Regulation of thermogenic capacity in brown and white adipocytes by the prebiotic high-esterified pectin and its postbiotic acetate.
Journal
International journal of obesity (2005)
ISSN: 1476-5497
Titre abrégé: Int J Obes (Lond)
Pays: England
ID NLM: 101256108
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
01
04
2019
accepted:
15
07
2019
revised:
24
06
2019
pubmed:
31
8
2019
medline:
11
5
2021
entrez:
31
8
2019
Statut:
ppublish
Résumé
High-esterified pectin (HEP) is a prebiotic able to modulate gut microbiota, associated with health-promoting metabolic effects in glucose and lipid metabolism and adipostatic hormone sensitivity. Possible effects regulating adaptive thermogenesis and energy waste are poorly known. Therefore, we aimed to study how physiological supplementation with HEP is able to affect microbiota, energy metabolism and adaptive thermogenic capacity, and to contribute to the healthier phenotype promoted by HEP supplementation, as previously shown. We also attempted to decipher some of the mechanisms involved in the HEP effects, including in vitro experiments. We used a model of metabolic malprogramming consisting of the progeny of rats with mild calorie restriction during pregnancy, both under control diet and an obesogenic (high-sucrose) diet, supplemented with HEP, combined with in vitro experiments in primary cultured brown and white adipocytes treated with the postbiotic acetate. Our main findings suggest that chronic HEP supplementation induces markers of brown and white adipose tissue thermogenic capacity, accompanied by a decrease in energy efficiency, and prevention of weight gain under an obesogenic diet. We also show that HEP promotes an increase in beneficial bacteria in the gut and peripheral levels of acetate. Moreover, in vitro acetate can improve adipokine production, and increase thermogenic capacity and browning in brown and white adipocytes, respectively, which could be part of the protection mechanism against excess weight gain observed in vivo. HEP and acetate stand out as prebiotic/postbiotic active compounds able to modulate both brown-adipocyte metabolism and browning and protect against obesity.
Identifiants
pubmed: 31467421
doi: 10.1038/s41366-019-0445-6
pii: 10.1038/s41366-019-0445-6
doi:
Substances chimiques
Acetates
0
Prebiotics
0
Pectins
89NA02M4RX
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
715-726Références
Hartstra AV, Bouter KE, Bäckhed F, Nieuwdorp M. Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care. 2015;38:159–65.
pubmed: 25538312
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14:491–502.
pubmed: 28611480
pmcid: 28611480
Adam CL, Williams PA, Garden KE, Thomson LM, Ross AW. Dose-dependent effects of a soluble dietary fibre (pectin) on food intake, adiposity, gut hypertrophy and gut satiety hormone secretion in rats. PLoS ONE. 2015;10:e0115438.
pubmed: 25602757
pmcid: 4300082
Hamaker BR, Tuncil YE. A perspective on the complexity of dietary fiber structures and their potential effect on the gut microbiota. J Mol Biol. 2014;426:3838–50.
pubmed: 25088686
Palou M, Sánchez J, García-Carrizo F, Palou A, Picó C. Pectin supplementation in rats mitigates age-related impairment in insulin and leptin sensitivity independently of reducing food intake. Mol Nutr Food Res. 2015;59:2022–33.
pubmed: 26201873
Sanchez D, Muguerza B, Moulay L, Hernandez R, Miguel M, Aleixandre A. Highly methoxylated pectin improves insulin resistance and other cardiometabolic risk factors in Zucker fatty rats. J Agric Food Chem. 2008;56:3574–81.
pubmed: 18433105
Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol. 2015;11:577–91.
pubmed: 26260141
Oh YS, Jun HS. Role of bioactive food components in diabetes prevention: effects on Beta-cell function and preservation. Nutr Metab Insights. 2014;7:51–9.
pubmed: 25092987
pmcid: 4116378
Galanakis CM. Nutraceutical and functional food components: effects of innovative processing techniques. London, UK: Academic Press; 2017. p. 1.
Garcia-Carrizo F, Pico C, Rodriguez AM, Palou A. High-esterified pectin reverses metabolic malprogramming, improving sensitivity to adipostatic/adipokine hormones. J Agric Food Chem. 2019;67:3633–42.
pubmed: 30855142
Palou M, Priego T, Sánchez J, Palou A, Picó C. Sexual dimorphism in the lasting effects of moderate caloric restriction during gestation on energy homeostasis in rats is related with fetal programming of insulin and leptin resistance. Nutr Metab. 2010;7:69.
Palou M, Konieczna J, Torrens JM, Sánchez J, Priego T, Fernandes ML, et al. Impaired insulin and leptin sensitivity in the offspring of moderate caloric-restricted dams during gestation is early programmed. J Nutr Biochem. 2012;23:1627–39.
pubmed: 22444870
Nedergaard J, Cannon B. The browning of white adipose tissue: some burning issues. Cell Metab. 2014;20:396–407.
pubmed: 25127354
Palou A, Pico C, Bonet ML, Oliver P. The uncoupling protein, thermogenin. Int J Biochem Cell Biol. 1998;30:7–11.
pubmed: 9597749
Rodriguez AM, Palou A. Uncoupling proteins: gender-dependence and their relation to body weight control. Int J Obes Relat Metab Disord. 2004;28:327–9.
pubmed: 14724666
Dongowski G, Lorenz A, Proll J. The degree of methylation influences the degradation of pectin in the intestinal tract of rats and in vitro. J Nutr. 2002;132:1935–44.
pubmed: 12097673
Fåk F, Jakobsdottir G, Kulcinskaja E, Marungruang N, Matziouridou C, Nilsson U, et al. The physico-chemical properties of dietary fibre determine metabolic responses, short-chain fatty acid profiles and gut microbiota composition in rats fed low- and high-fat diets. PloS ONE. 2015;10:e0127252.
pubmed: 25973610
pmcid: 4431822
Chaplin A, Parra P, Serra F, Palou A. Conjugated linoleic acid supplementation under a high-fat diet modulates stomach protein expression and intestinal microbiota in adult mice. PloS ONE. 2015;10:e0125091.
pubmed: 25915857
pmcid: 4411160
An HM, Park SY, Lee DKoK, Kim JR, Cha MK, Lee SW, et al. Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis. 2011;10:116.
pubmed: 21745411
pmcid: 3146849
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 USA. 2013;110:9066–71.
Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543–7.
pubmed: 21270894
Lecomte V, Kaakoush NO, Maloney CA, Raipuria M, Huinao KD, Mitchell HM, et al. Changes in gut microbiota in rats fed a high fat diet correlate with obesity-associated metabolic parameters. PloS ONE. 2015;10:e0126931.
pubmed: 25992554
pmcid: 4436290
Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, et al. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PloS ONE. 2011;6:e20944.
pubmed: 21695273
pmcid: 3111466
Koleva PT, Bridgman SL, Kozyrskyj AL. The infant gut microbiome: evidence for obesity risk and dietary intervention. Nutrients. 2015;7:2237–60.
pubmed: 25835047
pmcid: 4425142
Parnell JA, Reimer RA. Prebiotic fiber modulation of the gut microbiota improves risk factors for obesity and the metabolic syndrome. Gut Microbes. 2012;3:29–34.
pubmed: 22555633
pmcid: 3827018
Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. Host-gut microbiota metabolic interactions. Science. 2012;336:1262–7.
pubmed: 22674330
Jakobsdottir G, Nyman M, Fåk F. Designing future prebiotic fiber to target the metabolic syndrome. Nutrition. 2014;30:497–502.
pubmed: 24262515
Jakobsdottir G, Jädert C, Holm L, Nyman ME. Propionic and butyric acids, formed in the caecum of rats fed highly fermentable dietary fibre, are reflected in portal and aortic serum. Br J Nutr. 2013;110:1565–72.
pubmed: 23531375
Palou M, Priego T, Romero M, Szostaczuk N, Konieczna J, Cabrer C, et al. Moderate calorie restriction during gestation programs offspring for lower BAT thermogenic capacity driven by thyroid and sympathetic signaling. Int J Obes. 2015;39:339–45.
García AP, Palou M, Sánchez J, Priego T, Palou A, Picó C. Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring. PloS ONE. 2011;6:e17313.
pubmed: 21364997
pmcid: 3041800
Giordano A, Frontini A, Murano I, Tonello C, Marino MA, Carruba MO, et al. Regional-dependent increase of sympathetic innervation in rat white adipose tissue during prolonged fasting. J Histochem Cytochem. 2005;53:679–87.
pubmed: 15928317
Townsend KL, Tseng Y-HH. Brown fat fuel utilization and thermogenesis. Trends Endocrinol Metab. 2014;25:168–77.
pubmed: 24389130
pmcid: 3972344
Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003;278:11312–9.
pubmed: 12496283
Kalinovich AV, de Jong JM, Cannon B, Nedergaard J. UCP1 in adipose tissues: two steps to full browning. Biochimie. 2017;134:127–37.
pubmed: 28109720
Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8.
pubmed: 22237023
pmcid: 3522098
Petrovic N, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPARgamma agonist. Am J Physiol Endocrinol Metab. 2008;295:96.
Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun. 2013;4:1829.
pubmed: 3674247
pmcid: 3674247
Ortega-Molina A, Efeyan A, Lopez-Guadamillas E, Muñoz-Martin M, Gómez-López G, Cañamero M, et al. Pten positively regulates brown adipose function, energy expenditure, and longevity. Cell Metab. 2012;15:382–94.
pubmed: 22405073
Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277–59.
pubmed: 14715917
Urs S, Harrington A, Liaw L, Small D. Selective expression of an aP2/fatty acid binding protein 4-Cre transgene in non-adipogenic tissues during embryonic development. Transgenic Res. 2006;15:647–53.
pubmed: 16952017
Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J Biol Chem. 2010;285:7153–64.
pubmed: 20028987
Aberdein N, Schweizer M, Ball D. Sodium acetate decreases phosphorylation of hormone sensitive lipase in isoproterenol-stimulated 3T3-L1 mature adipocytes. Adipocyte. 2014;3:121–5.
pubmed: 24719785
pmcid: 3979876
Adam CL, Williams PA, Dalby MJ, Garden K, Thomson LM, Richardson AJ, et al. Different types of soluble fermentable dietary fibre decrease food intake, body weight gain and adiposity in young adult male rats. Nutr Metab. 2014;11:36.
Slavin J. Fiber and prebiotics: mechanisms and health benefits. Nutrients. 2013;5:1417–35.
pubmed: 23609775
pmcid: 3705355
Bonet ML, Oliver P, Palou A. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim et Biophys acta. 2013;1831:969–85.
Chevalier C, Stojanovic 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: 26638070
Li G, Xie C, Lu S, Nichols RG, Tian Y, Li L, et al. Intermittent fasting promotes white adipose browning and decreases obesity by shaping the gut microbiota. Cell Metab. 2017;26:672–85.e4.
pubmed: 28918936
pmcid: 5668683
Reynes B, Palou M, Rodriguez AM, Palou A. Regulation of adaptive thermogenesis and browning by prebiotics and postbiotics. Front Physiol. 2018;9:1908.
pubmed: 30687123
Zietak M, Kozak LP. Bile acids induce uncoupling protein 1-dependent thermogenesis and stimulate energy expenditure at thermoneutrality in mice. Am J Physiol Endocrinol Metab. 2016;310:E346–54.
pubmed: 26714852
Albrecht E, Norheim F, Thiede B, Holen T, Ohashi T, Schering L, et al. Irisin - a myth rather than an exercise-inducible myokine. Sci Rep. 2015;5:8889.
pubmed: 25749243
pmcid: 4352853
Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang A-HH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150:366–76.
pubmed: 22796012
pmcid: 3402601
Rosenwald M, Perdikari A, Rülicke T, Wolfrum C. Bi-directional interconversion of brite and white adipocytes. Nat Cell Biol. 2013;15:659–67.
pubmed: 23624403
Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen J-LL, et al. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology. 2008;149:4519–26.
pubmed: 18499755
Hong Y-HH, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, et al. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology. 2005;146:5092–9.
pubmed: 16123168
Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome. Nature. 2016;534:213–7.
pubmed: 27279214
pmcid: 4922538
Trent CM, Blaser MJ. Microbially produced acetate: a "missing link" in understanding obesity? Cell Metab. 2016;24:9–10.
pubmed: 27411005
Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58:1509–17.
pubmed: 19366864
pmcid: 2699871
Kondo T, Kishi M, Fushimi T, Kaga T. Acetic acid upregulates the expression of genes for fatty acid oxidation enzymes in liver to suppress body fat accumulation. J Agric Food Chem. 2009;57:5982–6.
pubmed: 19469536
pmcid: 19469536
Aoki R, Kamikado K, Suda W, Takii H, Mikami Y, Suganuma N, et al. A proliferative probiotic Bifidobacterium strain in the gut ameliorates progression of metabolic disorders via microbiota modulation and acetate elevation. Sci Rep. 2017;7:43522.
pubmed: 28252037
pmcid: 28252037
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.
pubmed: 27895388
pmcid: 5110936
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.