nach oben

Reviews in Endocrine and Metabolic Disorders

Erschienen in:

27.11.2019

The gut microbiota modulates both browning of white adipose tissue and the activity of brown adipose tissue

verfasst von: José María Moreno-Navarrete, José Manuel Fernandez-Real

Erschienen in: Reviews in Endocrine and Metabolic Disorders | Ausgabe 4/2019

Einloggen, um Zugang zu erhalten

Abstract

Given the increasing worldwide prevalence of obesity and associated metabolic disturbances, novel therapeutic strategies are imperatively required. A plausible manner to increase energy expenditure is the enhancement of thermogenic pathways in white (WAT) and brown adipose tissue (BAT). In the last 15 years, the identification of novel endogenous mechanisms to promote BAT activity or browning of WAT has pointed at gut microbiota as an important modulator of host metabolic homeostasis and energy balance. In this review, we focused on the relationship between gut microbiota composition and adipose tissue thermogenic program (including BAT activity and browning of WAT) in both physiological and stress conditions. Specifically, we reviewed the effects of fasting, caloric restriction, cold stress and metabolic endotoxemia on both browning and gut microbiota shifts. Mechanistically speaking, processes related to bile acid metabolism and the endocannabinoid system seem to play an important role. In summary, the gut microbiota seems to impact WAT and BAT physiology at multiple levels.

Czech MP. Insulin action and resistance in obesity and type 2 diabetes. Nat Med. 2017;23:804–14.PubMedPubMedCentral

LeBlanc ES, Patnode CD, Webber EM, Redmond N, Rushkin M, O'Connor EA. Behavioral and pharmacotherapy weight loss interventions to prevent obesity-related morbidity and mortality in adults: updated evidence report and systematic review for the US preventive services task force. JAMA. 2018;320:1172–91.PubMed

Panagiotou OA, Markozannes G, Adam GP, Kowalski R, Gazula A, Di M, et al. Comparative effectiveness and safety of bariatric procedures in Medicare-eligible patients: a systematic review. JAMA Surg. 2018;153:e183326.PubMed

Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281:31–5.PubMed

Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal physiological stress by living at thermoneutrality. Cell Metab. 2009;9:203–9.PubMed

Tomilov A, Bettaieb A, Kim K, Sahdeo S, Tomilova N, Lam A, et al. Shc depletion stimulates brown fat activity in vivo and in vitro. Aging Cell. 2014;13:1049–58.PubMedPubMedCentral

Cohen P, Levy JD, Zhang Y, Frontini A, Kolodin DP, Svensson KJ, et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell. 2014;156:304–16.PubMedPubMedCentral

Himms-Hagen J. Nonshivering thermogenesis. Brain Res Bull. 1984;12:151–60.PubMed

PMID:22269323: Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin B, Haman F, Turcotte EE, Richard D, Carpentier AC. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545–52.

10.

Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–25.PubMed

11.

Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101:15718–23.PubMedPubMedCentral

12.

Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213–23.PubMedPubMedCentral

13.

Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–9.PubMed

14.

Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–5.PubMed

15.

Canfora EE, Meex RCR, Venema K, Blaak EE. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol. 2019;15:261–73.PubMed

16.

Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67:1716–25.PubMedPubMedCentral

17.

Hersoug LG, Møller P, Loft S. Gut microbiota-derived lipopolysaccharide uptake and trafficking to adipose tissue: implications for inflammation and obesity. Obes Rev. 2016;17:297–312.PubMed

18.

Vallianou N, Stratigou T, Christodoulatos GS, Dalamaga M. Understanding the role of the gut microbiome and microbial metabolites in obesity and obesity-associated metabolic disorders: current evidence and perspectives. Curr Obes Rep. 2019;8:317–32. https://doi.org/10.1007/s13679-019-00352-2.CrossRefPubMed

19.

Mestdagh R, Dumas ME, Rezzi S, Kochhar S, Holmes E, Claus SP, et al. Gut microbiota modulate the metabolism of brown adipose tissue in mice. J Proteome Res. 2012;11:620–30.PubMed

20.

Suárez-Zamorano N, Fabbiano S, Chevalier C, Stojanović O, Colin DJ, Stevanović A, et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat Med. 2015;21:1497–501.PubMedPubMedCentral

21.

Nguyen KD, Qiu Y, Cui X, Goh YP, Mwangi J, David T, et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature. 2011;480:104–8.PubMedPubMedCentral

22.

Qiu Y, Nguyen KD, Odegaard JI, Cui X, Tian X, Locksley RM, et al. Eosinophils and type 2 cytokine signalling in macrophages orchestrate development of functional beige fat. Cell. 2014;157:1292–308.PubMedPubMedCentral

23.

Fischer K, Ruiz HH, Jhun K, Finan B, Oberlin DJ, van der Heide V, et al. Alternatively activated macrophages do not synthesize catecholamines or contribute to adipose tissue adaptive thermogenesis. Nat Med. 2017;23:623–30.PubMedPubMedCentral

24.

Li B, Li L, Li M, Lam SM, Wang G, Wu Y, Zhang H, Niu C, Zhang X, Liu X, Hambly C, Jin W, Shui G, Speakman JR. Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue. Cell Rep. 2019; 26:2720–37.e5.PubMed

25.

Hwang I, Park YJ, Kim YR, Kim YN, Ka S, Lee HY, et al. Alteration of gut microbiota by vancomycin and bacitracin improves insulin resistance via glucagon-like peptide 1 in diet-induced obesity. FASEB J. 2015;29:2397–411.PubMed

26.

Zarrinpar A, Chaix A, Xu ZZ, Chang MW, Marotz CA, Saghatelian A, et al. Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signalling and colonic metabolism. Nat Commun. 2018;9:2872.PubMedPubMedCentral

27.

Li G, Xie C, Lu S, Nichols RG, Tian Y, Li L, Patel D, Ma Y, Brocker CN, Yan T, Krausz KW, Xiang R, Gavrilova O, Patterson AD, Gonzalez FJ. Intermittent Fasting Promotes White Adipose Browning and Decreases Obesity by Shaping the Gut Microbiota. Cell Metab. 2017;26:672–85.e4.PubMedPubMedCentral

28.

Chevalier C, Stojanović O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163:1360–74.PubMed

29.

Hanatani S, Motoshima H, Takaki Y, Kawasaki S, Igata M, Matsumura T, et al. Acetate alters expression of genes involved in beige adipogenesis in 3T3-L1 cells and obese KK-ay mice. J Clin Biochem Nutr. 2016;59:207–14.PubMedPubMedCentral

30.

Sahuri-Arisoylu M, Brody LP, Parkinson JR, Parkes H, Navaratnam N, Miller AD, et al. Reprogramming of hepatic fat accumulation and 'browning' of adipose tissue by the short-chain fatty acid acetate. Int J Obes. 2016;40:955–63.

31.

Kim N, Nam M, Kang MS, Lee JO, Lee YW, Hwang GS, et al. Piperine regulates UCP1 through the AMPK pathway by generating intracellular lactate production in muscle cells. Sci Rep. 2017;7:41066.PubMedPubMedCentral

32.

den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325–40.

33.

Iwanaga T, Kuchiiwa T, Saito M. Histochemical demonstration of monocarboxylate transporters in mouse brown adipose tissue. Biomed Res. 2009;30:217–25.PubMed

34.

Desautels M, Dulos RA. Effects of repeated cycles of fasting-refeeding on brown adipose tissue composition in mice. Am J Phys. 1988;255:E120–8.

35.

Sivitz WI, Fink BD, Donohoue PA. Fasting and leptin modulate adipose and muscle uncoupling protein: divergent effects between messenger ribonucleic acid and protein expression. Endocrinology. 1999;140:1511–9.PubMed

36.

Kim YH, Lee JH, Yeung JL, Das E, Kim RY, Jiang Y, et al. Thermogenesis-independent metabolic benefits conferred by isocaloric intermittent fasting in Ob/Ob mice. Sci Rep. 2019;9:2479.PubMedPubMedCentral

37.

Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, Maratos-Flier E, et al. Role of leptin in the neuroendocrine response to fasting. Nature. 1996;382:250–2.PubMed

38.

Frederich RC, Löllmann B, Hamann A, Napolitano-Rosen A, Kahn BB, Lowell BB, et al. Expression of Ob mRNA and its encoded protein in rodents. Impact of nutrition and obesity. J Clin Invest. 1995;96:1658–63.PubMedPubMedCentral

39.

Gan L, Liu Z, Feng F, Wu T, Luo D, Hu C, et al. Foxc2 coordinates inflammation and browning of white adipose by leptin-STAT3-PRDM16 signal in mice. Int J Obes. 2018;42:252–9.

40.

Kim KH, Kim YH, Son JE, Lee JH, Kim S, Choe MS, et al. Intermittent fasting promotes adipose thermogenesis and metabolic homeostasis via VEGF-mediated alternative activation of macrophage. Cell Res. 2017;27:1309–26.PubMedPubMedCentral

41.

Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.PubMedPubMedCentral

42.

Fabbiano S, Suárez-Zamorano N, Chevalier C, Lazarević V, Kieser S, Rigo D, Leo S, Veyrat-Durebex C, Gaïa N, Maresca M, Merkler D, Gomez de Agüero M, Macpherson A, Schrenzel J, Trajkovski M. Functional Gut Microbiota Remodeling Contributes to the Caloric Restriction-Induced Metabolic Improvements. Cell Metab. 2018;28:907–921.e7.PubMedPubMedCentral

43.

Okla M, Zaher W, Alfayez M, Chung S. Inhibitory effects of toll-like receptor 4, NLRP3 Inflammasome, and interleukin-1β on white adipocyte Browning. Inflammation. 2018;41:626–42.PubMedPubMedCentral

44.

Okla M, Wang W, Kang I, Pashaj A, Carr T, Chung S. Activation of toll-like receptor 4 (TLR4) attenuates adaptive thermogenesis via endoplasmic reticulum physiological stress. J Biol Chem. 2015;290:26476–90.PubMedPubMedCentral

45.

Hailman E, Lichenstein HS, Wurfel MM, Miller DS, Johnson DA, Kelley M, et al. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J Exp Med. 1994;179:269–77.PubMed

46.

Tobias PS, Soldau K, Ulevitch RJ. Identification of a lipid a binding site in the acute phase reactant lipopolysaccharide binding protein. J Biol Chem. 1989;264:10867–71.PubMed

47.

Moreno-Navarrete JM, Ortega F, Serino M, Luche E, Waget A, Pardo G, et al. Circulating lipopolysaccharide-binding protein (LBP) as a marker of obesity-related insulin resistance. Int J Obes (Lond). 2012;36:1442–9.

48.

Tilves CM, Zmuda JM, Kuipers AL, Nestlerode CS, Evans RW, Bunker CH, et al. Association of Lipopolysaccharide-Binding Protein with Aging-Related Adiposity Change and Prediabetes among African Ancestry men. Diabetes Care. 2016;39:385–91.PubMed

49.

Liu X, Lu L, Yao P, Ma Y, Wang F, Jin Q, et al. Lipopolysaccharide binding protein, obesity status and incidence of metabolic syndrome: a prospective study among middle-aged and older Chinese. Diabetologia. 2014;57:1834–41.PubMed

50.

Moreno-Navarrete JM, Escoté X, Ortega F, Serino M, Campbell M, Michalski MC, et al. A role for adipocyte-derived lipopolysaccharide-binding protein in inflammation- and obesity-associated adipose tissue dysfunction. Diabetologia. 2013;56:2524–37.PubMed

51.

Moreno-Navarrete JM, Escoté X, Ortega F, Camps M, Ricart W, Zorzano A, et al. Lipopolysaccharide binding protein is an adipokine involved in the resilience of the mouse adipocyte to inflammation. Diabetologia. 2015;58:2424–34.PubMed

52.

Gavaldà-Navarro A, Moreno-Navarrete JM, Quesada-López T, Cairó M, Giralt M, Fernández-Real JM, et al. Lipopolysaccharide-binding protein is a negative regulator of adipose tissue browning in mice and humans. Diabetologia. 2016;59:2208–18.PubMed

53.

Moreno-Navarrete JM, Jové M, Padró T, Boada J, Ortega F, Ricart W, et al. Adipocyte lipopolysaccharide binding protein (LBP) is linked to a specific lipidomic signature. Obesity (Silver Spring). 2017;25:391–400.

54.

Nagata N, Xu L, Kohno S, Ushida Y, Aoki Y, Umeda R, et al. Glucoraphanin ameliorates obesity and insulin resistance through adipose tissue Browning and Reduction of metabolic Endotoxemia in mice. Diabetes. 2017;66:1222–36.PubMed

55.

Yore MM, Syed I, Moraes-Vieira PM, Zhang T, Herman MA, Homan EA, et al. Discovery of a class of endogenous mammalian lipids with anti-diabetic and anti-inflammatory effects. Cell. 2014;159:318–32.PubMedPubMedCentral

56.

Wang YM, Liu HX, Fang NY. 9-PAHSA promotes browning of white fat via activating G-protein-coupled receptor 120 and inhibiting lipopolysaccharide / NF-kappa B pathway. Biochem Biophys Res Commun. 2018;506:153–60.PubMed

57.

Cao W, Huang H, Xia T, Liu C, Muhammad S, Sun C. Homeobox a5 promotes white adipose tissue Browning through inhibition of the Tenascin C/toll-like receptor 4/nuclear factor kappa B inflammatory Signalling in mice. Front Immunol. 2018;9:647.PubMedPubMedCentral

58.

Yamamoto Y, Gesta S, Lee KY, Tran TT, Saadatirad P, Kahn CR. Adipose depots possess unique developmental gene signatures. Obesity (Silver Spring). 2010;18:872–8.

59.

Dankel SN, Fadnes DJ, Stavrum AK, Stansberg C, Holdhus R, Hoang T, et al. Switch from physiological stress response to homeobox transcription factors in adipose tissue after profound fat loss. PLoS One. 2010;5:e11033.PubMedPubMedCentral

60.

Lidell ME, Seifert EL, Westergren R, Heglind M, Gowing A, Sukonina V, et al. The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function. Diabetes. 2011;60:427–35.PubMedPubMedCentral

61.

Cederberg A, Grønning LM, Ahrén B, Taskén K, Carlsson P, Enerbäck S. FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell. 2001;106:563–73.PubMed

62.

Rahman S, Lu Y, Czernik PJ, Rosen CJ, Enerback S, Lecka-Czernik B. Inducible brown adipose tissue, or beige fat, is anabolic for the skeleton. Endocrinology. 2013;154:2687–701.PubMedPubMedCentral

63.

Kim JK, Kim HJ, Park SY, Cederberg A, Westergren R, Nilsson D, et al. Adipocyte-specific overexpression of FOXC2 prevents diet-induced increases in intramuscular fatty acyl CoA and insulin resistance. Diabetes. 2005;54:1657–63.PubMed

64.

Sommer F, Ståhlman M, Ilkayeva O, Arnemo JM, Kindberg J, Josefsson J, et al. The gut microbiota modulates energy metabolism in the hibernating Brown bear Ursus arctos. Cell Rep. 2016;14:1655–61.PubMed

65.

Zhang XY, Sukhchuluun G, Bo TB, Chi QS, Yang JJ, Chen B, et al. Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure. Microbiome. 2018;6:103.PubMedPubMedCentral

66.

Worthmann A, John C, Rühlemann MC, Baguhl M, Heinsen FA, Schaltenberg N, et al. Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat Med. 2017;23:839–49.PubMed

67.

Ziętak M, Kovatcheva-Datchary P, Markiewicz LH, Ståhlman M, Kozak LP, Bäckhed F. Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab. 2016;23:1216–23.PubMedPubMedCentral

68.

Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066–71.PubMedPubMedCentral

69.

Schneeberger M, Everard A, Gómez-Valadés AG, Matamoros S, Ramírez S, Delzenne NM, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.PubMedPubMedCentral

70.

Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L; MICRO-Obes consortium, Dumas ME, Rizkalla SW, Doré J, Cani PD, Clément K Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology Gut 2016;65:426–36.

71.

Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L, et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med. 2017;23:107–13.PubMed

72.

Li J, Lin S, Vanhoutte PM, Woo CW, Xu A. Akkermansia Muciniphila protects against atherosclerosis by preventing metabolic Endotoxemia-induced inflammation in Apoe−/− mice. Circulation. 2016;133:2434–46.PubMed

73.

Wahlström A, Sayin SI, Marschall HU, Bäckhed F. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 2016;24:41–50.PubMed

74.

Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A. 2007;104:979–84.PubMedPubMedCentral

75.

Jiang C, Xie C, Li F, Zhang L, Nichols RG, Krausz KW, et al. Intestinal farnesoid X receptor signalling promotes nonalcoholic fatty liver disease. J Clin Invest. 2015;125:386–402.PubMed

76.

Jiang C, Xie C, Lv Y, Li J, Krausz KW, Shi J, et al. Intestine-selective farnesoid X receptor inhibition improves obesity-related metabolic dysfunction. Nat Commun. 2015;6:10166.PubMedPubMedCentral

77.

Fang S, Suh JM, Reilly SM, Yu E, Osborn O, Lackey D, et al. Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance. Nat Med. 2015;21:159–65.PubMedPubMedCentral

78.

Pathak P, Liu H, Boehme S, Xie C, Krausz KW, Gonzalez F, et al. Farnesoid X receptor induces Takeda G-protein receptor 5 cross-talk to regulate bile acid synthesis and hepatic metabolism. J Biol Chem. 2017;292:11055–69.PubMedPubMedCentral

79.

Pathak P, Xie C, Nichols RG, Ferrell JM, Boehme S, Krausz KW, et al. Intestine farnesoid X receptor agonist and the gut microbiota activate G-protein bile acid receptor-1 signalling to improve metabolism. Hepatology. 2018;68:1574–88.PubMedPubMedCentral

80.

Pfeiffer N, Desmarchelier C, Blaut M, Daniel H, Haller D, Clavel T. Acetatifactor muris gen. Nov., sp. nov., a novel bacterium isolated from the intestine of an obese mouse. Arch Microbiol. 2012;194:901–7.PubMed

81.

Hirano S, Masuda N. Enhancement of the 7 alpha-dehydroxylase activity of a gram-positive intestinal anaerobe by Bacteroides and its significance in the 7-dehydroxylation of ursodeoxycholic acid. J Lipid Res. 1982;23:1152–8.PubMed

82.

Ishii M, Toda T, Ikarashi N, Kusunoki Y, Kon R, Ochiai W, et al. Gastrectomy increases the expression of hepatic cytochrome P450 3A by increasing lithocholic acid-producing enteric bacteria in mice. Biol Pharm Bull. 2014;37:298–305.PubMed

83.

Somm E, Henry H, Bruce SJ, Aeby S, Rosikiewicz M, Sykiotis GP, et al. β-Klotho deficiency protects against obesity through a crosstalk between liver, microbiota, and brown adipose tissue. JCI. Insight. 2017;2:91809.

84.

Broeders EP, Nascimento EB, Havekes B, Brans B, Roumans KH, Tailleux A, et al. The bile acid Chenodeoxycholic acid increases human Brown adipose tissue activity. Cell Metab. 2015;22:418–26.PubMed

85.

Geurts L, Everard A, Van Hul M, Essaghir A, Duparc T, Matamoros S, et al. Adipose tissue NAPE-PLD controls fat mass development by altering the browning process and gut microbiota. Nat Commun. 2015;6:6495.PubMedPubMedCentral

86.

Moreno-Navarrete JM, Serino M, Blasco-Baque V, Azalbert V, Barton RH, Cardellini M, et al. Gut Microbiota Interacts with Markers of Adipose Tissue Browning, Insulin Action and Plasma Acetate in Morbid Obesity. Mol Nutr Food Res. 2018;62(3). https://doi.org/10.1002/mnfr.201700721.

87.

Weitkunat K, Stuhlmann C, Postel A, Rumberger S, Fankhänel M, Woting A, et al. Short-chain fatty acids and inulin, but not guar gum, prevent diet-induced obesity and insulin resistance through differential mechanisms in mice. Sci Rep. 2017;7:6109.PubMedPubMedCentral

88.

Hu J, Kyrou I, Tan BK, Dimitriadis GK, Ramanjaneya M, Tripathi G, et al. Short-chain fatty acid acetate stimulates Adipogenesis and mitochondrial biogenesis via GPR43 in Brown adipocytes. Endocrinology. 2016;157:1881–94.PubMed

89.

Lu Y, Fan C, Li P, Lu Y, Chang X, Qi K. Short chain fatty acids prevent high-fat-diet-induced obesity in mice by regulating G protein-coupled receptors and gut microbiota. Sci Rep. 2016;6:37589.PubMedPubMedCentral

90.

Stanford KI, Middelbeek RJ, Goodyear LJ. Exercise effects on white adipose tissue: Beiging and metabolic adaptations. Diabetes. 2015;64:2361–8.PubMedPubMedCentral

91.

Sidossis L, Kajimura S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015;125:478–86.PubMedPubMedCentral

92.

Moreno-Navarrete JM, Ortega F, Moreno M, Xifra G, Ricart W, Fernández-Real JM. PRDM16 sustains white fat gene expression profile in human adipocytes in direct relation with insulin action. Mol Cell Endocrinol. 2015;405:84–93.PubMed

93.

Comas F, Martínez C, Sabater M, Ortega F, Latorre J, Díaz-Sáez F, et al. Neuregulin 4 is a novel marker of beige adipocyte precursor cells in human adipose tissue. Front Physiol. 2019 Jan 31;10:39.PubMedPubMedCentral

94.

Barquissau V, Léger B, Beuzelin D, Martins F, Amri EZ, Pisani DF, et al. Caloric restriction and diet-induced weight loss do not induce Browning of human subcutaneous white adipose tissue in women and men with obesity. Cell Rep. 2018;22:1079–89.PubMed

Titel: The gut microbiota modulates both browning of white adipose tissue and the activity of brown adipose tissue
verfasst von: José María Moreno-Navarrete
José Manuel Fernandez-Real
Publikationsdatum: 27.11.2019
Verlag: Springer US
Erschienen in: Reviews in Endocrine and Metabolic Disorders / Ausgabe 4/2019
Print ISSN: 1389-9155
Elektronische ISSN: 1573-2606
DOI: https://doi.org/10.1007/s11154-019-09523-x

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Innere Medizin

19.04.2024 | Vorhofflimmern | Nachrichten

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

The gut microbiota modulates both browning of white adipose tissue and the activity of brown adipose tissue

Abstract

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Parodontalbehandlung verbessert Prognose bei Katheterablation

Prostatakarzinom: EU initiiert neues Screeningkonzept

Blasenkarzinom – Biomarker statt Zytologie?

Antihypertensiva schützen auch alte Menschen noch vor Demenz

Update Innere Medizin

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 4/2019

Oral microbiota-induced periodontitis: a new risk factor of metabolic diseases

Consider the microbiome in the equation! They were here before us...and hosted us!

Microbiota impacts on chronic inflammation and metabolic syndrome - related cognitive dysfunction

Dietary lipids, gut microbiota and lipid metabolism

Keto microbiota: A powerful contributor to host disease recovery

The gut microbiome and heart failure: A better gut for a better heart

Leitlinien kompakt für die Innere Medizin

Neu im Fachgebiet Innere Medizin

Parodontalbehandlung verbessert Prognose bei Katheterablation

Prostatakarzinom: EU initiiert neues Screeningkonzept

Blasenkarzinom – Biomarker statt Zytologie?

Antihypertensiva schützen auch alte Menschen noch vor Demenz

Update Innere Medizin