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Endocrine

, Volume 49, Issue 3, pp 583–587 | Cite as

Does microbiota composition affect thyroid homeostasis?

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Abstract

The intestinal microbiota is essential for the host to ensure digestive and immunologic homeostasis. When microbiota homeostasis is impaired and dysbiosis occurs, the malfunction of epithelial barrier leads to intestinal and systemic disorders, chiefly immunologic and metabolic. The role of the intestinal tract is crucial in the metabolism of nutrients, drugs, and hormones, including exogenous and endogenous iodothyronines as well as micronutrients involved in thyroid homeostasis. However, the link between thyroid homeostasis and microbiota composition is not yet completely ascertained. A pathogenetic link with dysbiosis has been described in different autoimmune disorders but not yet fully elucidated in autoimmune thyroid disease which represents the most frequent of them. Anyway, it has been suggested that intestinal dysbiosis may trigger autoimmune thyroiditis. Furthermore, hypo- and hyper-thyroidism, often of autoimmune origin, were respectively associated to small intestinal bacterial overgrowth and to changes in microbiota composition. Whether some steps of this thyroid network may be affected by intestinal microbiota composition is briefly discussed below.

Keywords

Intestinal microbiota Selenium Thyroxine malabsorption Autoimmune thyroiditis Deiodinase Dysbiosis 
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Notes

Acknowledgments

This study has been supported by “Sapienza” University of Rome—(University Grants—prot.0006345).

Disclosure

The authors have nothing to disclose.

References

  1. 1.
    M. Montalto, F. D’Onofrio, A. Gallo, A. Cazzato, G. Gasbarrini, Intestinal microbiota and its functions. Dig. Liver. Dis. Suppl. 3, 30–34 (2009)CrossRefGoogle Scholar
  2. 2.
    M. Arumugam, J. Raes, E. Pelletier, D. Le Paslier, T. Yamada, D.R. Mende, G.R. Fernandes, J. Tap, T. Bruls, J.M. Batto, M. Bertalan, N. Borruel, F. Casellas, L. Fernandez, L. Gautier, T. Hansen, M. Hattori, T. Hayashi, M. Kleerebezem, K. Kurokawa, M. Leclerc, F. Levenez, C. Manichanh, H.B. Nielsen, T. Nielsen, N. Pons, J. Poulain, J. Qin, T. Sicheritz-Ponten, S. Tims, D. Torrents, E. Ugarte, E.G. Zoetendal, J. Wang, F. Guarner, O. Pedersen, W.M. de Vos, S. Brunak, J. Doré, MetaHIT Consortium, M. Antolín, F. Artiguenave, H.M. Blottiere, M. Almeida, C. Brechot, C. Cara, C. Chervaux, A. Cultrone, C. Delorme, G. Denariaz, R. Dervyn, K.U. Foerstner, C. Friss, M. van de Guchte, E. Guedon, F. Haimet, W. Huber, J. van Hylckama-Vlieg, A. Jamet, C. Juste, G. Kaci, J. Knol, O. Lakhdari, S. Layec, K. Le Roux, E. Maguin, A. Mérieux, R. Melo Minardi, C. M’rini, J. Muller, R. Oozeer, J. Parkhill, P. Renault, M. Rescigno, N. Sanchez, S. Sunagawa, A. Torrejon, K. Turner, G. Vandemeulebrouck, E. Varela, Y. Winogradsky, G. Zeller, J. Weissenbach, S.D. Ehrlich, P. Bork, Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011)PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    D. Festi, R. Schiumerini, C. Birtolo, L. Marzi, L. Montrone, E. Scaioli, A.R. Di Biase, A. Colecchia, Gut microbiota and its pathophysiology in disease paradigms. Dig. Dis. 29, 518–524 (2011)PubMedCrossRefGoogle Scholar
  4. 4.
    F. Shanahan, Translating the microbiota to medicine. Nat. Rev. Gastrenterol. Hepatol. 9, 72–74 (2012)CrossRefGoogle Scholar
  5. 5.
    J.M.M. Natividad, E.F. Verdu, Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol. Res. 69, 42–51 (2013)PubMedCrossRefGoogle Scholar
  6. 6.
    A.J. Macpherson, N.L. Harris, Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4, 478–485 (2004)PubMedCrossRefGoogle Scholar
  7. 7.
    H. Tlaskalová-Hogenová, R. Stěpánková, H. Kozáková, T. Hudcovic, L. Vannucci, L. Tučková, P. Rossmann, T. Hrnčíř, M. Kverka, Z. Zákostelská, K. Klimešová, J. Přibylová, J. Bártová, D. Sanchez, P. Fundová, D. Borovská, D. Srůtková, Z. Zídek, M. Schwarzer, P. Drastich, D.P. Funda, The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8, 110–120 (2011)PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    E.C. Lauritano, A.L. Bilotta, M. Gabrielli, E. Scarpellini, A. Lupascu, A. Laginestra, M. Novi, S. Sottili, M. Serricchio, G. Cammarota, G. Gasbarrini, A. Pontecorvi, A. Gasbarrini, Association between hypothyroidism and small intestinal bacterial overgrowth. J. Clin. Endocrinol. Metab. 92, 4180–4184 (2007)PubMedCrossRefGoogle Scholar
  9. 9.
    L. Zhou, X. Li, A. Ahmed, D. Wu, L. Liu, J. Qiu, Y. Yan, M. Jin, Y. Xin, Gut microbe analysis between hyperthyroid and healthy individuals. Curr. Microbiol. 69(5), 675–680 (2014)PubMedCrossRefGoogle Scholar
  10. 10.
    A.M. Navarro, V.M. Suen, I.M. Souza, J.E. De Oliveira, J.S. Marchini, Patients with severe bowel malabsorption do not have changes in iodine status. Nutrition 21, 895–900 (2005)PubMedCrossRefGoogle Scholar
  11. 11.
    J. Hrdina, A. Banning, A. Kipp, G. Loh, M. Blaut, R. Brigelius-Flohé, The gastrointestinal microbiota affects the selenium status and selenoprotein expression in mice. J. Nutr. Biochem. 20, 638–648 (2009)PubMedCrossRefGoogle Scholar
  12. 12.
    M. Michalaki, S. Volonakis, I. Mamali, F. Kalfarentzos, A.G. Vagenakis, K.B. Markou, Dietary iodine absorption is not influenced by malabsorptive bariatric surgery. Obes. Surg. 24, 1921–1925 (2014)PubMedCrossRefGoogle Scholar
  13. 13.
    R.L. Vought, F.A. Brown, K.H. Sibinovic, G. McDaniel, Effect of changing intestinal bacterial flora on thyroid function in the rat. Horm. Metab. Res. 4, 43–47 (1972)PubMedCrossRefGoogle Scholar
  14. 14.
    T.T. Nguyen, J.J. DiStefano 3rd, L.M. Huang, H. Yamada, H.J. Cahnmann, 5′- and 5-deiodinase activities in adult rat cecum and large bowel contents inhibited by intestinal microflora. Am. J. Physiol. 265, E521–E524 (1993)PubMedGoogle Scholar
  15. 15.
    L. Sabatino, G. Iervasi, P. Ferrazzi, D. Francesconi, I.J. Chopra, A study of iodothyronine 5′-monodeiodinase activities in normal and pathological tissues in man and their comparison with activities in rat tissues. Life Sci. 68, 191–202 (2000)PubMedCrossRefGoogle Scholar
  16. 16.
    S.Y. Wu, W.L. Green, W.S. Huang, M.T. Hays, I.J. Chopra, Alternate pathways of thyroid hormone metabolism. Thyroid 15, 943–958 (2005)PubMedCrossRefGoogle Scholar
  17. 17.
    M.P. Hazenberg, W.W. de Herder, T.J. Visser, Hydrolysis of iodothyronine conjugates by intestinal bacteria. FEMS Microbiol. Rev. 4, 9–16 (1988)PubMedCrossRefGoogle Scholar
  18. 18.
    M.T. Hays, Thyroid hormone and the gut. Endocr. Res. 14, 203–224 (1988)PubMedCrossRefGoogle Scholar
  19. 19.
    J.J. DiStefano 3rd, A. de Luze, T.T. Nguyen, Binding and degradation of 3,5,3′-triiodothyronine and thyroxine by rat intestinal bacteria. Am. J. Physiol. 264, E966–E972 (1993)PubMedGoogle Scholar
  20. 20.
    T.T. Nguyen, J.J. DiStefano 3rd, H. Yamada, Y.M. Yen, Steady state organ distribution and metabolism of thyroxine and 3,5,3′-triiodothyronine in intestines, liver, kidneys, blood, and residual carcass of the rat in vivo. Endocrinology 133, 2973–2983 (1993)PubMedGoogle Scholar
  21. 21.
    B. Gereben, A. Zeöld, M. Dentice, D. Salvatore, A.C. Bianco, Activation and inactivation of thyroid hormone by deiodinases: local action with general consequences. Cell Mol. Life Sci. 65(4), 570–590 (2008)PubMedCrossRefGoogle Scholar
  22. 22.
    A.M. Faria, A.C. Gomes-Santos, J.L. Gonçalves, T.G. Moreira, S.R. Medeiros, L.P. Dourado, D.C. Cara, Food components and the immune system: from tonic agents to allergens. Front. Immunol. 17, 1–16 (2013)Google Scholar
  23. 23.
    T.T. Macdonald, G. Monteleone, Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925 (2005)PubMedCrossRefGoogle Scholar
  24. 24.
    H.J. Wu, E. Wu, The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 4–14 (2012)PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    K. Mori, Y. Nakagawa, H. Ozaki, Does the gut microbiota trigger Hashimoto’s thyroiditis? Discov. Med. 14, 321–326 (2012)PubMedGoogle Scholar
  26. 26.
    M. Rotondi, L. Chiovato, S. Romagnani, M. Serio, P. Romagnani, Role of chemokines in endocrine autoimmune diseases. Endocr. Rev. 28(5), 492–520 (2007)PubMedCrossRefGoogle Scholar
  27. 27.
    E. Bosi, L. Molteni, M.G. Radaelli, L. Folini, I. Fermo, E. Bazzigaluppi, L. Piemonti, M.R. Pastore, R. Paroni, Increased intestinal permeability precedes clinical onset of type 1 diabetes. Diabetologia 49, 2824–2827 (2006)PubMedCrossRefGoogle Scholar
  28. 28.
    F.C. Sasso, O. Carbonara, R. Torella, A. Mezzogiorno, V. Esposito, L. Demagistris, M. Secondulfo, R. Carratu’, D. Iafusco, M. Cartenì, Ultrastructural changes in enterocytes in subjects with Hashimoto’s thyroiditis. Gut 53, 1878–1880 (2004)PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    A.P. Weetman, Cellular immune responses in autoimmune thyroid disease. Clin. Endocrinol. 61, 405–413 (2004)CrossRefGoogle Scholar
  30. 30.
    I. Horie, N. Abiru, Y. Nagayama, G. Kuriya, O. Saitoh, T. Ichikawa, Y. Iwakura, K. Eguchi, T helper type 17 immune response plays an indispensable role for development of iodine-induced autoimmune thyroiditis in nonobese diabetic-H2h4 mice. Endocrinology 150, 5135–5142 (2009)PubMedCrossRefGoogle Scholar
  31. 31.
    C.L. Burek, M.V. Talor, Environmental triggers of autoimmune thyroiditis. J. Autoimmun. 33, 183–189 (2009)PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    S. Yu, P.K. Maiti, M. Dyson, R. Jain, H. Braley-Mullen, B cell-deficient NOD.H-2h4 mice have CD4+ CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. J. Exp. Med. 203, 349–358 (2006)PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    B. Deplancke, Gaskins, H.R: Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr. 73, 1131S–1141S (2001)PubMedGoogle Scholar
  34. 34.
    D. Pabla, F. Akhlaghi, H. Zia, A comparative pH-dissolution profile study of selected commercial levothyroxine products using inductively coupled plasma mass spectrometry. Eur. J. Pharm. Biopharm. 72, 105–110 (2009)PubMedCrossRefGoogle Scholar
  35. 35.
    S. Benvenga, L. Bartolone, S. Squadrito, F. Lo Giudice, F. Trimarchi, Delayed intestinal absorption of levothyroxine. Thyroid 5, 249–253 (1995)PubMedCrossRefGoogle Scholar
  36. 36.
    W.E. Visser, E.C. Friesema, T.J. Visser, Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol. Endocrinol. 25, 1–14 (2011)PubMedCrossRefGoogle Scholar
  37. 37.
    L.F. de Sousa Moraes, L.M. Grzeskowiak, T.F. de Sales Teixeira, C. Gouveia Peluzio Mdo, Intestinal microbiota and probiotics in celiac disease. Clin. Microbiol. Rev. 27, 482–489 (2014)PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    C. Virili, G. Bassotti, M.G. Santaguida, R. Iuorio, S.C. Del Duca, V. Mercuri, A. Picarelli, P. Gargiulo, L. Gargano, M. Centanni, Atypical celiac disease as cause of increased need for thyroxine: a systematic study. J. Clin. Endocrinol. Metab. 97, E419–E422 (2012)PubMedCrossRefGoogle Scholar
  39. 39.
    M. Cellini, M.G. Santaguida, I. Gatto, C. Virili, S.C. Del Duca, N. Brusca, S. Capriello, L. Gargano, M. Centanni, Systematic appraisal of lactose intolerance as cause of increased need for oral thyroxine. J. Clin. Endocrinol. Metab. 99, E1454–E1458 (2014)PubMedCrossRefGoogle Scholar
  40. 40.
    M. Ruchała, E. Szczepanek-Parulska, A. Zybek, The influence of lactose intolerance and other gastro-intestinal tract disorders on L-thyroxine absorption. Endokrynol. Pol. 63, 318–323 (2012)PubMedGoogle Scholar
  41. 41.
    M. Centanni, Thyroxine treatment: absorption, malabsorption, and novel therapeutic approaches. Endocrine 43, 8–9 (2013)PubMedCrossRefGoogle Scholar
  42. 42.
    T. He, K. Venema, M.G. Priebe, G.W. Welling, R.J. Brummer, R.J. Vonk, The role of colonic metabolism in lactose intolerance. Eur. J. Clin. Invest. 38, 541–547 (2008)PubMedCrossRefGoogle Scholar
  43. 43.
    M.M. Walker, N.J. Talley, Review article: bacteria and pathogenesis of disease in the upper gastrointestinal tract—beyond the era of Helicobacter pylori. Aliment. Pharmacol. Ther. 39, 767–779 (2014)PubMedCrossRefGoogle Scholar
  44. 44.
    M. Centanni, L. Gargano, G. Canettieri, N. Viceconti, A. Franchi, G. Delle Fave, B. Annibale, Thyroxine in goiter, Helicobacter pylori infection, and chronic gastritis. N. Engl. J. Med. 354, 1787–1795 (2006)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Endocrinology Section, Department of Medico-Surgical Sciences and Biotechnologies“Sapienza” University of RomeLatinaItaly
  2. 2.Endocrinology UnitAUSL LatinaLatinaItaly

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