Immune manipulation for Graves' disease: Re-exploring an unfulfilled promise with modern translational research

European Journal of Internal Medicine

Volumn 23, Issue 8, 2012, Pages 682-691

  Dalan, Rinkoo ^a   Leow, Melvin Khee Shing ^b  

^a TAN TOCK SENG HOSPITAL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Autoiummunity; Immunomodulation; Thyroid

Indexed keywords

ALEMTUZUMAB; CARBIMAZOLE; CD20 ANTIBODY; DEXAMETHASONE; ETANERCEPT; GLUCOCORTICOID; IMMUNOMODULATING AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; PROPYLTHIOURACIL; RITUXIMAB; SOMATOMEDIN C; THIAMAZOLE; THIONAMIDE;

APOPTOSIS; AUTOIMMUNITY; B LYMPHOCYTE; DRUG TARGETING; ENDOCRINE OPHTHALMOPATHY; GRAVES DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEREDITY; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MEDICAL LITERATURE; NONHUMAN; PATHOGENESIS; PROPHYLAXIS; REVIEW; T LYMPHOCYTE ACTIVATION; TRANSLATIONAL RESEARCH;

ANIMALS; AUTOIMMUNITY; GRAVES DISEASE; HUMANS; IMMUNOLOGIC FACTORS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84869083738     PISSN: 09536205     EISSN: 18790828     Source Type: Journal    
DOI: 10.1016/j.ejim.2012.07.007     Document Type: Review

References (106)

1. M.W. Russo, J.A. Galanko, R. Shrestha, M.W. Fried, and P. Watkins Liver transplantation for acute liver failure from drug-induced liver injury in the United States Liver Transpl 10 2004 1018 1023 (Pubitemid 39232756)
2. Y. Tomer, and A. Huber The etiology of autoimmune thyroid disease: a story of genes and environment J Autoimmun 32 2009 231 239
3. R. Wilson, J.H. Mckillop, C. Pearson, A.K. Burnett, and J.A. Thomson Differential immunosuppressive action of carbimazole and propylthiouracil Clin Exp Immunol 73 1988 312 315
4. D.S. Cooper Antithyroid drugs N Engl J Med 352 2005 905 917 (Pubitemid 40300299)
5. T.H. Brix, K.O. Kyvik, K. Christensen, and L. Hegedus Evidence for a major role of heredity in Graves' disease: a population based study of two Danish twin cohorts J Clin Endocrinol Metab 86 2001 930 934 (Pubitemid 32207518)
6. Y. Ban, T.F. Davies, D.A. Greenberg, E.S. Concepcion, R. Osman, and T. Oashi Arginine at position 74 of the HLA-DR β1 chain is associated with Graves' disease Genes Immun 5 2004 203 208 (Pubitemid 38967653)
7. N.R. Rose, R. Bonita, and C.L. Burek Iodine: an environmental trigger of thyroiditis Autoimmun Rev 1 2002 97 103 (Pubitemid 38367432)
8. K. Yamazaki, K. Tanigawa, K. Suzuki, E. Yamada, T. Yamada, and K. Takano Iodide-induced chemokines and genes related to immunological function in cultured human thyroid follicles in the presence of thyrotropin Thyroid 20 2010 67 76
9. Y. Oppenheim, Y. Ban, and Y. Tomer Interferon induced autoimmune thyroid disease (AITD): a model for human autoimmunity Autoimmun Rev 3 2004 388 393 (Pubitemid 38993361)
10. Y. Tomer, and T.F. Davies Infections and autoimmune endocrine disease Baillieres Clin Endocrinol Metab 9 1995 47 70
11. A. Matos-Santos, E.L. Nobre, J.G. Costa, P.J. Noguera, A. Macedo, and A. Galvao-Teles Relationship between the number and impact of stressful life events and the onset of Graves' disease and toxic nodular goitre Clin Endocrinol 55 2001 15 19 (Pubitemid 34204294)
12. M.j. Simmonds, and C.L. Gough The search for the genetic contribution to autoimmune thyroid disease: the never ending story? Brief Funct Genomics 10 2011 77 90
13. M.J. Simmonds, J.M. Howson, J.M. Heward, H.J. Cordell, H. Foxall, and J. Carr-Smith Regression mapping of association between human leukocyte antigen region and Graves disease Am J Hum Genet 76 2005 157 163 (Pubitemid 40023775)
14. P.L. Chen, C.S. Fann, C.C. Chu, C.C. Chang, S.W. Chang, and H.Y. Hsieh Comprehensive genotyping in two homogenous Graves' disease samples reveals major and novel HLA association alleles PLoS One 6 2011 e16635
15. D. Meyer, R.M. Single, S.J. Mack, A. Lancaster, M.P. Nelson, and H.A. Erlich Single locus polymorphism of classical HLA genes J.A. Hansen, Immunobiology of the human MHC 2006 International Histocompatibility Working Group Press Seattle, Washington, USA 653 704
16. S. Fountaoulakis, and A. Tsatsoulis On the pathogenesis of autoimmune thyroid disease: a unifying hypothesis Clin Endocrinol 60 2004 397 409 (Pubitemid 38482501)
17. C.-R. Chen, P. Pichurin, Y. Nagayama, F. Latrofa, B. Rapoport, and S.M. Mclachlan The thyrotropin receptor autoantigen in Graves' disease is the culprit as well as the victim J Clin Invest 111 2003 1897 1904 (Pubitemid 38057734)
18. G.D. Chazenbalk, J.C. Jaume, S.M. McLachlan, and B. Rapoport Engineering the human thyrotropin receptor ectodomain from a non-secreted form to a secreted, highly immunoreactive glycoprotein that neutralizes autoantibodies in Graves' patients' sera J Biol Chem 272 1997 18959 18965 (Pubitemid 27318250)
19. G.D. Chazenbalk, P.N. Pichurin, J. Guo, B. Rapoport, and S.M. McLachlan Interactions between the mannose receptor and thyroid autoimmunity Clin Exp Immunol 139 2005 216 224 (Pubitemid 40222839)
20. A.J. Engering, M. Cella, D. Fluitsma, M. Brockhaus, E.C. Hoefsmit, and A. Lanzavecchia The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells Eur J Immunol 27 1997 2417 2425 (Pubitemid 27404329)
21. S.M. McLachlan, Y. Nagayama, and B. Rapoport Insights into Graves' hyperthyroidism from animal models Endocr Rev 26 2005 800 832 (Pubitemid 41428539)
22. C.H. Nielsen, R.G. Leslie, B.S. Jepsen, M.D. Kazatchkine, S.V. Kaveri, and E. Fischer Natural autoantibodies and complement promote the uptake of self antigen, human thyroglobulin, by B cells and the proliferation of thyroglobulin-reactive CD(4 +) T cells in healthy individuals Eur J Immunol 31 2001 2660 2668 (Pubitemid 32898733)
23. H. Kimura, M. Kimura, S.C. Tzou, Y.C. Chen, K. Suzuki, and N.R. Rose Expression of class II major histocompatibility complex molecules on thyrocytes does not cause spontaneous thyroiditis but mildly increases its severity after immunization Endocrinology 146 2005 1154 1162 (Pubitemid 40289304)
24. H.A. Voorby, P.J. Kabel, M. de Haan, P.H. Jeucken, R.D. van der Gaag, and M.H. de Baets Dendritic cells and class II MHC expression on thyrocytes during the autoimmune thyroid disease of the BB rat Clin Immunol Immunopathol 55 1990 9 22 (Pubitemid 20116697)
25. T. Yamada, A. Sato, I. Komiya, T. Nishimori, Y. Ito, and A. Terao An elevation of serum immunoglobulin E provides a new aspect of hyperthyroid Graves' disease J Clin Endocrinol Metab 85 2000 2775
26. A. Coles, M. Wing, S. Smith, F. Coraddu, F. Greer, and C. Taylor Pulsed monoclonal antibody treatment and autoimmune thyroid disease in multiple sclerosis Lancet 354 1999 1691
27. P.E. Posch, H.A. Araujo, K. Creswell, C. Praud, A.H. Johnson, and C.K. Hurley Microvariation creates significant functional differences in the DR3 molecules Hum Immunol 42 1995 61 71
28. P. Ghosh, M. Amaya, E. Mellins, and D.C. Wiley The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3 Nature 378 1995 457 462
29. P.J. Kabel, H.A. Voorbij, M. de Haan-Meulman, S.T. Pals, and H.A. Drexhage High endothelial venules present in lymphoid cell accumulation in thyroids affected by autoimmune disease: a study in men and BB rats of functional activity and development J Clin Endocrinol Metab 68 1989 1744 1751
30. R. Paschke, N. Brückner, T. Eck, L. Schaaf, W. Back, and K.H. Usadel Regional stimulation of thyroid epithelial cells in Graves' disease by lymphocyte aggregrates in plasma cells Acta Endocrinol 15 1991 459 465
31. A.P. Weetman, A.M. McGregor, M.H. Wheeler, and R. Hall Extrathyroidal sites of autoantibody synthesis in Graves' disease Clin Exp Immunol 56 1984 330 336 (Pubitemid 14137453)
32. B. Rapoport, and S.M. McLachlan Thyroid autoimmunity J Clin Invest 108 2001 1253 1259 (Pubitemid 33107748)
33. J.P. Aniszewski, R.W. Valyasevi, and R.S. Bahn Relationship between disease duration and predominant orbital T cell subset in Graves' ophthalmopathy J Clin Endocrinol Metab 85 2000 776 780 (Pubitemid 32273668)
34. A.P. Weetman, and R.A. Ajjan Cytokines and autoimmune thyroid disease Hot Thyroidol 1 2002
35. A. Antonelli, M. Rotondi, P. Fallahi, P. Romagnani, S.M. Ferrari, and L. Barani Increase of interferon gamma inducible alpha chemokine CXCL10 but not beta chemokine CCL2 serum levels in chronic autoimmune thyroiditis Eur J Endocrinol 152 2005 171 177 (Pubitemid 40309561)
36. P. Romagnani, M. Rotondi, E. Lazzeri, L. Lasagni, M. Francalanci, and A. Buonamano Expression of IP-10/CXCL10 and Mig/CXCL9 in the thyroid and increased serum levels of IP-10/ CXCL10 in the serum of subjects with recent onset Graves' disease Am J Pathol 161 2002 195 206 (Pubitemid 34760785)
37. A. Antonelli, M. Rotondi, P. Fallahi, P. Romagnani, S.M. Ferrari, and L. Barani Increase of interferon gamma inducible CXC chemokine CXCL10 serum levels in patients with active Graves' disease and modulation by methimazole therapy Clin Endocrinol 24 2006 189 195
38. A. Antonelli, P. Fallahi, M. Rotondi, S.M. Ferrari, P. Romagnani, and M. Grosso Increased serum CXCL10 in Graves' disease or autoimmune thyroiditis is not associated with hyper or hypothyroidism per se, but is specifically sustained by the autoimmune, inflammatory process Eur J Endocrinol 154 2006 651 658 (Pubitemid 43810850)
39. M.A. Garcià-Lòpez, D. Sancho, F. Sànchez-Madrid, and M. Marazuela Thyrocytes from autoimmune thyroid disorders produce the chemokines IP-10 and Mig and attract CXCR3 + lymphocytes J Clin Endocrinol Metab 86 2001 5008 5016 (Pubitemid 33020557)
40. A. Antonelli, S.M. Ferrari, P. Fallahi, S. Frascerra, E. Santini, and S.S. Franceschini Monokine induced by interferon alpha (CXCL9) and IFNγ inducible T cell α- attractant (CXCL11) involvement in Graves' disease and opthalmopathy:modulation by peroxisome-proliferator-activated receptor-γ agonists J Clin Endocrinol Metab 94 2009 1803 1809
41. T. Nanba, M. Watanabe, N. Inoue, and Y. Iwatani Increases of the Th1/Th2 cell ratio in severe Hashimoto's disease and in the proportion of Th17 cells in intractable Graves' disease Thyroid 19 2009 495 501
42. T. Bohgaki, T. Atsumi, and T. Koike Multiple autoimmune diseases after autologous stem cell transplantation N Engl J Med 357 2007 2734 2736
43. M. Marazuela, M.A. García-López, N. Figueroa-Vega, H. de la Fuente, B. Alvarado-Sánchez, and A. Monsiváis-Urenda Regulatory T cells in human autoimmune thyroid disease J Clin Endocrinol Metab 91 2006 3639 3646 (Pubitemid 44402149)
44. J.A. Gilbert, S.L. Kalled, J. Moorhead, D.M. Hess, P. Rennert, and Z. Li Treatment of autoimmune hyperthyroidism in a murine model of Graves' disease with tumour necrosis factor-family ligand inhibitors suggests a key role for B cell activating factor in disease pathology Endocrinology 147 2006 4561 4568 (Pubitemid 44402161)
45. H. Braley-Mullen, and S. Yu Early requirement for B cells for development of spontaneous autoimmune thyroiditis in NOD.H-2 h4 mice J Immunol 165 2000 7262 7269 (Pubitemid 32001205)
46. P.J. Linton, J. Harbertson, and L.M. Bradley A critical role for B cells in the development of memory CD4 cells J Immunol 165 2000 5558 5565
47. Y. Nagayama, H. Mizuguchi, T. Hayakawa, M. Niwa, S.M. McLachlan, and B. Ropoport Prevention of auto-antibody-mediated Graves' like hyperthyroidism in mice with Il-4, a Th2 cytokine J Immunol 170 2003 3522 3527 (Pubitemid 36359218)
48. C. Salmaso, M. Bagnasco, G. Pesce, P. Montagna, R. Brizzolara, and V. Altrinetti Regulation of apoptosis in endocrine autoimmunity: insights from Hashimoto's thyroiditis and Graves' disease Ann N Y Acad Sci 966 2002 496 501 (Pubitemid 34729212)
49. R.S. Douglas, A.G. Gianoukakis, S. Kamat, and T.J. Smith Aberrant expression of the insulin-like growth factor-1 receptor by T cells from patients with Graves' disease may carry functional consequences for disease pathogenesis J Immunol 178 2007 3281 3287 (Pubitemid 46333212)
50. R.S. Douglas, V. Naik, C.J. Hwang, N.F. Afifiyan, A.G. Gianoukakis, and D. Sand B cells from patients with Graves' disease aberrantly express the IGF-1 receptor: implications for disease pathogenesis J Immunol 181 2007 5768 5774
51. T.H. Totterman, F.A. Karlsson, M. Bengtsson, and I. Mendel-Hardvig Induction of circulating activated suppressor-like T cells by methimazole therapy for Graves' disease N Engl J Med 316 1987 15 22 (Pubitemid 17050164)
52. P.W. Wang, S.F. Luo, and M.J. Huang Depressed natural killer activity in Graves' disease and during antithyroid medication Clin Endocrinol 28 1988 205 214
53. J.J. Corrales, A. Lopez, J. Ciudad, M.T. Mories, J.M. Miralles, and A. Orfao Methimazole therapy in Graves' disease influences the abnormal expression of CD69 (early activation antigen) on T cells J Endocrinol 155 1997 491 500 (Pubitemid 27524056)
54. F.A. Karlsson, and T.H. Tötterman Immunomodulation by methimazole therapy in Graves' disease: rapid changes in activation stage of circulatory regulatory T cell subsets, B cells and NK cells Clin Exp Immunol 74 1988 258 263
55. A.B. Pedro, J.H. Romaldini, and K. Takei Changes of serum cytokines in hyperthyroid Graves' disease patients at diagnosis and during methimazole treatment Neuroimmunomodulation 13 2010 45 51
56. A. Antonelli, M. Rotondi, P. Fallahi, P. Romagnani, S.M. Ferrari, and L. Barani Increase of interferon-inducible CXC chemokine CXCL10 serum levels in patients with active Graves' disease, and modulation by methimazole therapy Clin Endocrinol 64 2006 189 195
57. A. Bossowski, N. Stasaik-Barmuta, and M. Urban Relationship between CTLA-4 and CD28 expression on T lymphocytes and stimulating and blocking autoantibodies to the TSH-receptor in children with Graves' disease Horm Res 64 2005 189 197 (Pubitemid 41642763)
58. A. Bossowski, N. Stasaik-Barmuta, M. Urban, and A. Bossowska Analysis of costimulatory molecules OX40/4-1 BB (CD134/CD137) detection on chosen mononuclear cells in children and adolescents with Graves' disease during methimazole therapy J Pediatr Endocrinol Metab 18 2005 1365 1372 (Pubitemid 43109373)
59. A. Antonelli, S.M. Ferrari, S. Frascerra, I. Ruffilli, S. Gelmini, and M. Minuto Peroxisome proliferator-activated receptor-a agonists modulate CXCL9 and CXCL11 chemokines in Graves' ophthalmopathy fibroblasts and preadipocytes Mol Cell Endocrinol 349 2012 255 261
60. D. Pasquali, G.M. Pierantoni, A. Fusco, S. Staibano, V. Colantuoni, and A. De Bellis Fenofibrate increases the expression of high mobility group AT-hook 2 (HMGA2) gene and induces adipocyte differentiation of orbital fibroblasts from Graves' ophthalmopathy J Mol Endocrinol 33 2004 133 143 (Pubitemid 39206353)
61. A.W. van Lieshout, M.C. Creemers, T.R. Radstake, L.D. Elving, and P.L. van Riel Graves' disease in a patient with rheumatoid arthritis during treatment with anti-tumor necrosis factor-α [letter] J Rheumatol 35 2008 938 939 (Pubitemid 351747144)
62. J.I. Shin, J.M. Park, J.S. Lee, D.H. Kim, and H.J. Jeong Development of Graves' disease during cyclosporin treatment for severe Henoch-Schönlein nephritis Nephrol Dial Transplant 20 2005 2014 2015 (Pubitemid 41222632)
63. G. Hofle, R. Moncayo, I. Baldissera, R. Pfister, and G. Finkenstedt Endocrine ophthalmopathy in a patient under continuous immunosuppressive therapy after cardiac transplantation Thyroid 5 1995 477 480 (Pubitemid 26036910)
64. Y. Allanore, C. Brémont, A. Kahan, and C.J. Menkès Transient hyperthyroidism in a patient with rheumatoid arthritis treated by etanercept Clin Exp Rheumatol 19 2001 356 357 (Pubitemid 32529840)
65. A. Weetman Immune reconstitution syndrome and the thyroid Best Pract Res Clin Endocrinol Metab 23 2009 693 702
66. S. Aktaran, E. Akarsu, I. Erbaǧci, M. Araz, S. Okumuş, and M. Kartal Comparison of intravenous methylprednisolone therapy vs. oral methylprednisolone therapy in patients with Graves' ophthalmopathy Int J Clin Pract 61 2007 45 51
67. G.J. Kahaly, S. Pitz, G. Hommel, and M. Dittmar Randomized, single blind trial of intravenous versus oral steroid monotherapy in Graves' orbitopathy J Clin Endocrinol Metab 90 2005 5234 5240 (Pubitemid 41262280)
68. A. De Bellis, A. Bizzarro, M. Conte, C. Coronella, S. Solimeno, and S. Perrino Relationship between longitudinal behaviour of some markers of eye autoimmunity and changes in ocular findings in patients with Graves' ophthalmopathy receiving corticosteroid therapy Clin Endocrinol 59 2003 388 395 (Pubitemid 37046994)
69. E. Arteaga, J.M. López, J.A. Rodríguez, P. Michaud, and G. López Effect of the combination of dexamethasone and sodium ipodate on serum thyroid hormones in Graves' disease Clin Endocrinol 19 1983 619 627 (Pubitemid 14226002)
70. A. Gamstedt, B. Kågedal, and L. Tegler Serum free thyroid hormones are decreased by betamethasone treatment in Graves' disease Horm Metab Res 20 1988 54 56 (Pubitemid 18053230)
71. S.A. Peter Remission of Graves' disease with hyperthyroidism by a combination of glucocorticoids and antithyroid drugs J Natl Med Assoc 83 1991 261 264
72. X.M. Mao, H.Q. Li, Q. Li, D.M. Li, X.J. Xie, and G.P. Yin Prevention of relapse of Graves' disease by treatment with an intrathyroid injection of dexamethasone J Clin Endocrinol Metab 94 2009 4984 4991
73. P.J. Quesenberry, G. Colvin, and M. Abedi Perspective: fundamental and clinical concepts on stem cell homing and engraftment: a journey to niches and beyond Exp Hematol 33 2005 9
74. I.W. Abrahamsen, S. Somme, D. Heldal, T. Egeland, D. Kvale, and G.E. Tjonnfjord Immune reconstitution after allogeneic stem cell transplantation: the impact of stem cell source and graft-versus-host disease Haematologica 90 2005 86
75. A.M. Marmont Autoimmunity and allogeneic bone marrow transplantation Bone Marrow Transplant 9 1990 1 2
76. Y. Sherer, and Y. Shoenfeld Autoimmune diseases and autoimmunity post transplantation Bone Marrow Transplant 22 1998 873 888
77. A.M. Marmont Stem cell transplantation for severe autoimmune diseases: progress and problems Haematologica 83 1998 733 743 (Pubitemid 28492156)
78. M. Karthaus, T. Gabrysiak, G. Brabant, A. Prahst, H. Link, and B. Soudah Immune thyroiditis after transplantation of allogeneic CD34 + selected peripheral blood cells Bone Marrow Transplant 20 1997 697 699 (Pubitemid 27477586)
79. S. Díez, H. Banias, J.L. Díez-Martin, M. Briz, J. Estrado, and B. Barceló Apparent cure of Graves Basedow disease after sibling allogeneic bone marrow transplantation Clin Endocrinol 50 1999 267 270 (Pubitemid 29100016)
80. W.Y. Lee, E.S. Oh, C.K. Min, D.W. Kim, J.W. Lee, and M.I. Kang Changes in autoimmune thyroid disease following allogeneic bone marrow transplantation Bone Marrow Transplant 28 2001 63 66 (Pubitemid 32707619)
81. A.V. Misharin, Y. Nagayama, H.A. Aliesky, Y. Mizutori, B. Rapoport, and S.M. McLachlan Attenuation of induced hyperthyroidism in mice by pre-treatment with thyrotropin receptor protein: deviation from thyroid-stimulating to non-functional antibodies Endocrinology 150 2009 3944 3952
82. R.N. Dogan, C. Vasu, M.J. Holterman, and B.S. Prabhakar Absence of IL-4 and not suppression of the Th2 response, prevents development of experimental autoimmune Graves' disease J Immunol 170 2003 2195 2204 (Pubitemid 36197444)
83. C. Vasu, S.R. Gorla, B.S. Prabhakar, and M.J. Holterman Targeted engagement of CTLA-4 prevents autoimmune thyroiditis Int Immunol 15 2003 641 654 (Pubitemid 36519401)
84. C. Lenzner, and N.G. Morgenthaler The effect of thyrotropin-receptor blocking antibodies on stimulating autoantibodies from patients with Graves' disease Thyroid 13 2003 1153 1161 (Pubitemid 38032401)
85. J. Sanders, M. Evans, C. Betterle, P. Sanders, A. Bhardwaja, and S. Young A human monoclonal auto-antibody to the thyrotropin receptor with thyroid-stimulating blocking activity Thyroid 18 2008 735 746 (Pubitemid 352009924)
86. J.C. Edwards, and G. Cambridge B-cell targeting in rheumatoid arthritis and other autoimmune diseases Nat Rev Immunol 6 2006 394 403
87. H.C. Hasselbach B-cell depletion with rituximab-a targeted therapy for Graves' disease and autoimmune thyroiditis Immunol Lett 88 2003 85 86
88. D. El Fassi, C.H. Nielsen, S.J. Bonnema, H.C. Hasselbalch, and L. Hegedüs B lymphocyte depletion with the monoclonal antibody Rituximab in Graves' disease. A controlled pilot study J Clin Endocrinol Metab 92 2007 1769 1772 (Pubitemid 46997186)
89. M. Salvi, G. Vannucchi, I. Campi, N. Currò, D. Dazzi, and S. Simonetta Treatment of Graves' disease and associated opthalmopathy with the anti-CD20 monoclonal antibody rituximab: an open study Eur J Endocrinol 156 2007 33 40 (Pubitemid 46553901)
90. K.A. Heemstra, R.E. Toes, J. Sepers, A.M. Pereira, E.P. Corssmit, and T.W. Huizinga Rituximab in relapsing Graves' disease, a phase II study Eur J Endocrinol 159 2008 609 615
91. M.K. Slifka, and R. Ahmed Long-lived plasma cells: a mechanism for maintaining persistent antibody production Curr Opin Immunol 10 1998 252 258 (Pubitemid 28286950)
92. M.J. Leandro, G. Cambridge, M.R. Ehrenstein, and J.C. Edwards Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis Arthritis Rheum 54 2006 613 620 (Pubitemid 43228639)
93. D. El Fassi, O. Clemmensen, C.H. Nielsen, R.Z. Silkiss, and L. Hegedüs Evidence of intrathyroidal B-lymphocyte depletion after rituximab therapy in a patient with Graves' disease J Clin Endocrinol Metab 92 2007 3762 3763 (Pubitemid 47607619)
94. C.H. Nielsen, R.G. Leslie, B.S. Jepsen, M.D. Kazatchkine, S.V. Kaveri, and E. Fischer Natural autoantibodies and complement promote the uptake of a self antigen, human thyroglobulin, by B cells and the proliferation of thyroglobulin-reactive CD4(+) T cells in healthy individuals Eur J Immunol 31 2001 2660 2668 (Pubitemid 32898733)
95. C.H. Nielsen, L. Hegedüs, and R.G. Leslie Autoantibodies in autoimmune thyroid disease promote immune complex formation with self antigens and increase B cell and CD4 + T cell proliferation in response to self antigens Eur J Immunol 34 2004 263 272 (Pubitemid 38111542)
96. E. Toubi, A. Kessel, G. Slobodin, N. Boulman, E. Pavlotzky, and D. Zisman Changes in macrophage function afterrituximab treatment in patients with rheumatoid arthritis Ann Rheum Dis 66 2007 818 820 (Pubitemid 46846705)
97. Z. Keren, Y. Braun-Moscovici, D. Markovits, A. Rozin, M. Nahir, and A. Balbir-Gurman Depletion of B lymphocytes in rheumatoid arthritis patients modifies IL-8-anti-IL-8 autoantibody network Clin Immunol 113 2009 108 116
98. A.J. Ferraro, M.T. Drayson, C.O. Savage, and I.C. MacLennan Levels of autoantibodies, unlike antibodies to all extrinsic antigen groups, fall following B cell depletion with Rituximab Eur J Immunol 38 2008 292 298
99. D. El Fassi, C.H. Nielsen, H.C. Hasselbalch, and L. Hegedüs Treatment-resistant severe, active Graves' ophthalmopathy successfully treated with B lymphocyte depletion Thyroid 16 2006 709 710
100. M. Salvi, G. Vannucchi, I. Campi, S. Rossi, P. Bonara, and F. Sbrozzi Efficacy of rituximab treatment for thyroid-associated ophthalmopathy as a result of intraorbital B-cell depletion in one patient unresponsive to steroid immunosuppression Eur J Endocrinol 154 2006 511 517
101. E. Mössner, P. Brünker, S. Moser, U. Püntener, C. Schmidt, and S. Herter Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell mediated B-cell cytotoxicity Blood 15 2010 4393 4402
102. J.A. Gilbert Treatment of autoimmune hyperthyroidism in a murine model of Graves' disease with tumor necrosis factor-family ligand inhibitors suggests a key role for B cell activating factor in disease pathology Endocrinology 147 2006 4561 4568 (Pubitemid 44402161)
103. E. Toubi, and Y. Shoenfeld The role of CD40-CD154 interactions in autoimmunity and the benefit of disrupting this pathway Autoimmunity 37 2004 457 464 (Pubitemid 40123415)
104. A. Bhushan, and L.R. Covey CD40:CD40L interactions in X-linked and non-X-linked hyper-IgM syndromes Immunol Res 24 2001 311 324 (Pubitemid 33064389)
105. G. Carayanniotis, S.R. Masters, and R.J. Noelle Suppression of murine thyroiditis via blockade of the CD40-CD40 L interaction Immunology 90 1997 421 426 (Pubitemid 27102110)
106. T.J. Smith Insulin-like growth factor-I regulation of immune function: a potential therapeutic target in autoimmune diseases? Pharmacol Rev 62 2010 199 236