Reduced CD5+CD24hiCD38hi and interleukin-10+ regulatory B cells in active anti-neutrophil cytoplasmic autoantibody-associated vasculitis permit increased circulating autoantibodies

Clinical and Experimental Immunology

Volumn 180, Issue 2, 2015, Pages 178-188

  Aybar, L T ^a   Mcgregor, J G ^a   Hogan, S L ^a   Hu, Y ^a   Mendoza, C E ^a   Brant, E J ^a   Poulton, C J ^a   Henderson, C D ^a   Falk, R J ^a   Bunch, D O ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

AAV; ANCA; CD5; Interleukin 10; Regulatory B cells

Indexed keywords

AUTOANTIBODY; AZATHIOPRINE; CD19 ANTIGEN; CD24 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; CD40 LIGAND; CD5 ANTIGEN; CYCLOPHOSPHAMIDE; INTERLEUKIN 10; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; NEUTROPHIL CYTOPLASMIC ANTIBODY; PREDNISOLONE; PREDNISONE; RITUXIMAB; CD24 PROTEIN, HUMAN; CD38 PROTEIN, HUMAN; CD40 ANTIGEN; CPG-OLIGONUCLEOTIDE; IL10 PROTEIN, HUMAN; IMMUNOLOGICAL ADJUVANT; MEMBRANE PROTEIN; OLIGODEOXYRIBONUCLEOTIDE;

ADULT; ANCA ASSOCIATED VASCULITIS; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MEGADOSE; FEMALE; FLOW CYTOMETRY; HISTOGRAM; HUMAN; HUMAN CELL; MAINTENANCE THERAPY; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; REMISSION; SEROTYPE; AGED; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; BLOOD; CLINICAL TRIAL; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADJUVANTS, IMMUNOLOGIC; ADULT; AGED; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; ANTIBODIES, ANTINEUTROPHIL CYTOPLASMIC; ANTIGENS, CD24; ANTIGENS, CD38; ANTIGENS, CD40; ANTIGENS, CD5; B-LYMPHOCYTES, REGULATORY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-10; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; OLIGODEOXYRIBONUCLEOTIDES; REMISSION INDUCTION;

EID: 84927622116     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12483     Document Type: Article

References (44)

1. Jennette JC, Falk RJ, Hu P, Xiao H. Pathogenesis of antineutrophil cytoplasmic autoantibody associated small-vessel vasculitis. Annu Rev Pathol 2013; 8:139-160.
2. Kallenberg CGM. Pathogenesis of ANCA-associated vasculitides. Ann Rheum Dis 2011; 70 (Suppl. 1):i59-i63.
3. Xiao H, Heeringa P, Hu P etal. Antineutrophil cytoplasmic autoantibodies specific for myeloperoxidase cause glomerulonephritis and vasculitis in mice. J Clin Invest 2002; 110:955-963.
4. Little MA, Al-Ani B, Ren S etal. Anti-proteinase 3 anti-neutrophil cytoplasm autoantibodies recapitulate systemic vasculitis in mice with a humanized immune system. PLOS ONE 2012; 7:e28626.
5. Jones RB, Cohen Tervaert JW, Hauser T etal. Rituximab versus cyclophosphamide in ANCA-associated renal vasculitis. N Engl J Med 2012; 363:211-220.
6. Stone JH, Merkel PA, Spiera R etal. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med 2010; 363:221-232.
7. Blair PA, Norena LY, Flores-Borja F etal. 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.
8. Bouaziz JD, Le Buanec H, Saussine A, Bensussan A, Bagot M. IL-10 producing regulatory B cells in mice and humans: state of the art. Curr Mol Med 2012; 12:519-527.
9. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002; 3:944-950.
10. Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg R, Bhan A. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002; 16:219-230.
11. Iwata Y, Matsushita T, Horikawa M etal. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117:530-541.
12. Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 2002; 20:253-300.
13. Bunch DO, McGregor JAG, Khandoobhai NB etal. Decreased CD5+ B cells in active ANCA vasculitis and relapse after rituximab. Clin J Am Soc Nephrol 2013; 8:382-391.
14. Yanaba K, Bouaziz J, Haas K, Poe J, Fujimoto M, Tedder T. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008; 28:639-650.
15. Jennette JC, Falk RJ, Bacon PA etal. 2012 revised international chapel hill consensus conference nomenclature of vasculitides. Arthritis Rheum 2013; 65:1-11.
16. Lionaki S, Blyth ER, Hogan SL etal. Classification of antineutrophil cytoplasmic autoantibody vasculitides: the role of antineutrophil cytoplasmic autoantibody specificity for myeloperoxidase or proteinase 3 in disease recognition and prognosis. Arthritis Rheum 2012; 64:3452-3462.
17. Jennette JC, Falk RJ, Andrassy K etal. Nomenclature of systemic vasculitides. Arthritis Rheum 1994; 37:187-192.
18. Luqmani R, Bacon P, Moots R etal. Birmingham vasculitis activity score (BVAS) Dim system necrotizing vasculitis. Q J Med 1994; 87:671-678.
19. Jennette JC, Wilkman AS, Falk R. Anti-neutrophil cytoplasmic autoantibody-associated glomerulonephritis and vasculitis. Am J Pathol 1989; 135:921-930.
20. Hogan SL, Falk RJ, Chin H etal. Predictors of relapse and treatment resistance in antineutrophil cytoplasmic antibody associated small-vessel vasculitis. Ann Intern Med 2005; 143:621-631.
21. Herzenberg LA, Tung J, Moore WA, Herzenberg LA, Parks DR. Interpreting flow cytometry data: a guide for the perplexed. Nat Immunol 2006; 7:681-685.
22. Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest 2008; 118:3420-3430.
23. Qian L, Qian C, Chen Y etal. Regulatory dendritic cells program B cells to differentiate into CD19hiFcγIIbhi regulatory B cells through IFN-β and CD40L. Blood 2012; 120:581-591.
24. Klinker MW, Lundy SK. Multiple mechanisms of immune suppression by B lymphocytes. Mol Med 2012; 18:123-137.
25. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003; 197:489-501.
26. 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; 100:4537-4543.
27. Garaud S, Morva A, Lemoine S etal. CD5 promotes IL-10 production in chronic lymphocytic leukemia B cells through STAT3 and NFAT2 activation. J Immunol 2011; 186:4835-4844.
28. 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 2005; 22:711-717.
29. von Herrath M, Sanda S, Herold K. Type 1 diabetes as a relapsing-remitting disease? Nat Rev Immunol 2007; 7:988-994.
30. Abdulahad WH, Stegeman CA, van der Geld YM, Doornbos-van der Meer B, Limburg PC, Kallenberg CGM. Functional defect of circulating regulatory CD4+ T cells in patients with Wegener's granulomatosis in remission. Arthritis Rheum 2007; 56:2080-2091.
31. Lindley S, Dayan C, Bishop A, Roep B, Peakman M, Tree T. Defective suppressor function in CD4+CD25+ T-cells from patients with type 1 diabetes. Diabetes 2005; 54:92-99.
32. Roncarolo M, Bacchetta R, Bordignon C, Narula S, Levings M. Type 1 T regulatory cells. Immunol Rev 2002; 182:68-79.
33. Roncarolo M, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings M. Interleukin 10 secreting type 1 regulatory T cells in rodents and humans. Immunol Rev 2006; 212:28-50.
34. Duddy M, Niino M, Adatia F etal. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol 2007; 178:6092.
35. Mann M, Maresz K, Shriver L, Tan Y, Dittel B. B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol 2007; 178:3447.
36. Mauri C, Feldmann M, Williams R. Down-regulation of Th1-mediated pathology in experimental arthritis by stimulation of the Th2 arm of the immune response. Arthritis Rheum 2003; 48:839-845.
37. van Exel E, Gussekloo J, de Craen A, Frölich M, Bootsma-van der Wiel A, Westendorp R. Low production capacity of interleukin-10 associates with the metabolic syndrome and type 2 diabetes. Diabetes 2002; 51:1088-1092.
38. Hruskova Z, Rihova Z, Mareckova H etal. Intracellular cytokine production in ANCA-associated vasculitis: low levels of interleukin-10 in remission are associated with a higher relapse rate in the long-term follow-up. Arch Med Res 2009; 40:276-284.
39. Bártfai ZGK, Russell KA, Muraközy G, Müller-Quernheim J, Specks U. Different gender-associated genotype risks of Wegener's granulomatosis and microscopic polyangiitis. Clin Immunol 2003; 109:330-337.
40. Wilde B, Thewissen M, Damoiseaux J etal. Regulatory B cells in ANCA-associated vasculitis. Ann Rheum Dis 2013; 72:1416-1419.
41. Todd SK, Pepper RJ, Draibe J etal. Regulatory B cells are numerically but not functionally deficient in anti-neutrophil cytoplasm antibody-associated vasculitis. Rheumatology 2014; 53:1693-1703.
42. Lepse N, Abdulahad WH, Rutgers A, Kallenberg CG, Stegeman CA, Heeringa P. Altered B cell balance, but unaffected B cell capacity to limit monocyte activation in anti-neutrophil cytoplasmic antibody-associated vasculitis in remission. Rheumatology 2014; 53:1683-1692.
43. Lyons PA, Rayner TF, Trivedi S etal. Genetically distinct subsets within ANCA-associated vasculitis. N Engl J Med 2012; 367:214-223.
44. Palanichamy A, Barnard J, Zheng B etal. Novel human transitional B cell populations revealed by B cell depletion therapy. J Immunol 2009; 182:5982-5993.