Follicular Helper CD4+ T Cells in Human Neuroautoimmune Diseases and Their Animal Models

Mediators of Inflammation

Volumn 2015, Issue , 2015, Pages

  Fan, Xueli ^a   Lin, Chenhong ^a   Han, Jinming ^a   Jiang, Xinmei ^a   Zhu, Jie ^a,b   Jin, Tao ^a  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; CHEMOKINE RECEPTOR CXCR5; INDUCIBLE COSTIMULATOR; INTERLEUKIN 21; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN BCL 6; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; BCL6 PROTEIN, HUMAN; DNA BINDING PROTEIN; ICOS PROTEIN, HUMAN; INDUCIBLE T CELL COSTIMULATOR; INTERLEUKIN DERIVATIVE;

B CELL LYMPHOMA; CD4+ T LYMPHOCYTE; DISEASE MODEL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; EXPERIMENTAL AUTOIMMUNE MYASTHENIA GRAVIS; FOLLICULAR HELPER CD4+ T LYMPHOCYTE; HELPER CELL; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; MYELOOPTIC NEUROPATHY; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGY; NEUROMYELITIS OPTICA; PHYSIOLOGY;

ANIMALIA;

ANIMALS; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; CD4-POSITIVE T-LYMPHOCYTES; DNA-BINDING PROTEINS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; INTERLEUKINS; MULTIPLE SCLEROSIS; MYASTHENIA GRAVIS; NEUROMYELITIS OPTICA; PROTO-ONCOGENE PROTEINS C-BCL-6; RECEPTORS, CXCR5;

EID: 84939826011     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2015/638968     Document Type: Review

References (102)

1. R. I. Nurieva, Y. Chung, D. Hwang et al., "Generation of Tfollicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages," Immunity, vol. 29, no. 1, pp. 138-149, 2008.
2. +T cells," Science, vol. 327, no. 5969, pp. 1098-1102, 2010.
3. L. Steinman, "A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage," Nature Medicine, vol. 13, no. 2, pp. 139-145, 2007.
4. F. Annunziato, L. Cosmi, F. Liotta, E. Maggi, and S. Romagnani, "Type 17 T helper cells-origins, features and possible roles in rheumatic disease," Nature Reviews Rheumatology, vol. 5, no. 6, pp. 325-331, 2009.
5. S. Z. Josefowicz, L.-F. Lu, and A. Y. Rudensky, "Regulatory T cells: mechanisms of differentiation and function," Annual Review of Immunology, vol. 30, pp. 531-564, 2012.
6. S. Crotty, "Follicular helper CD4 T cells (TFH)," Annual Review of Immunology, vol. 29, pp. 621-663, 2011.
7. Z. Shulman, A. D. Gitlin, S. Targ et al., "T follicular helper cell dynamics in germinal centers," Science, vol. 341, no. 6146, pp. 673-677, 2013.
8. D. Yu and C. G. Vinuesa, "The elusive identity of T follicular helper cells," Trends in Immunology, vol. 31, no. 10, pp. 377-383, 2010.
9. D. Gómez-Martín, M. Díaz-Zamudio, J. Romo-Tena, M. J. Ibarra-Sánchez, and J. Alcocer-Varela, "Follicular helper T cells poise immune responses to the development of autoimmune pathology," Autoimmunity Reviews, vol. 10, no. 6, pp. 325-330, 2011.
10. H. Qi, X. Chen, C. Chu, P. Lu, H. Xu, and J. Yan, "Follicular T-helper cells: controlled localization and cellular interactions," Immunology and Cell Biology, vol. 92, no. 1, pp. 28-33, 2014.
11. S. Crotty, "T follicular helper cell differentiation, function, and roles in disease," Immunity, vol. 41, no. 4, pp. 529-542, 2014.
12. E. K. Deenick and C. S. Ma, "The regulation and role of T follicular helper cells in immunity," Immunology, vol. 134, no. 4, pp. 361-367, 2011.
13. C. S. Ma, E. K. Deenick, M. Batten, and S. G. Tangye, "The origins, function, and regulation of T follicular helper cells," Journal of Experimental Medicine, vol. 209, no. 7, pp. 1241-1253, 2012.
14. A. Ballesteros-Tato and T. D. Randall, "Priming of T follicular helper cells by dendritic cells," Immunologyand Cell Biology, vol. 92, no. 1, pp. 22-27, 2014.
15. J. L. Cannons, K. T. Lu, and P. L. Schwartzberg, "T follicular helper cell diversity and plasticity," Trends in Immunology, vol. 34, no. 5, pp. 200-207, 2013.
16. highgerminal center-associated subpopulation," Journal of Immunology, vol. 179, no. 8, pp. 5099-5108, 2007.
17. A. Pratama and C. G. Vinuesa, "Control of TFH cell numbers: why and how?" Immunology and Cell Biology, vol. 92, no. 1, pp. 40-48, 2014.
18. C. G. Vinuesa, S. G. Tangye, B. Moser, and C. R. Mackay, "Follicular B helper T cells in antibody responses and autoimmunity," Nature Reviews Immunology, vol. 5, no. 11, pp. 853-865, 2005.
19. R. A. Sweet, S. K. Lee, and C. G. Vinuesa, "Developing connections amongst key cytokines and dysregulated germinal centers in autoimmunity," Current Opinion in Immunology, vol. 24, no. 6, pp. 658-664, 2012.
20. H. Qi, D. Liu, W. Ma, Y. Wang, and H. Yan, "Bcl-6 controlled TFH polarization and memory: the known unknowns," Current Opinion in Immunology, vol. 28, no. 1, pp. 34-41, 2014.
21. D. Yu, S. Rao, L. M. Tsai et al., "The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment," Immunity, vol. 31, no. 3, pp. 457-468, 2009.
22. K. Lüthje, A. Kallies, Y. Shimohakamada et al., "The development and fate of follicular helper T cells defined by an IL-21 reportermouse," Nature Immunology, vol. 13, no. 5, pp. 491-498, 2012.
23. R. J. Johnston, A. C. Poholek, D. DiToro et al., "Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation," Science, vol. 325, no. 5943, pp. 1006-1010, 2009.
24. Y. S. Choi, J. A. Yang, and S. Crotty, "Dynamic regulation of Bcl6 in follicular helper CD4 T (Tfh) cells," Current Opinion in Immunology, vol. 25, no. 3, pp. 366-372, 2013.
25. D. Breitfeld, L. Ohl, E. Kremmer et al., "Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production," Journal of Experimental Medicine, vol. 192, no. 11, pp. 1545-1551, 2000.
26. C.N. Arnold, D. J. Campbell, M. Lipp, and E. C. Butcher, "The germinal center response is impaired in the absence of T cellexpressed CXCR5,"European Journal of Immunology, vol. 37, no. 1, pp. 100-109, 2007.
27. K. L. Good-Jacobson, C. G. Szumilas, L. Chen, A. H. Sharpe, M. M. Tomayko, and M. J. Shlomchik, "PD-1 regulates germinal center B cell survival and the formation and affinity of longlived plasma cells," Nature Immunology, vol. 11, no. 6, pp. 535-542, 2010.
28. A. L. Kinter, E. J. Godbout, J. P. McNally et al., "The common γ-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands," The Journal of Immunology, vol. 181, no. 10, pp. 6738-6746, 2008.
29. H. Akiba, K. Takeda, Y. Kojima et al., "The role of ICOS in the CXCR5+ follicular B helper T cellmaintenance in vivo," Journal of Immunology, vol. 175, no. 4, pp. 2340-2348, 2005.
30. K. Warnatz, L. Bossaller, U. Salzer et al., "Human ICOS deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency," Blood, vol. 107, no. 8, pp. 3045-3052, 2006.
31. J. Tellier and S. L. Nutt, "The unique features of follicular T cell subsets," Cellular and Molecular Life Sciences, vol. 70, no. 24, pp. 4771-4784, 2013.
32. Y. Takahashi, P. R. Dutta, D. M. Cerasoli, and G. Kelsoe, "In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. v. affinity maturation develops in two stages of clonal selection," Journal of Experimental Medicine, vol. 187, no. 6, pp. 885-895, 1998.
33. T.D. Randall, A.W. Heath, L. Santos-Argumedo, M. C. Howard, I. L. Weissman, and F. E. Lund, "Arrest of B lymphocyte terminal differentiation by CD40 signaling:mechanism for lack of antibody-secreting cells in germinal centers," Immunity, vol. 8, no. 6, pp. 733-742, 1998.
34. M. A. Linterman, L. Beaton, D. Yu et al., "IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses," The Journal of Experimental Medicine, vol. 207, no. 2, pp. 353-363, 2010.
35. +T cell-B cell collaboration," Journal of Immunology, vol. 179, no. 9, pp. 5886-5896, 2007.
36. K. Ozaki, R. Spolski, R. Ettinger et al., "Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6," The Journal of Immunology, vol. 173, no. 9, pp. 5361-5371, 2004.
37. S.G. Tangye, C. S. Ma, R. Brink, and E. K. Deenick, "The good, the bad and the ugly-TFH cells in human health and disease," Nature Reviews Immunology, vol. 13, no. 6, pp. 412-426, 2013.
38. H. Qi, J. L. Cannons, F. Klauschen, P. L. Schwartzberg, and R. N. Germain, "SAP-controlled T-B cell interactions underlie germinal centre formation," Nature, vol. 455, no. 7214, pp. 764-769, 2008.
39. N. Schmitt and H. Ueno, "Blood Tfh cells come with colors," Immunity, vol. 39, no. 4, pp. 629-630, 2013.
40. C. G. Vinuesa and M. C. Cook, "Blood relatives of follicular helper T cells," Immunity, vol. 34, no. 1, pp. 10-12, 2011.
41. N. Simpson, P. A. Gatenby, A. Wilson et al., "Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus," Arthritis & Rheumatism, vol. 62, no. 1, pp. 234-244, 2010.
42. +) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion," Immunity, vol. 34, no. 1, pp. 108-121, 2011.
43. 4+ T cells indicate tfh cell activity and promote antibody responses upon antigen reexposure," Immunity, vol. 39, no. 4, pp. 770-781, 2013.
44. L. M. Tsai and D. Yu, "Follicular helper T-cell memory: establishing new frontiers during antibody response," Immunology and Cell Biology, vol. 92, no. 1, pp. 57-63, 2014.
45. X. Feng, D. Wang, J. Chen et al., "Inhibition of aberrant circulating Tfh cell proportions by corticosteroids in patients with systemic lupus erythematosus," PLoS ONE, vol. 7, no. 12, Article ID e51982, 2012.
46. J. Ma, C. Zhu, B. Ma et al., "Increased frequency of circulating follicular helper T cells in patients with rheumatoid arthritis," Clinical and Developmental Immunology, vol. 2012, Article ID 827480, 7 pages, 2012.
47. F. Xiao, H.-Y. Zhang, Y.-J. Liu, D. Zhao, Y.-X. Shan, and Y.- F. Jiang, "Higher frequency of peripheral blood interleukin 21 positive follicular helper T cells in patients with ankylosing spondylitis," Journal of Rheumatology, vol. 40, no. 12, pp. 2029-2037, 2013.
48. Q. Li, Z. Liu, E. Dang et al., "Follicular helper T Cells (Tfh) and IL-21 involvement in the pathogenesis of bullous pemphigoid," PLoS ONE, vol. 8, no. 7, Article ID e68145, 2013.
49. K. Szabo, G. Papp, S. Barath, E. Gyimesi, A. Szanto, and M. Zeher, "Follicular helper T cells may play an important role in the severity of primary Sjögren's syndrome," Clinical Immunology, vol. 147, no. 2, pp. 95-104, 2013.
50. C. King, S. G. Tangye, and C. R. Mackay, "T follicular helper (TFH) cells in normal and dysregulated immune responses," Annual Review of Immunology, vol. 26, pp. 741-766, 2008.
51. C. S. Ma and E. K. Deenick, "Human T follicular helper (Tfh) cells and disease," Immunology and Cell Biology, vol. 92, no. 1, pp. 64-71, 2014.
52. K. L. Boswell, R. Paris, E. Boritz et al., "Loss of circulating CD4 T cells with B cell helper function during chronic HIV infection," PLoS Pathogens, vol. 10, no. 1, Article IDe1003853, 2014.
53. M. Pennisi, A.-M. Rajput, L. Toldo, and F. Pappalardo, "Agent based modeling of Treg-Teff cross regulation in relapsingremitting multiple sclerosis," BMC Bioinformatics, vol. 14, no. 16, article S9, 2013.
54. E.N. Benveniste, Y. Liu, B. C. McFarland, and H. Qin, "Involvement of the janus kinase/signal transducer and activator of transcription signaling pathway in multiple sclerosis and the animal model of experimental autoimmune encephalomyelitis," Journal of Interferon & Cytokine Research, vol. 34, no. 8, pp. 577-588, 2014.
55. A. Compston and A. Coles, "Multiple sclerosis," The Lancet, vol. 372, no. 9648, pp. 1502-1517, 2008.
56. F. D. Lublin and S. C. Reingold, "Defining the clinical course of multiple sclerosis: results of an international survey," Neurology, vol. 46, no. 4, pp. 907-911, 1996.
57. F. Jadidi-Niaragh and A. Mirshafiey, "Th17 cell, the newplayer of neuroinflammatory process inmultiple sclerosis," Scandinavian Journal of Immunology, vol. 74, no. 1, pp. 1-13, 2011.
58. J. M. Fletcher, S. J. Lalor, C. M. Sweeney, N. Tubridy, and K. H. G. Mills, "T cells in multiple sclerosis and experimental autoimmune encephalomyelitis," Clinical and Experimental Immunology, vol. 162, no. 1, pp. 1-11, 2010.
59. M. Krumbholz and E. Meinl, "B cells in MS and NMO: pathogenesis and therapy," Seminars in Immunopathology, vol. 36, no. 3, pp. 339-350, 2014.
60. A. Ray, M. K. Mann, S. Basu, and B.N. Dittel, "A case for regulatory B cells in controlling the severity of autoimmune-mediated inflammation in experimental autoimmune encephalomyelitis and multiple sclerosis," Journal of Neuroimmunology, vol. 230, no. 1-2, pp. 1-9, 2011.
61. J. H. Anolik, R. J. Looney, F. E. Lund, T. D. Randall, and I. Sanz, "Insights into the heterogeneity of human B cells: diverse functions, roles in autoimmunity, and use as therapeutic targets," Immunologic Research, vol. 45, no. 2-3, pp. 144-158, 2009.
62. B. Serafini, B. Rosicarelli, R. Magliozzi, E. Stigliano, and F. Aloisi, "Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis," Brain Pathology, vol. 14, no. 2, pp. 164-174, 2004.
63. R. Magliozzi, O. Howell, A. Vora et al., "Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology," Brain, vol. 130, no. 4, pp. 1089-1104, 2007.
64. J. R. Christensen, L. Börnsen, R. Ratzer et al., "Systemic inflammation in progressive multiple sclerosis involves follicular T-helper, Th17- and activated B-cells and correlates with progression," PLoS ONE, vol. 8, no. 3, Article ID e57820, 2013.
65. +T lymphocytes inhibit T cell activation "in vitro" and attenuate autoimmune encephalitis "in vivo"," International Immunology, vol. 20, no. 4, pp. 577-589, 2008.
66. J. S. Tzartos, M. J. Craner, M. A. Friese et al., "IL-21 and IL-21 receptor expression in lymphocytes and neurons in multiple sclerosis brain," The American Journal of Pathology, vol. 178, no. 2, pp. 794-802, 2011.
67. R. Nohra, A. D. Beyeen, J. P. Guo et al., "RGMA and IL21R show association with experimental inflammation andmultiple sclerosis," Genes and Immunity, vol. 11, no. 4, pp. 279-293, 2010.
68. X. Wang, C. Ma, J. Wu, and J. Zhu, "Roles of T helper 17 cells and interleukin-17 in neuroautoimmune diseases with emphasis on multiple sclerosis and Guillain-Barré syndrome as well as their animal models," Journal of Neuroscience Research, vol. 91, no. 7, pp. 871-881, 2013.
69. R. Magliozzi, S. Columba-Cabezas, B. Serafini, and F. Aloisi, "Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis," Journal of Neuroimmunology, vol. 148, no. 1-2, pp. 11-23, 2004.
70. L. V. Bagaeva, P. Rao, J. M. Powers, and B. M. Segal, "CXC chemokine ligand 13 plays a role in experimental autoimmune encephalomyelitis," Journal of Immunology, vol. 176, no. 12, pp. 7676-7685, 2006.
71. hi CD4 T cells and is independent of CD57 expression," European Journal of Immunology, vol. 36, no. 7, pp. 1892-1903, 2006.
72. T. Drori and J. Chapman, "Diagnosis and classification of neuromyelitis optica (Devic's Syndrome)," Autoimmunity Reviews, vol. 13, no. 4-5, pp. 531-533, 2014.
73. R. Nandhagopal, A. Al-Asmi, and A. R. Gujjar, "Neuromyelitis optica: an overview," Postgraduate Medical Journal, vol. 86, no. 1013, pp. 153-159, 2010.
74. A. Nagaishi, M. Takagi, A. Umemura et al., "Clinical features of neuromyelitis optica in a large Japanese cohort: comparison between phenotypes," Journal of Neurology, Neurosurgery and Psychiatry, vol. 82, no. 12, pp. 1360-1364, 2011.
75. A. Jacob, A. McKeon, I. Nakashima et al., "Current concept of neuromyelitis optica (NMO) and NMO spectrum disorders," Journal of Neurology, Neurosurgery and Psychiatry, vol. 84, no. 8, pp. 922-930, 2013.
76. P. V. A. Lennon, D.M. Wingerchuk, T. J. Kryzer et al., "A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis," The Lancet, vol. 364, no. 9451, pp. 2106-2112, 2004.
77. A. S. Verkman, P.-W. Phuan, N. Asavapanumas, and L. Tradtrantip, "Biology of AQP4 and Anti-AQP4 antibody: therapeutic implications for NmO," Brain Pathology, vol. 23, no. 6, pp. 684-695, 2013.
78. S. Jarius and B. Wildemann, "AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance," Nature Reviews Neurology, vol. 6, no. 7, pp. 383-392, 2010.
79. J. Ratelade and A. S. Verkman, "Neuromyelitis optica: aquaporin-4 based pathogenesis mechanisms and new therapies," International Journal of Biochemistry and Cell Biology, vol. 44, no. 9, pp. 1519-1530, 2012.
80. M. Levy, B. Wildemann, S. Jarius et al., "Immunopathogenesis of neuromyelitis optica," Advances in Immunology, vol. 121, pp. 213-242, 2014.
81. E. P. Flanagan and B. G. Weinshenker, "Neuromyelitis optica spectrum disorders," Current Neurology and Neuroscience Reports, vol. 14, no. 9, article 483, 2014.
82. C. Quan, H. Yu, J. Qiao et al., "Impaired regulatory function and enhanced intrathecal activation of B cells in neuromyelitis optica: distinct from multiple sclerosis," Multiple Sclerosis, vol. 19, no. 3, pp. 289-298, 2013.
83. Y. J. Li, F. Zhang, Y. Qi et al., "Associationof circulating follicular helper T cells with disease course of NMO spectrum disorders," Journal of Neuroimmunology, vol. 278, pp. 239-246, 2015.
84. +T cells is directly associated with neurological disability in neuromyelitis optica patients," Journal of Clinical Immunology, vol. 33, no. 1, pp. 179-189, 2013.
85. E. Alvarez, L. Piccio, R. J. Mikesell et al., "CXCL13 is a biomarker of inflammation inmultiple sclerosis, neuromyelitis optica, and other neurological conditions," Multiple Sclerosis, vol. 19, no. 9, pp. 1204-1208, 2013.
86. D. B. Drachman, "Myasthenia gravis," The New England Journal of Medicine, vol. 330, no. 25, pp. 1797-1810, 1994.
87. M. G. Huijbers, A. F. Lipka, J. J. Plomp, E. H. Niks, S. M. van der Maarel, and J. J. Verschuuren, "Pathogenic immune mechanisms at the neuromuscular synapse: the role of specific antibody-binding epitopes in myasthenia gravis," Journal of Internal Medicine, vol. 275, no. 1, pp. 12-26, 2014.
88. S. Mori and K. Shigemoto, "Mechanisms associated with the pathogenicity of antibodies against muscle-specific kinase in myasthenia gravis," Autoimmunity Reviews, vol. 12, no. 9, pp. 912-917, 2013.
89. J. J. G. M. Verschuuren, M. G. Huijbers, J. J. Plomp et al., "Pathophysiology of myasthenia gravis with antibodies to the acetylcholine receptor, muscle-specific kinase and low-density lipoprotein receptor-related protein 4," Autoimmunity Reviews, vol. 12, no. 9, pp. 918-923, 2013.
90. R. le Panse and S. Berrih-Aknin, "Autoimmune myasthenia gravis: autoantibody mechanisms and new developments on immune regulation," Current Opinion in Neurology, vol. 26, no. 5, pp. 569-576, 2013.
91. E. Gallardo, E. Martínez-Hernández, M. J. Titulaer et al., "Cortactin autoantibodies inmyasthenia gravis," Autoimmunity Reviews, vol. 13, no. 10, pp. 1003-1007, 2014.
92. P. Cavalcante, P. Bernasconi, and R. Mantegazza, "Autoimmune mechanisms in myasthenia gravis," Current Opinion in Neurology, vol. 25, no. 5, pp. 621-629, 2012.
93. N. E. Gilhus, "Myasthenia and the neuromuscular junction," Current Opinion in Neurology, vol. 25, no. 5, pp. 523-529, 2012.
94. M. Zhang, Y. Zhou, J. Guo et al., "Thymic TFH cells involved in the pathogenesis of myasthenia gravis with thymoma," Experimental Neurology, vol. 254, pp. 200-205, 2014.
95. S. Berrih-Aknin, M. Frenkian-Cuvelier, and B. Eymard, "Diagnostic and clinical classification of autoimmune myasthenia gravis," Journal of Autoimmunity, vol. 48-49, pp. 143-148, 2014.
96. J. P. Sieb, "Myasthenia gravis: an update for the clinician," Clinical & Experimental Immunology, vol. 175, no. 3, pp. 408-418, 2014.
97. R. Saito, H. Onodera, H. Tago et al., "Altered expression of chemokine receptor CXCR5 on T cells of myasthenia gravis patients," Journal of Neuroimmunology, vol. 170, no. 1-2, pp. 172-178, 2005.
98. C. Luo, Y. Li, W. Liu et al., "Expansion of circulating counterparts of follicular helper T cells in patients with myasthenia gravis," Journal of Neuroimmunology, vol. 256, no. 1-2, pp. 55-61, 2013.
99. Y.-M. Shiao, C.-C. Lee, Y.-H. Hsu et al., "Ectopic and high CXCL13 chemokine expression in myasthenia gravis with thymic lymphoid hyperplasia," Journal of Neuroimmunology, vol. 221, no. 1-2, pp. 101-106, 2010.
100. A. Meraouna, G. Cizeron-Clairac, R. Le Panse et al., "The chemokine CXCL13 is a keymolecule in autoimmunemyasthenia gravis," Blood, vol. 108, no. 2, pp. 432-440, 2006.
101. S. Fuchs, R. Aricha, D. Reuveni, and M. C. Souroujon, "Experimental Autoimmune Myasthenia Gravis (EAMG): from immunochemical characterization to therapeutic approaches," Journal of Autoimmunity C, vol. 54, pp. 51-59, 2014.
102. N. Xin, L. Fu, Z. Shao et al., "RNA interference targeting Bcl-6 ameliorates experimental autoimmune myasthenia gravis in mice," Molecular and Cellular Neuroscience, vol. 58, pp. 85-94, 2014.