Chemically or surgically induced thyroid dysfunction altered gut microbiota in rat models.
Animals
Bacteria
/ genetics
Bacteroidetes
/ genetics
Disease Models, Animal
Feces
/ microbiology
Gastrointestinal Microbiome
/ genetics
Hypothyroidism
/ microbiology
Male
Metagenomics
/ methods
Microbiota
/ genetics
RNA, Ribosomal, 16S
/ genetics
Rats
Rats, Sprague-Dawley
Thyroid Gland
/ microbiology
gut microbiota
hyperthyroidism
hypothyroidism
thyroid function
thyroidectomy
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
10
12
2019
revised:
17
04
2020
accepted:
18
04
2020
pubmed:
2
5
2020
medline:
16
1
2021
entrez:
2
5
2020
Statut:
ppublish
Résumé
Thyroid hormones are essential for the regulation of energy homeostasis and metabolic processes. However, the relationship between thyroid function and host gut microbial communities is not properly understood. To determine whether and how gut microbiota is associated with thyroid function, metagenomics analysis of the bacterial population in fecal samples of rat models of hyperthyroidism (induced by levothyroxine) and hypothyroidism (induced by propylthiouracil or thyroidectomy) was conducted through 16S rRNA gene sequencing. Our results revealed that all thyroid dysfunction models were definitely established and gut microbial composition varied according to different thyroid functional status. The relative abundance of Ruminococcus was significantly higher in the hyperthyroidism group (HE) vs both the normal and hypothyroidism groups (HO) while S24-7 was significantly higher in the HO group. The population of Prevotellaceae and Prevotella were significantly lower in the HO group vs the normal. Firmicutes and Oscillospira were significantly higher in the SHO (surgery-induced hypothyroidism) group, while Prevotellaceae and Prevotella showed lower abundance in the SHO group than the SHAM group. Present results suggest that thyroid functions may have the potential to influence the profile of gut microbiota and could be used as foundation to investigate interaction mechanism between thyroid and gut microbiome.
Identifiants
pubmed: 32356337
doi: 10.1096/fj.201903091RR
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8686-8701Informations de copyright
© 2020 Federation of American Societies for Experimental Biology.
Références
Brent GA. Mechanisms of thyroid hormone action. J Clin Investig. 2012;122:3035.
Reinehr T. Obesity and thyroid function. Mol Cell Endocrinol. 2010;316:165-171.
Biondi B. Thyroid and obesity: an intriguing relationship. J Clin Endocrinol Metab. 2010;95(8):3614-3617. https://doi.org/10.1210/jc.2010-1245.
Sari R, Balci MK, Altunbas H, Karayalcin U. The effect of body weight and weight loss on thyroid volume and function in obese women. Clin Endocrinol. 2003;59:258-262.
Salam MHA, Edrees HM. Effect of different conditions of thyroid function on serum adiponectin, visfatin and vaspin levels in rats. Basic Sci Med. 2015;4:12-19.
Mullur R, Liu Y-Y, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev. 2014;94:355-382.
Cooper DS, Biondi B. Subclinical thyroid disease. Lancet. 2012;379:1142-1154.
Taylor PN, Razvi S, Pearce SH, Dayan CM. A review of the clinical consequences of variation in thyroid function within the reference range. J Clin Endocrinol Metab. 2013;98:3562-3571.
Knudsen N, Laurberg P, Rasmussen LB, et al. Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J Clin Endocrinol Metab. 2005;90:4019-4024.
Hage MP, Azar ST. The link between thyroid function and depression. J Thyroid Res. 2012;2012:1-8. https://doi.org/10.1155/2012/590648.
Vijay-Kumar M, Aitken JD, Carvalho FA, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science. 2010;328:228-231.
Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242-249.
Bäckhed F, Ding H, Wang T, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA. 2004;101:15718-15723.
Shin NR, Bose S, Wang J-H, et al. Flos Lonicera combined with metformin ameliorates hepatosteatosis and glucose intolerance in association with gut microbiota modulation. Front Microbiol. 2017;8:2271.
Wang J-H, Bose S, Kim G-C, et al. Flos Lonicera ameliorates obesity and associated endotoxemia in rats through modulation of gut permeability and intestinal microbiota. PLoS ONE. 2014;9:e86117.
Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55-60.
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027-1031. https://doi.org/10.1038/nature05414.
Zheng P, Zeng B, Zhou C, et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host’s metabolism. Mol Psychiatry. 2016;21:786.
Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science. 2013;339:1084-1088.
Vilsbøll T, Holst JJ. Incretins, insulin secretion and type 2 diabetes mellitus. Diabetologia. 2004;47:357-366.
Vrieze A, Holleman F, Zoetendal E, De Vos W, Hoekstra J, Nieuwdorp M. The environment within: how gut microbiota may influence metabolism and body composition. Diabetologia. 2010;53:606-613.
Lauritano EC, Bilotta AL, Gabrielli M, et al. Association between hypothyroidism and small intestinal bacterial overgrowth. J Clin Endocrinol Metab. 2007;92:4180-4184.
Zhou L, Li X, Ahmed A, et al. Gut microbe analysis between hyperthyroid and healthy individuals. Curr Microbiol. 2014;69:675-680.
National Research Council. Guide for the care and use of laboratory animals. Washington, DC: Institute of Laboratory Animal Resources, Commission on Life Sciences. National Academy of Sciences; 1996.
Kim S-M, Kim S-C, Chung I-K, Cheon W-H, Ku S-K. Antioxidant and protective effects of Bupleurum falcatum on the L-thyroxine-induced hyperthyroidism in rats. J Evid Based Integr Med. 2012;2012:1-12.
Limonard E, Bisschop P, Fliers E, Nieveen van Dijkum E. Thyroid function after subtotal thyroidectomy in patients with graves’ hyperthyroidism. Sci World J. 2012;2012:1-5. https://doi.org/10.1100/2012/548796
Pearson K. Determination of the coefficient of correlation. Science. 1909;30:23-25.
Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-336.
Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27:863-864.
Bray JR, Curtis JT. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr. 1957;27:325-349.
Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:1.
Bárcena C, Valdés-Mas R, Mayoral P, et al. Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice. Nat Med. 2019;25:1234-1242.
Conley MN, Wong CP, Duyck KM, Hord N, Ho E, Sharpton TJ. Aging and serum MCP-1 are associated with gut microbiome composition in a murine model. PeerJ. 2016;4:e1854.
Johnson BM, Gaudreau M-C, Gudi R, Brown R, Gilkeson G, Vasu C. Gut microbiota differently contributes to intestinal immune phenotype and systemic autoimmune progression in female and male lupus-prone mice. J Autoimmun. 2020;108:102420.
Varian B, Poutahidis T, Levkovich T, et al. Beneficial bacteria stimulate youthful thyroid gland activity. J Obes Weight Loss Ther. 2014;4.
Köhling HL, Plummer SF, Marchesi JR, Davidge KS, Ludgate M. The microbiota and autoimmunity: their role in thyroid autoimmune diseases. Clin Immunol. 2017;183:63-74.
Shenkman L, Bottone EJ. Antibodies to Yersinia enterocolitica in thyroid disease. Ann Intern Med. 1976;85:735-739.
Wenzel B, Heesmann J, Wenzel K, Scriba PC. Antibodies to plasmid-encoded Proteins of enteropathogenic Yersinia in patiens with autoimmune thyroid disease. Lancet. 1988:56.
Çorapçioğlu D, Tonyukuk V, Kiyan M, et al. Relationship between thyroid autoimmunity and Yersinia enterocolitica antibodies. Thyroid. 2002;12:613-617.
Arscott P, Rosen ED, Koenig RJ, et al. Immunoreactivity to Yersinia enterocolitica antigens in patients with autoimmune thyroid disease. J Clin Endocrinol Metab. 1992;75:295-300.
Byfield P, Davies S, Copping S, Barclay F, Borriello S. Thyrotrophin (TSH)-binding proteins in bacteria and their cross-reaction with autoantibodies against the human TSH receptor. J Endocrinol. 1989;121:571-577.
Ishaq HM, Mohammad IS, Shahzad M, et al. Molecular alteration analysis of human gut microbial composition in graves' disease patients. Int J Biol Sci. 2018;14:1558-1570.
Jiang W, Wu N, Wang X, et al. Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci Rep. 2015;5:8096.
MKGarg NM, Kumar KH. Laboratory evaluation of thyroid functions: dilemmas and pitfalls. Princ Pract Thyroid Gland Disord. 2017;22:3-332.
Nilsson M, Fagman H. Development of the thyroid gland. Development. 2017;144(12):2123-2140. https://doi.org/10.1242/dev.145615.
Hoshi N, Kusakabe T, Taylor BJ, Kimura S. Side population cells in the mouse thyroid exhibit stem/progenitor cell-like characteristics. Endocrinology. 2007;148:4251-4258.
Okamoto M, Hayase S, Miyakoshi M, Murata T, Kimura S. Stem cell antigen 1-positive mesenchymal cells are the origin of follicular cells during thyroid regeneration. PLoS ONE. 2013;8:e80801.