Table of Contents
Advances in Endocrinology
Volume 2014 (2014), Article ID 189194, 7 pages
http://dx.doi.org/10.1155/2014/189194
Review Article

The Emerging Roles of Thyroglobulin

1Laboratory of Molecular Diagnostics, Department of Mycobacteriology, Leprosy Research Center, National Institute of Infectious Diseases, 4-2-1 Aoba-cho, Higashimurayama-shi, Tokyo 189-0002, Japan
2Department of Education Planning and Development, Faculty of Medicine, Toho University, Tokyo 143-8540, Japan

Received 10 February 2014; Accepted 12 March 2014; Published 10 April 2014

Academic Editor: James M. Lenhard

Copyright © 2014 Yuqian Luo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Salvatore and H. Edelhoch, “Chemistry and biosythesis of thyroid iodoproteins,” in Hormonal Proteins and Peptides, C. H. Li, Ed., pp. 201–244, Academic Press, New York, NY, USA, 1973. View at Google Scholar
  2. J. Robbins, J. E. Rall, and P. Gorden, “The thyroid and iodine metabolism,” in Duncan's Diseases of Metabolism, P. K. Bondy and L. E. Rosenberg, Eds., pp. 1009–1104, Saunders, Philadelphia, Pa, USA, 1974. View at Google Scholar
  3. G. Dai, O. Levy, and N. Carrasco, “Cloning and characterization of the thyroid iodide transporter,” Nature, vol. 379, no. 6564, pp. 458–460, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. L. A. Everett, B. Glaser, J. C. Beck et al., “Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS),” Nature Genetics, vol. 17, no. 4, pp. 411–422, 1997. View at Google Scholar · View at Scopus
  5. I. E. Royaux, K. Suzuki, A. Mori et al., “Pendrin, the protein encoded by the pendred syndrome gene (PDS), is an apical porter of iodide in the thyroid and is regulated by thyroglobulin in FRTL-5 cells,” Endocrinology, vol. 141, no. 2, pp. 839–845, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Ekholm, G. Engstrom, L. E. Ericson, and A. Melander, “Exocytosis of protein into the thyroid follicle lumen: an early effect of TSH,” Endocrinology, vol. 97, no. 2, pp. 337–346, 1975. View at Google Scholar · View at Scopus
  7. L. E. Ericson and B. R. Johansson, “Early effects of thyroid stimulating hormone (TSH) on exocytosis and endocytosis in the thyroid,” Acta Endocrinologica, vol. 86, no. 1, pp. 112–118, 1977. View at Google Scholar · View at Scopus
  8. P. G. Malan, J. Strang, and W. Tong, “TSH initiation of hormone secretion by rat thyroid lobes in vitro,” Endocrinology, vol. 95, no. 2, pp. 397–405, 1974. View at Google Scholar · View at Scopus
  9. Y. Mizukami, T. Hashimoto, A. Nonomura et al., “Immunohistochemical demonstration of thyrotropin (TSH)-receptor in normal and diseased human thyroid tissues using monoclonal antibody against recombinant human TSH-receptor protein,” Journal of Clinical Endocrinology and Metabolism, vol. 79, no. 2, pp. 616–619, 1994. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Tanaka, H. Inoue, H. Miki, K. Komaki, and Y. Monden, “Heterogeneous distribution of thyrotrophin receptor messenger ribonucleic acid (TSH-R mRNA) in papillary thyroid carcinomas detected by in situ hybridization,” Clinical Endocrinology, vol. 44, no. 3, pp. 259–267, 1996. View at Google Scholar · View at Scopus
  11. S. Aeschimann, P. A. Kopp, E. T. Kimura et al., “Morphological and functional polymorphism within clonal thyroid nodules,” Journal of Clinical Endocrinology and Metabolism, vol. 77, no. 3, pp. 846–851, 1993. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Gerber, H. J. Peter, and H. Studer, “Diffusion of thyroglobulin in the follicular colloid. (Minireview),” Endocrinologia Experimentalis, vol. 20, no. 1, pp. 23–33, 1986. View at Google Scholar · View at Scopus
  13. H. Gerber, H. J. Peter, and H. Studer, “Age-related failure of endocytosis may be the pathogenetic mechanism responsible for 'cold' follicle formation in the aging mouse thyroid,” Endocrinology, vol. 120, no. 5, pp. 1758–1764, 1987. View at Google Scholar · View at Scopus
  14. S. Smeds, H. J. Peter, and E. Jortso, “Naturally occurring clones of cells with high intrinsic proliferation potential within the follicular epithelium of mouse thyroids,” Cancer Research, vol. 47, no. 6, pp. 1646–1651, 1987. View at Google Scholar · View at Scopus
  15. K. Suzuki, H. Matsumoto, M. Kobayashi, A. Kawaoi, K. Asayama, and S. I. Moriyama, “Immunohistochemical localization of copper-zinc and manganese superoxide dismutases in diisopropanolnitrosamine-induced rat thyroid lesions,” Acta Histochemica et Cytochemica, vol. 24, no. 1, pp. 69–73, 1991. View at Google Scholar
  16. K. Yamamoto, Y. Xue, R. Katoh, and A. Kawaoi, “Differential immunolocalization of thyroglobulin (Tg) in the follicular epithelium of rat thyroid glands and its kinetics under thyrotropin (TSH) stimulation—a quantitative immunoelectron microscopic analysis using post-embedding immunogold technique,” Acta Histochemica et Cytochemica, vol. 30, no. 2, pp. 147–155, 1997. View at Google Scholar · View at Scopus
  17. K. Suzuki, S. Lavaroni, A. Mori et al., “Autoregulation of thyroid-specific gene transcription by thyroglobulin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 14, pp. 8251–8256, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Suzuki, A. Mori, S. Lavaroni et al., “In vivo expression of thyroid transcription factor-1 RNA and its relation to thyroid function and follicular heterogeneity: identification of follicular thyroglobulin feedback suppressor of thyroid transcription factor-1 RNA levels and thyroglobulin synthesis,” Thyroid, vol. 9, no. 4, pp. 319–331, 1999. View at Google Scholar · View at Scopus
  19. K. Suzuki, A. Hemmi, R. Katoh, and A. Kawaoi, “Differential image analysis of proliferating cell nuclear antigen (PCNA) expression level during experimental thyroid carcinogenesis,” Acta Histochemica et Cytochemica, vol. 29, no. 2, pp. 99–105, 1996. View at Google Scholar · View at Scopus
  20. X. Yi, K. Yamamoto, L. Shu, R. Katoh, and A. Kawaoi, “Effects of propylthiouracil (PTU) administration on the synthesis and secretion of thyroglobulin in the rat thyroid gland: a quantitative immunoelectron microscopic study using immunogold technique,” Endocrine Pathology, vol. 8, no. 4, pp. 315–325, 1997. View at Google Scholar · View at Scopus
  21. L. D. Kohn, K. Suzuki, M. Nakazato, I. Royaux, and E. D. Green, “Effects of thyroglobulin and pendrin on iodide flux through the thyrocyte,” Trends in Endocrinology and Metabolism, vol. 12, no. 1, pp. 10–16, 2001. View at Google Scholar · View at Scopus
  22. D. F. Sellitti and K. Suzuki, “Intrinsic regulation of thyroid function by thyroglobulin,” Thyroid. In press.
  23. K. Suzuki, A. Kawashima, A. Yoshihara et al., “Role of thyroglobulin on negative feedback autoregulation of thyroid follicular function and growth,” Journal of Endocrinology, vol. 209, no. 2, pp. 169–174, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Suzuki and L. D. Kohn, “Differential regulation of apical and basal iodide transporters in the thyroid by thyroglobulin,” Journal of Endocrinology, vol. 189, no. 2, pp. 247–255, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Suzuki, A. Mori, S. Lavaroni, R. Katoh, L. D. Kohn, and A. Kawaoi, “Thyroglobulin: a master regulator of follicular function via transcriptional suppression of thyroid specific genes,” Acta Histochemica et Cytochemica, vol. 32, no. 2, pp. 111–119, 1999. View at Google Scholar · View at Scopus
  26. K. Suzuki, A. Mori, S. Lavaroni et al., “Thyroglobulin regulates follicular function and heterogeneity by suppressing thyroid-specific gene expression,” Biochimie, vol. 81, no. 4, pp. 329–340, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Suzuki, A. Mori, J. Saito, E. Moriyama, L. Ullianich, and L. D. Kohn, “Follicular thyroglobulin suppresses iodide uptake by suppressing expression of the sodium/iodide symporter gene,” Endocrinology, vol. 140, no. 11, pp. 5422–5430, 1999. View at Google Scholar · View at Scopus
  28. K. Suzuki, M. Nakazato, L. Ulianich et al., “Thyroglobulin autoregulation of thyroid-specific gene expression and follicular function,” Reviews in Endocrine and Metabolic Disorders, vol. 1, no. 3, pp. 217–224, 2000. View at Google Scholar · View at Scopus
  29. A. Yoshihara, T. Hara, A. Kawashima et al., “Regulation of dual oxidase expression and H2O2 production by thyroglobulin,” Thyroid, vol. 22, no. 10, pp. 1054–1062, 2012. View at Publisher · View at Google Scholar
  30. Y. Ishido, K. Yamazaki, M. Kammori et al., “Thyroglobulin suppresses thyroid-specific gene expression in cultures of normal, but not neoplastic human thyroid follicular cells,” Journal of Clinical Endocrinology and Metabolism, 2014. View at Publisher · View at Google Scholar
  31. M. Sue, M. Hayashi, A. Kawashima et al., “Thyroglobulin (Tg) activates MAPK pathway to induce thyroid cell growth in the absence of TSH, insulin and serum,” Biochemical and Biophysical Research Communications, vol. 420, no. 3, pp. 611–615, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Nakazato, H.-K. Chung, L. Ulianich, A. Grassadonia, K. Suzuki, and L. D. Kohn, “Thyroglobulin repression of thyroid transcription factor 1 (TTF-1) gene expression is mediated by decreased DNA binding of nuclear factor I proteins which control constitutive TTF-1 expression,” Molecular and Cellular Biology, vol. 20, no. 22, pp. 8499–8512, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Suzuki, I. E. Royaux, L. A. Everett et al., “Expression of PDS/Pds, the Pendred syndrome gene, in endometrium,” Journal of Clinical Endocrinology and Metabolism, vol. 87, no. 2, pp. 938–941, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Pacifico, N. Montuori, S. Mellone et al., “The RHL-1 subunit of the asialoglycoprotein receptor of thyroid cells: cellular localization and its role in thyroglobulin endocytosis,” Molecular and Cellular Endocrinology, vol. 208, no. 1-2, pp. 51–59, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. R. J. Stockert, “The asialoglycoprotein receptor: relationships between structure, function, and expression,” Physiological Reviews, vol. 75, no. 3, pp. 591–609, 1995. View at Google Scholar · View at Scopus
  36. D. A. Wall and A. L. Hubbard, “Receptor-mediated endocytosis of asialoglycoproteins by rat liver hepatocytes: biochemical characterization of the endosomal compartments,” Journal of Cell Biology, vol. 101, no. 6, pp. 2104–2112, 1985. View at Google Scholar · View at Scopus
  37. L. Ulianich, K. Suzuki, A. Mori et al., “Follicular thyroglobulin (TG) suppression of thyroid-restricted genes involves the apical membrane asialoglycoprotein receptor and TG phosphorylation,” Journal of Biological Chemistry, vol. 274, no. 35, pp. 25099–25107, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. S. S. Huang, M. A. Cerullo, F. W. Huang, and J. S. Huang, “Activated thyroglobulin possesses a transforming growth factor-β activity,” Journal of Biological Chemistry, vol. 273, no. 40, pp. 26036–26041, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. D. F. Sellitti, K. Suzuki, S. Q. Doi et al., “Thyroglobulin increases cell proliferation and suppresses Pax-8 in mesangial cells,” Biochemical and Biophysical Research Communications, vol. 285, no. 3, pp. 795–799, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Noguchi, N. Harii, C. Giuliani, I. Tatsuno, K. Suzuki, and L. D. Kohn, “Thyroglobulin (Tg) induces thyroid cell growth in a concentration-specific manner by a mechanism other than thyrotropin/cAMP stimulation,” Biochemical and Biophysical Research Communications, vol. 391, no. 1, pp. 890–894, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Kimura, A. van Keymeulen, J. Golstein, A. Fusco, J. E. Dumont, and P. P. Roger, “Regulation of thyroid cell proliferation by tsh and other factors: a critical evaluation of in vitro models,” Endocrine Reviews, vol. 22, no. 5, pp. 631–656, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Nedachi, M. Akahori, M. Ariga et al., “Tyrosine kinase and phosphatidylinositol 3-kinase activation are required for cyclic adenosine 3′,5′-monophosphate-dependent potentiation of deoxyribonucleic acid synthesis induced by insulin-like growth factor-I in FRTL-5 cells,” Endocrinology, vol. 141, no. 7, pp. 2429–2438, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. S.-I. Takahashi, M. Conti, C. Prokop, J. J. van Wyk, and H. S. Earp III, “Thyrotropin and insulin-like growth factor I regulation of tyrosine phosphorylation in FRTL-5 cells: interaction between cAMP-dependent and growth factor-dependent signal transduction,” Journal of Biological Chemistry, vol. 266, no. 12, pp. 7834–7841, 1991. View at Google Scholar · View at Scopus
  44. K. Brix, R. Wirtz, and V. Herzog, “Paracrine interaction between hepatocytes and macrophages after extrathyroidal proteolysis of thyroglobulin,” Hepatology, vol. 26, no. 5, pp. 1232–1240, 1997. View at Google Scholar · View at Scopus
  45. D. F. Sellitti, T. Akamizu, S. Q. Doi et al., “Renal expression of two 'thyroid-specific' genes: thyrotropin receptor and thyroglobulin,” Experimental Nephrology, vol. 8, no. 4-5, pp. 235–243, 2000. View at Google Scholar · View at Scopus
  46. D. Plachov, K. Chowdhurry, C. Walther, D. Simon, J.-L. Guenet, and P. Gruss, “Pax8, a murine paired box gene expressed in the developing excretory system and thyroid gland,” Development, vol. 110, no. 2, pp. 643–651, 1990. View at Google Scholar · View at Scopus
  47. G. Zheng, M. Marino, J. Zhao, and R. T. McCluskey, “Megalin (gp330): a putative endocytic receptor for thyroglobulin (Tg),” Endocrinology, vol. 139, no. 3, pp. 1462–1465, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. S. C. Jordan, B. Buckingham, R. Sakai, and D. Olson, “Studies of immune-complex glomerulonephritis mediated by human thyroglobulin,” New England Journal of Medicine, vol. 304, no. 20, pp. 1212–1215, 1981. View at Google Scholar · View at Scopus
  49. D. F. Sellitti, E. Puggina, C. Lagranha et al., “TGF-β-like transcriptional effects of thyroglobulin (Tg) in mouse mesangial cells,” Endocrine Journal, vol. 54, no. 3, pp. 449–458, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Wu, S. Suzuki, D. F. Sellitti et al., “Expression of a thyroglobulin (Tg) variant in mouse kidney glomerulus,” Biochemical and Biophysical Research Communications, vol. 389, no. 2, pp. 269–273, 2009. View at Publisher · View at Google Scholar · View at Scopus