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Genetic immunization of outbred mice with thyrotropin receptor cDNA provides a model of Graves’ disease

Sabine Costagliola, … , Samuel Refetoff, Gilbert Vassart

Sabine Costagliola, … , Samuel Refetoff, Gilbert Vassart

Published March 15, 2000
Citation Information: J Clin Invest. 2000;105(6):803-811. https://doi.org/10.1172/JCI7665.

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Citations to this article (114)

Title and authors	Publication	Year
Graves disease: latest understanding of pathogenesis and treatment options. Lanzolla G, Marinò M, Menconi F	Nature reviews. Endocrinology	2024
Insight Into Mouse Models of Hyperthyroidism. Zhang M, Jiang W, Lu G, Wang R, Lv Z, Li D	Frontiers in Endocrinology	2022
Antibodies against thyroid‑stimulating hormone receptor cause maternal‑neonatal transmission of Graves' Disease Y Yu, QQ Liu, DY Liu, DD Wang, LQ Yang, SM Ye	Experimental and therapeutic medicine	2021
Lessons from mouse models of Graves’ disease A Eckstein, S Philipp, G Goertz, JP Banga, U Berchner-Pfannschmidt	Endocrine	2020
A Novel Long-Term Graves’ Disease Animal Model Confirmed by Functional Thyrotropin Receptor Antibodies T Diana, HP Holthoff, J Fassbender, C Wüster, M Kanitz, GJ Kahaly, M Ungerer	European Thyroid Journal	2020
A methodological review of induced animal models of autoimmune diseases X Yu, F Petersen	Autoimmunity Reviews	2018
Noninflammatory Diffuse Follicular Hypertrophy/Hyperplasia of Graves Disease: Morphometric Evaluation in an Experimental Mouse Model A Schlüter, AK Eckstein, A Brenzel, M Horstmann, S Lang, U Berchner-Pfannschmidt, JP Banga, S Diaz-Cano	European Thyroid Journal	2018
Graves’ orbitopathy occurs sex-independently in an autoimmune hyperthyroid mouse model A Schlüter, U Flögel, S Diaz-Cano, GE Görtz, K Stähr, M Oeverhaus, S Plöhn, S Mattheis, LC Moeller, S Lang, NE Bechrakis, JP Banga, A Eckstein, U Berchner-Pfannschmidt	Scientific Reports	2018
Insulin-like Growth Factor-I Receptor and Thyroid-Associated Ophthalmopathy TJ Smith, JA Janssen	Endocrine reviews	2018
The Association between ocular problems and Serum Testosterone, Prolactin and Thyroglobulin concentrations in Delayed phase of Sulfur Mustard exposure Hassan Ghasemi, Nayere Askari, Sakine Moaiedmohseni, Soghrat Faghihzadeh, Susan Kabudanian Ardestani, Elham Faghihzadeh, Tooba Ghazanfari	Iranian Journal of Pathology	2018
An improved method for the establishment of a model of Graves' disease in BALB/c mice W Zheng, R Wang, J Tan, N Li, Z Meng	Molecular medicine reports	2017
Effects of Combined Exposure to Chronic High-Fat Diet and Arsenic on Thyroid Function and Lipid Profile in Male Mouse A Ahangarpour, S Alboghobeish, AA Oroojan, L Zeidooni, A Samimi, G Afshari	Biological Trace Element Research	2017
EBI2 receptor regulates myelin development and inhibits LPC-induced demyelination A Rutkowska, AW Sailer, KK Dev	Journal of Neuroinflammation	2017
Overexpression of IL-4 in the thyroid of transgenic mice upregulates the expression of Duox1 and the anion transporter pendrin Z Eskalli, Y Achouri, S Hahn, MC Many, J Craps, S Refetoff, XH Liao, JE Dumont, JV sande, B Corvilain, F Miot, XD Deken	Thyroid	2016
Excessive Cytosolic DNA Fragments as a Potential Trigger of Graves’ Disease: An Encrypted Message Sent by Animal Models Y Luo, A Yoshihara, K Oda, Y Ishido, K Suzuki	Frontiers in Endocrinology	2016
Review of Mouse Models of Graves’ Disease and Orbitopathy—Novel Treatment by Induction of Tolerance M Ungerer, J Faßbender, Z Li, G Münch, HP Holthoff	Clinical Reviews in Allergy & Immunology	2016
Endocrinology: Adult and Pediatric M Gurnell, TJ Visser, P Beck-Peccoz, VK Chatterjee	Endocrinology: Adult and Pediatric	2016
The fully synthetic MAG-Tn3 therapeutic vaccine containing the tetanus toxoid-derived TT830-844 universal epitope provides anti-tumor immunity D Laubreton, S Bay, C Sedlik, C Artaud, C Ganneau, E Dériaud, S Viel, AL Puaux, S Amigorena, C Gérard, R Lo-Man, C Leclerc	Cancer Immunology, Immunotherapy	2016
A Unique Mouse Strain That Develops Spontaneous, Iodine-Accelerated, Pathogenic Antibodies to the Human Thyrotrophin Receptor B Rapoport, HA Aliesky, B Banuelos, CR Chen, SM McLachlan	Journal of immunology (Baltimore, Md. : 1950)	2015
Crystal Structure of a TSH Receptor Monoclonal Antibody: Insight Into Graves' Disease Pathogenesis CR Chen, PA Hubbard, LM Salazar, SM McLachlan, R Murali, B Rapoport	Molecular Endocrinology	2015
Graves’ Disease Mechanisms: The Role of Stimulating, Blocking, and Cleavage Region TSH Receptor Antibodies S Morshed, T Davies	Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et métabolisme	2015
Breaking Tolerance to Thyroid Antigens: Changing Concepts in Thyroid Autoimmunity SM McLachlan, B Rapoport	Endocrine reviews	2014
EBI2 regulates intracellular signaling and migration in human astrocyte: EBI2 Signaling and Role in Astrocytes A Rutkowska, I Preuss, F Gessier, AW Sailer, KK Dev	Glia	2014
Immunization of mice with a newly identified thyroid-stimulating hormone receptor splice variant induces Graves'-like disease T Endo, T Kobayashi	Journal of Autoimmunity	2013
Receptor-activating autoantibodies and disease: preeclampsia and beyond Y Xia, RE Kellems	Expert Review of Clinical Immunology	2011
Orbital fibrosis in a mouse model of Graves' disease induced by genetic immunization of thyrotropin receptor cDNA SX Zhao, S Tsui, A Cheung, RS Douglas, TJ Smith, JP Banga	The Journal of endocrinology	2011
Distinct Genetic Signatures for Variability in Total and Free Serum Thyroxine Levels in Four Sets of Recombinant Inbred Mice SM McLachlan, L Lu, HA Aliesky, RW Williams, B Rapoport	Endocrinology	2011
Cloning of the TSH receptor: The story from a Brussels perspective G Vassart	Annales d'Endocrinologie	2011
Mast cell-derived prostaglandin D2 controls hyaluronan synthesis in human orbital fibroblasts via DP1 activation: implications for thyroid eye disease N Guo, CJ Baglole, CW O'Loughlin, SE Feldon, RP Phipps	The Journal of biological chemistry	2010
Effects of hyperthyroidism on the rectus muscles in mice CJ Nien, JV Jester, S Bose	Frontiers in neurology	2010
Mast Cell-derived Prostaglandin D 2 Controls Hyaluronan Synthesis in Human Orbital Fibroblasts via DP1 Activation: IMPLICATIONS FOR THYROID EYE DISEASE N Guo, CJ Baglole, CW O'Loughlin, SE Feldon, RP Phipps	The Journal of biological chemistry	2010
Immunoendocrinology: Scientific and Clinical Aspects GS Eisenbarth		2010
Immunization with thyroglobulin induces Graves'-like disease in mice T Endo, T Kobayashi	The Journal of endocrinology	2009
Pulmonary surfactant: an immunological perspective ZC Chroneos, Z Sever-Chroneos, VL Shepherd	Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology	2009
Immune response of mice transgenic for human histocompatibility leukocyte Antigen-DR to human thyrotropin receptor-extracellular domain H Inaba, D Pan, YH Shin, W Martin, G Buchman, LJ de Groot	Thyroid : official journal of the American Thyroid Association	2009
Thyroid antigens, not central tolerance, control responses to immunization in BALB/c versus C57BL/6 mice AV Misharin, B Rapoport, SM McLachlan	Thyroid : official journal of the American Thyroid Association	2009
Toward Better Models of Hyperthyroid Graves' Disease S Dağdelen, YM Kong, JP Banga	Endocrinology & Metabolism Clinics of North America	2009
Analytical aspects of thyroid antibodies estimation D Sinclair	Autoimmunity	2008
Identification of apoptotic proteins in thyroid gland from patients with Graves' disease and Hashimoto's thyroiditis A Bossowski, B Czarnocka, K Bardadin, A Stasiak-Barmuta, M Urban, J Dadan, K Ratomski, A Bossowska	Autoimmunity	2008
Autoimmune Diseases in Endocrinology AP Weetman		2008
An Improved Graves’ Disease Model Established by Using in Vivo Electroporation Exhibited Long-Term Immunity to Hyperthyroidism in BALB/c Mice T Kaneda, A Honda, A Hakozaki, T Fuse, A Muto, T Yoshida	Endocrinology	2007
Association between thyroid-stimulating immunoglobulin levels and ocular findings in pediatric patients with Graves disease OM Acuna, I Athannassaki, EA Paysse	Transactions of the American Ophthalmological Society	2007
Functional Characterization of Human Thyroid Tissue with Immunohistochemistry A Faggiano, B Caillou, L Lacroix, M Talbot, S Filetti, J Bidart, M Schlumberger	Thyroid	2007
Monoclonal Pathogenic Antibodies to the Thyroid-Stimulating Hormone Receptor in Graves’ Disease with Potent Thyroid-Stimulating Activity but Differential Blocking Activity Activate Multiple Signaling Pathways JA Gilbert, AG Gianoukakis, S Salehi, J Moorhead, PV Rao, MZ Khan, AM McGregor, TJ Smith, JP Banga	Journal of immunology (Baltimore, Md. : 1950)	2006
Antibodies Focused on the Human Autoantibody Immunodominant Region Are Induced by B Lymphocytes that Constitutively Express Thyroid Peroxidase Diverted to the Major Histocompatibility Complex II Pathway J Guo, SM McLachlan, B Rapoport	Thyroid	2006
New insights into antibody-mediated hyperthyroidism R Ajjan, A Weetman	Expert Review of Endocrinology & Metabolism	2006
Longitudinal Correlation of Thyroid-Stimulating Immunoglobulin With Clinical Activity of Disease in Thyroid-Associated Orbitopathy LR Dragan, SR Seiff, DC Lee	Ophthalmic Plastic & Reconstructive Surgery	2006
Differential Susceptibility of BALB/c and BALB/cBy Mice to Graves' Hyperthyroidism GS Seetharamaiah, KJ Land	Thyroid	2006
The Autoimmune Diseases I Kang, J Craft	The Autoimmune Diseases	2006
Interferon- -induced hyperthyroidism: a three-stage evolution from silent thyroiditis towards Graves' disease NL Bohbot, J Young, J Orgiazzi, C Buffet, M Francois, B Bernard-Chabert, C Lukas-Croisier, B Delemer	European Journal of Endocrinology	2006
Insight into Graves’ Hyperthyroidism from Animal Models SM McLachlan, Y Nagayama, B Rapoport	Endocrine reviews	2005
Cathepsin S is not crucial to TSHR processing and presentation in a murine model of Graves' disease M Kala, CR Chen, SM McLachlan, B Rapoport, H Aliesky, HA Chapman	Immunology	2005
Thyrotropin receptor antibodies: new insights into their actions and clinical relevance T Ando, R Latif, TF Davies	Best Practice & Research Clinical Endocrinology & Metabolism	2005
Dissociation between Iodide-Induced Thyroiditis and Antibody-Mediated Hyperthyroidism in NOD.H-2h4 Mice SM McLachlan, H Braley-Mullen, CR Chen, H Aliesky, PN Pichurin, B Rapoport	Endocrinology	2005
Quantification of cells expressing the thyrotropin receptor in extraocular muscles in thyroid associated orbitopathy A Boschi, C Daumerie, M Spiritus, C Beguin, M Senou, D Yuksel, M Duplicy, S Costagliola, M Ludgate, MC Many	The British journal of ophthalmology	2005
Animal Models of Graves' Hyperthyroidism Y NAGAYAMA	Endocrine Journal	2005
DNA vaccination against tumors GJ Prud'homme	The Journal of Gene Medicine	2005
The Clinicopathologic Basis of Graves' Ophthalmopathy: A Review S Kloprogge, L Kowal, J Wall, AG Frauman	European journal of ophthalmology	2005
Monoclonal Antibodies to the Thyrotropin Receptor T Ando, TF Davies	Clinical and Developmental Immunology	2005
Concentration-dependent regulation of thyrotropin receptor function by thyroid stimulating antibody Takao Ando, Rauf Latif, and Terry F Davies	Journal of Clinical Investigation	2004
Superiority of thyroid peroxidase DNA over protein immunization in replicating human thyroid autoimmunity in HLA-DRB1*0301 (DR3) transgenic mice JC Flynn, A Gardas, Q Wan, M Gora, G Alsharabi, WZ Wei, AA Giraldo, CS David, YM Kong, JP Banga	Clinical & Experimental Immunology	2004
Role of Apoptosis in Autoimmunity M Todaro, A Zeuner, G Stassi	Journal of Clinical Immunology	2004
“Hijacking” the Thyrotropin Receptor: A Chimeric Receptor-Lysosome Associated Membrane Protein Enhances Deoxyribonucleic Acid Vaccination and Induces Graves’ Hyperthyroidism PN Pichurin, GD Chazenbalk, H Aliesky, O Pichurina, B Rapoport, SM McLachlan	Endocrinology	2004
Low-Dose Immunization with Adenovirus Expressing the Thyroid-Stimulating Hormone Receptor A-Subunit Deviates the Antibody Response toward That of Autoantibodies in Human Graves’ Disease CR Chen, P Pichurin, GD Chazenbalk, H Aliesky, Y Nagayama, SM McLachlan, B Rapoport	Endocrinology	2004
Dissecting Linear and Conformational Epitopes on the Native Thyrotropin Receptor T Ando, R Latif, S Daniel, K Eguchi, TF Davies	Endocrinology	2004
Induction of hyperthyroidism in mice by intradermal immunization with DNA encoding the thyrotropin receptor K Barrett, E Liakata, PV Rao, PF Watson, AP Weetman, P Lymberi, JP Banga, G Carayanniotis	Clinical & Experimental Immunology	2004
Susceptibility Rather than Resistance to Hyperthyroidism Is Dominant in a Thyrotropin Receptor Adenovirus-Induced Animal Model of Graves’ Disease as Revealed by BALB/c-C57BL/6 Hybrid Mice CR Chen, H Aliesky, PN Pichurin, Y Nagayama, SM McLachlan, B Rapoport	Endocrinology	2004
Thyroid stimulating monoclonal antibodies: overcoming the road blocks and the way forward SM McLachlan, B Rapoport	Clinical Endocrinology	2004
Graves' hyperthyroidism and thyroiditis in HLA-DRB1*0301 (DR3) transgenic mice after immunization with thyrotropin receptor DNA JC Flynn, PV Rao, M Gora, G Alsharabi, W Wei, AA Giraldo, CS David, JP Banga, YM Kong	Clinical & Experimental Immunology	2004
Infection and Autoimmunity C Dugué, Y Renaudineau, P Youinou	Infection and Autoimmunity	2004
Inducing Graves’ ophthalmopathy M Ludgate, G Baker	Journal of Endocrinological Investigation	2004
Eye muscle antibodies in Graves’ ophthalmopathy: Pathogenic or secondary epiphenomenon? T Mizokami, M Salvi, JR Wall	Journal of Endocrinological Investigation	2004
Graves’ ophthalmopathy: State of the art and perspectives L Bartalena, WM Wiersinga, A Pinchera	Journal of Endocrinological Investigation	2004
New understanding of the role of cytokines in the pathogenesis of Graves’ ophthalmopathy RA Ajjan, AP Weetman	Journal of Endocrinological Investigation	2004
Immunoendocrinology in Health and Disease N Martens, E Hooghe-Peters, R Hooghe	Immunoendocrinology in Health and Disease	2004
The thyrotropin receptor autoantigen in Graves' disease is the culprit as well as the victim Chun-Rong Chen, Pavel Pichurin, Yuji Nagayama, Francesco Latrofa, Basil Rapoport and Sandra M. McLachlan	Journal of Clinical Investigation	2003
Insight into antibody responses induced by plasmid or adenoviral vectors encoding thyroid peroxidase, a major thyroid autoantigen J Guo, P Pichurin, Y Nagayama, B Rapoport, SM McLachlan	Clinical & Experimental Immunology	2003
Thyrotrophin receptor-specific memory T cell responses require normal B cells in a murine model of Graves' disease P Pichurin, H Aliesky, CR Chen, Y Nagayama, B Rapoport, SM McLachlan	Clinical & Experimental Immunology	2003
Current Perspective on the Pathogenesis of Graves’ Disease and Ophthalmopathy BS Prabhakar, RS Bahn, TJ Smith	Endocrine reviews	2003
Thyrotropin Receptor-DNA Vaccination of Transgenic Mice Expressing HLA-DR3 or HLA-DQ6b P Pichurin, CR Chen, O Pichurina, C David, B Rapoport, SM McLachlan	Thyroid	2003
Dendritic cells infected with adenovirus expressing the thyrotrophin receptor induce Graves' hyperthyroidism in BALB/c mice M Kita-Furuyama, Y Nagayama, P Pichurin, SM McLachlan, B Rapoport, K Eguchi	Clinical & Experimental Immunology	2003
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Novel murine models of thyroid autoimmunity Y Nagayama	Current Opinion in Endocrinology & Diabetes	2003
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A Major Role for Non-Major Histocompatibility Complex Genes But not for Microorganisms in a Novel Murine Model of Graves' Hyperthyroidism Y Nagayama, SM McLachlan, B Rapoport, M Niwa	Thyroid	2003
Novel murine models of thyroid autoimmunity: Y Nagayama	Current Opinion in Endocrinology & Diabetes	2003
Monoclonal Antibodies to Thyroid Specific Autoantigens T Akamizu	Autoimmunity	2003
HLA and H2 Class II Transgenic Mouse Models to Study Susceptibility and Protection in Autoimmune Thyroid Disease YC Kong, JC Flynn, Q Wan, CS David	Autoimmunity	2003
Contrasting Activities of Thyrotropin Receptor Antibodies in Experimental Models of Graves’ Disease Induced by Injection of Transfected Fibroblasts or Deoxyribonucleic Acid Vaccination PV Rao, PF Watson, AP Weetman, G Carayanniotis, JP Banga	Endocrinology	2003
Induction of Thyroid-Stimulating Hormone Receptor Autoimmunity in Hamsters T Ando, M Imaizumi, P Graves, P Unger, TF Davies	Endocrinology	2003
Prevention of Autoantibody-Mediated Graves’-Like Hyperthyroidism in Mice with IL-4, a Th2 Cytokine Y Nagayama, H Mizuguchi, T Hayakawa, M Niwa, SM McLachlan, B Rapoport	Journal of immunology (Baltimore, Md. : 1950)	2003
THE FREE A SUBUNIT, NOT THE HOLORECEPTOR, IS PREFERENTIALLY RECOGNIZED BY THYROID STIMULATING AUTOANTIBODIES IN GRAVES’ DISEASE Gregorio D. Chazenbalk, Pavel Pichurin, Chun-Rong Chen, Francesco Latrofa, Alan P. Johnstone, Sandra M. McLachlan, Basil Rapoport	Journal of Clinical Investigation	2002
Demonstration of immunoglobulin G, A, and E autoantibodies to the human thyrotropin receptor using flow cytometry R Metcalfe, N Jordan, P Watson, S Gullu, M Wiltshire, M Crisp, C Evans, A Weetman, M Ludgate	The Journal of clinical endocrinology and metabolism	2002
Igs from patients with Graves' disease induce the expression of T cell chemoattractants in their fibroblasts J Pritchard, N Horst, W Cruikshank, TJ Smith	Journal of immunology (Baltimore, Md. : 1950)	2002
Role of Cytokines in the Pathogenesis of Thyroid-Associated Ophthalmopathy Y Hiromatsu, H Kaku, I Miyake, S Murayama, E Soejima	Thyroid	2002
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AUTOIMMUNE THYROID DISEASE: NEW MODELS OF CELL DEATH IN AUTOIMMUNITY G Stassi, RD Maria	Nature Reviews Immunology	2002
Autoimmune endocrine disease MS Anderson	Current Opinion in Immunology	2002
Generation of a mouse monoclonal TSH receptor antibody with stimulating activity S Costagliola, JD Franssen, M Bonomi, E Urizar, M Willnich, A Bergmann, G Vassart	Biochemical and Biophysical Research Communications	2002
Use of DNA immunization to produce polyclonal antibodies against the native human neurokinin-1 receptor for substance P S Tymciu, A Wijkhuisen, MA Sagot, Y Frobert, J Grassi, C Créminon, JY Couraud, D Boquet	Journal of Neuroimmunology	2002
Animal Models of Thyroid-Associated Ophthalmopathy ME Ludgate	Thyroid	2002
Peptide Scanning for Thyrotropin Receptor T-Cell Epitopes in Mice Vaccinated with Naked DNA P Pichurin, L Schwarz-Lauer, H Braley-Mullen, C Paras, O Pichurina, JC Morris, B Rapoport, SM McLachlan	Thyroid	2002
Monoclonal Antibodies with Thyroid Stimulating Activity, at Last S Costagliola, G Vassart	Thyroid	2002
Thyroid-Stimulating Monoclonal Antibodies J Sanders, J Jeffreys, H Depraetere, T Richards, M Evans, A Kiddie, K Brereton, M Groenen, Y Oda, J Furmaniak, BR Smith	Thyroid	2002
Characterization of the Thyrotropin Binding Pocket J Jeffreys, H Depraetere, J Sanders, Y Oda, M Evans, A Kiddie, T Richards, J Furmaniak, BR Smith	Thyroid	2002
Thyroid Eye Disease: Diagnosis and Treatment J Noort	Thyroid Eye Disease: Diagnosis and Treatment	2002
A Novel Murine Model of Graves’ Hyperthyroidism with Intramuscular Injection of Adenovirus Expressing the Thyrotropin Receptor Y Nagayama, M Kita-Furuyama, T Ando, K Nakao, H Mizuguchi, T Hayakawa, K Eguchi, M Niwa	Journal of immunology (Baltimore, Md. : 1950)	2002
Antithyrotropin Receptor Antibody: An Update T Akamizu	Thyroid	2001
Thyroid Eye Disease RS Bahn		2001
Helper T cells in antibody-mediated, organ-specific autoimmunity CJ Elson, RN Barker	Current Opinion in Immunology	2000
Cytokines, IgG subclasses and costimulation in a mouse model of thyroid autoimmunity induced by injection of fibroblasts co-expressing MHC class II and thyroid autoantigens XM Yan, J Guo, P Pichurin, K Tanaka, JC Jaume, B Rapoport, SM McLachlan	Clinical & Experimental Immunology	2000
Progress in our understanding of the pathogenesis of Graves ophthalmopathy M Ludgate, K Starkey	Current Opinion in Endocrinology & Diabetes	2000
Graves' Ophthalmopathy in the Absence of Elevated Free Thyroxine and Triiodothyronine Levels: Prevalence, Natural History, and Thyrotropin Receptor Antibody Levels DH Khoo, PH Eng, SC Ho, ES Tai, NG Morgenthaler, LL Seah, KS Fong, SP Chee, CT Choo, SE Aw	Thyroid	2000

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