Lessons from mouse models of Graves' disease.
Journal
Endocrine
ISSN: 1559-0100
Titre abrégé: Endocrine
Pays: United States
ID NLM: 9434444
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
26
11
2019
accepted:
07
04
2020
pubmed:
14
5
2020
medline:
22
6
2021
entrez:
14
5
2020
Statut:
ppublish
Résumé
Graves' disease (GD) is an autoimmune condition with the appearance of anti-TSH receptor (TSHR) autoantibodies in the serum. The consequence is the development of hyperthyroidism in most of the patients. In addition, in the most severe cases, patients can develop orbitopathy (GO), achropachy and dermopathy. The central role of the TSHR for the disease pathology has been well accepted. Therefore immunization against the TSHR is pivotal for the creation of in vivo models for the disease. However, TSHR is well preserved among the species and therefore the immune system is highly tolerant. Many differing attempts have been performed to break tolerance and to create a proper animal model in the last decades. The most successful have been achieved by introducing the human TSHR extracellular domain into the body, either by injection of plasmid or adenoviruses. Currently available models develop the whole spectrum of Graves' disease-autoimmune thyroid disease and orbitopathy and are suitable to study disease pathogenesis and to perform treatment studies. In recent publications new immunomodulatory therapies have been assessed and also diseaseprevention by inducing tolerance using small cyclic peptides from the antigenic region of the extracellular subunit of the TSHR.
Identifiants
pubmed: 32399893
doi: 10.1007/s12020-020-02311-7
pii: 10.1007/s12020-020-02311-7
pmc: PMC7266836
doi:
Substances chimiques
Autoantibodies
0
Receptors, Thyrotropin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
265-270Références
R.S. Bahn, Current insights into the pathogenesis of Graves’ ophthalmopathy. Horm. Metab. Res. 47, 773–778 (2015)
doi: 10.1055/s-0035-1555762
T.F. Davies, T. Ando, R.Y. Lin et al. Thyrotropin receptor-associated diseases: from adenomata to Graves disease. J. Clin. Investig. 115, 1972–1983 (2005)
doi: 10.1172/JCI26031
R.S. Bahn, Thyrotropin receptor expression in orbital adipose/connective tissues from patients with thyroid-associated ophthalmopathy. Thyroid 12, 193–195 (2002)
doi: 10.1089/105072502753600124
S. Kumar, S. Iyer, H. Bauer et al. A stimulatory thyrotropin receptor antibody enhances hyaluronic acid synthesis in graves’ orbital fibroblasts: inhibition by an IGF-I receptor blocking antibody. J. Clin. Endocrinol. Metab. 97, 1681–1687 (2012)
doi: 10.1210/jc.2011-2890
S. Kumar, S. Nadeem, M.N. Stan et al. A stimulatory TSH receptor antibody enhances adipogenesis via phosphoinositide 3-kinase activation in orbital preadipocytes from patients with Graves’ ophthalmopathy. J. Mol. Endocrinol. 46, 155–163 (2011)
doi: 10.1530/JME-11-0006
S. Kumar, R. Schiefer, M.J. Coenen et al. A stimulatory thyrotropin receptor antibody (M22) and thyrotropin increase interleukin-6 expression and secretion in Graves’ orbital preadipocyte fibroblasts. Thyroid 20, 59–65 (2010)
doi: 10.1089/thy.2009.0278
A. Eckstein, J. Esser, S. Mattheis et al. [Graves’ Orbitopathy]. Klin. Monbl Augenheilkd. 233, 1385–1407 (2016)
doi: 10.1055/s-0042-118040
C.C. Krieger, S. Neumann, B. Marcus-Samuels et al. TSHR/IGF-1R Cross-Talk, not IGF-1R stimulating antibodies, mediates Graves’ ophthalmopathy pathogenesis. Thyroid 27, 746–747 (2017)
doi: 10.1089/thy.2017.0105
C.C. Krieger, R.F. Place, C. Bevilacqua, et al., Thyrotropin/IGF-1 receptor crosstalk in Graves’ ophthalmopathy pathogenesis. J. Clin. Endocrinol. Metab. 101, 2340–2347 (2016)
doi: 10.1210/jc.2016-1315
T.J. Smith, J. Janssen, Insulin-like growth factor-I receptor and thyroid-associated ophthalmopathy. Endocr. Rev. 40, 236–267 (2019)
doi: 10.1210/er.2018-00066
Y. Hiromatsu, D. Yang, T. Bednarczuk et al. Cytokine profiles in eye muscle tissue and orbital fat tissue from patients with thyroid-associated ophthalmopathy. J. Clin. Endocrinol. Metab. 85, 1194–1199 (2000)
pubmed: 10720061
S.J. Shan, R.S. Douglas, The pathophysiology of thyroid eye disease. J. Neuroophthalmol. 34, 177–185 (2014)
doi: 10.1097/WNO.0000000000000132
S. Plohn, B. Edelmann, L. Japtok et al. CD40 enhances sphingolipids in orbital fibroblasts: potential role of sphingosine-1-phosphate in inflammatory T-cell migration in Graves’ orbitopathy. Investig. Ophthalmol. Vis. Sci. 59, 5391–5397 (2018)
doi: 10.1167/iovs.18-25466
G.E. Gortz, M. Horstmann, B. Aniol et al. Hypoxia-dependent HIF-1 activation impacts on tissue remodeling in Graves’ ophthalmopathy-implications for smoking. J. Clin. Endocrinol. Metab. 101, 4834–4842 (2016)
doi: 10.1210/jc.2016-1279
S.M. Mclachlan, Y. Nagayama, B. Rapoport, Insight into Graves’ hyperthyroidism from animal models. Endocr. Rev. 26, 800–832 (2005)
doi: 10.1210/er.2004-0023
B. Wiesweg, K.T. Johnson, A.K. Eckstein et al. Current insights into animal models of Graves’ disease and orbitopathy. Horm. Metab. Res. 45, 549–555 (2013)
doi: 10.1055/s-0033-1343451
Y. Nagayama, M. Kita-Furuyama, T. Ando et al. A novel murine model of Graves’ hyperthyroidism with intramuscular injection of adenovirus expressing the thyrotropin receptor. J. Immunol. 168, 2789–2794 (2002)
doi: 10.4049/jimmunol.168.6.2789
G.D. Chazenbalk, P. Pichurin, C.R. Chen et al. Thyroid-stimulating autoantibodies in Graves disease preferentially recognize the free A subunit, not the thyrotropin holoreceptor. J. Clin. Investig. 110, 209–218 (2002)
doi: 10.1172/JCI0215745
C.R. Chen, P. Pichurin, Y. Nagayama et al. The thyrotropin receptor autoantigen in Graves disease is the culprit as well as the victim. J. Clin. Investig. 111, 1897–1904 (2003)
doi: 10.1172/JCI200317069
O. Saitoh, Y. Nagayama, Regulation of Graves’ hyperthyroidism with naturally occurring CD4+CD25+ regulatory T cells in a mouse model. Endocrinology 147, 2417–2422 (2006)
doi: 10.1210/en.2005-1024
S. Costagliola, M.C. Many, J.F. Denef et al. Genetic immunization of outbred mice with thyrotropin receptor cDNA provides a model of Graves’ disease. J. Clin. Investig. 105, 803–811 (2000)
doi: 10.1172/JCI7665
S. Costagliola, M.C. Many, M. Stalmans-Falys et al. Transfer of thyroiditis, with syngeneic spleen cells sensitized with the human thyrotropin receptor, to naive BALB/c and NOD mice. Endocrinology 137, 4637–4643 (1996)
doi: 10.1210/endo.137.11.8895327
M.C. Many, S. Costagliola, M. Detrait et al. Development of an animal model of autoimmune thyroid eye disease. J. Immunol. 162, 4966–4974 (1999)
pubmed: 10202044
S.C. Ho, S.S. Goh, I.H. Kee et al. Effects of genetic immunization of Swiss outbred mice with human thyroid stimulating hormone receptor cDNA plasmids harboring gain-of-function mutations. J. Mol. Endocrinol. 38, 277–288 (2007)
doi: 10.1677/JME-06-0027
S.X. Zhao, S. Tsui, A. Cheung et al. Orbital fibrosis in a mouse model of Graves’ disease induced by genetic immunization of thyrotropin receptor cDNA. J. Endocrinol. 210, 369–377 (2011)
doi: 10.1530/JOE-11-0162
G. Masetti, S. Moshkelgosha, H.L. Köhling, D. Covelli, J.P. Banga, U. Berchner-Pfannschmidt, M. Horstmann, S. Diaz-Cano, G.E. Goertz, S. Plummer, A. Eckstein, M. Ludgate, F. Biscarini, J.R. Marchesi Jr, INDIGO consortium, Gut microbiota in experimental murine model of Graves’ orbitopathy established in different environments may modulate clinical presentation of disease. Microbiome 6, 97 (2018)
U. Berchner-Pfannschmidt, S. Moshkelgosha, S. Diaz-Cano et al. Comparative assessment of female mouse model of Graves’ orbitopathy under different environments, accompanied by proinflammatory cytokine T cell responses to TSH-receptor antigen. Endocrinology, in revision (2020)
U. Flögel, A. Schlüter, C. Jacoby, S. Temme, J.P. Banga, A. Eckstein, J. Schrader, U. Berchner-Pfannschmidt, Multimodal assessment of orbital immune cell infiltration and tissue remodeling during development of graves disease by 1 H19 F MRI. Magn. Reson. Med. 80, 711–718 (2018)
doi: 10.1002/mrm.27064
A. Schluter, U. Flogel, S. Diaz-Cano et al. Graves’ orbitopathy occurs sex-independently in an autoimmune hyperthyroid mouse model. Sci. Rep. 8, 13096 (2018)
doi: 10.1038/s41598-018-31253-4
G. Masetti, S. Moshkelgosha, H.L. Kohling et al. Gut microbiota in experimental murine model of Graves’ orbitopathy established in different environments may modulate clinical presentation of disease. Microbiome 6, 97 (2018)
doi: 10.1186/s40168-018-0478-4
L. Goschl, C. Scheinecker, M. Bonelli, Treg cells in autoimmunity: from identification to Treg-based therapies. Semin Immunopathol. 41, 301–314 (2019)
doi: 10.1007/s00281-019-00741-8
M. Romano, G. Fanelli, C.J. Albany et al. Past, present, and future of regulatory T Cell therapy in transplantation and autoimmunity. Front Immunol. 10, 43 (2019)
doi: 10.3389/fimmu.2019.00043
S. Plöhn, M. Hose, A. Schlüter, L. Michel, S. Diaz-Cano, U.B. Hendgen-Cotta, J.P. Banga, N.E. Bechrakis, W. Hansen, A. Eckstein, U. Berchner-Pfannschmidt, Fingolimod improves the outcome of experimental Graves’ disease and associated orbitopathy by modulating the autoimmune response to the thyroid-stimulating hormone receptor. Thyroid. 29, 1286–1301 (2019)
doi: 10.1089/thy.2018.0754
Q. Yuan, Y. Zhao, X. Zhu et al. Low regulatory T cell and high IL-17 mRNA expression in a mouse Graves’ disease model. J. Endocrinol. Investig. 40, 397–407 (2017)
doi: 10.1007/s40618-016-0575-9
F. Zhao, L. Wu, Y. Wang et al. Dihydrotestosterone regulates oxidative stress and immunosuppressive cytokines in a female BALB/c mouse model of Graves’ disease. Autoimmunity 52, 117–125 (2019)
doi: 10.1080/08916934.2019.1621857
J. Zhou, M. Bi, C. Fan et al. Regulatory T cells but not T helper 17 cells are modulated in an animal model of Graves’ hyperthyroidism. Clin. Exp. Med. 12, 39–46 (2012)
doi: 10.1007/s10238-011-0137-6
L. Liu, L. Wu, A. Gao et al. The Influence of dihydrotestosterone on the development of Graves’ disease in female BALB/c mice. Thyroid 26, 449–457 (2016)
doi: 10.1089/thy.2015.0620
J. Fassbender, H.P. Holthoff, Z. Li et al. Therapeutic effects of short cyclic and combined epitope peptides in a long-term model of Graves’ disease and orbitopathy. Thyroid 29, 258–267 (2019)
doi: 10.1089/thy.2018.0326
H.P. Holthoff, Z. Li, J. Fassbender et al. Cyclic peptides for effective treatment in a long-term model of Graves disease and orbitopathy in female mice. Endocrinology 158, 2376–2390 (2017)
doi: 10.1210/en.2016-1845
L. Jansson, K. Vrolix, A. Jahraus et al. Immunotherapy with apitopes blocks the immune response to TSH receptor in HLA-DR transgenic mice. Endocrinology 159, 3446–3457 (2018)
doi: 10.1210/en.2018-00306
S.H.S. Pearce, C. Dayan, D.C. Wraith, K. Barrell, N. Olive, L. Jansson, T. Walker-Smith, C. Carnegie, K.F. Martin, K. Boelaert, J. Gilbert, C.E. Higham, I. Muller, R.D. Murray, P. Perros, S. Razvi, B. Vaidya, F. Wernig, G.J. Kahaly, Antigen-specific immunotherapy with thyrotropin receptor peptides in Graves’ hyperthyroidism: a Phase I study. Thyroid 29, 1003–1011 (2019)
doi: 10.1089/thy.2019.0036
H. Rakov, K. Engels, G.S. Hones et al. Sex-specific phenotypes of hyperthyroidism and hypothyroidism in mice. Biol. Sex. Differ. 7, 36 (2016)
doi: 10.1186/s13293-016-0089-3