A unique mouse strain that develops spontaneous, iodine-accelerated, pathogenic antibodies to the human thyrotrophin receptor

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4154-4161

  Rapoport, Basil ^a   Aliesky, Holly A ^a   Banuelos, Bianca ^a   Chen, Chun Rong ^a   McLachlan, Sandra M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IODINE; THYROGLOBULIN ANTIBODY; THYROID PEROXIDASE ANTIBODY; THYROTROPIN; THYROTROPIN RECEPTOR; THYROTROPIN RECEPTOR ANTIBODY; THYROXINE; AUTOANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; GRAVES DISEASE; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEX DIFFERENCE; THYROTOXICOSIS; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; ANIMAL; BAGG ALBINO MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; HUMAN; IMMUNOLOGY; NONOBESE DIABETIC MOUSE; TRANSGENIC MOUSE;

ANIMALS; AUTOANTIBODIES; DISEASE MODELS, ANIMAL; FEMALE; GRAVES DISEASE; HUMANS; IODINE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, TRANSGENIC; RECEPTORS, THYROTROPIN;

EID: 84928494105     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500126     Document Type: Article

References (48)

1. Rapoport, B., G. D. Chazenbalk, J. C. Jaume, and S. M. McLachlan. 1998. The thyrotropin (TSH) receptor: interaction with TSH and autoantibodies. Endocr. Rev. 19: 673-716.
2. McLeod, D. S., and D. S. Cooper. 2012. The incidence and prevalence of thyroid autoimmunity. Endocrine 42: 252-265.
3. Aliesky, H., C. L. Courtney, B. Rapoport, and S. M. McLachlan. 2013. Thyroid autoantibodies are rare in nonhuman great apes and hypothyroidism cannot be attributed to thyroid autoimmunity. Endocrinology 154: 4896-4907.
4. Shimojo, N., Y. Kohno, K. Yamaguchi, S. Kikuoka, A. Hoshioka, H. Niimi, A. Hirai, Y. Tamura, Y. Saito, L. D. Kohn, and K. Tahara. 1996. Induction of Graves-like disease in mice by immunization with fibroblasts transfected with the thyrotropin receptor and a class II molecule. Proc. Natl. Acad. Sci. USA 93: 11074-11079.
5. Costagliola, S., M. C. Many, J. F. Denef, J. Pohlenz, S. Refetoff, and G. Vassart. 2000. Genetic immunization of outbred mice with thyrotropin receptor cDNA provides a model of Graves' disease. J. Clin. Invest. 105: 803-811.
6. Nagayama, Y., M. Kita-Furuyama, T. Ando, K. Nakao, H. Mizuguchi, T. Hayakawa, K. Eguchi, and M. Niwa. 2002. A novel murine model of Graves' hyperthyroidism with intramuscular injection of adenovirus expressing the thyrotropin receptor. J. Immunol. 168: 2789-2794.
7. Chen, C.-R., P. Pichurin, Y. Nagayama, F. Latrofa, B. Rapoport, and S. M. McLachlan. 2003. The thyrotropin receptor autoantigen in Graves disease is the culprit as well as the victim. J. Clin. Invest. 111: 1897-1904.
8. Gilbert, J. A., A. G. Gianoukakis, S. Salehi, J. Moorhead, P. V. Rao, M. Z. Khan, A. M. McGregor, T. Smith, and J. P. Banga. 2006. 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. J. Immunol. 176: 5084-5092.
9. Holthoff, H. P., S. Göbel, Z. Li, J. Faßbender, A. Reimann, S. Zeibig, M. J. Lohse, G. Münch, and M. Ungerer. 2015. Prolonged TSH receptor A subunit immunization of female mice leads to a long-term model of Graves' disease, tachycardia and cardiac hypertrophy. Endocrinology. In press.
10. Ando, T., M. Imaizumi, P. Graves, P. Unger, and T. F. Davies. 2003. Induction of thyroid-stimulating hormone receptor autoimmunity in hamsters. Endocrinology 144: 671-680.
11. Wang, Y., L. P. Wu, J. Fu, H. J. Lv, X. Y. Guan, L. Xu, P. Chen, C. Q. Gao, P. Hou, M. J. Ji, and B. Y. Shi. 2013. Hyperthyroid monkeys: a nonhuman primate model of experimental Graves' disease. J. Endocrinol. 219: 183-193.
12. McLachlan, S. M., Y. Nagayama, P. N. Pichurin, Y. Mizutori, C. R. Chen, A. Misharin, H. A. Aliesky, and B. Rapoport. 2007. The link between Graves' disease and Hashimoto's thyroiditis: a role for regulatory T cells. Endocrinology 148: 5724-5733.
13. Pichurin, P. N., C.-R. Chen, G. D. Chazenbalk, H. Aliesky, N. Pham, B. Rapoport, and S. M. McLachlan. 2006. Targeted expression of the human thyrotropin receptor A-subunit to the mouse thyroid: insight into overcoming the lack of response to A-subunit adenovirus immunization. J. Immunol. 176: 668-676.
14. Chazenbalk, G. D., J. C. Jaume, S. M. McLachlan, and B. Rapoport. 1997. 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: 18959-18965.
15. Chazenbalk, G. D., Y. Wang, J. Guo, J. S. Hutchison, D. Segal, J. C. Jaume, S. M. McLachlan, and B. Rapoport. 1999. A mouse monoclonal antibody to a thyrotropin receptor ectodomain variant provides insight into the exquisite antigenic conformational requirement, epitopes and in vivo concentration of human autoantibodies. J. Clin. Endocrinol. Metab. 84: 702-710.
16. Rapoport, B., R. W. Williams, C. R. Chen, and S. M. McLachlan. 2010. Immunoglobulin heavy chain variable region genes contribute to the induction of thyroid-stimulating antibodies in recombinant inbred mice. Genes Immun. 11: 254-263.
17. Sanders, J., M. Evans, L. D. Premawardhana, H. Depraetere, J. Jeffreys, T. Richards, J. Furmaniak, and B. Rees Smith. 2003. Human monoclonal thyroid stimulating autoantibody. Lancet 362: 126-128.
18. Chen, C. R., S. Hamidi, H. Braley-Mullen, Y. Nagayama, C. Bresee, H. A. Aliesky, B. Rapoport, and S. M. McLachlan. 2010. Antibodies to thyroid peroxidase arise spontaneously with age in NOD.H-2h4 mice and appear after thyroglobulin antibodies. Endocrinology 151: 4583-4593.
19. McLachlan, S. M., H. A. Aliesky, C. R. Chen, G. Chong, and B. Rapoport. 2012. Breaking tolerance in transgenic mice expressing the human TSH receptor Asubunit: thyroiditis, epitope spreading and adjuvant as a 'double edged sword'. PLoS ONE 7: e43517. Available at: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0043517.
20. Ruf, J., M. E. Toubert, B. Czarnocka, J. M. Durand-Gorde, M. Ferrand, and P. Carayon. 1989. Relationship between immunological structure and biochemical properties of human thyroid peroxidase. Endocrinology 125: 1211-1218.
21. Pohlenz, J., A. Maqueem, K. Cua, R. E. Weiss, J. Van Sande, and S. Refetoff. 1999. Improved radioimmunoassay for measurement of mouse thyrotropin in serum: strain differences in thyrotropin concentration and thyrotroph sensitivity to thyroid hormone. Thyroid 9: 1265-1271.
22. Rasooly, L., C. L. Burek, and N. R. Rose. 1996. Iodine-induced autoimmune thyroiditis in NOD-H-2h4 mice. Clin. Immunol. Immunopathol. 81: 287-292.
23. Braley-Mullen, H., G. C. Sharp, B. Medling, and H. Tang. 1999. Spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Autoimmun. 12: 157-165.
24. Hutchings, P. R., S. Verma, J. M. Phillips, S. Z. Harach, S. Howlett, and A. Cooke. 1999. Both CD4(+) T cells and CD8(+) T cells are required for iodine accelerated thyroiditis in NOD mice. Cell. Immunol. 192: 113-121.
25. Sanders, J., D. Y. Chirgadze, P. Sanders, S. Baker, A. Sullivan, A. Bhardwaja, J. Bolton, M. Reeve, N. Nakatake, M. Evans, et al. 2007. Crystal structure of the TSH receptor in complex with a thyroid-stimulating autoantibody. Thyroid 17: 395-410.
26. Misharin, A. V., B. Rapoport, and S. M. McLachlan. 2009. Thyroid antigens, not central tolerance, control responses to immunization in BALB/c versus C57BL/6 mice. Thyroid 19: 503-509.
27. Chen, C.-R., P. Pichurin, G. D. Chazenbalk, H. Aliesky, Y. Nagayama, S. M. McLachlan, and B. Rapoport. 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. Endocrinology 145: 228-233.
28. Chen, C. R., H. Aliesky, P. N. Pichurin, Y. Nagayama, S. M. McLachlan, and B. Rapoport. 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. Endocrinology 145: 4927-4933.
29. McLachlan, S. M., S. Hamidi, H. Aliesky, R. W. Williams, and B. Rapoport. 2014. Sex, genetics, and the control of thyroxine and thyrotropin in mice. Thyroid 24: 1080-1087.
30. Couet, J., S. Sar, A. Jolivet, M. T. Hai, E. Milgrom, and M. Misrahi. 1996. Shedding of human thyrotropin receptor ectodomain. Involvement of a matrix metalloprotease. J. Biol. Chem. 271: 4545-4552.
31. Tanaka, K., G. D. Chazenbalk, S. M. McLachlan, and B. Rapoport. 1999. The shed thyrotropin receptor is primarily a carboxyl terminal truncated form of the A subunit, not the entire A subunit. Mol. Cell. Endocrinol. 150: 113-119.
32. Chazenbalk, G. D., P. Pichurin, C. R. Chen, F. Latrofa, A. P. Johnstone, S. M. McLachlan, and B. Rapoport. 2002. Thyroid-stimulating autoantibodies in Graves disease preferentially recognize the free A subunit, not the thyrotropin holoreceptor. J. Clin. Invest. 110: 209-217.
33. Mizutori, Y., C. R. Chen, F. Latrofa, S. M. McLachlan, and B. Rapoport. 2009. Evidence that shed thyrotropin receptor A subunits drive affinity maturation of autoantibodies causing Graves' disease. J. Clin. Endocrinol. Metab. 94: 927-935.
34. Hillhouse, E. E., R. Collin, G. Chabot-Roy, M. J. Guyon, N. Tessier, M. Boulay, P. Liscourt, and S. Lesage. 2013. Nearby construction impedes the progression to overt autoimmune diabetes in NOD mice. J. Diabetes Res. 2013: 620313.
35. Damotte, D., E. Colomb, C. Cailleau, N. Brousse, J. Charreire, and C. Carnaud. 1997. Analysis of susceptibility of NOD mice to spontaneous and experimentally induced thyroiditis. Eur. J. Immunol. 27: 2854-2862.
36. Nakahara, M., N. Mitsutake, H. Sakamoto, C. R. Chen, B. Rapoport, S. M. McLachlan, and Y. Nagayama. 2010. Enhanced response to mouse thyroid-stimulating hormone (TSH) receptor immunization in TSH receptor-knockout mice. Endocrinology 151: 4047-4054.
37. McLachlan, S. M., H. Braley-Mullen, C. R. Chen, H. Aliesky, P. N. Pichurin, and B. Rapoport. 2005. Dissociation between iodide-induced thyroiditis and antibody-mediated hyperthyroidism in NOD.H-2h4 mice. Endocrinology 146: 294-300.
38. Luo, S. C., and R. B. Bankert. 1987. A new cross-reactive idiotype-defined family in the phthalate humoral immune response of mice. I. Linkage of VH-Xmp to IgCH allotype locus and mapping with respect to other known VH genes. J. Immunol. 138: 2311-2315.
39. Yoshida, H., L. Fossati, M. Yoshida, M. Abdelmoula, S. Herrera, J. Merino, P. H. Lambert, and S. Izui. 1988. Igh-C allotype-linked control of anti-DNA production and clonotype expression in mice infected with Plasmodium yoelii. J. Immunol. 141: 2125-2131.
40. Chang, S., and C. Mohan. 2005. Identification of novel VH1/J558 immunoglobulin germline genes of C57BL/6 (Igh b) allotype. Mol. Immunol. 42: 1293-1301.
41. Martin, R. M., J. L. Brady, and A. M. Lew. 1998. The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J. Immunol. Methods 212: 187-192.
42. Akamizu, T., F. Matsuda, J. Okuda, H. Li, H. Kanda, T. Watanabe, T. Honjo, and T. Mori. 1996. Molecular analysis of stimulatory anti-thyrotropin receptor antibodies (TSAbs) involved in Graves' disease. Isolation and reconstruction of antibody genes, and production of monoclonal TSAbs. J. Immunol. 157: 3148-3152.
43. Kim-Saijo, M., T. Akamizu, K. Ikuta, Y. Iida, K. Ohmori, K. Matsubara, Y. Matsuda, M. Suzuki, F. Matsuda, and K. Nakao. 2003. Generation of a transgenic animal model of hyperthyroid Graves' disease. Eur. J. Immunol. 33: 2531-2538.
44. Ando, T., R. Latif, and T. F. Davies. 2004. Concentration-dependent regulation of thyrotropin receptor function by thyroid-stimulating antibody. J. Clin. Invest. 113: 1589-1595.
45. Flynn, J. C., J. A. Gilbert, C. Meroueh, D. P. Snower, C. S. David, Y. C. Kong, and J. P. Banga. 2007. Chronic exposure in vivo to thyrotropin receptor stimulating monoclonal antibodies sustains high thyroxine levels and thyroid hyperplasia in thyroid autoimmunity-prone HLA-DRB1∗0301 transgenic mice. Immunology 122: 261-267.
46. Dedecjus, M., M. Stasiolek, J. Brzezinski, K. Selmaj, and A. Lewinski. 2011. Thyroid hormones influence human dendritic cells' phenotype, function, and subsets distribution. Thyroid 21: 533-540.
47. Mao, C., S. Wang, Y. Xiao, J. Xu, Q. Jiang, M. Jin, X. Jiang, H. Guo, G. Ning, and Y. Zhang. 2011. Impairment of regulatory capacity of CD4+CD25+ regulatory T cells mediated by dendritic cell polarization and hyperthyroidism in Graves' disease. J. Immunol. 186: 4734-4743.
48. Hamidi, S., H. A. Aliesky, R. W. Williams, B. Rapoport, and S. M. McLachlan. 2013. Genetic linkages for thyroxine released in response to thyrotropin stimulation in three sets of recombinant inbred mice provide evidence for shared and novel genes controlling thyroid function. Thyroid 23: 360-370.