Splenic proliferative lymphoid nodules distinct from germinal centers are sites of autoantigen stimulation in immune thrombocytopenia

Blood

Volumn 120, Issue 25, 2012, Pages 5021-5031

  Daridon, Capucine ^a   Loddenkemper, Christoph ^a   Spieckermann, Simone ^a   Kühl, Anja A ^a,b   Salama, Abdulgabar ^a   Burmester, Gerd R ^a   Lipsky, Peter E ^c   Dörner, Thomas ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Research Center ImmunoScience (RCIS)   (Germany)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; AZATHIOPRINE; CD36 ANTIGEN; DEXAMETHASONE; FIBRINOGEN RECEPTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN M; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PREDNISOLONE; PREDNISOLONE SODIUM SUCCINATE; VINCRISTINE;

ADULT; AGED; ARTICLE; AUTOIMMUNE THROMBOCYTOPENIA; B LYMPHOCYTE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; HELPER CELL; HUMAN; HUMAN TISSUE; HUMORAL IMMUNITY; LYMPHOID TISSUE; PRIORITY JOURNAL; PROLIFERATIVE LYMPHOID NODULE; SPLEEN; THROMBOCYTE; THROMBOCYTE TRANSFUSION;

EID: 84870996379     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-04-424648     Document Type: Article

References (44)

1. Odegard JM, Marks BR, DiPlacido LD, et al. ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity. J Exp Med. 2008;205(12):2873-2886.
2. Valencia X, Lipsky PE. CD4+CD25+FoxP3+ regulatory T cells in autoimmune diseases. Nat Clin Pract Rheumatol. 2007;3(11):619-626.
3. MacLennan IC. Germinal centers. Annu Rev Immunol. 1994;12:117-139. (Pubitemid 24140411)
4. de Vinuesa CG, Cook MC, Ball J, et al. Germinal centers without T cells. J Exp Med. 2000;191(3):485-494.
5. MacLennan IC, Toellner KM, Cunningham AF, et al. Extrafollicular antibody responses. Immunol Rev. 2003;194:8-18. (Pubitemid 36886424)
6. Pone EJ, Zan H, Zhang J, Al-Qahtani A, Xu Z, Casali P. Toll-like receptors and B-cell receptors synergize to induce immunoglobulin class-switch DNA recombination: relevance to microbial antibody responses. Crit Rev Immunol. 2010;30(1):1-29.
7. Cesta MF. Normal structure, function, and histology of the spleen. Toxicol Pathol. 2006;34(5):455-465. (Pubitemid 44652213)
8. Rodeghiero F, Stasi R, Gernsheimer T, 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): 2386-2393.
9. Karpatkin S. Autoimmune (idiopathic) thrombocytopenic purpura. Lancet. 1997;349(9064):1531-1536. (Pubitemid 27216374)
10. Semple JW, Freedman J. Increased antiplatelet T helper lymphocyte reactivity in patients with autoimmune thrombocytopenia. Blood. 1991;78(10):2619-2625.
11. Kuwana M, Okazaki Y, Kaburaki J, Kawakami Y, Ikeda Y. Spleen is a primary site for activation of platelet-reactive T and B cells in patients with immune thrombocytopenic purpura. J Immunol. 2002;168(7):3675-3682. (Pubitemid 34250440)
12. Kuwana M, Kawakami Y, Ikeda Y. Suppression of autoreactive T-cell response to glycoprotein IIb/IIIa by blockade of CD40/CD154 interaction: implications for treatment of immune thrombocytopenic purpura. Blood. 2003;101(2):621-623. (Pubitemid 36077585)
13. Audia S, Samson M, Guy J, et al. Immunologic effects of rituximab on the human spleen in immune thrombocytopenia. Blood. 2011;118(16):4394-4400.
14. 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. (Pubitemid 24058552)
15. Godeau B, Michel M. Treatment of chronic immune thrombocytopenic purpura in adults [published online ahead of print April 14, 2010]. Ann Hematol. doi:10.1007/s00277-010-0952-y.
16. Daridon C, Pers JO, Devauchelle V, et al. Identification of transitional type II B cells in the salivary glands of patients with Sjogren's syndrome. Arthritis Rheum. 2006;54(7):2280-2288. (Pubitemid 44051085)
17. Johnston RJ, Poholek AC, DiToro D, et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science. 2009;325(5943):1006-1010.
18. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 2000;102(5):553-563.
19. Tavassoli M, McMillan R. Structure of the spleen in idiopathic thrombocytopenic purpura. Am J Clin Pathol. 1975;64(2):180-191.
20. Hayes MM, Jacobs P, Wood L, Dent DM. Splenic pathology in immune thrombocytopenia. J Clin Pathol. 1985;38(9):985-988. (Pubitemid 16249803)
21. Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity. 2007;27(2):190-202. (Pubitemid 47284923)
22. Allen CD, Ansel KM, Low C, et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol. 2004;5(9):943-952. (Pubitemid 39276239)
23. Steiniger B, Trabandt M, Barth PJ. The follicular dendritic cell network in secondary follicles of human palatine tonsils and spleens. Histochem Cell Biol. 2011;135(4):327-336.
24. Zhang X, Park CS, Yoon SO, et al. BAFF supports human B cell differentiation in the lymphoid follicles through distinct receptors. Int Immunol. 2005;17(6):779-788. (Pubitemid 41417976)
25. Gorelik L, Cutler AH, Thill G, et al. Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function. J Immunol. 2004;172(2):762-766. (Pubitemid 38113731)
26. Zhou Z, Li X, Li J, et al. Direct B-cell stimulation by peripheral blood monocyte-derived dendritic cells in idiopathic thrombocytopenic purpura patients. J Clin Immunol. 2010;30(6):814-822.
27. Emmerich F, Bal G, Barakat A, et al. High-level serum B-cell activating factor and promoter polymorphisms in patients with idiopathic thrombocytopenic purpura. Br J Haematol. 2007;136(2):309-314. (Pubitemid 46020761)
28. Ferguson AR, Youd ME, Corley RB. Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol. 2004;16(10):1411-1422. (Pubitemid 39341554)
29. Victoratos P, Kollias G. Induction of autoantibody-mediated spontaneous arthritis critically depends on follicular dendritic cells. Immunity. 2009;30(1):130-142.
30. Henn V, Slupsky JR, Grafe M, et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature. 1998;391(6667):591-594. (Pubitemid 28157601)
31. Solanilla A, Pasquet JM, Viallard JF, et al. Platelet-associated CD154 in immune thrombocytopenic purpura. Blood. 2005;105(1):215-218. (Pubitemid 40053085)
32. Poholek AC, Hansen K, Hernandez SG, et al. In vivo regulation of Bcl6 and T follicular helper cell development. J Immunol. 2010;185(1):313-326.
33. Fukuda T, Yoshida T, Okada S, et al. Disruption of the Bcl6 gene results in an impaired germinal center formation. J Exp Med. 1997;186(3):439-448. (Pubitemid 27332902)
34. Kitano M, Moriyama S, Ando Y, et al. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity. 2011;34(6):961-972.
35. McHeyzer-Williams M, Okitsu S, Wang N, McHeyzer-Williams L. Molecular programming of B cell memory. Nat Rev Immunol. 2012;12(1):24-34.
36. Olsson B, Ridell B, Jernas M, Wadenvik H. Increased number of B-cells in the red pulp of the spleen in ITP. Ann Hematol. 2012;91(2):271-277.
37. Nishimoto T, Satoh T, Takeuchi T, Ikeda Y, Kuwana M. Critical role of CD4(+)CD25(+) regulatory T cells in preventing murine autoantibody-mediated thrombocytopenia. Exp Hematol. 2012;40(4):279-289.
38. Jacob J, Kassir R, Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J Exp Med. 1991;173(5):1165-1175.
39. Cattoretti G, Buttner M, Shaknovich R, Kremmer E, Alobeid B, Niedobitek G. Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood. 2006;107(10):3967-3975. (Pubitemid 43726803)
40. Weinstein JS, Nacionales DC, Lee PY, et al. Co-localization of antigen-specific B and T cells within ectopic lymphoid tissue following immunization with exogenous antigen. J Immunol. 2008;181(5):3259-3267.
41. Nacionales DC, Weinstein JS, Yan XJ, et al. B cell proliferation, somatic hypermutation, class switch recombination, and autoantibody production in ectopic lymphoid tissue in murine lupus. J Immunol. 2009;182(7):4226-4236.
42. Vinuesa CG, Linterman MA, Goodnow CC, Randall KL. T cells and follicular dendritic cells in germinal center B-cell formation and selection. Immunol Rev. 2010;237(1):72-89.
43. 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.
44. Cines DB, Bussel JB, Liebman HA, Luning Prak ET. The ITP syndrome: pathogenic and clinical diversity. Blood. 2009;113(26):6511-6521.