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International Journal of Endocrinology
Volume 2018, Article ID 4682876, 10 pages
https://doi.org/10.1155/2018/4682876
Research Article

Histopathological Characterization and Whole Exome Sequencing of Ectopic Thyroid: Fetal Architecture in a Functional Ectopic Gland from Adult Patient

1Thyroid Unit, Cellular and Molecular Endocrine Laboratory, LIM-25, Faculdade de Medicina da Universidade de São Paulo (FMUSP), Avenida Doutor Arnaldo 455, Cerqueira César, 01246-904 São Paulo, SP, Brazil
2Adolfo Lutz Institute, São Paulo Public Health Service, Av. Dr. Arnaldo 355, Cerqueira César, 01246-000 São Paulo, SP, Brazil
3Head and Neck Surgery of Santa Catarina Hospital, Av. Paulista 200, Bela Vista, 01310-000 São Paulo, SP, Brazil
4Department of Internal Medicine, Botucatu School of Medicine, UNESP, Av. Prof. Montenegro, s/n Distrito de Rubião Junior, 18618-687 Botucatu, SP, Brazil
5Servicio de Endocrinología, Hospital de Pediatría Dr. Juan Garrahan, Combate de los Pozos 1881, C1245AAM Buenos Aires, Argentina
6Departamento de Cirurgia na Disciplina de Cirurgia de Cabeça e Pescoço da Faculdade de Ciências Médicas da UNICAMP, R. Tessália Vieira de Camargo 126, 13083-887 Campinas, SP, Brazil
7Medicine School, Universidade de Fortaleza (Unifor), Av. Washington Soares 1321, Edson Queiroz, 60811-905 Fortaleza, CE, Brazil
8Postgraduate Program in Biotechnology, Universidade Federal de São Paulo (UNIFESP), Pedro de Toledo 669, 040399-032 São Paulo, SP, Brazil
9Thyroid Molecular Sciences Laboratory, Universidade Federal de São Paulo, Departamento de Ciências Biológicas, Postgraduation Programs in Biotechnology and Structural and Functional Biology, UNIFESP, Pedro de Toledo 669, 040399-032 São Paulo, SP, Brazil
10Molecular Oncology Center, Hospital Sírio-Libanés, Rua Prof. Daher Cutait 69, 01308-060 São Paulo, SP, Brazil

Correspondence should be addressed to Ileana Gabriela Sanchez Rubio; rb.psefinu@oibur.anaeli

Received 30 August 2017; Accepted 16 November 2017; Published 8 February 2018

Academic Editor: Maria L. Dufau

Copyright © 2018 Rosalinda Yasato Camargo 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. H. Fagman and M. Nilsson, “Morphogenesis of the thyroid gland,” Molecular and Cellular Endocrinology, vol. 323, no. 1, pp. 35–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. R. O'Rahilly, “The timing and sequence of events in the development of the human endocrine system during the embryonic period proper,” Anatomy and Embryology, vol. 166, no. 3, pp. 439–451, 1983. View at Publisher · View at Google Scholar · View at Scopus
  3. M. De Felice and R. Di Lauro, “Thyroid development and its disorders: genetics and molecular mechanisms,” Endocrine Reviews, vol. 25, no. 5, pp. 722–746, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Amendola, P. de Luca, P. E. Macchia et al., “A mouse model demonstrates a multigenic origin of congenital hypothyroidism,” Endocrinology, vol. 146, no. 12, pp. 5038–5047, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Parlato, A. Rosica, A. Rodriguez-Mallon et al., “An integrated regulatory network controlling survival and migration in thyroid organogenesis,” Developmental Biology, vol. 276, no. 2, pp. 464–475, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. M. De Felice, C. Ovitt, E. Biffali et al., “A mouse model for hereditary thyroid dysgenesis and cleft palate,” Nature Genetics, vol. 19, no. 4, pp. 395–398, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Noussios, P. Anagnostis, D. G. Goulis, D. Lappas, and K. Natsis, “Ectopic thyroid tissue: anatomical, clinical, and surgical implications of a rare entity,” European Journal of Endocrinology, vol. 165, no. 3, pp. 375–382, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. V. M. Dias, A. P. Campos, A. J. Chagas, and R. M. Silva, “Congenital hypothyroidism: etiology,” Journal of Pediatric Endocrinology and Metabolism, vol. 23, no. 8, pp. 815–826, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Castanet, M. Polak, C. Bonaïti-Pellié et al., “Nineteen years of national screening for congenital hypothyroidism: familial cases with thyroid dysgenesis suggest the involvement of genetic factors,” The Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 5, pp. 2009–2014, 2001. View at Publisher · View at Google Scholar
  10. S. Stoppa-Vaucher, G. Van Vliet, and J. Deladoey, “Variation by ethnicity in the prevalence of congenital hypothyroidism due to thyroid dysgenesis,” Thyroid, vol. 21, no. 1, pp. 13–18, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. J. Tincani, A. S. Martins, A. Del Negro, P. P. Araújo, and G. Barretto, “Lingual thyroid causing dysphonia: evaluation and management. Case report,” Sao Paulo Medical Journal, vol. 122, no. 2, pp. 67–69, 2004. View at Publisher · View at Google Scholar
  12. T. W. Barnes, K. D. Olsen, and T. I. Morgenthaler, “Obstructive lingual thyroid causing sleep apnea: a case report and review of the literature,” Sleep Medicine, vol. 5, no. 6, pp. 605–607, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Kumar Choudhury, U. Kaimal Saikia, D. Sarma et al., “Dual ectopic thyroid with normally located thyroid: a case report,” Journal of Thyroid Research, vol. 2011, Article ID 159703, 4 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Gu, B. Jiang, N. Wang et al., “New insight into ectopic thyroid glands between the neck and maxillofacial region from a 42-case study,” BMC Endocrine Disorders, vol. 15, no. 1, p. 70, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Narumi, K. Muroya, Y. Asakura, M. Adachi, and T. Hasegawa, “Transcription factor mutations and congenital hypothyroidism: systematic genetic screening of a population-based cohort of Japanese patients,” The Journal of Clinical Endocrinology and Metabolism, vol. 95, no. 4, pp. 1981–1985, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Carre, A. Stoupa, D. Kariyawasam et al., “Mutations in BOREALIN cause thyroid dysgenesis,” Human Molecular Genetics, vol. 26, no. 3, pp. 599–610, 2017. View at Publisher · View at Google Scholar · View at Scopus
  17. M. M. L. Kizys, R. A. Louzada, M. Mitne-Neto et al., “DUOX2 mutations are associated with congenital hypothyroidism with ectopic thyroid gland,” The Journal of Clinical Endocrinology and Metabolism, vol. 102, no. 11, pp. 4060–4071, 2017. View at Publisher · View at Google Scholar
  18. K. Wang, M. Li, and H. Hakonarson, “ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data,” Nucleic Acids Research, vol. 38, no. 16, article e164, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Gonzalez-Perez and N. Lopez-Bigas, “Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel,” The American Journal of Human Genetics, vol. 88, no. 4, pp. 440–449, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Schwarz, D. N. Cooper, M. Schuelke, and D. Seelow, “MutationTaster2: mutation prediction for the deep-sequencing age,” Nature Methods, vol. 11, no. 4, pp. 361-362, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Choi, G. E. Sims, S. Murphy, J. R. Miller, and A. P. Chan, “Predicting the functional effect of amino acid substitutions and indels,” PLoS One, vol. 7, no. 10, article e46688, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Abu-Khudir, J. Paquette, A. Lefort et al., “Transcriptome, methylome and genomic variations analysis of ectopic thyroid glands,” PLoS One, vol. 5, no. 10, article e13420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Opitz, E. Maquet, M. Zoenen, R. Dadhich, and S. Costagliola, “TSH receptor function is required for normal thyroid differentiation in zebrafish,” Molecular Endocrinology, vol. 25, no. 9, pp. 1579–1599, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Catalano, M. Dentice, R. Ambrosio et al., “Activated thyroid hormone promotes differentiation and chemotherapeutic sensitization of colorectal cancer stem cells by regulating Wnt and BMP4 signaling,” Cancer Research, vol. 76, no. 5, pp. 1237–1244, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. A. W. Ross, G. Helfer, L. Russell, V. M. Darras, and P. J. Morgan, “Thyroid hormone signalling genes are regulated by photoperiod in the hypothalamus of F344 rats,” PLoS One, vol. 6, no. 6, article e21351, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Leone, D. D'Angelo, A. Ferraro et al., “A TSH-CREB1-microRNA loop is required for thyroid cell growth,” Molecular Endocrinology, vol. 25, no. 10, pp. 1819–1830, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Szinnai, L. Lacroix, A. Carré et al., “Sodium/iodide symporter (NIS) gene expression is the limiting step for the onset of thyroid function in the human fetus,” The Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 1, pp. 70–76, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Kurihara, H. Kurihara, K. Maemura, T. Kuwaki, M. Kumada, and Y. Yazaki, “Impaired development of the thyroid and thymus in endothelin-1 knockout mice,” Journal of Cardiovascular Pharmacology, vol. 26, no. Suppl 3, pp. S13–S16, 1995. View at Publisher · View at Google Scholar
  29. O. A. Elsalini, J. Gartzen, M. Cramer, and K. B. Rohr, “Zebrafish hhex, nk2.1a, and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors,” Developmental Biology, vol. 263, no. 1, pp. 67–80, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Cooley, C. B. Kern, V. M. Fresco et al., “Fibulin-1 is required for morphogenesis of neural crest-derived structures,” Developmental Biology, vol. 319, no. 2, pp. 336–345, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. F. B. Davis, S. A. Mousa, L. O'Connor et al., “Proangiogenic action of thyroid hormone is fibroblast growth factor-dependent and is initiated at the cell surface,” Circulation Research, vol. 94, no. 11, pp. 1500–1506, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Hannenhalli and K. H. Kaestner, “The evolution of Fox genes and their role in development and disease,” Nature Reviews Genetics, vol. 10, no. 4, pp. 233–240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Kameda, M. Ito, T. Nishimaki, and N. Gotoh, “FRS2a is required for the separation, migration, and survival of pharyngeal-endoderm derived organs including thyroid, ultimobranchial body, parathyroid, and thymus,” in Yearbook of Pediatric Endocrinology, J.-C. Carel and Z. E. Rochberg, Eds., pp. 32-33, Karger, Basel, Switzeland, 2009. View at Google Scholar
  34. V. Panicker, “Genetics of thyroid function and disease,” Clinical Biochemist Reviews, vol. 32, no. 4, pp. 165–175, 2011. View at Google Scholar
  35. T. Di Palma, A. Conti, T. de Cristofaro, S. Scala, L. Nitsch, and M. Zannini, “Identification of novel Pax8 targets in FRTL-5 thyroid cells by gene silencing and expression microarray analysis,” PLoS One, vol. 6, no. 9, article e25162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ruiz-Llorente, E. C. de Pau, A. Sastre-Perona et al., “Genome-wide analysis of Pax8 binding provides new insights into thyroid functions,” BMC Genomics, vol. 13, no. 1, p. 147, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. L. P. Fernandez, A. López-Márquez, A. M. Martínez, G. Gómez-López, and P. Santisteban, “New insights into FoxE1 functions: identification of direct FoxE1 targets in thyroid cells,” PLoS One, vol. 8, no. 5, article e62849, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Deladoey, J. Ruel, Y. Giguère, and G. Van Vliet, “Is the incidence of congenital hypothyroidism really increasing? A 20-year retrospective population-based study in Quebec,” The Journal of Clinical Endocrinology & Metabolism, vol. 96, no. 8, pp. 2422–2429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. J. S. Yoon, K. C. Won, I. H. Cho, J. T. Lee, and H. W. Lee, “Clinical characteristics of ectopic thyroid in Korea,” Thyroid, vol. 17, no. 11, pp. 1117–1121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. I. Vandernoot, H. Sartelet, R. Abu-Khudir, J. P. Chanoine, and J. Deladoëy, “Evidence for calcitonin-producing cells in human lingual thyroids,” The Journal of Clinical Endocrinology and Metabolism, vol. 97, no. 3, pp. 951–956, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Kamijo, “Lingual thyroid associated with Graves’ disease and Graves’ ophthalmopathy,” Thyroid, vol. 15, no. 12, pp. 1407-1408, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. J. Wang, P. Y. Chu, and S. K. Tai, “Ectopic thyroid papillary carcinoma presenting as bilateral neck masses,” Journal of the Chinese Medical Association, vol. 73, no. 4, pp. 219–221, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. B. C. Shah, C. S. Ravichand, S. Juluri, A. Agarwal, C. S. Pramesh, and R. C. Mistry, “Ectopic thyroid cancer,” Annals of Thoracic and Cardiovascular Surgery, vol. 13, no. 2, pp. 122–124, 2007. View at Google Scholar
  44. G. Tucci and F. Rulli, “Follicular carcinoma in ectopic thyroid gland. A case report,” Il Giornale di Chirurgia, vol. 20, no. 3, pp. 97–99, 1999. View at Google Scholar
  45. Y. Y. Mishriki, B. P. Lane, M. S. Lozowski, and H. Epstein, “Hurthle-cell tumor arising in the mediastinal ectopic thyroid and diagnosed by fine needle aspiration. Light microscopic and ultrastructural features,” Acta Cytologica, vol. 27, no. 2, pp. 188–192, 1983. View at Google Scholar
  46. T. H. Shepard, H. Andersen, and H. J. Andersen, “Histochemical studies of the human fetal thyroid during the first half of fetal life,” The Anatomical Record, vol. 149, no. 3, pp. 363–379, 1964. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Narumi, A. Yoshida, K. Muroya et al., “PAX8 mutation disturbing thyroid follicular growth: a case report,” The Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 12, pp. E2039–E2044, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Studer, R. Forster, A. Conti, H. Kohler, A. Haeberli, and H. Engler, “Transformation of normal follicles into thyrotropin-refractory “cold” follicles in the aging mouse thyroid gland,” Endocrinology, vol. 102, no. 5, pp. 1576–1586, 1978. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Faggiano, B. Caillou, L. Lacroix et al., “Functional characterization of human thyroid tissue with immunohistochemistry,” Thyroid, vol. 17, no. 3, pp. 203–211, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. S. S. Trueba, J. Augé, G. Mattei et al., “PAX8, TITF1, and FOXE1 gene expression patterns during human development: new insights into human thyroid development and thyroid dysgenesis-associated malformations,” The Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 1, pp. 455–462, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Montanelli and M. Tonacchera, “Genetics and phenomics of hypothyroidism and thyroid dys- and agenesis due to PAX8 and TTF1 mutations,” Molecular and Cellular Endocrinology, vol. 322, no. 1-2, pp. 64–71, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. A. R. Laury, R. Perets, H. Piao et al., “A comprehensive analysis of PAX8 expression in human epithelial tumors,” The American Journal of Surgical Pathology, vol. 35, no. 6, pp. 816–826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Sequeira, B. Jasani, D. Fuhrer, M. Wheeler, and M. Ludgate, “Demonstration of reduced in vivo surface expression of activating mutant thyrotrophin receptors in thyroid sections,” European Journal of Endocrinology, vol. 146, no. 2, pp. 163–171, 2002. View at Publisher · View at Google Scholar
  54. A. Thorwarth, I. Mueller, H. Biebermann et al., “Screening chromosomal aberrations by array comparative genomic hybridization in 80 patients with congenital hypothyroidism and thyroid dysgenesis,” The Journal of Clinical Endocrinology and Metabolism, vol. 95, no. 7, pp. 3446–3452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Devdhar, R. Drooger, M. Pehlivanova, G. Singh, and J. Jonklaas, “Levothyroxine replacement doses are affected by gender and weight, but not age,” Thyroid, vol. 21, no. 8, pp. 821–827, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. F. Magne, R. Serpa, G. van Vliet, M. E. Samuels, and J. Deladoëy, “Somatic mutations are not observed by exome sequencing of lymphocyte DNA from monozygotic twins discordant for congenital hypothyroidism due to thyroid dysgenesis,” Hormone Research in Pædiatrics, vol. 83, no. 2, pp. 79–85, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Abu-Khudir, F. Magne, J. P. Chanoine, C. Deal, G. van Vliet, and J. Deladoëy, “Role for tissue-dependent methylation differences in the expression of FOXE1 in nontumoral thyroid glands,” The Journal of Clinical Endocrinology and Metabolism, vol. 99, no. 6, pp. E1120–E1129, 2014. View at Publisher · View at Google Scholar · View at Scopus