Central role of interferon-beta in thymic events leading to myasthenia gravis

Journal of Autoimmunity

Volumn 52, Issue , 2014, Pages 44-52

  Cufi, Perrine ^a,b,c,d   Dragin, Nadine ^a,b,c,d   Ruhlmann, Nathalie ^a,b,c   Weiss, Julia Miriam ^a,b,c,d   Fadel, Elie ^e   Serraf, Alain ^e,f   Berrih Aknin, Sonia ^a,b,c,d   Le Panse, Rozen ^a,b,c,d  

^a Sorbonne Université   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d AIM   (France)

^e CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^f Jacques Cartier Hospital   (France)

Author keywords

Chemokines; Germinal centers; Glucocorticoids; Interferon; Thymus; Virus

Indexed keywords

ALPHA2 INTERFERON; B CELL ACTIVATING FACTOR; BETA INTERFERON; CXCL13 CHEMOKINE; GLUCOCORTICOID; INTERFERON RECEPTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; CHOLINERGIC RECEPTOR ANTIBODY; CHOLINESTERASE INHIBITOR; INTERFERON; INTERFERON III; INTERLEUKIN 28A; INTERLEUKIN 28B; INTERLEUKIN 29; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; CHOLINERGIC RECEPTOR; POLYINOSINIC POLYCYTIDYLIC ACID; TNFSF13B PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; ENDOTHELIUM CELL; EPITHELIUM CELL; FEMALE; GENE OVEREXPRESSION; GERMINAL CENTER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYASTHENIA GRAVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ADULT; ANIMAL CELL; AUTOIMMUNITY; B LYMPHOCYTE; CELL CULTURE; CELL DEATH; CELL VIABILITY; CORTICOSTEROID THERAPY; HYPERPLASIA; LYMPHATIC ENDOTHELIAL CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; THYMIC EPITHELIAL CELL; THYMUS; THYMUS HYPERPLASIA; UPREGULATION; ADOLESCENT; ANIMAL; APOPTOSIS; C57BL MOUSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFANT; KNOCKOUT MOUSE; MALE; METABOLISM; NEWBORN; PATHOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; APOPTOSIS; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CELLS, CULTURED; CHEMOKINE CCL21; CHEMOKINE CXCL13; CHILD, PRESCHOOL; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; GERMINAL CENTER; HUMANS; HYPERPLASIA; INFANT; INFANT, NEWBORN; INTERFERON-BETA; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYASTHENIA GRAVIS; POLY I-C; RECEPTOR, INTERFERON ALPHA-BETA; RECEPTORS, CHOLINERGIC; THYMUS GLAND; YOUNG ADULT;

EID: 84904369154     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2013.12.016     Document Type: Article

References (54)

1. Meriggioli M.N. Myasthenia gravis with anti-acetylcholine receptor antibodies. Front Neurol Neurosci 2009, 26:94-108.
2. Vrolix K., Fraussen J., Molenaar P.C., Losen M., Somers V., Stinissen P., et al. The auto-antigen repertoire in myasthenia gravis. Autoimmunity 2010, 43:380-400.
3. Weiss J.M., Cufi P., Bismuth J., Eymard B., Fadel E., Berrih-Aknin S., et al. SDF-1/CXCL12 recruits B cells and antigen-presenting cells to the thymus of autoimmune myasthenia gravis patients. Immunobiology 2013, 218:373-381.
4. Le Panse R., Bismuth J., Cizeron-Clairac G., Weiss J.M., Cufi P., Dartevelle P., et al. Thymic remodeling associated with hyperplasia in myasthenia gravis. Autoimmunity 2010, 43:1-12.
5. Wakkach A., Guyon T., Bruand C., Tzartos S., Cohen-Kaminsky S., Berrih-Aknin S. Expression of acetylcholine receptor genes in human thymic epithelial cells: implications for myasthenia gravis. JImmunol 1996, 157:3752-3760.
6. Melms A., Schalke B.C., Kirchner T., Muller-Hermelink H.K., Albert E., Wekerle H. Thymus in myasthenia gravis. Isolation of T-lymphocyte lines specific for the nicotinic acetylcholine receptor from thymuses of myasthenic patients. JClin Invest 1988, 81:902-908.
7. Safar D., Berrih-Aknin S., Morel E. Invitro anti-acetylcholine receptor antibody synthesis by myasthenia gravis patient lymphocytes: correlations with thymic histology and thymic epithelial-cell interactions. JClin Immunol 1987, 7:225-234.
8. Leprince C., Cohen-Kaminsky S., Berrih-Aknin S., Vernet-Der Garabedian B., Treton D., Galanaud P., et al. Thymic B cells from myasthenia gravis patients are activated B cells. Phenotypic and functional analysis. JImmunol 1990, 145:2115-2122.
9. Savino W. The thymus is a common target organ in infectious diseases. PLoS Path 2006, 2:e62.
10. Le Panse R., Cizeron-Clairac G., Bismuth J., Berrih Aknin S. Microarrays reveal distinct gene signatures in the thymus of seropositive and seronegative Myasthenia Gravis patients and the role of CCL21 in thymic hyperplasia. JImmunol 2006, 177:7868-7879.
11. Cavalcante P., Barberis M., Cannone M., Baggi F., Antozzi C., Maggi L., et al. Detection of poliovirus-infected macrophages in thymus of patients with myasthenia gravis. Neurology 2010, 74:1118-1126.
12. Cavalcante P., Serafini B., Rosicarelli B., Maggi L., Barberis M., Antozzi C., et al. Epstein-Barr virus persistence and reactivation in myasthenia gravis thymus. Ann Neurol 2010, 67:726-738.
13. Cufi P., Dragin N., Weiss J.M., Martinez-Martinez P., De Baets M.H., Roussin R., et al. Implication of double-stranded RNA signaling in the etiology of autoimmune myasthenia gravis. Ann Neurol 2013, 73:281-293.
14. Piccolo G., Franciotta D., Versino M., Alfonsi E., Lombardi M., Poma G. Myasthenia gravis in a patient with chronic active hepatitis C during interferon-alpha treatment. JNeurol Neurosurg Psychiatr 1996, 60:348.
15. Mase G., Zorzon M., Biasutti E., Vitrani B., Cazzato G., Urban F., et al. Development of myasthenia gravis during interferon-alpha treatment for anti-HCV positive chronic hepatitis. JNeurol Neurosurg Psychiatry 1996, 60:348-349.
16. Dionisiotis J., Zoukos Y., Thomaides T. Development of myasthenia gravis in two patients with multiple sclerosis following interferon beta treatment. JNeurol Neurosurg Psychiatry 2004, 75:1079.
17. Batocchi A.P., Evoli A., Servidei S., Palmisani M.T., Apollo F., Tonali P. Myasthenia gravis during interferon alfa therapy. Neurology 1995, 45:382-383.
18. Poëa-Guyon S., Christadoss P., Le Panse R., Guyon T., De Baets M., Wakkach A., et al. Effects of cytokines on acetylcholine receptor expression: implications for myasthenia gravis. JImmunol 2005, 174:5941-5949.
19. Le Panse R., Cizeron-Clairac G., Cuvelier M., Truffault F., Bismuth J., Nancy P., et al. Regulatory and pathogenic mechanisms in human autoimmune myasthenia gravis. Ann N Y Acad Sci 2008, 1132:135-142.
20. Meager A., Wadhwa M., Dilger P., Bird C., Thorpe R., Newsom-Davis J., et al. Anti-cytokine autoantibodies in autoimmunity: preponderance of neutralizing autoantibodies against interferon-alpha, interferon-omega and interleukin-12 in patients with thymoma and/or myasthenia gravis. Clin Exp Immunol 2003, 132:128-136.
21. Meloni A., Furcas M., Cetani F., Marcocci C., Falorni A., Perniola R., et al. Autoantibodies against type I interferons as an additional diagnostic criterion for autoimmune polyendocrine syndrome type I. JClin Endocrinol Metab 2008, 93:4389-4397.
22. Cufi P., Soussan P., Truffault F., Fetouchi R., Fadel E., Berrih-Aknin S., et al. Thymoma-associated Myasthenia Gravis: on the search for a pathogen signature. JAutoimmun 2014, 52:29-35.
23. Pestka S., Krause C.D., Walter M.R. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 2004, 202:8-32.
24. Banchereau J., Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006, 25:383-392.
25. Levy D.E., Marie I.J., Durbin J.E. Induction and function of type I and III interferon in response to viral infection. Current opinion in virology 2011, 1:476-486.
26. Sommereyns C., Paul S., Staeheli P., Michiels T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells invivo. PLoS Path 2008, 4:e1000017.
27. Zahn S., Rehkamper C., Kummerer B.M., Ferring-Schmidt S., Bieber T., Tuting T., et al. Evidence for a pathophysiological role of keratinocyte-derived type III interferon (IFNλ) in cutaneous lupus erythematosus. JInvest Dermatol 2011, 131:133-140.
28. Méraouna A., Cizeron-Clairac G., Le Panse R., Bismuth J., Truffault F., Talaksen C., et al. The chemokine CXCL13 is a key molecule in autoimmune Myasthenia Gravis. Blood 2006, 108:432-440.
29. Berrih-Aknin S., Ruhlmann N., Bismuth J., Cizeron-Clairac G., Zelman E., Shachar I., et al. CCL21 overexpressed on lymphatic vessels drives thymic hyperplasia in Myasthenia. Ann Neurol 2009, 66:521-531.
30. Cizeron-Clairac G., Le Panse R., Frenkian-Cuvelier M., Meraouna A., Truffault F., Bismuth J., et al. Thymus and Myasthenia Gravis: what can we learn from DNA microarrays?. JNeuroimmunol 2008, 201-202:57-63.
31. Honda K., Sakaguchi S., Nakajima C., Watanabe A., Yanai H., Matsumoto M., et al. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc Natl Acad Sci U S A 2003, 100:10872-10877.
32. Fujii Y., Monden Y., Hashimoto J., Nakahara K., Kawashima Y. Acetylcholine receptor antibody-producing cells in thymus and lymph nodes in myasthenia gravis. Clin Immunol Immunopathol 1985, 34:141-146.
33. Kalled S.L. Impact of the BAFF/BR3 axis on B cell survival, germinal center maintenance and antibody production. Semin Immunol 2006, 18:290-296.
34. Thangarajh M., Masterman T., Helgeland L., Rot U., Jonsson M.V., Eide G.E., et al. The thymus is a source of B-cell-survival factors-APRIL and BAFF-in myasthenia gravis. JNeuroimmunol 2006, 178:161-166.
35. Sakamoto S., Qin J., Navarro A., Gamero A., Potla R., Yi T., et al. Cells previously desensitized to type 1 interferons display different mechanisms of activation of stat-dependent gene expression from naive cells. JBiol Chem 2004, 279:3245-3253.
36. Giraud M., Taubert R., Vandiedonck C., Ke X., Levi-Strauss M., Pagani F., et al. An IRF8-binding promoter variant and AIRE control CHRNA1 promiscuous expression in thymus. Nature 2007, 448:934-937.
37. Gray D., Abramson J., Benoist C., Mathis D. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire. JExp Med 2007, 204:2521-2528.
38. Leite M.I., Jones M., Strobel P., Marx A., Gold R., Niks E., et al. Myasthenia gravis thymus: complement vulnerability of epithelial and myoid cells, complement attack on them, and correlations with autoantibody status. Am J Pathol 2007, 171:893-905.
39. Kordossi A.A., Tzartos S.J. Monoclonal antibodies against the main immunogenic region of the acetylcholine receptor. Mapping on the intact molecule. JNeuroimmunol 1989, 23:35-40.
40. Loutrari H., Kokla A., Trakas N., Tzartos S.J. Expression of human-Torpedo hybrid acetylcholine receptor (AChR) for analysing the subunit specificity of antibodies in sera from patients with myasthenia gravis (MG). Clin Exp Immunol 1997, 109:538-546.
41. Lehmann P.V., Forsthuber T., Miller A., Sercarz E.E. Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature 1992, 358:155-157.
42. Feferman T., Im S.H., Fuchs S., Souroujon M.C. Breakage of tolerance to hidden cytoplasmic epitopes of the acetylcholine receptor in experimental autoimmune myasthenia gravis. JNeuroimmunol 2003, 140:153-158.
43. McHeyzer-Williams L.J., Driver D.J., McHeyzer-Williams M.G. Germinal center reaction. Curr Opin Hematol 2001, 8:52-59.
44. Barone F., Bombardieri M., Manzo A., Blades M.C., Morgan P.R., Challacombe S.J., et al. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjogren's syndrome. Arthritis Rheum 2005, 52:1773-1784.
45. Badr G., Borhis G., Treton D., Richard Y. IFN{alpha} enhances human B-cell chemotaxis by modulating ligand-induced chemokine receptor signaling and internalization. Int Immunol 2005, 17:459-467.
46. Brink R. Regulation of B cell self-tolerance by BAFF. Semin Immunol 2006, 18:276-283.
47. Berrih-Aknin S., Ragheb S., Le Panse R., Lisak R.P. Ectopic germinal centers, BAFF and anti-B-cell therapy in myasthenia gravis. Autoimmun Rev 2013, 12:885-893.
48. Balandina A., Lecart S., Dartevelle P., Saoudi A., Berrih-Aknin S. Functional defect of regulatory CD4(+)CD25+ T cells in the thymus of patients with autoimmune myasthenia gravis. Blood 2005, 105:735-741.
49. Vandiedonck C., Raffoux C., Eymard B., Tranchant C., Dulmet E., Krumeich S., et al. Association of HLA-A in autoimmune myasthenia gravis with thymoma. JNeuroimmunol 2009, 210:120-123.
50. Papadopoulou A.S., Dooley J., Linterman M.A., Pierson W., Ucar O., Kyewski B., et al. The thymic epithelial microRNA network elevates the threshold for infection-associated thymic involution via miR-29a mediated suppression of the IFN-alpha receptor. Nat Immunol 2012, 13:181-187.
51. Flammer J.R., Dobrovolna J., Kennedy M.A., Chinenov Y., Glass C.K., Ivashkiv L.B., et al. The type I interferon signaling pathway is a target for glucocorticoid inhibition. Mol Cell Biol 2010, 30:4564-4574.
52. Lichtman E.I., Helfgott S.M., Kriegel M.A. Emerging therapies for systemic lupus erythematosus-focus on targeting interferon-alpha. Clin Immunol 2012, 143:210-221.
53. Merrill J.T., Wallace D.J., Petri M., Kirou K.A., Yao Y., White W.I., et al. Safety profile and clinical activity of sifalimumab, a fully human anti-interferon alpha monoclonal antibody, in systemic lupus erythematosus: a phase I, multicentre, double-blind randomised study. Ann Rheum Dis 2011, 70:1905-1913.
54. Yao Y., Richman L., Higgs B.W., Morehouse C.A., de los Reyes M., Brohawn P., et al. Neutralization of interferon-alpha/beta-inducible genes and downstream effect in a phase I trial of an anti-interferon-alpha monoclonal antibody in systemic lupus erythematosus. Arthritis Rheum 2009, 60:1785-1796.