Central nervous system infiltrates are characterized by features of ongoing B cell-related immune activity in MP4-induced experimental autoimmune encephalomyelitis

Clinical Immunology

Volumn 158, Issue 1, 2015, Pages 47-58

  Batoulis, Helena ^a   Wunsch, Marie ^b   Birkenheier, Johannes ^a   Rottlaender, Andrea ^b   Gorboulev, Valentin ^b   Kuerten, Stefanie ^b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

B cells; EAE; Epitope spreading; MS; TLO

Indexed keywords

AUTOANTIGEN; CD5 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; CXCL13 CHEMOKINE; EPITOPE; HYBRID PROTEIN; IMMUNOGLOBULIN M; INTERLEUKIN 10; LEUKOSIALIN; MYELIN BASIC PROTEIN; MYELIN BASIC PROTEIN PROTEOLIPID PROTEIN FUSION PROTEIN; PROTEOLIPID PROTEIN; UNCLASSIFIED DRUG; CXCL13 PROTEIN, MOUSE; MEMBRANE METALLOENDOPEPTIDASE; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL AGGREGATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; IMMUNE RESPONSE; LYMPHOCYTIC INFILTRATION; MOUSE; MULTIPLE SCLEROSIS; MYCOBACTERIUM TUBERCULOSIS; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PYROSEQUENCING; SOMATIC HYPERMUTATION; TH17 CELL; ANIMAL; DISEASE MODEL; IMMUNOLOGY; METABOLISM; MYELIN SHEATH; SPLEEN;

ANIMALS; AUTOANTIGENS; B-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CHEMOKINE CXCL13; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; MICE; MULTIPLE SCLEROSIS; MYELIN BASIC PROTEIN; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; NEPRILYSIN; RNA, MESSENGER; SPLEEN;

EID: 84928343293     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.03.009     Document Type: Article

References (68)

1. Sospedra M., Martin R. Immunology of MS. Annu. Rev. Immunol. 2005, 23:683-747.
2. Baranzini S.E., Jeong M.C., Butunoi C., Murray R.S., Bernard C.C., Oksenberg J.R. B cell repertoire diversity and clonal expansion in MS brain lesions. J. Immunol. 1999, 165:5133-5144.
3. Owens G.P., Kraus H., Burgoon M.P., Smith-Jensen T., Devlin M.E., Gilden D.H. Restricted use of VH4 germline segments in an acute MS brain. Ann. Neurol. 1998, 43:236-243.
4. Owens G.P., Winges K.M., Ritchie A.M., Edwards S., Burgoon M.P., Lehnhoff L., Nielsen K., Corboy J., Gilden D.H., Bennett J.L. VH4 gene segments dominate the intrathecal humoral immune response in MS. J. Immunol. 2007, 179:6343-6351.
5. Corcione A., Casazza S., Ferretti E., Giunti D., Zappia E., Pistorio A., Gambini C., Mancardi G.L., Uccelli A., Pistoia V. Recapitulation of B cell differentiation in the central nervous system of patients with MS. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11064-11069.
6. Lucchinetti C., Brück W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of MS lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 2000, 47:707-717.
7. Carragher D.M., Rangel-Moreno J., Randall T.D. Ectopic lymphoid tissues and local immunity. Semin. Immunol. 2008, 20:26-42.
8. Howell O.W., Reeves C.A., Nicholas R., Carassiti D., Radotra B., Gentleman S.M., Serafini B., Aloisi F., Roncaroli F., Magliozzi R., Reynolds R. Meningeal inflammation is widespread and linked to cortical pathology in MS. Brain 2011, 134:2755-2771.
9. Magliozzi R., Howell O., Vora A., Serafini B., Nicholas R., Puopolo M., Reynolds R., Aloisi F. Meningeal B-cell follicles in secondary progressive MS associate with early onset of disease and severe cortical pathology. Brain 2007, 130:1089-1104.
10. 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 MS. Brain Pathol. 2004, 14:164-174.
11. Kooi E.J., Geurts J.J., van Horssen J., Bø L., van der Valk P. Meningeal inflammation is not associated with cortical demyelination in chronic MS. J. Neuropathol. Exp. Neurol. 2009, 68:1021-1028.
12. Torkildsen Ø., Stansberg C., Angelskår S.M., Kooi E.J., Geurts J.J., van der Valk P., Myhr K.M., Steen V.M., Bø L. Upregulation of immunoglobulin-related genes in cortical sections from MS patients. Brain Pathol. 2010, 20:720-729.
13. Kuerten S., Angelov D.N. Comparing the CNS morphology and immunobiology of different EAE models in C57BL/6 mice - a step towards understanding the complexity of MS. Ann. Anat. 2008, 190:1-15.
14. Kuerten S., Lichtenegger F.S., Faas S., Angelov D.N., Tary-Lehmann M., Lehmann P.V. MBP-PLP fusion protein-induced EAE in C57BL/6 mice. J. Neuroimmunol. 2006, 177:99-111.
15. Kuerten S., Javeri S., Tary-Lehmann M., Lehmann P.V., Angelov D.N. Fundamental differences in the dynamics of CNS lesion development and composition in MP4- and MOG peptide 35-55-induced experimental autoimmune encephalomyelitis. Clin. Immunol. 2008, 129:256-267.
16. Kuerten S., Pauly R., Rottlaender A., Rodi M., Gruppe T.L., Addicks K., Tary-Lehmann M., Lehmann P.V. Myelin-reactive antibodies mediate the pathology of MBP-PLP fusion protein MP4-induced EAE. Clin. Immunol. 2011, 140:54-62.
17. Hundgeburth L.C., Wunsch M., Rovituso D., Recks M.S., Addicks K., Lehmann P.V., Kuerten S. The complement system contributes to the pathology of experimental autoimmune encephalomyelitis by triggering demyelination and modifying the antigen-specific T and B cell response. Clin. Immunol. 2013, 155-164.
18. Kuerten S., Schickel A., Kerkloh C., Recks M.S., Addicks K., Ruddle N.H., Lehmann P.V. Tertiary lymphoid organ development coincides with determinant spreading of the myelin-specific T cell response. Acta Neuropathol. 2012, 124:861-873.
19. White H.N. Restriction-PCR fingerprinting of the immunoglobulin VH repertoire: direct detection of an immune response and global analysis of B cell clonality. Eur. J. Immunol. 1998, 28:3268-3279.
20. Lefranc M.P., Giudicelli V., Ginestoux C., Jabado-Michaloud J., Folch G., Bellahcene F., Wu Y., Gemrot E., Brochet X., Lane J., Regnier L., Ehrenmann F., Lefranc G., Duroux P. IMGT, The International ImMunoGeneTics Information System. Nucleic Acids Res. 2009, 37:D1006-D1012.
21. Rogosch T., Kerzel S., Hoi K.H., Zhang Z., Maier R.F., Ippolito G.C., Zemlin M. Immunoglobulin Analysis Tool: a novel tool for the analysis of human and mouse heavy and light chain transcripts. Front. Immunol. 2012, 3:176.
22. Dogan A., Bagdi E., Munson P., Isaacson P.G. CD10 and BCL-6 expression in paraffin sections of normal lymphoid tissue and B-cell lymphomas. Am. J. Surg. Pathol. 2000, 24:846-852.
23. Baumgarth N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 2011, 11:34-46.
24. Tørring C., Petersen C.C., Bjerg L., Kofod-Olsen E., Petersen T., Höllsberg P. The B1-cell subpopulation is diminished in patients with relapsing-remitting multiple sclerosis. J. Neuroimmunol. 2013, 262:92-99.
25. Rovituso D., Heller S., Schroeter M., Kleinschnitz C., Kuerten S. B1 cells are unaffected by immune modulatory treatment in remitting-relapsing multiple sclerosis patients. J. Neuroimmunol. 2014, 272:86-90.
26. Griffin D.O., Rothstein T.L. A small CD11b+ human B1 cell subpopulation stimulates T cells and is expanded in lupus. J. Exp. Med. 2011, 208:2591-2598.
27. Manis J.P., Tian M., Alt F.W. Mechanism and control of class-switch recombination. Trends Immunol. 2002, 23:31-39.
28. Stavnezer J. Immunoglobulin class switching. Curr. Opin. Immunol. 1996, 8:199-205.
29. Stavnezer J. Molecular processes that regulate class switching. Curr. Top. Microbiol. Immunol. 2000, 245:127-168.
30. Suto A., Nakajima H., Hirose K., Suzuki K., Kagami S., Seto Y., Hoshimoto A., Saito Y., Foster D.C., Iwamoto I. Interleukin 21 prevents antigen-induced IgE production by inhibiting germ line C(epsilon) transcription of IL-4-stimulated B cells. Blood 2002, 100:4565-4573.
31. Mitsdoerffer M., Lee Y., Jäger A., Kim H.J., Korn T., Kolls J.K., Cantor H., Bettelli E., Kuchroo V.K. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14292-14297.
32. Peng S.L., Szabo S.J., Glimcher L.H. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5545-5550.
33. Snapper C.M., Peschel C., Paul W.E. IFN-gamma stimulates IgG2a secretion by murine B cells stimulated with bacterial lipopolysaccharide. J. Immunol. 1998, 140:2121-2127.
34. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374-1377.
35. Wu T.T., Johnson G., Kabat E.A. Length distribution of CDRH3 in antibodies. Proteins 1993, 16:1-7.
36. Drayton D.L., Liao S., Mounzer R.H., Ruddle N.H. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 2006, 7:344-353.
37. Peters A., Pitcher L.A., Sullivan J.M., Mitsdoerffer M., Acton S.E., Franz B., Wucherpfennig K., Turley S., Carroll M.C., Sobel R.A., Bettelli E., Kuchroo V.K. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 2011, 35:986-996.
38. Rangel-Moreno J., Carragher D.M., de la Luz Garcia-Hernandez M., Hwang J.Y., Kusser K., Hartson L., Kolls J.K., Khader S.A., Randall T.D. The development of inducible bronchus associated lymphoid tissue depends on IL-17. Nat. Immunol. 2011, 12:639-646.
39. Grogan J.L., Ouyang W. A role for Th17 cells in the regulation of tertiary lymphoid follicles. Eur. J. Immunol. 2012, 42:2255-2262.
40. Gommerman J.L., Browning J.L. Lymphotoxin/light, lymphoid microenvironments and autoimmune disease. Nat. Rev. Immunol. 2003, 3:642-655.
41. Jeong H.D., Komisar J.L., Kraig E., Teale J.M. Strain-dependent expression of VH gene families. J. Immunol. 1998, 140:2436-2441.
42. Sheehan K.M., Brodeur P.H. Molecular cloning of the primary IgH repertoire: a quantitative analysis of VH gene usage in adult mice. EMBO J. 1989, 8:2313-2320.
43. Viale A.C., Coutinho A., Freitas A.A. Differential expression of VH gene families in peripheral B cell repertoires of newborn or adult immunoglobulin H chain congenic mice. J. Exp. Med. 1992, 175:1449-1456.
44. Ivanov I.I., Schelonka R.L., Zhuang Y., Gartland G.L., Zemlin M., Schroeder HW H.W. Development of the expressed Ig CDR-H3 repertoire is marked by focusing of constraints in length, amino acid use, and charge that are first established in early B cell progenitors. J. Immunol. 2005, 174:7773-7780.
45. Khass M., Buckley K., Kapoor P., Schelonka R.L., Watkins L.S., Zhuang Y., Schroeder H.W. Recirculating bone marrow B cells in C57BL/6 mice are more tolerant of highly hydrophobic and highly charged CDR-H3s than those in BALB/c mice. Eur. J. Immunol. 2013, 43:629-640.
46. Zemlin M., Klinger M., Link J., Zemlin C., Bauer K., Engler J.A., Schroeder H.W., Kirkham P.M. Expressed murine and human CDR-H3 intervals of equal length exhibit distinct repertoires that differ in their amino acid composition and predicted range of structures. J. Mol. Biol. 2003, 334:733-749.
47. Qin Y., Duquette P., Zhang Y., Talbot P., Poole R., Antel J. Clonal expansion and somatic hypermutation of V(H) genes of B cells from cerebrospinal fluid in MS. J. Clin. Invest. 1998, 102:1045-1050.
48. Targoni O.S., Baus J., Hofstetter H.H., Hesse M.D., Karulin A.Y., Boehm B.O., Forsthuber T.G., Lehmann P.V. Frequencies of neuroantigen-specific T cells in the central nervous system versus the immune periphery during the course of experimental allergic encephalomyelitis. J. Immunol. 2001, 166:4757-4764.
49. Cserr H., Knopf P.M. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunol. Today 1992, 13:507-512.
50. Weller R.O., Engelhardt B., Philipps M.J. Lymphocyte targeting of the central nervous system: a review of afferent and efferent CNS-immune pathways. Brain Pathol. 1996, 6:275-288.
51. Kuerten S., Kostova-Bales D.A., Frenzel L.P., Tigno J.T., Tary-Lehmann M., Angelov D.N., Lehmann P.V. MP4- and MOG:35-55-induced EAE in C57BL/6 mice differentially targets brain, spinal cord and cerebellum. J. Neuroimmunol. 2007, 189:31-40.
52. Bourquin C., Schubart A., Tobollik S., Mather I., Ogg S., Liblau R., Linington C. Selective unresponsiveness to conformational B cell epitopes of the myelin oligodendrocyte glycoprotein in H-2b mice. J. Immunol. 2003, 171:455-461.
53. Stubbs E.B., Lawlor M.W., Richards M.P., Siddiqui K., Fisher M.A., Bhoopalam N., Siegel G.J. Anti-neurofilament antibodies in neuropathy with monoclonal gammopathy of undetermined significance produce experimental motor nerve conduction block. Acta Neuropathol. 2003, 105:109-116.
54. Bjartmar C., Yin X., Trapp B.D. Axonal pathology in myelin disorders. J. Neurocytol. 1999, 28:383-395.
55. Ehling R., Lutterotti A., Wanschitz J., Khalil M., Gneiss C., Deisenhammer F., Reindl M., Berger T. Increased frequencies of serum antibodies to neurofilament light in patients with primary chronic progressive MS. Mult. Scler. 2004, 10:601-606.
56. Eikelenboom M.J., Petzold A., Lazeron R.H., Silber E., Sharief M., Thompson E.J., Barkhof F., Giovannoni G., Polman C.H., Uitdehaag B.M. MS: neurofilament light chain antibodies are correlated to cerebral atrophy. Neurology 2003, 60:219-223.
57. Silber E., Semra Y.K., Gregson N.A., Sharief M.K. Patients with progressive MS have elevated antibodies to neurofilament subunit. Neurology 2002, 58:1372-1381.
58. Constant S.L. B lymphocytes as antigen-presenting cells for CD4+ T cell priming in vivo. J. Immunol. 1999, 162:5695-5703.
59. De Simone R., Giampaolo A., Giometto B., Gallo P., Levi G., Peschle C., Aloisi F. The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J. Neuropathol. Exp. Neurol. 1995, 54:175-187.
60. Windhagen A., Newcombe J., Dangond F., Strand C., Woodroofe M.N., Cuzner M.L., Hafler D.A. Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J. Exp. Med. 1995, 182:985-996.
61. Hayakawa K., Hardy R.R., Parks D.R., Herzenberg L.A. The Ly-1 B cell subpopulation in normal immunodefective, and autoimmune mice. J. Exp. Med. 1983, 157:202-218.
62. Mizoguchi A., Mizoguchi E., Takedatsu H., Blumberg R.S., Bhan A.K. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002, 16:219-230.
63. Fujio K., Okamura T., Yamamoto K. The family of IL-10-secreting CD4+ T cells. Adv. Immunol. 2010, 105:99-130.
64. McCoy K.D., Stoel M., Stettler R., Merky P., Fink K., Senn B.M., Schaer C., Massacand J., Odermatt B., Oettgen H.C., Zinkernagel R.M., Bos N.A., Hengartner H., Macpherson A.J., Harris N.L. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 2008, 4:362-373.
65. Toellner K.M., Luther S.A., Sze D.M., Choy R.K., Taylor D.R., MacLennan I.C., Acha-Orbea H. T helper 1 (Th1) and Th2 characteristics start to develop during T cell priming and are associated with an immediate ability to induce immunoglobulin class switching. J. Exp. Med. 1998, 187:1193-1204.
66. Pinaud E., Khamlichi A.A., Le Morvan C., Drouet M., Nalesso V., Le Bert M., Cogné M. Localization of the 3' IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 2001, 15:187-199.
67. 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, 102:553-563.
68. Handa P., Tupper J.C., Jordan K.C., Harlan J.M. FLIP (Flice-like inhibitory protein) suppresses cytoplasmic double-stranded-RNA-induced apoptosis and NF-κB and IRF3-mediated signalling. Cell. Commun. Signal. 2011, 9:16.