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

Journal of Immunology

Volumn 176, Issue 8, 2006, Pages 5084-5092

  Gilbert, Jacqueline A ^a   Gianoukakis, Andrew G ^b   Salehi, Siamak ^a   Moorhead, Jane ^c   Rao, Prakash V ^a   Khan, M Zareen ^c   McGregor, Alan M ^a   Smith, Terry J ^b   Banga, J Paul ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UCLA MEDICAL CENTER   (United States)

^c KING S COLLEGE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; IODINE 125; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; THYROTROPIN; THYROTROPIN RECEPTOR; THYROTROPIN RECEPTOR ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GRAVES DISEASE; HYBRIDOMA; HYPERTHYROIDISM; IMMUNIZATION; ISOTOPE LABELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; SIGNAL TRANSDUCTION; THYROID CELL; THYROID DISEASE; THYROID FUNCTION TEST; THYROTROPIN BLOOD LEVEL;

EID: 33645759708     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.8.5084     Document Type: Article

References (50)

1. Rapoport, B., and S. M. McLachlan. 2001. Thyroid autoimmunity. J. Clin. Invest. 108: 1253-1259.
2. Prabhakar, B. S., R. S. Bahn, and T. J. Smith. 2003. Current perspectives on the pathogenesis of Graves' disease and ophthalmopathy. Endocr. Rev. 24: 802-835.
3. Rees Smith, B., S. M. McLachlan, and J. Furmaniak. 1988. Autoantibodies to the thyrotropin receptor. Endocr. Rev. 9: 106-121.
4. Pritchard, J., R. Han, N. Horst, W. W. Cruikshank, and T. J. Smith. 2003. Immunoglobulin activation of T cell chemoattractant expression in fibroblasts from patients with Graves' disease is mediated through the insulin-like growth factor I receptor pathway. J. Immunol. 170: 6348-6354.
5. Smith, T. J., and N. Hoa. 2004. Immunoglobulins from patients with Graves' disease induce hyaluronan synthesis in their orbital fibroblasts through the self antigen, insulin-like growth factor-1 receptor. J. Clin. Endocrinol. Metab. 89: 5076-5080.
6. 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.
7. Laurent, E., J. Mockel, J. Van Sande, I. Graff, and J. E. Dumont. 1987. Dual activation by thyrotropin of the phospholipase C and cAMP cascades in human thyroid. Mol. Cell. Endocrinol. 52: 273-278.
8. Cooper, D. S. 2003. Hyperthyroidism. Lancet 362: 459-468.
9. Kajita, Y., C. R. Rickards, P. R. Buckland, R. D. Howells, and B. Rees Smith 1985. Analysis of thyrotropin receptors by photoaffinity labeling: orientation of receptor subunits in the cell membrane. Biochem. J. 227: 413-420.
10. Loosfelt, H., C. Pichon, A. Jolivet, M. Misrahi, B. Caillou, M. Jamous, B. Vannier, and E. Milgrom. 1992. Two subunit structure of the human thyrotropin receptor. Proc. Natl. Acad. Sci. USA 89: 3765-3769.
11. 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.
12. Iacovelli, L., L. Capobianco, L. Salvatore, M. Sallese, G. M. D'Ancona, and A. DeBlasi. 2001. Thyrotropin activates mitogen-activated protein kinase pathway in FRTL-5 by a cAMP-dependent protein kinase A-independent mechanism. Mol. Pharmacol. 60: 924-933.
13. Saunier, B., C. Tournier, C. Jacquemin, and M. Pierre. 1995. Stimulation of mitogen-activated protein kinase by thyrotropin in primary cultured human thyroid follicles. J. Biol. Chem. 270: 3693-3697.
14. Vandeput, F., S. Perpete, K. Coulonval, F. Lamy, and J. E. Dumont. 2003. Role of the different mitogen-activated protein kinase subfamilies in the stimulation of dog and human thyroid epithelial cell proliferation by cyclic adenosine 5′-monophosphate and growth factors. Endocrinology 144: 1341-1349.
15. Lefkowitz, R. J., and S. K. Shenoy. 2005. Transduction of receptor signals by β-arrestins. Science 308: 512-517.
16. Tramontano, D., G. W. Cushing, A. C. Moses, and S. H. Ingbar. 1986. Insulin-like growth factor-I stimulates the growth of rat thyroid cells in culture and synergizes the stimulation of DNA synthesis induced by TSH and Graves'-IgG. Endocrinology 119: 940-942.
17. McLachlan, S. M., and B. Rapoport. 2004. Thyroid-stimulating monoclonal antibodies: overcoming the road blocks and the way forward. Clin. Endocrinol. 61: 10-18.
18. Ando, T., R. Latif, A. Pritsker, T. Moran, Y. Nagayama, and T. F. Davies. 2002. A monoclonal thyroid-stimulating antibody. J. Clin. Invest. 110: 1667-1674.
19. Sanders, J., J. Jeffreys, H. Depraetere, T. Richards, M. Evans, A. Kiddie, K. Brereton, M. Groenen, Y. Oda, J. Furmaniak, and B. Rees Smith. 2002. Thyroid-stimulating monoclonal antibodies. Thyroid 12: 1043-1050.
20. Costagliola, S., J. D. F. Franssen, M. Bonomi, E. Urizar, M. Willnich, A. Bergmann, and G. Vassart 2002. Generation of a mouse monoclonal TSH receptor antibody with stimulating activity. Biochem. Biophys. Res. Commun. 299: 891-896.
21. Sanders, J., M. Evans, L. D. K. E. Premawardhana, H. Depraetere, J. Jeffreys, T. Richards, J. Furmaniak, and B. Rees Smith. 2003. Human monoclonal thyroid-stimulating autoantibody. Lancet 362: 126-128.
22. Sanders, J., J. Jeffreys, H. Depraetere, M. Evans, T. Richards, A. Kiddie, K. Bretton, L. D. K. E. Premawardhana, D. Y. Chirgadze, R. Nunez Miguel, T. L. Blundell, J. Furmaniak, and B. Rees Smith. 2004. Characteristics of a human monoclonal autoantibody to the thyrotropin receptor: sequence structure and function. Thyroid 14: 560-570.
23. Costagliola, S., M. Bonomi, N. G. Morgenthaler, J. Van Durme, V. Panneels, S. Refetoff, and G. Vassart. 2004. Delineation of the discontinuous conformational epitope of a monoclonal antibody displaying full in vitro and in vivo thyrotropin activity. Mol. Endocrinol. 18: 3020-3034.
24. Jaume, J. C., A. Kakinuma, O. D. Chazenbalk, B. Rapoport, and S. M. McLachlan. 1997. Thyrotropin receptor autoantibodies in serum are present at much lower levels than thyroid peroxidase autoantibodies by flow cytometry. J. Clin. Endocrinol. Metab. 82: 500-507.
25. de Forteza, R., C. U. Smith, J. Amin, Z. M. McKenzie, and M. Zakarija. 1994. Visualization of the thyrotropin receptor on the cell surface by potent autoantibodies. J. Clin. Endocrinol. Metab. 78: 1271-1273.
26. Rao, P. V., P. F. Watson, A. P. Weetman, G. Carayanniotis, and J. P. Banga. 2003. Contrasting activities of thyrotropin receptor antibodies in experimental models of Graves' disease induced by injection of transfected fibroblasts or deoxyribonucleic acid vaccination. Endocrinology 144: 260-266.
27. Perret, J., M. Ludgate, F. Libert, C. Gerard, J. E. Dumont, G. Vassart, and M. Parmentier. 1990. Stable expression of the human TSH receptor in CHO cells and characterization of differently expressing clones. Biochem. Biophys. Res. Comm. 171: 1044-1050.
28. Muehlberg, T., J. A. Gilbert, P. V. Rao, A. M. McGregor, and J. P. Banga. 2004. Dynamics of thyroid-stimulating and blocking antibodies to the thyrotropin receptor in a murine model of Graves' disease. Endocrinology 145: 1539-1545.
29. 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.
30. 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.
31. 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.
32. Metcalfe, R., N. Jordan, P. F. Watson, S. Gullu, M. Wiltshire, M. Crisp, C. Evans, A. P. Weetman, and M. Ludgate. 2002. Demonstration of immunoglobulin G, A, and E autoantibodies to the human thyrotropin receptor using flow cytometry. J. Clin. Endocrinol. Metab. 87: 1754-1761.
33. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor.
34. Johnstone, A. P. and R. Thorpe. 1987. Radiolabeling techniques. In Immunochemistry in Practice, 2nd Ed. A. P. Johnstone and R. Thorpe, eds. Blackwell Scientific, Oxford, p. 113.
35. Gianoukakis, A. G., H. J. Cao, T. A. Jennings, and T. J. Smith. 2001. Prostaglandin endoperoxide H synthase expression in human thyroid epithelial cells. Am. J. Physiol. 280: C701-C708.
36. Kasagi, K., J. Konishi, Y. Iida, K. Ikekubo, T. Mori, K. Kuma, and K. Torizuka. 1982. A new in vitro assay for human thyroid stimulator using cultured thyroid cells: effect of sodium chloride on adenosine 3′,5′- monophosphate increase. J. Clin. Endocrinol. Metab. 54: 108-114.
37. Nicholson, L. B., H. Vlase, P. Graves, M. Nilsson, J. Molne, G. C. Huang, N. G. Morgenthaler, T. F. Davies, A. M. McGregor, and J. P. Banga. 1996. Monoclonal antibodies to the human TSH receptor: epitope mapping and binding to the native receptor on the basolateral plasma membrane of thyroid follicular cells. J. Mol. Endocrinol. 16: 159-170.
38. Morgenthaler, N. G., W. B. Minich, M. Willnich, T. Bogusch, J. M. Hollidt, W. Weglohner, C. Lenzner, and A. Bergmann. 2003. Affinity purification and diagnostic use of TSH receptor autoantibodies from human sera. Mol. Cell Endocrinol. 212: 73-79.
39. Pomerance, M., H. B. Abdullah, S. Kamerji, C. Correze, and J. P. Blondeau. 2000. Thyroid-stimulating hormone and cyclic AMP activate p38 mitogen-activated protein kinase cascade. J. Biol. Chem. 275: 40539-40546.
40. Corrèze, C., J. P. Blondeau, and M. Pomerance. 2000. The thyrotropin receptor is not involved in the activation of p42/p44 mitogen-activated protein kinases by thyrotropin preparations in Chinese hamster ovary cells expressing the human thyrotropin receptor. Thyroid 10: 747-752.
41. Kraiem, Z., E. Baron, L. Kahana, O. Sadeh, and M. Shinfeld. 1992. Changes in stimulating and blocking TSH receptor antibodies in a patient undergoing three cycles of transition from hypo to hyperthyroidism and back to hypothyroidism. Clin. Endocrinol. 36: 211-214.
42. Kasagi, K., A. Hidaka, K. Endo, S. Miyamoto, R. Takeuchi, T. Misaki, H. Sakahara, and J. Konishi. 1993. Fluctuating thyroid function depending on the balance between stimulating and blocking types of TSH receptor antibodies: a case report. Thyroid 3: 315-318.
43. Kim, W. B., H. K. Chung, H. K. Lee, L. D. Kohn, K. Tahara, and B. Y. Cho. 1997. Changes in epitopes for thyroid-stimulating antibodies in Graves' disease sera during treatment of hyperthyroidism: therapeutic implications. J. Clin. Endocrinol. Metab. 82: 1953-1959.
44. Smith, T. J. 2003. The putative role of fibroblasts in the pathogenesis of Graves' disease: evidence for the involvement of the insulin-like growth factor-1 receptor in fibroblast activation. Autoimmunity 36: 409-415.
45. Noh, J. Y., N. Hamada, Y. Inoue, Y. Abe, K. Ito, and K. Ito. 2000. Thyroid-stimulating antibody is related to Graves' ophthalmopathy, but thyrotropin-binding inhibitor immunoglobulin is related to hyperthyroidism in patients with Graves' disease. Thyroid 10: 809-813.
46. 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.
47. Denef, J. F., M. C. Many, and M. F. Van der Hove. 1996. Iodine induced thyroid inhibition and cell necrosis: two consequences of the same free radical-mediated mechanism. Mol. Cell. Endocrinol. 121: 101-103.
48. Riou, C., H. Tonoli, F. Bernier-Valentin, R. Rabilloud, P. Fonupt, and B. Rousse. 1999. Susceptibility of differentiated thyrocytes in primary culture to undergo apoptosis after exposure to hydrogen peroxide: relation with the level of expression of apoptosis regulatory proteins, Bcl-2 and Bax. Endocrinology 140: 1990-1997.
49. 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.
50. Dromey, J. A., S. M. Weenink, G. H. Peters, J. Endl, P. J. Tighe, I. Todd, and M. R. Christie. 2004. Mapping of epitopes for autoantibodies to the type 1 diabetes autoantigen IA-2 by peptide phage display and molecular modeling: overlap of antibody and T cell determinants. J. Immunol. 172: 4084-4090.