Unaltered regulatory B-cell frequency and function in patients with multiple sclerosis

Clinical Immunology

Volumn 155, Issue 2, 2014, Pages 198-208

  Michel, Laure ^a,b,c   Chesneau, Melanie ^a,e   Manceau, Philippe ^a   Genty, Athenais ^a   Garcia, Alexandra ^a   Salou, Marion ^a   Elong Ngono, Annie ^a   Pallier, Annaïck ^a,e   Jacq Foucher, Marylène ^b,c   Lefrère, Fabienne ^b,c   Wiertlewski, Sandrine ^b,c   Soulillou, Jean Paul ^a,d,e   Degauque, Nicolas ^a,d,e   Laplaud, David Axel ^a,b,c,d   Brouard, Sophie ^a,d,e  

^a Centre National de la Recherche Scientifique   (France)

^b CHU de Nantes   (France)

^c INSERM   (France)

^d UNIVERSITÉ DE NANTES   (France)

^e NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

B cells; ; Multiple sclerosis; ; Regulation

Indexed keywords

CD19 ANTIGEN; CD24 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; CD40 LIGAND; CD5 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 6; OLIGONUCLEOTIDE; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE; MEMBRANE ANTIGEN;

ADULT; ARTICLE; B LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE STRUCTURE; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; MEMORY CELL; MULTIPLE SCLEROSIS; PATHOPHYSIOLOGY; PHENOTYPE; PRE B LYMPHOCYTE; ADOLESCENT; AGED; BIOSYNTHESIS; CASE CONTROL STUDY; CELL COMMUNICATION; DRUG EFFECTS; FEMALE; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MIDDLE AGED; T LYMPHOCYTE SUBPOPULATION; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIGENS, SURFACE; B-LYMPHOCYTES, REGULATORY; CASE-CONTROL STUDIES; CD40 LIGAND; CELL COMMUNICATION; CYTOKINES; FEMALE; HUMANS; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; OLIGONUCLEOTIDES; PHENOTYPE; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 84908384767     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.09.011     Document Type: Article

References (54)

1. Hohlfeld R., Wekerle H. Autoimmune concepts of multiple sclerosis as a basis for selective immunotherapy: from pipe dreams to (therapeutic) pipelines. Proc. Natl. Acad. Sci. U. S. A. Oct 5 2004, 101(Suppl. 2):14599-14606.
2. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
3. Elong Ngono A.P.S., Salou M., Bahbouhi B., Soulillou J.-P., Brouard S., Laplaud D.-A. Frequency of circulating autoreactive T cells committed to myelin determinants in relapsing-remitting multiple sclerosis patients. Clin. Immunol. 2012, 144(2):117-126.
4. Bahbouhi B., Pettre S., Berthelot L., Garcia A., Elong Ngono A., Degauque N., et al. T cell recognition of self-antigen presenting cells by protein transfer assay reveals a high frequency of anti-myelin T cells in multiple sclerosis. Brain Jun 2010, 133(Pt 6):1622-1636.
5. Berthelot L., Laplaud D.A., Pettre S., Ballet C., Michel L., Hillion S., et al. Blood CD8+ T cell responses against myelin determinants in multiple sclerosis and healthy individuals. Eur. J. Immunol. Jul 2008, 38(7):1889-1899.
6. Chou Y.K., Bourdette D.N., Offner H., Whitham R., Wang R.Y., Hashim G.A., et al. Frequency of T cells specific for myelin basic protein and myelin proteolipid protein in blood and cerebrospinal fluid in multiple sclerosis. J. Neuroimmunol. May 1992, 38(1-2):105-113.
7. Crawford M.P., Yan S.X., Ortega S.B., Mehta R.S., Hewitt R.E., Price D.A., et al. High prevalence of autoreactive, neuroantigen-specific CD8+ T cells in multiple sclerosis revealed by novel flow cytometric assay. Blood Jun 1 2004, 103(11):4222-4231.
8. Hellings N., Baree M., Verhoeven C., D'Hooghe M.B., Medaer R., Bernard C.C., et al. T-cell reactivity to multiple myelin antigens in multiple sclerosis patients and healthy controls. J. Neurosci. Res. Feb 1 2001, 63(3):290-302.
9. Hong J., Zang Y.C., Li S., Rivera V.M., Zhang J.Z. Ex vivo detection of myelin basic protein-reactive T cells in multiple sclerosis and controls using specific TCR oligonucleotide probes. Eur. J. Immunol. Mar 2004, 34(3):870-881.
10. Jingwu Z., Medaer R., Hashim G.A., Chin Y., van den Berg-Loonen E., Raus J.C. Myelin basic protein-specific T lymphocytes in multiple sclerosis and controls: precursor frequency, fine specificity, and cytotoxicity. Ann. Neurol. Sep 1992, 32(3):330-338.
11. Martin R., Jaraquemada D., Flerlage M., Richert J., Whitaker J., Long E.O., et al. Fine specificity and HLA restriction of myelin basic protein-specific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals. J. Immunol. Jul 15 1990, 145(2):540-548.
12. Moldovan I.R., Rudick R.A., Cotleur A.C., Born S.E., Lee J.C., Karafa M.T., et al. Interferon gamma responses to myelin peptides in multiple sclerosis correlate with a new clinical measure of disease progression. J. Neuroimmunol. Aug 2003, 141(1-2):132-140.
13. Olsson T., Sun J., Hillert J., Hojeberg B., Ekre H.P., Andersson G., et al. Increased numbers of T cells recognizing multiple myelin basic protein epitopes in multiple sclerosis. Eur. J. Immunol. Apr 1992, 22(4):1083-1087.
14. Olsson T., Zhi W.W., Hojeberg B., Kostulas V., Jiang Y.P., Anderson G., et al. Autoreactive T lymphocytes in multiple sclerosis determined by antigen-induced secretion of interferon-gamma. J. Clin. Invest. Sep 1990, 86(3):981-985.
15. Ota K., Matsui M., Milford E.L., Mackin G.A., Weiner H.L., Hafler D.A. T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis. Nature Jul 12 1990, 346(6280):183-187.
16. Pender M.P., Csurhes P.A., Greer J.M., Mowat P.D., Henderson R.D., Cameron K.D., et al. Surges of increased T cell reactivity to an encephalitogenic region of myelin proteolipid protein occur more often in patients with multiple sclerosis than in healthy subjects. J. Immunol. Nov 1 2000, 165(9):5322-5331.
17. Pette M., Fujita K., Wilkinson D., Altmann D.M., Trowsdale J., Giegerich G., et al. Myelin autoreactivity in multiple sclerosis: recognition of myelin basic protein in the context of HLA-DR2 products by T lymphocytes of multiple-sclerosis patients and healthy donors. Proc. Natl. Acad. Sci. U. S. A. Oct 1990, 87(20):7968-7972.
18. Wallstrom E., Khademi M., Andersson M., Weissert R., Linington C., Olsson T. Increased reactivity to myelin oligodendrocyte glycoprotein peptides and epitope mapping in HLA DR2(15)+multiple sclerosis. Eur. J. Immunol. Oct 1998, 28(10):3329-3335.
19. Zhang J., Markovic-Plese S., Lacet B., Raus J., Weiner H.L., Hafler D.A. Increased frequency of interleukin 2-responsive T cells specific for myelin basic protein and proteolipid protein in peripheral blood and cerebrospinal fluid of patients with multiple sclerosis. J. Exp. Med. Mar 1 1994, 179(3):973-984.
20. Zhang J., Weiner H.L., Hafler D.A. Autoreactive T cells in multiple sclerosis. Int. Rev. Immunol. 1992, 9(3):183-201.
21. Serafini B., Rosicarelli B., Magliozzi R., Stigliano E., Aloisi F. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. Apr 2004, 14(2):164-174.
22. Magliozzi R., Howell O., Vora A., Serafini B., Nicholas R., Puopolo M., et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain Apr 2007, 130(Pt 4):1089-1104.
23. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. Feb 14 2008, 358(7):676-688.
24. Kappos L., Li D., Calabresi P.A., O'Connor P., Bar-Or A., Barkhof F., et al. Ocrelizumab in relapsing-remitting multiple sclerosis: a phase 2, randomised, placebo-controlled, multicentre trial. Lancet Nov 19 2011, 378(9805):1779-1787.
25. Duddy M., Niino M., Adatia F., Hebert S., Freedman M., Atkins H., et al. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. May 15 2007, 178(10):6092-6099.
26. Mauri C., Bosma A. Immune regulatory function of B cells. Annu. Rev. Immunol. 2012, 30:221-241.
27. Wolf S.D., Dittel B.N., Hardardottir F., Janeway C.A. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. Dec 1 1996, 184(6):2271-2278.
28. Fillatreau S., Sweenie C.H., McGeachy M.J., Gray D., Anderton S.M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. Oct 2002, 3(10):944-950.
29. Tian J., Zekzer D., Hanssen L., Lu Y., Olcott A., Kaufman D.L. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J. Immunol. Jul 15 2001, 167(2):1081-1089.
30. Hagn M., Sontheimer K., Dahlke K., Brueggemann S., Kaltenmeier C., Beyer T., et al. Human B cells differentiate into granzyme B-secreting cytotoxic B lymphocytes upon incomplete T-cell help. Immunol. Cell Biol. Apr 2012, 90(4):457-467.
31. Mann M.K., Maresz K., Shriver L.P., Tan Y., Dittel B.N. B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol. Mar 15 2007, 178(6):3447-3456.
32. Mizoguchi E., Mizoguchi A., Preffer F.I., Bhan A.K. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int. Immunol. May 2000, 12(5):597-605.
33. Correale J., Farez M., Razzitte G. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. Aug 2008, 64(2):187-199.
34. Knippenberg S., Peelen E., Smolders J., Thewissen M., Menheere P., Cohen Tervaert J.W., et al. Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J. Neuroimmunol. Oct 28 2011, 239(1-2):80-86.
35. Iwata Y., Matsushita T., Horikawa M., Dilillo D.J., Yanaba K., Venturi G.M., et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood Jan 13 2011, 117(2):530-541.
36. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.P., Kappos L., et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the "McDonald Criteria". Ann. Neurol. Dec 2005, 58(6):840-846.
37. Carsetti R., Rosado M.M., Wardmann H. Peripheral development of B cells in mouse and man. Immunol. Rev. Feb 2004, 197:179-191.
38. Yanaba K., Bouaziz J.D., Haas K.M., Poe J.C., Fujimoto M., Tedder T.F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity May 2008, 28(5):639-650.
39. Lowther D.E., Hafler D.A. Regulatory T cells in the central nervous system. Immunol. Rev. Jul 2012, 248(1):156-169.
40. Mauri C., Gray D., Mushtaq N., Londei M. Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. Feb 17 2003, 197(4):489-501.
41. Evans J.G., Chavez-Rueda K.A., Eddaoudi A., Meyer-Bahlburg A., Rawlings D.J., Ehrenstein M.R., et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. Jun 15 2007, 178(12):7868-7878.
42. Matsushita T., Yanaba K., Bouaziz J.D., Fujimoto M., Tedder T.F. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. Oct 2008, 118(10):3420-3430.
43. Bar-Or A., Fawaz L., Fan B., Darlington P.J., Rieger A., Ghorayeb C., et al. Abnormal B-cell cytokine responses a trigger of T-cell-mediated disease in MS?. Ann. Neurol. Apr 2010, 67(4):452-461.
44. Niino M., Hirotani M., Miyazaki Y., Sasaki H. Memory and naive B-cell subsets in patients with multiple sclerosis. Neurosci. Lett. Oct 16 2009, 464(1):74-78.
45. Blair P.A., Norena L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., 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 Jan 29 2010, 32(1):129-140.
46. Bouaziz J.D., Calbo S., Maho-Vaillant M., Saussine A., Bagot M., Bensussan A., et al. IL-10 produced by activated human B cells regulates CD4(+) T-cell activation in vitro. Eur. J. Immunol. Oct 2010, 40(10):2686-2691.
47. Lemoine S., Morva A., Youinou P., Jamin C. Human T cells induce their own regulation through activation of B cells. J. Autoimmun. May 2011, 36(3-4):228-238.
48. Niimi M., Hara M., Witzke O., Morris P.J., Wood K.J. Donor resting B cells induce indefinite prolongation of fully allogeneic cardiac grafts when delivered with anti-immunoglobulin-D monoclonal antibody: evidence for tolerogenicity of donor resting B cells in vivo. Transplantation Dec 27 1998, 66(12):1786-1792.
49. Lassila O., Vainio O., Matzinger P. Can B cells turn on virgin T cells?. Nature Jul 21 1988, 334(6179):253-255.
50. Korn T., Reddy J., Gao W., Bettelli E., Awasthi A., Petersen T.R., et al. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. Apr 2007, 13(4):423-431.
51. Tzartos J.S., Friese M.A., Craner M.J., Palace J., Newcombe J., Esiri M.M., et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. Jan 2008, 172(1):146-155.
52. Fritzsching B., Haas J., Konig F., Kunz P., Fritzsching E., Poschl J., et al. Intracerebral human regulatory T cells: analysis of CD4+ CD25+ FOXP3+ T cells in brain lesions and cerebrospinal fluid of multiple sclerosis patients. PLoS One 2011, 6(3):e17988.
53. von Budingen H.C., Harrer M.D., Kuenzle S., Meier M., Goebels N. Clonally expanded plasma cells in the cerebrospinal fluid of MS patients produce myelin-specific antibodies. Eur. J. Immunol. Jul 2008, 38(7):2014-2023.
54. Lambracht-Washington D., O'Connor K.C., Cameron E.M., Jowdry A., Ward E.S., Frohman E., et al. Antigen specificity of clonally expanded and receptor edited cerebrospinal fluid B cells from patients with relapsing remitting MS. J. Neuroimmunol. May 2007, 186(1-2):164-176.