Pulsed high-dose dexamethasone improves interleukin 10 secretion by CD5+ B cells in patients with primary immune thrombocytopenia

Journal of Clinical Immunology

Volumn 32, Issue 6, 2012, Pages 1233-1242

  Hua, Fanli ^a   Ji, Lili ^a   Zhan, Yanxia ^a   Li, Feng ^a   Zou, Shanhua ^a   Wang, Xiaoyun ^a   Song, Dongli ^a   Min, Zhihui ^a   Gao, Song ^a   Wu, Yangjiong ^a   Chen, Hao ^a   Cheng, Yunfeng ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

B cell; CD5; high dose dexamethasone; immune thrombocytopenia; interleukin 10

Indexed keywords

DEXAMETHASONE; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; MESSENGER RNA; ANTIINFLAMMATORY AGENT; CD5 ANTIGEN; IL10 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; AUTOIMMUNE THROMBOCYTOPENIA; B LYMPHOCYTE; BIOACCUMULATION; CD5+ BETA CELL; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EFFECT; DRUG PULSE THERAPY; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE COUNT; MALE; MOLECULAR DYNAMICS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIMARY IMMUNE THROMBOCYTOPENIA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CELL CULTURE; DRUG ADMINISTRATION; GENE EXPRESSION; GENETICS; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY; SECRETION (PROCESS);

ADULT; AGED; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD5; B-LYMPHOCYTES; CELLS, CULTURED; DEXAMETHASONE; DRUG ADMINISTRATION SCHEDULE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; INTERLEUKIN-10; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; PURPURA, THROMBOCYTOPENIC, IDIOPATHIC; RNA, MESSENGER;

EID: 84878227048     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-012-9714-z     Document Type: Article

References (47)

1. Stasi R. Pathophysiology and therapeutic options in primary immune thrombocytopenia. Blood Transfus. 2011;9(3):262-73. doi: 10.2450/2010.0080-10.
2. Andersson PO, Wadenvik H. Chronic idiopathic thrombocytopenic purpura (ITP): molecular mechanisms and implications for therapy. Expert Rev Mol Med. 2004;6(24):1-17. doi: 10.1017/S1462399404008415.
3. Cines DB, Blanchette VS. Immune thrombocytopenic purpura. N Engl J Med. 2002;346(13):995-1008. doi: 10.1056/NEJMra010501.
4. Stasi R, Newland AC. ITP: a historical perspective. Br J Haematol. 2011;153(4):437-50. doi: 10.1111/j.1365-2141.2010.08562.x.
5. DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci. 2010;1183:38-57. doi: 10.1111/j.1749-6632.2009.05137.x.
6. hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32(1):129-40. doi: 10.1016/j.immuni.2009.11.009.
7. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944-50. doi: 10.1038/ni833.
8. + phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28(5):639-50. doi: 10.1016/j.immuni.2008.03.017.
9. Hedrich CM, Bream JH. Cell type-specific regulation of IL-10 expression in inflammation and disease. Immunol Res. 2010;47(1-3):185-206. doi: 10.1007/s12026-009-8150-5.
10. Mocellin S, Marincola F, Rossi CR, Nitti D, Lise M. The multifaceted relationship between IL-10 and adaptive immunity: putting together the pieces of a puzzle. Cytokine Growth Factor Rev. 2004;15(1):61-76.
11. Gray D, Gray M. What are regulatory B cells? Eur J Immunol. 2010;40(10):2677-9. doi: 10.1002/eji.201040961.
12. Mauri C. Regulation of immunity and autoimmunity by B cells. Curr Opin Immunol. 2010;22(6):761-7. doi: 10.1016/j.coi.2010.10.009.
13. Maseda D, Smith SH, DiLillo DJ, Bryant JM, Candando KM, Weaver CT, et al. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J Immunol. 2012;188(3):1036-48. doi: 10.4049/jimmunol.1102500.
14. Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S. IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol. 2011;178(2):735-43. doi: 10.1016/j.ajpath.2010.10.022.
15. Ding Q, Yeung M, Camirand G, Zeng Q, Akiba H, Yagita H, et al. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest. 2011;121(9):3645-56. doi: 10.1172/JCI46274.
16. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530-41. doi: 10.1182/blood-2010-07-294249.
17. Soldevila G, Raman C, Lozano F. The immunomodulatory properties of the CD5 lymphocyte receptor in health and disease. Curr Opin Immunol. 2011;23(3):310-8. doi: 10.1016/j.coi.2011.03.003.
18. Shaw PX, Horkko S, Chang MK, Curtiss LK, Palinski W, Silverman GJ, et al. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest. 2000;105(12):1731-40. doi: 10.1172/JCI8472.
19. Hardy RR. B-1 B cells: development, selection, natural autoantibody and leukemia. Curr Opin Immunol. 2006;18(5):547-55. doi: 10.1016/j.coi.2006.07.010.
20. Dalloul A. CD5: A safeguard against autoimmunity and a shield for cancer cells. Autoimmun Rev. 2009;8(4):349-53. doi: 10.1016/j.autrev.2008.11.007.
21. + B cells control the IL-12-dependent Th1-priming capacity of neonatal DCs. Immunity. 2005;22(4):467-77. doi: 10.1016/j.immuni.2005.02.008.
22. Ochoa-Reparaz J, Mielcarz DW, Haque-Begum S, Kasper LH. Induction of a regulatory B cell population in experimental allergic encephalomyelitis by alteration of the gut commensal microflora. Gut Microbes. 2010;1(2):103-8. doi: 10.4161/gmic.1.2.11515.
23. Cheng Y, Wong RS, Soo YO, Chui CH, Lau FY, Chan NP, et al. Initial treatment of immune thrombocytopenic purpura with high-dose dexamethasone. N Engl J Med. 2003;349(9):831-6. doi: 10.1056/NEJMoa030254.
24. Provan D, Stasi R, Newland AC, Blanchette VS, Bolton-Maggs P, Bussel JB, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010;115(2):168-86. doi: 10.1182/blood-2009-06-225565.
25. Mazzucconi MG, Fazi P, Bernasconi S, De Rossi G, Leone G, Gugliotta L, et al. Therapy with high-dose dexamethasone (HD-DXM) in previously untreated patients affected by idiopathic thrombocytopenic purpura: a GIMEMA experience. Blood. 2007;109(4):1401-7. doi: 10.1182/blood-2005-12-015222.
26. Liu XG, Ma SH, Sun JZ, Ren J, Shi Y, Sun L, et al. High-dose dexamethasone shifts the balance of stimulatory and inhibitory Fcγ receptors on monocytes in patients with primary immune thrombocytopenia. Blood. 2011;117(6):2061-9. doi: 10.1182/blood-2010-07-295477.
27. Guo C, Chu X, Shi Y, He W, Li L, Wang L, et al. Correction of Th1-dominant cytokine profiles by high-dose dexamethasone in patients with chronic idiopathic thrombocytopenic purpura. J Clin Immunol. 2007;27(6):557-62. doi: 10.1007/s10875-007-9111-1.
28. Chu XX, Huang BH, Zhang XL, Chen LM, Wang Y, Yu WJ, et al. Dexamethasone inhibits immunoreactivity of dendritic cells in patients with chronic idiopathic thrombocytopenic purpura. Blood Coagul Fibrinolysis. 2010;21(6):564-7. doi: 10.1097/MBC.0b013e32833c2b8c.
29. Shan NN, Zhu XJ, Wang Q, Wang CY, Qin P, Peng J, et al. High-dose dexamethasone regulates interleukin-18 and interleukin-18 binding protein in idiopathic thrombocytopenic purpura. Haematologica. 2009;94(11):1603-7. doi: 10.3324/haematol.2009.007708.
30. Zhu XJ, Shi Y, Sun JZ, Shan NN, Peng J, Guo CS, et al. High-dose dexamethasone inhibits BAFF expression in patients with immune thrombocytopenia. J Clin Immunol. 2009;29(5):603-10. doi: 10.1007/s10875-009-9303-y.
31. Cao J, Chen C, Li L, Zeng LY, Li ZY, Yan ZL, et al. Effects of high-dose dexamethasone on regulating interleukin-22 production and correcting Th1 and Th22 polarization in immune thrombocytopenia. J Clin Immunol. 2012 Feb 1. doi: 10.1007/s10875-012-9649-4. [Epub ahead of print].
32. Rodeghiero F, Stasi R, Gernsheimer T, Michel M, Provan D, Arnold DM, et al. Standardization of terminology, definitions and outcome criteria in immune thrombocytopenic purpura of adults and children: report from an international working group. Blood. 2009;113(11):2386-93. doi: 10.1182/blood-2008-07-162503.
33. Jamin C, Lamour A, Pennec YL, Hirn M, Le Goff P, Youinou P. Expression of CD5 and CD72 on T and B cell subsets in rheumatoid arthritis and Sjogren's syndrome. Clin Exp Immunol. 1993;92(2):245-50.
34. Taniguchi O, Miyajima H, Hirano T, Noguchi M, Ueda A, Hashimoto H, et al. The Leu-1 B-cell subpopulation in patients with rheumatoid arthritis. J Clin Immunol. 1987;7(6):441-8.
35. Cantaert T, Doorenspleet M E, Francosalinas G, Paramarta JE, Klarenbeek PL, Tiersma Y, et al. Increase of CD5(+) B lymphocytes with a regulatory phenotype in spondyloarthritis. Arthritis Rheum. 2012. 2012 Jan 9. doi: 10.1002/art.34364. [Epub ahead of print]
36. Villar LM, Espino M, Roldan E, Marin N, Costa-Frossard L, Muriel A, et al. Increased peripheral blood CD5+ B cells predict earlier conversion to MS in high-risk clinically isolated syndromes. Mult Scler. 2011;17(6):690-4. doi: 10.1177/1352458510396922.
37. Mizutani H, Furubayashi T, Kashiwagi H, Honda S, Take H, Kurata Y, et al. B cells expressing CD5 antigen are markedly increased in peripheral blood and spleen lymphocytes from patients with immune thrombocytopenic purpura. Br J Haematol. 1991;78(4):474-9.
38. Iyori H, Fujisawa K, Akatsuka J. Autoantibodies and CD5+ B cells in childhood onset immune thrombocytopenic purpura. Acta Paediatr Jpn. 1995;37(3):325-30.
39. Hou M, Lv B, He Q, Lu L, Shi Y, Ji X, et al. Both splenic CD5(+) B and CD5(-) B cells produce platelet glycoprotein-specific autoantibodies in chronic ITP. Thromb Res. 2003;110(1):1-5.
40. 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):228-38. doi: 10.1016/j.jaut.2011.01.005.
41. O'Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol. 1992;22(3):711-7. doi: 10.1002/eji.1830220314.
42. Garaud S, Morva A, Lemoine S, Hillion S, Bordron A, Pers JO, et al. CD5 promotes IL-10 production in chronic lymphocytic leukemia B cells through STAT3 and NFAT2 activation. J Immunol. 2011;186(8):4835-44. doi: 10.4049/jimmunol. 1003050.
43. Gary-Gouy H, Harriague J, Bismuth G, Platzer C, Schmitt C, Dalloul AH. Human CD5 promotes B-cell survival through stimulation of autocrine IL-10 production. Blood. 2002;100(13):4537-43. doi: 10.1182/blood-2002-05-1525.
44. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol. 2009;182(12):7459-72. doi: 10.4049/jimmunol.0900270.
45. Bao W, Bussel JB, Heck S, He W, Karpoff M, Boulad N, et al. Improved regulatory T-cell activity in patients with chronic immune thrombocytopenia treated with thrombopoietic agents. Blood. 2010;116(22):4639-45. doi: 10.1182/blood-2010-04-281717.
46. Del VG, Giordano P, Tesse R, Piacente L, Altomare M, De Mattia D. Clinical significance of serum cytokine levels and thrombopoietic markers in childhood idiopathic thrombocytopenic purpura. Blood Transfus. 2012;10(2):194-9. doi: 10.2450/2011.0055-11.
47. Audia S, Samson M, Guy J, Janikashvili N, Fraszczak J, Trad M, et al. Immunologic effects of rituximab on the human spleen in immune thrombocytopenia. Blood. 2011;118(16):4394-400. doi: 10.1182/blood-2011-03-344051.