Does microbiota composition affect thyroid homeostasis?

Endocrine

Volumn 49, Issue 3, 2015, Pages 583-587

  Virili, Camilla ^a,b   Centanni, Marco ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Endocrinology Unit   (Italy)

Author keywords

Autoimmune thyroiditis; Deiodinase; Dysbiosis; Intestinal microbiota; Selenium; Thyroxine malabsorption

Indexed keywords

IODOTHYRONINE; THYROXINE; TRACE ELEMENT; THYRONINE DERIVATIVE;

AMINO ACID METABOLISM; ARTICLE; AUTOIMMUNITY; BACTERIAL OVERGROWTH; DRUG ABSORPTION; DYSBIOSIS; GASTROINTESTINAL ABSORPTION; HOMEOSTASIS; HUMAN; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; SPECIES COMPOSITION; THYROID FUNCTION; THYROID HOMEOSTASIS; THYROXINE METABOLISM; AUTOIMMUNE THYROIDITIS; METABOLISM; MICROBIOLOGY; MICROFLORA; NUTRITIONAL STATUS; PATHOLOGY; PHYSIOLOGY; THYROID GLAND;

HOMEOSTASIS; HUMANS; MICROBIOTA; NUTRITIONAL STATUS; THYROID GLAND; THYROIDITIS, AUTOIMMUNE; THYRONINES;

EID: 84937916991     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-014-0509-2     Document Type: Article

References (44)

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)
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)
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)
4. F. Shanahan, Translating the microbiota to medicine. Nat. Rev. Gastrenterol. Hepatol. 9, 72–74 (2012)
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)
6. A.J. Macpherson, N.L. Harris, Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4, 478–485 (2004)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
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)
18. M.T. Hays, Thyroid hormone and the gut. Endocr. Res. 14, 203–224 (1988)
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)
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)
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)
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)
23. T.T. Macdonald, G. Monteleone, Immunity, inflammation, and allergy in the gut. Science 307, 1920–1925 (2005)
24. H.J. Wu, E. Wu, The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 4–14 (2012)
25. K. Mori, Y. Nakagawa, H. Ozaki, Does the gut microbiota trigger Hashimoto’s thyroiditis? Discov. Med. 14, 321–326 (2012)
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)
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)
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)
29. A.P. Weetman, Cellular immune responses in autoimmune thyroid disease. Clin. Endocrinol. 61, 405–413 (2004)
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)
31. C.L. Burek, M.V. Talor, Environmental triggers of autoimmune thyroiditis. J. Autoimmun. 33, 183–189 (2009)
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)
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)
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)
35. S. Benvenga, L. Bartolone, S. Squadrito, F. Lo Giudice, F. Trimarchi, Delayed intestinal absorption of levothyroxine. Thyroid 5, 249–253 (1995)
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)
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)
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)
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)
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)
41. M. Centanni, Thyroxine treatment: absorption, malabsorption, and novel therapeutic approaches. Endocrine 43, 8–9 (2013)
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)
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)
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)