. B cells from patients with chronic GVHD are activated and primed for survival via BAFF-mediated pathways. Blood. 2012;120(12):2529-2536.
14. Jacobson CA, Sun L, Kim HT, et al. Post-transplantation B cell activating factor and B cell recovery before onset of chronic graft-versus-host disease. Biol Blood Marrow Transplant. 2014; 20(5):668-675.
15. Sarantopoulos S, Stevenson KE, Kim HT, et al. High levels of B-cell activating factor in patients with active chronic graft-versus-host disease. Clin Cancer Res. 2007;13(20):6107-6114.
16. Kuzmina Z, Krenn K, Petkov V, et al. CD19(+)CD21(low) B cells and patients at risk for NIH-defined chronic graft-versus-host disease with bronchiolitis obliterans syndrome. Blood. 2013;121(10):1886-1895.
17. Moins-Teisserenc H, Busson M, Herda A, et al. CD19+CD5+ B cells and B1-like cells following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2013;19(6):988-991.
18. Kuzmina Z, Greinix HT, Weigl R, et al. Significant differences in B-cell subpopulations characterize patients with chronic graft-versus-host disease-associated dysgammaglobulinemia. Blood. 2011; 117(7):2265-2274.
19. Cutler C, Kim HT, Bindra B, et al. Rituximab prophylaxis prevents corticosteroid-requiring chronic GVHD after allogeneic peripheral blood stem cell transplantation: results of a phase 2 trial. Blood. 2013;122(8):1510-1517.
20. Kapur R, Ebeling S, Hagenbeek A. B-cell involvement in chronic graft-versus-host disease. Haematologica. 2008;93(11):1702-1711.
21. Blair PA, Noreña 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(1): 129-140.
22. Flores-Borja F, Bosma A, Ng D, Reddy V, Ehrenstein MR, Isenberg DA, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med. 2013;5(173):173ra23.
23. Li X, Zhong H, Bao W, et al. Defective regulatory B-cell compartment in patients with immune thrombocytopenia. Blood. 2012;120(16): 3318-3325.
24. Khoder A, Sarvaria A, Alsuliman A, et al. Regulatory B cells are enriched within the IgM memory and transitional subsets in healthy donors but deficient in chronic GVHD. Blood. 2014;124(13):2034-2045.
25. Flynn R, Du J, Veenstra RG, et al. Increased T follicular helper cells and germinal center B cells are required for cGVHD and bronchiolitis obliterans. Blood. 2014;123(25):3988-3998.
26. Srinivasan M, Flynn R, Price A, et al. Donor B-cell alloantibody deposition and germinal center formation are required for the development of murine chronic GVHD and bronchiolitis obliterans. Blood. 2012;119(6):1570-1580.
27. Pai CC, Chen M, Mirsoian A, et al. Treatment of chronic graft-versus-host disease with bortezomib. Blood. 2014;124(10):1677-1688.
28. Dang VD, Hilgenberg E, Ries S, Shen P, Fillatreau S. From the regulatory functions of B cells to the identification of cytokine-producing plasma cell subsets. Curr Opin Immunol. 2014;28: 77-83.
29. Shen P, Roch T, Lampropoulou V, et al. IL-35- producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature. 2014;507(7492):366-370.
30. Ries S, Hilgenberg E, Lampropoulou V, et al. B-type suppression: a role played by "regulatory B cells" or "regulatory plasma cells"? Eur J Immunol. 2014;44(5):1251-1257.
31. Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity. 2014;41(6):1040-1051.
32. Klein U, Rajewsky K, Küppers 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(9):1679-1689.
33. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002;298(5601):2199-2202.
34. Tangye SG, Liu YJ, Aversa G, Phillips JH, de Vries JE. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J Exp Med. 1998;188(9):1691-1703.
35. Sanz I, Wei C, Lee FE, Anolik J. Phenotypic and functional heterogeneity of human memory B cells. Semin Immunol. 2008;20(1):67-82.
36. Galibert L, Burdin N, de Saint-Vis B, et al. CD40 and B cell antigen receptor dual triggering of resting B lymphocytes turns on a partial germinal center phenotype. J Exp Med. 1996;183(1):77-85.
37. Wehr C, Kivioja T, Schmitt C, et al. The EUROclass trial: defining subgroups in common variable immunodeficiency. Blood. 2008;111(1): 77-85.
38. Ridderstad A, Tarlinton DM. Kinetics of establishing the memory B cell population as revealed by CD38 expression. J Immunol. 1998; 160(10):4688-4695.
39. Avery DT, Kalled SL, Ellyard JI, et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest. 2003;112(2):286-297.
40. Filipovich AH, Weisdorf D, Pavletic S, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant. 2005;11(12):945-956.
41. Jourdan M, Caraux A, De Vos J, et al. An in vitro model of differentiation of memory B cells into plasmablasts and plasma cells including detailed phenotypic and molecular characterization. Blood. 2009;114(25):5173-5181.
42. Yoshizaki A, Miyagaki T, DiLillo DJ, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 2012;491(7423):264-268.
43. Liu B-S, Cao Y, Huizinga TW, Hafler DA, Toes RE. TLR-mediated STAT3 and ERK activation controls IL-10 secretion by human B cells. Eur J Immunol. 2014;44(7):2121-2129.
44. Griffin DO, Holodick NE, Rothstein TL. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70-. J Exp Med. 2011;208(1):67-80.
45. Corre E, Carmagnat M, Busson M, et al. Longterm immune deficiency after allogeneic stem cell transplantation: B-cell deficiency is associated with late infections. Haematologica. 2010;95(6): 1025-1029.
46. Joo H, Coquery C, Xue Y, et al. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J Exp Med. 2012;209(7):1335-1348.
47. Liu BS, Stoop JN, Huizinga TW, Toes RE. IL-21 enhances the activity of the TLR-MyD88-STAT3 pathway but not the classical TLR-MyD88-NF-κB pathway in human B cells to boost antibody production. J Immunol. 2013;191(8):4086-4094.
48. Berglund LJ, Avery DT, Ma CS, et al. IL-21 signalling via STAT3 primes human naive B cells to respond to IL-2 to enhance their differentiation into plasmablasts. Blood. 2013;122(24): 3940-3950.
49. Deenick EK, Avery DT, Chan A, et al. Naive and memory human B cells have distinct requirements for STAT3 activation to differentiate into antibody-secreting plasma cells. J Exp Med. 2013;210(12):2739-2753.
50. Rodríguez-Bayona B, Ramos-Amaya A, López-Blanco R, Campos-Caro A, Brieva JA. STAT-3 activation by differential cytokines is critical for human in vivo-generated plasma cell survival and Ig secretion. J Immunol. 2013;191(10): 4996-5004.
51. Zhao X-Y, Lv M, Xu L-L, Qian X, Huang X-J. Donor Th17 cells and IL-21 may contribute to the development of chronic graft-versus-host disease after allogeneic transplantation. Eur J Immunol. 2013;43(3):838-850.
52. Hippen KL, Bucher C, Schirm DK, et al. Blocking IL-21 signaling ameliorates xenogeneic GVHD induced by human lymphocytes. Blood. 2012; 119(2):619-628.
53. Florek M, Sega EI, Leveson-Gower DB, et al. Autologous apoptotic cells preceding transplantation significantly enhances survival in lethal murine graft versus host models. Blood. 2014;124(11):1832-1842.
54. Whittle R, Taylor PC. Circulating B-cell activating factor level predicts clinical response of chronic graft-versus-host disease to extracorporeal photopheresis. Blood. 2011;118(24):6446-6449.
55. Peng Y, Chen X, Liu Q, et al. Mesenchymal stromal cells infusions improve refractory chronic graft versus host disease through an increase of CD5+ regulato, ry B cells producing interleukin 10 [published online ahead of print July 18, 2014]. Leukemia.
56. Lemoine S, Morva A, Youinou P, Jamin C. Human T cells induce their own regulation through activation of B cells. J Autoimmun. 2011;36(3-4): 228-238.
57. de Masson A, Le Buanec H, Bouaziz JD. Purification and immunophenotypic characterization of human B cells with regulatory functions. Methods Mol Biol. 2014;1190:45-52.
58. van der Vlugt LE, Haeberlein S, de Graaf W, Martha TE, Smits HH. Toll-like receptor ligation for the induction of regulatory B cells. Methods Mol Biol. 2014;1190:127-141.
59. Wilde B, Thewissen M, Damoiseaux J, et al. Regulatory B cells in ANCA-associated vasculitis. Ann Rheum Dis. 2013;72(8):1416-1419.
60. Heine G, Drozdenko G, Grün JR, Chang H-D, Radbruch A, Worm M. Autocrine IL-10 promotes human B-cell differentiation into IgM- or IgG-secreting plasmablasts. Eur J Immunol. 2014; 44(6):1615-1621.
61. Maseda D, Smith SH, DiLillo DJ, et al. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J Immunol. 2012;188(3):1036-1048.