CD8+ T cells are predominantly protective and required for effective steroid therapy in murine models of immune thrombocytopenia

Blood

Volumn 126, Issue 2, 2015, Pages 247-256

  Ma, Li ^a,b,c   Simpson, Elisa ^a,b,d   Li, June ^a,b,d   Xuan, Min ^a,b,e   Xu, Miao ^a,b,d   Baker, Laura ^a,b,c   Shi, Yan ^a,b,f   Yougbaré, Issaka ^a,b,c   Wang, Xiaozhong ^a,b,g   Zhu, Guangheng ^a,b   Chen, Pingguo ^a,b,c   Prudhomme, Gerald J ^b,d   Lazarus, Alan H ^a,b,c,d,h   Freedman, John ^a,b,d,h   Ni, Heyu ^a,b,c,d,h  

^a Toronto Platelet Immunobiology Group   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c CANADIAN BLOOD SERVICES   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^f SHANDONG UNIVERSITY   (China)

^g NANCHANG UNIVERSITY   (China)

^h ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CD19 ANTIGEN; DEXAMETHASONE; IMMUNOGLOBULIN G; INTERLEUKIN 10; FIBRINOGEN RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONFERENCE PAPER; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DISEASE SEVERITY; DRUG EFFICACY; DRUG SELECTIVITY; FLOW CYTOMETRY; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IN VITRO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE TRANSFUSION; MOUSE; MURINE MODEL; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; STEROID THERAPY; T CELL DEPLETION; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE DEPLETION; MULTIMODALITY CANCER THERAPY; PHYSIOLOGY; PURPURA, THROMBOCYTOPENIC, IDIOPATHIC; THROMBOCYTE; TRANSPLANTATION; TREATMENT OUTCOME;

ANIMALS; BLOOD PLATELETS; CD8-POSITIVE T-LYMPHOCYTES; COMBINED MODALITY THERAPY; DEXAMETHASONE; DISEASE MODELS, ANIMAL; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PURPURA, THROMBOCYTOPENIC, IDIOPATHIC; T-LYMPHOCYTES, CYTOTOXIC; TREATMENT OUTCOME;

EID: 84937825485     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-03-635417     Document Type: Conference Paper

References (69)

1. Harrington WJ, Sprague CC, Minnich V, Moore CV, Aulvin RC, Dubach R. Immunologic mechanisms in idiopathic and neonatal thrombocytopenic purpura. Ann Intern Med. 1953; 38(3):433-469.
2. He R, Reid DM, Jones CE, Shulman NR. Spectrum of Ig classes, specificities, and titers of serum antiglycoproteins in chronic idiopathic thrombocytopenic purpura. Blood. 1994;83(4): 1024-1032.
3. Portielje JE, Westendorp RG, Kluin-Nelemans HC, Brand A. Morbidity and mortality in adults with idiopathic thrombocytopenic purpura. Blood. 2001;97(9):2549-2554.
4. Cines DB, Bussel JB. How I treat idiopathic thrombocytopenic purpura (ITP). Blood. 2005; 106(7):2244-2251.
5. McMillan R. The pathogenesis of chronic immune thrombocytopenic purpura. Semin Hematol. 2007; 44(4 Suppl 5):S3-S11.
6. Beardsley DS, Ertem M. Platelet autoantibodies in immune thrombocytopenic purpura. Transfus Sci. 1998;19(3):237-244.
7. McMillan R. Antiplatelet antibodies in chronic adult immune thrombocytopenic purpura: Assays and epitopes. J Pediatr Hematol Oncol. 2003; 25(Suppl 1):S57-S61.
8. Stasi R, Stipa E, Masi M, et al. Long-term observation of 208 adults with chronic idiopathic thrombocytopenic purpura. Am J Med. 1995; 98(5):436-442.
9. Zeng Q, Zhu L, Tao L, et al. Relative efficacy of steroid therapy in immune thrombocytopenia mediated by anti-platelet GPIIbIIIa versus GPIba antibodies. Am J Hematol. 2012;87(2):206-208.
10. Provan D, Stasi R, Newland AC, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010;115(2):168-186.
11. Peng J, Ma SH, Liu J, et al. Association of autoantibody specificity and response to intravenous immunoglobulin G therapy in immune thrombocytopenia: A multicenter cohort study. J Thromb Haemost. 2014;12(4):497-504.
12. Psaila B, Bussel JB. Refractory immune thrombocytopenic purpura: Current strategies for investigation and management. Br J Haematol. 2008;143(1):16-26.
13. Schwartz J, Leber MD, Gillis S, Giunta A, Eldor A, Bussel JB. Long term follow-up after splenectomy performed for immune thrombocytopenic purpura (ITP). Am J Hematol. 2003;72(2):94-98.
14. Li J, Van Der Wal DE, Zhu L, et al. Fc-independent phagocytosis: Implications for IVIG and other therapies in immune-mediated thrombocytopenia. Cardiovasc Hematol Disord Drug Targets. 2013; 13(1):50-58.
15. Cines DB, Bussel JB, Liebman HA, Luning Prak ET. The ITP syndrome: Pathogenic and clinical diversity. Blood. 2009;113(26):6511-6521.
16. Li C, Li J, Li Y, et al. Crosstalk between platelets and the immune system: Old systems with new discoveries. Adv Hematol. 2012;2012:1-14.
17. Olsson B, Andersson PO, Jern°as M, et al. T-cellmediated cytotoxicity toward platelets in chronic idiopathic thrombocytopenic purpura. Nat Med. 2003;9(9):1123-1124.
18. Zhang F, Chu X, Wang L, et al. Cell-mediated lysis of autologous platelets in chronic idiopathicthrombocytopenic purpura. Eur J Haematol. 2006 76 5 427-431.
19. Zhang J, Ma D, Zhu X, Qu X, Ji C, Hou M. Elevated profile of Th17, Th1 and Tc1 cells in patients with immune thrombocytopenic purpura. Haematologica. 2009;94(9):1326-1329.
20. Chow L, Aslam R, Speck ER, et al. A murine model of severe immune thrombocytopenia is induced by antibody-and CD81 T cell-mediated responses that are differentially sensitive to therapy. Blood. 2010;115(6):1247-1253.
21. Zhao C, Li X, Zhang F, Wang L, Peng J, Hou M. Increased cytotoxic T-lymphocyte-mediated cytotoxicity predominant in patients with idiopathic thrombocytopenic purpura without platelet autoantibodies. Haematologica. 2008;93(9): 1428-1430.
22. Audia S, Samson M, Mahévas M, et al. Preferential splenic CD8(1) T-cell activation in rituximab-nonresponder patients with immune thrombocytopenia. Blood. 2013;122(14): 2477-2486.
23. Yazdanbakhsh K, Zhong H, Bao W. Immune dysregulation in immune thrombocytopenia. Semin Hematol. 2013;50(Suppl 1):S63-S67.
24. Liu B, Zhao H, Poon MC, et al. Abnormality of CD4(1)CD25(1) regulatory T cells in idiopathic thrombocytopenic purpura. Eur J Haematol. 2007; 78(2):139-143.
25. Nishimoto T, Kuwana M. CD41CD251Foxp31 regulatory T cells in the pathophysiology of immune thrombocytopenia. Semin Hematol. 2013;50(Suppl 1):S43-S49.
26. Aslam R, Hu Y, Gebremeskel S, et al. Thymic retention of CD41CD251FoxP31 T regulatory cells is associated with their peripheral deficiency and thrombocytopenia in a murine model of immune thrombocytopenia. Blood. 2012;120(10): 2127-2132.
27. Nishimoto T, Satoh T, Takeuchi T, Ikeda Y, Kuwana M. Critical role of CD4(1)CD25(1) regulatory T cells in preventing murine autoantibody-mediated thrombocytopenia. Exp Hematol. 2012;40(4):279-289.
28. McKenzie CG, Guo L, Freedman J, Semple JW. Cellular immune dysfunction in immune thrombocytopenia (ITP). Br J Haematol. 2013; 163(1):10-23.
29. Yu J, Heck S, Patel V, et al. Defective circulating CD25 regulatory T cells in patients with chronic immune thrombocytopenic purpura. Blood. 2008; 112(4):1325-1328.
30. Ling Y, Cao X, Yu Z, Ruan C. Circulating dendritic cells subsets and CD41Foxp31 regulatory T cells in adult patients with chronic ITP before and after treatment with high-dose dexamethasome. Eur J Haematol. 2007;79(4): 310-316.
31. Stasi R, Cooper N, Del Poeta G, et al. Analysis of regulatory T-cell changes in patients with idiopathic thrombocytopenic purpura receiving B cell-depleting therapy with rituximab. Blood. 2008;112(4):1147-1150.
32. Bao W, Bussel JB, Heck S, et al. Improved regulatory T-cell activity in patients with chronic immune thrombocytopenia treated with thrombopoietic agents. Blood. 2010;116(22): 4639-4645.
33. Cantor H, Shen FW, Boyse EA. Separation of helper T cells from suppressor T cells expressing different Ly components. II. Activation by antigen: After immunization, antigen-specific suppressor and helper activities are mediated by distinct T-cell subclasses. J Exp Med. 1976;143(6):1391-40.
34. Gershon RK, Kondo K. Cell interactions in the induction of tolerance: The role of thymic lymphocytes. Immunology. 1970;18(5):723-737.
35. Lu L, Cantor H. Generation and regulation of CD8(1) regulatory T cells. Cell Mol Immunol. 2008;5(6):401-406.
36. Jiang H, Canfield SM, Gallagher MP, et al. HLAE-restricted regulatory CD8(1) T cells are involved in development and control of human autoimmune type 1 diabetes. J Clin Invest. 2010; 120(10):3641-3650.
37. Leavenworth JW, Tang X, Kim HJ, Wang X, Cantor H. Amelioration of arthritis through mobilization of peptide-specific CD81 regulatory T cells. J Clin Invest. 2013;123(3):1382-1389.
38. Chess L, Jiang H. Resurrecting CD81 suppressor T cells. Nat Immunol. 2004;5(5):469-471.
39. Koh DR, Fung-Leung WP, Ho A, Gray D, Acha-Orbea H, Mak TW. Less mortality but more relapses in experimental allergic encephalomyelitis in CD8-/-mice. Science. 1992; 256(5060):1210-1213.
40. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, et al. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest. 1999; 103(2):229-238.
41. Ni H, Chen P, Spring CM, et al. A novel murine model of fetal and neonatal alloimmune thrombocytopenia: Response to intravenous IgG therapy. Blood. 2006;107(7):2976-2983.
42. Li C, Piran S, Chen P, et al. The maternal immune response to fetal platelet GPIba causes frequent miscarriage in mice that can be prevented by intravenous IgG and anti-FcRn therapies. J Clin Invest. 2011;121(11):4537-4547.
43. Li C, Chen P, Vadasz B, et al. Co-stimulation with LPS or Poly I:C markedly enhances the antiplatelet immune response and severity of fetal and neonatal alloimmune thrombocytopenia. Thromb Haemost. 2013;110(6):1250-1258.
44. Chen P, Li C, Lang S, et al. Animal model of fetal and neonatal immune thrombocytopenia: Role of neonatal Fc receptor in the pathogenesis and therapy. Blood. 2010;116(18):3660-3668.
45. Yougbaré I, Lang S, Yang H, et al. Maternal antiplatelet b3 integrins impair angiogenesis and cause intracranial hemorrhage. J Clin Invest. 2015;125(4):1545-1556.
46. Webster ML, Sayeh E, Crow M, et al. Relative efficacy of intravenous immunoglobulin G in ameliorating thrombocytopenia induced by antiplatelet GPIIbIIIa versus GPIbalpha antibodies. Blood. 2006;108(3):943-946.
47. Crow AR, Song S, Semple JW, Freedman J, Lazarus AH. IVIg inhibits reticuloendothelial system function and ameliorates murine passiveimmune thrombocytopenia independent of antiidiotype reactivity. Br J Haematol. 2001;115(3): 679-686.
48. Zhu G, Chen P, Reheman A, Li J, Ni H. Psi domain of b3 integrin has endogenous thiol isomerase function and is a potential new target for anti-thrombotic therapy [abstract]. Blood. 2; 120(21). Abstract 382.
49. Van Der Wal DE, Zhu G, Li J, et al. Desialylation: A novel platelet clearance mechanism and a potential new therapeutic target in anti-GPIb antibody mediated [abstract]. Blood. 2012;120 (21). Abstract 265.
50. Yang H, Lang S, Zhai Z, et al. Fibrinogen is required for maintenance of platelet intracellular and cell-surface P-selectin expression. Blood. 2009;114(2):425-436.
51. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32(6):435-443.
52. Hagenström H, Schlenke P, Hennig H, Kirchner H, Kl üter H. Quantification of platelet-associated IgG for differential diagnosis of patients with thrombocytopenia. Thromb Haemost. 2000;84(5): 779-783.
53. Wüst S, Van Den Brandt J, Tischner D, et al. Peripheral T cells are the therapeutic targets of glucocorticoids in experimental autoimmune encephalomyelitis. J Immunol. 2008;180(12): 8434-8443.
54. Donia M, Mangano K, Quattrocchi C, et al. Specific and strain-independent effects of dexamethasone in the prevention and treatment of experimental autoimmune encephalomyelitis in rodents. Scand J Immunol. 2010;72(5):396-407.
55. Andersson J. Cytokines in idiopathic thrombocytopenic purpura (ITP). Acta Paediatr Suppl. 1998;424:61-64.
56. Semple JW. T cell and cytokine abnormalities in patients with autoimmune thrombocytopenic purpura. Transfus Apheresis Sci. 2003;28(3): 237-242.
57. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature. 1997;390(6658):350-351.
58. Tsai S, Clemente-Casares X, Santamaria P. CD8(1) Tregs in autoimmunity: Learning "self"-control from experience. Cell Mol Life Sci. 2011; 68(23):3781-3795.
59. Guo L, Yang L, Speck ER, et al. Allogeneic platelet transfusions prevent murine T-cellmediated immune thrombocytopenia. Blood. 2014;123(3):422-427.
60. Warner MN, Moore JC, Warkentin TE, Santos AV, Kelton JG. A prospective study of protein-specific assays used to investigate idiopathic thrombocytopenic purpura. Br J Haematol. 1999; 104(3):442-447.
61. Garba ML, Pilcher CD, Bingham AL, Eron J, Frelinger JA. HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD81 T cells. J Immunol. 2002;168(5):2247-2254.
62. Filaci G, Bacilieri S, Fravega M, et al. Impairment of CD81 T suppressor cell function in patients with active systemic lupus erythematosus. J Immunol. 2001;166(10):6452-6457.
63. Mikulkova Z, Praksova P, Stourac P, et al. Numerical defects in CD81CD28-Tsuppressor lymphocyte population in patients with type 1 diabetes mellitus and multiple sclerosis. Cell Immunol. 2010;262(2):75-79.
64. Kashi VP, Ortega SB, Karandikar NJ. Neuroantigen-specific autoregulatory CD81 T cells inhibit autoimmune demyelination through modulation of dendritic cell function. PLoS ONE. 2014;9(8):e105763.
65. Chambers CA, Kuhns MS, Egen JG, Allison JP. CTLA-4-mediated inhibition in regulation of T cell responses: Mechanisms and manipulation in tumor immunotherapy. Annu Rev Immunol. 2001; 19:565-594.
66. Fiorentino DF, Zlotnik A, Vieira P, et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol. 1991;146(10): 3444-3451.
67. Panitsas FP, Theodoropoulou M, Kouraklis A, et al. Adult chronic idiopathic thrombocytopenic purpura (ITP) is the manifestation of a type-1 polarized immune response. Blood. 2004;103(7): 2645-2647.
68. Endharti AT, Rifa'I M, Shi Z, et al. Cutting edge: CD81CD1221 regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD81 T cells. J Immunol. 2005;175(11): 7093-7097.
69. Yang L, Wang L, Zhao CH, et al. Contributions of TRAIL-mediated megakaryocyte apoptosis to impaired megakaryocyte and platelet production in immune thrombocytopenia. Blood. 2010; 116(20):4307-4316.