Improving Metabolic Control Through Functional Foods

Author(s): João C.P. Silva, John G. Jones*

Journal Name: Current Medicinal Chemistry

Volume 26 , Issue 19 , 2019


  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Abstract:

Background: Functional foods are designed to have physiological benefits and reduce the risk of chronic disease beyond basic nutritional functions. Conditions related to overnutrition such as Metabolic Syndrome and Type 2 diabetes are increasingly serious concerns in Western societies. Several nutrient classes are considered to protect against these conditions and this review focuses on the latest clinical and preclinical evidence supporting their efficacy and the molecular mechanisms by which they act.

Methods: The review searched the literature for information and data on the following functional food components and their protective effects against Metabolic Syndrome and Type 2 Diabetes: Dietary fiber; Medium-chain triglycerides and Ketone esters; ω3 Polyunsaturated fatty acids and Antioxidants.

Results: Data from a hundred and four studies were reviewed and summarized. They indicate that dietary fiber results in the production of beneficial short chain fatty acids via intestinal microbiota, as well as increasing intestinal secretion of incretins and satiety peptides. Medium chain triglycerides and ketone esters promote thermogenesis, inhibit lipolysis and reduce inflammation. They also decrease endogenous synthesis of triglycerides and fatty acids. ω3-PUFA’s act to soften inflammation through an increase in adiponectin secretion. Antioxidants are involved in the protection of insulin sensitivity by PTP1B suppression and SIRT1 activation.

Conclusion: Functional foods have actions that complement and/or potentiate other lifestyle interventions for reversing Metabolic Syndrome and Type 2 Diabetes. Functional foods contribute to reduced food intake by promoting satiety, less weight gain via metabolic uncoupling and improved insulin sensitivity via several distinct mechanisms.

Keywords: Insulin sensitivity, type 2 diabetes, non-alcoholic fatty liver disease, inflammation, short-chain fatty acids, mitochondrial uncoupling.

[1]
Whitmer, R.A. Type 2 diabetes and risk of cognitive impairment and dementia. Curr. Neurol. Neurosci. Rep., 2007, 7(5), 373-380.
[http://dx.doi.org/10.1007/s11910-007-0058-7] [PMID: 17764626]
[2]
Li, L.; Hölscher, C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res. Brain Res. Rev., 2007, 56(2), 384-402.
[http://dx.doi.org/10.1016/j.brainresrev.2007.09.001] [PMID: 17920690]
[3]
Xu, W.L.; von Strauss, E.; Qiu, C.X.; Winblad, B.; Fratiglioni, L. Uncontrolled diabetes increases the risk of Alzheimer’s disease: a population-based cohort study. Diabetologia, 2009, 52(6), 1031-1039.
[http://dx.doi.org/10.1007/s00125-009-1323-x] [PMID: 19280172]
[4]
Cohen, E.; Dillin, A. The insulin paradox: aging, proteotoxicity and neurodegeneration. Nat. Rev. Neurosci., 2008, 9(10), 759-767.
[http://dx.doi.org/10.1038/nrn2474] [PMID: 18769445]
[5]
van Dijk, G.; van Heijningen, S.; Reijne, A.C.; Nyakas, C.; van der Zee, E.A.; Eisel, U.L.M. Integrative neurobiology of metabolic diseases, neuroinflammation, and neurodegeneration. Front. Neurosci., 2015, 9, 173.
[http://dx.doi.org/10.3389/fnins.2015.00173] [PMID: 26041981]
[6]
Slavin, J.L. Position of the American Dietetic Association: health implications of dietary fiber. J. Am. Diet. Assoc., 2008, 108(10), 1716-1731.
[http://dx.doi.org/10.1016/j.jada.2008.08.007] [PMID: 18953766]
[7]
Wanders, A.J.; Jonathan, M.C.; van den Borne, J.J.G.C.; Mars, M.; Schols, H.A.; Feskens, E.J.M.; de Graaf, C. The effects of bulking, viscous and gel-forming dietary fibres on satiation. Br. J. Nutr., 2013, 109(7), 1330-1337.
[http://dx.doi.org/10.1017/S0007114512003145] [PMID: 22850326]
[8]
Zhang, Y.; Zhang, H.; Wang, L.; Qian, H.; Qi, X.; Ding, X.; Hu, B.; Li, J. The effect of oat β-glucan on in vitro glucose diffusion and glucose transport in rat small intestine. J. Sci. Food Agric., 2016, 96(2), 484-491.
[http://dx.doi.org/10.1002/jsfa.7114] [PMID: 25639602]
[9]
Rebello, C.J.; O’Neil, C.E.; Greenway, F.L. Dietary fiber and satiety: the effects of oats on satiety. Nutr. Rev., 2016, 74(2), 131-147.
[http://dx.doi.org/10.1093/nutrit/nuv063] [PMID: 26724486]
[10]
Juvonen, K.R.; Purhonen, A-K.; Salmenkallio-Marttila, M.; Lähteenmäki, L.; Laaksonen, D.E.; Herzig, K-H.; Uusitupa, M.I.; Poutanen, K.S.; Karhunen, L.J. Viscosity of oat bran-enriched beverages influences gastrointestinal hormonal responses in healthy humans. J. Nutr., 2009, 139(3), 461-466.
[http://dx.doi.org/10.3945/jn.108.099945] [PMID: 19176745]
[11]
Adam, C.L.; Williams, P.A.; Garden, K.E.; Thomson, L.M.; Ross, A.W. 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(1)e0115438
[http://dx.doi.org/10.1371/journal.pone.0115438] [PMID: 25602757]
[12]
Adam, C.L.; Thomson, L.M.; Williams, P.A.; Ross, A.W. Soluble fermentable dietary fibre (pectin) decreases caloric intake, adiposity and lipidaemia in high-fat diet-induced obese rats. PLoS One, 2015, 10(10)e0140392
[http://dx.doi.org/10.1371/journal.pone.0140392] [PMID: 26447990]
[13]
Hadri, Z.; Chaumontet, C.; Fromentin, G.; Even, P.C.; Darcel, N.; Bouras, A.D.; Tomé, D.; Rasoamanana, R. Long term ingestion of a preload containing fructo-oligosaccharide or guar gum decreases fat mass but not food intake in mice. Physiol. Behav., 2015, 147, 198-204.
[http://dx.doi.org/10.1016/j.physbeh.2015.04.039] [PMID: 25914171]
[14]
Wanders, A.J.; Feskens, E.J.M.; Jonathan, M.C.; Schols, H.A.; de Graaf, C.; Mars, M. Pectin is not pectin: a randomized trial on the effect of different physicochemical properties of dietary fiber on appetite and energy intake. Physiol. Behav., 2014, 128, 212-219.
[http://dx.doi.org/10.1016/j.physbeh.2014.02.007] [PMID: 24534170]
[15]
Sandberg, J.C.; Björck, I.M.E.; Nilsson, A.C. Rye-based evening meals favorably affected glucose regulation and appetite variables at the following breakfast; a randomized controlled study in healthy subjects. PLoS One, 2016, 11(3)e0151985
[http://dx.doi.org/10.1371/journal.pone.0151985] [PMID: 26990559]
[16]
Korczak, R.; Lindeman, K.; Thomas, W.; Slavin, J.L. Bran fibers and satiety in women who do not exhibit restrained eating. Appetite, 2014, 80, 257-263.
[http://dx.doi.org/10.1016/j.appet.2014.05.025] [PMID: 24874565]
[17]
Lafond, D.W.; Greaves, K.A.; Maki, K.C.; Leidy, H.J.; Romsos, D.R. Effects of two dietary fibers as part of ready-to-eat cereal (RTEC) breakfasts on perceived appetite and gut hormones in overweight women. Nutrients, 2015, 7(2), 1245-1266.
[http://dx.doi.org/10.3390/nu7021245] [PMID: 25689743]
[18]
Klosterbuer, A.S.; Thomas, W.; Slavin, J.L. Resistant starch and pullulan reduce postprandial glucose, insulin, and GLP-1, but have no effect on satiety in healthy humans. J. Agric. Food Chem., 2012, 60(48), 11928-11934.
[http://dx.doi.org/10.1021/jf303083r] [PMID: 23136915]
[19]
Howarth, N.C.; Saltzman, E.; McCrory, M.A.; Greenberg, A.S.; Dwyer, J.; Ausman, L.; Kramer, D.G.; Roberts, S.B. Fermentable and nonfermentable fiber supplements did not alter hunger, satiety or body weight in a pilot study of men and women consuming self-selected diets. J. Nutr., 2003, 133(10), 3141-3144.
[http://dx.doi.org/10.1093/jn/133.10.3141] [PMID: 14519798]
[20]
Clark, M.J.; Slavin, J.L. The effect of fiber on satiety and food intake: a systematic review. J. Am. Coll. Nutr., 2013, 32(3), 200-211.
[http://dx.doi.org/10.1080/07315724.2013.791194] [PMID: 23885994]
[21]
Slavin, J. Fiber and prebiotics: mechanisms and health benefits. Nutrients, 2013, 5(4), 1417-1435.
[http://dx.doi.org/10.3390/nu5041417] [PMID: 23609775]
[22]
Shen, R.L.; Dang, X.Y.; Dong, J.L.; Hu, X.Z. Effects of oat β-glucan and barley β-glucan on fecal characteristics, intestinal microflora, and intestinal bacterial metabolites in rats. J. Agric. Food Chem., 2012, 60(45), 11301-11308.
[http://dx.doi.org/10.1021/jf302824h] [PMID: 23113683]
[23]
Gibson, G.R.; Roberfroid, M.B. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr., 1995, 125(6), 1401-1412.
[http://dx.doi.org/10.1093/jn/125.6.1401] [PMID: 7782892]
[24]
May, T.; Mackie, R.I.; Fahey, G.C. Jr., Cremin, J.C.; Garleb, K.A. Effect of fiber source on short-chain fatty acid production and on the growth and toxin production by Clostridium difficile. Scand. J. Gastroenterol., 1994, 29(10), 916-922.
[http://dx.doi.org/10.3109/00365529409094863] [PMID: 7839098]
[25]
Seljeset, S.; Siehler, S. Receptor-specific regulation of ERK1/2 activation by members of the “free fatty acid receptor” family. J. Recept. Signal Transduct. Res., 2012, 32(4), 196-201.
[http://dx.doi.org/10.3109/10799893.2012.692118] [PMID: 22712802]
[26]
Blaut, M. Gut microbiota and energy balance: role in obesity. Proc. Nutr. Soc., 2015, 74(3), 227-234.
[http://dx.doi.org/10.1017/S0029665114001700] [PMID: 25518735]
[27]
Han, J-H.; Kim, I-S.; Jung, S-H.; Lee, S-G.; Son, H-Y.; Myung, C-S. The effects of propionate and valerate on insulin responsiveness for glucose uptake in 3T3-L1 adipocytes and C2C12 myotubes via G protein-coupled receptor 41. PLoS One, 2014, 9(4)e95268
[http://dx.doi.org/10.1371/journal.pone.0095268] [PMID: 24748202]
[28]
De Vadder, F.; Kovatcheva-Datchary, P.; Goncalves, D.; Vinera, J.; Zitoun, C.; Duchampt, A.; Bäckhed, F.; Mithieux, G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell, 2014, 156(1-2), 84-96.
[http://dx.doi.org/10.1016/j.cell.2013.12.016] [PMID: 24412651]
[29]
Wong, J.M.W.; de Souza, R.; Kendall, C.W.C.; Emam, A.; Jenkins, D.J.A. Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol., 2006, 40(3), 235-243.
[http://dx.doi.org/10.1097/00004836-200603000-00015] [PMID: 16633129]
[30]
Topping, D. Cereal complex carbohydrates and their contribution to human health. J. Cereal Sci., 2007, 46(3), 220-229.
[http://dx.doi.org/10.1016/j.jcs.2007.06.004]
[31]
Donohoe, D.R.; Garge, N.; Zhang, X.; Sun, W.; O’Connell, T.M.; Bunger, M.K.; Bultman, S.J. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab., 2011, 13(5), 517-526.
[http://dx.doi.org/10.1016/j.cmet.2011.02.018] [PMID: 21531334]
[32]
Gao, Z.; Yin, J.; Zhang, J.; Ward, R.E.; Martin, R.J.; Lefevre, M.; Cefalu, W.T.; Ye, J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes, 2009, 58(7), 1509-1517.
[http://dx.doi.org/10.2337/db08-1637] [PMID: 19366864]
[33]
Li, H.; Gao, Z.; Zhang, J.; Ye, X.; Xu, A.; Ye, J.; Jia, W. Sodium butyrate stimulates expression of fibroblast growth factor 21 in liver by inhibition of histone deacetylase 3. Diabetes, 2012, 61(4), 797-806.
[http://dx.doi.org/10.2337/db11-0846] [PMID: 22338096]
[34]
Vinolo, M.A.; Rodrigues, H.G.; Festuccia, W.T.; Crisma, A.R.; Alves, V.S.; Martins, A.R.; Amaral, C.L.; Fiamoncini, J.; Hirabara, S.M.; Sato, F.T.; Fock, R.A.; Malheiros, G.; dos Santos, M.F.; Curi, R. Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. Am. J. Physiol. Endocrinol. Metab., 2012, 303(2), E272-E282.
[http://dx.doi.org/10.1152/ajpendo.00053.2012] [PMID: 22621868]
[35]
Leng, R.A. Glucose synthesis in ruminants. Adv. Vet. Sci. Comp. Med., 1970, 14, 209-260.
[PMID: 4922144]
[36]
Bloemen, J.G.; Venema, K.; van de Poll, M.C.; Olde Damink, S.W.; Buurman, W.A.; Dejong, C.H. Short chain fatty acids exchange across the gut and liver in humans measured at surgery. Clin. Nutr., 2009, 28(6), 657-661.
[http://dx.doi.org/10.1016/j.clnu.2009.05.011] [PMID: 19523724]
[37]
Demigné, C.; Morand, C.; Levrat, M.A.; Besson, C.; Moundras, C.; Rémésy, C. Effect of propionate on fatty acid and cholesterol synthesis and on acetate metabolism in isolated rat hepatocytes. Br. J. Nutr., 1995, 74(2), 209-219.
[http://dx.doi.org/10.1079/BJN19950124] [PMID: 7547838]
[38]
Patel, T.B.; DeBuysere, M.S.; Olson, M.S. The effect of propionate on the regulation of the pyruvate dehydrogenase complex in the rat liver. Arch. Biochem. Biophys., 1983, 220(2), 405-414.
[http://dx.doi.org/10.1016/0003-9861(83)90430-7] [PMID: 6824332]
[39]
Lin, Y.; Vonk, R.J.; Slooff, M.J.H.; Kuipers, F.; Smit, M.J. Differences in propionate-induced inhibition of cholesterol and triacylglycerol synthesis between human and rat hepatocytes in primary culture. Br. J. Nutr., 1995, 74(2), 197-207.
[http://dx.doi.org/10.1079/BJN19950123] [PMID: 7547837]
[40]
Wolever, T.M.S.; Spadafora, P.J.; Cunnane, S.C.; Pencharz, P.B. Propionate inhibits incorporation of colonic [1,2-13C]acetate into plasma lipids in humans. Am. J. Clin. Nutr., 1995, 61(6), 1241-1247.
[http://dx.doi.org/10.1093/ajcn/61.6.1241] [PMID: 7762524]
[41]
Frost, G.; Sleeth, M.L.; Sahuri-Arisoylu, M.; Lizarbe, B.; Cerdan, S.; Brody, L.; Anastasovska, J.; Ghourab, S.; Hankir, M.; Zhang, S.; Carling, D.; Swann, J.R.; Gibson, G.; Viardot, A.; Morrison, D.; Louise Thomas, E.; Bell, J.D. The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat. Commun., 2014, 5, 3611.
[http://dx.doi.org/10.1038/ncomms4611] [PMID: 24781306]
[42]
Montgomery, M.K.; Osborne, B.; Brown, S.H.J.; Small, L.; Mitchell, T.W.; Cooney, G.J.; Turner, N. Contrasting metabolic effects of medium- versus long-chain fatty acids in skeletal muscle. J. Lipid Res., 2013, 54(12), 3322-3333.
[http://dx.doi.org/10.1194/jlr.M040451] [PMID: 24078708]
[43]
Turner, N.; Hariharan, K. TidAng, J.; Frangioudakis, G.; Beale, S.M.; Wright, L.E.; Zeng, X.Y.; Leslie, S.J.; Li, J.Y.; Kraegen, E.W.; Cooney, G.J.; Ye, J.M. Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: potent tissue-specific effects of medium-chain fatty acids. Diabetes, 2009, 58(11), 2547-2554.
[http://dx.doi.org/10.2337/db09-0784] [PMID: 19720794]
[44]
Takeuchi, H.; Noguchi, O.; Sekine, S.; Kobayashi, A.; Aoyama, T. Lower weight gain and higher expression and blood levels of adiponectin in rats fed medium-chain TAG compared with long-chain TAG. Lipids, 2006, 41(2), 207-212.
[http://dx.doi.org/10.1007/s11745-006-5089-3] [PMID: 17707987]
[45]
Han, J.; Hamilton, J.A.; Kirkland, J.L.; Corkey, B.E.; Guo, W. Medium-chain oil reduces fat mass and down-regulates expression of adipogenic genes in rats. Obes. Res., 2003, 11(6), 734-744.
[http://dx.doi.org/10.1038/oby.2003.103] [PMID: 12805394]
[46]
Nagao, K.; Yanagita, T. Medium-chain fatty acids: functional lipids for the prevention and treatment of the metabolic syndrome. Pharmacol. Res., 2010, 61(3), 208-212.
[http://dx.doi.org/10.1016/j.phrs.2009.11.007] [PMID: 19931617]
[47]
Hoeks, J.; Mensink, M.; Hesselink, M.K.C.; Ekroos, K.; Schrauwen, P. Long- and medium-chain fatty acids induce insulin resistance to a similar extent in humans despite marked differences in muscle fat accumulation. J. Clin. Endocrinol. Metab., 2012, 97(1), 208-216.
[http://dx.doi.org/10.1210/jc.2011-1884] [PMID: 22031508]
[48]
Veech, R.L. The therapeutic implications of ketone bodies: the effects of ketone bodies in pathological conditions: ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot. Essent. Fatty Acids, 2004, 70(3), 309-319.
[http://dx.doi.org/10.1016/j.plefa.2003.09.007] [PMID: 14769489]
[49]
Jornayvaz, F.R.; Jurczak, M.J.; Lee, H-Y.; Birkenfeld, A.L.; Frederick, D.W.; Zhang, D.; Zhang, X.M.; Samuel, V.T.; Shulman, G.I. A high-fat, ketogenic diet causes hepatic insulin resistance in mice, despite increasing energy expenditure and preventing weight gain. Am. J. Physiol. Endocrinol. Metab., 2010, 299(5), E808-E815.
[http://dx.doi.org/10.1152/ajpendo.00361.2010] [PMID: 20807839]
[50]
Kinzig, K.P.; Honors, M.A.; Hargrave, S.L. Insulin sensitivity and glucose tolerance are altered by maintenance on a ketogenic diet. Endocrinology, 2010, 151(7), 3105-3114.
[http://dx.doi.org/10.1210/en.2010-0175] [PMID: 20427477]
[51]
Badman, M.K.; Kennedy, A.R.; Adams, A.C.; Pissios, P.; Maratos-Flier, E. A very low carbohydrate ketogenic diet improves glucose tolerance in ob/ob mice independently of weight loss. Am. J. Physiol. Endocrinol. Metab., 2009, 297(5), E1197-E1204.
[http://dx.doi.org/10.1152/ajpendo.00357.2009] [PMID: 19738035]
[52]
Park, S.; Kim, D.S.; Daily, J.W. Central infusion of ketone bodies modulates body weight and hepatic insulin sensitivity by modifying hypothalamic leptin and insulin signaling pathways in type 2 diabetic rats. Brain Res., 2011, 1401, 95-103.
[http://dx.doi.org/10.1016/j.brainres.2011.05.040] [PMID: 21652033]
[53]
Johnston, C.S.; Tjonn, S.L.; Swan, P.D.; White, A.; Hutchins, H.; Sears, B. Ketogenic low-carbohydrate diets have no metabolic advantage over nonketogenic low-carbohydrate diets. Am. J. Clin. Nutr., 2006, 83(5), 1055-1061.
[http://dx.doi.org/10.1093/ajcn/83.5.1055] [PMID: 16685046]
[54]
Clarke, K.; Tchabanenko, K.; Pawlosky, R.; Carter, E.; Knight, N.S.; Murray, A.J.; Cochlin, L.E.; King, M.T.; Wong, A.W.; Roberts, A.; Robertson, J.; Veech, R.L. Oral 28-day and developmental toxicity studies of (R)-3-hydroxybutyl (R)-3-hydroxybutyrate. Regul. Toxicol. Pharmacol., 2012, 63(2), 196-208.
[http://dx.doi.org/10.1016/j.yrtph.2012.04.001] [PMID: 22504461]
[55]
Clarke, K.; Tchabanenko, K.; Pawlosky, R.; Carter, E.; Todd King, M.; Musa-Veloso, K.; Ho, M.; Roberts, A.; Robertson, J.; Vanitallie, T.B.; Veech, R.L. Kinetics, safety and tolerability of (R)-3-hydroxybutyl (R)-3-hydroxybutyrate in healthy adult subjects. Regul. Toxicol. Pharmacol., 2012, 63(3), 401-408.
[http://dx.doi.org/10.1016/j.yrtph.2012.04.008] [PMID: 22561291]
[56]
Srivastava, S.; Kashiwaya, Y.; King, M.T.; Baxa, U.; Tam, J.; Niu, G.; Chen, X.; Clarke, K.; Veech, R.L. Mitochondrial biogenesis and increased uncoupling protein 1 in brown adipose tissue of mice fed a ketone ester diet. FASEB J., 2012, 26(6), 2351-2362.
[http://dx.doi.org/10.1096/fj.11-200410] [PMID: 22362892]
[57]
Sato, K.; Kashiwaya, Y.; Keon, C.A.; Tsuchiya, N.; King, M.T.; Radda, G.K.; Chance, B.; Clarke, K.; Veech, R.L. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J., 1995, 9(8), 651-658.
[http://dx.doi.org/10.1096/fasebj.9.8.7768357] [PMID: 7768357]
[58]
Carrière, A.; Jeanson, Y.; Berger-Müller, S.; André, M.; Chenouard, V.; Arnaud, E.; Barreau, C.; Walther, R.; Galinier, A.; Wdziekonski, B.; Villageois, P.; Louche, K.; Collas, P.; Moro, C.; Dani, C.; Villarroya, F.; Casteilla, L. Browning of white adipose cells by intermediate metabolites: an adaptive mechanism to alleviate redox pressure. Diabetes, 2014, 63(10), 3253-3265.
[http://dx.doi.org/10.2337/db13-1885] [PMID: 24789919]
[59]
Taggart, A.K.P.; Kero, J.; Gan, X.; Cai, T.Q.; Cheng, K.; Ippolito, M.; Ren, N.; Kaplan, R.; Wu, K.; Wu, T.J.; Jin, L.; Liaw, C.; Chen, R.; Richman, J.; Connolly, D.; Offermanns, S.; Wright, S.D.; Waters, M.G. (D)-beta-Hydroxybutyrate inhibits adipocyte lipolysis via the nicotinic acid receptor PUMA-G. J. Biol. Chem., 2005, 280(29), 26649-26652.
[http://dx.doi.org/10.1074/jbc.C500213200] [PMID: 15929991]
[60]
Graff, E.C.; Fang, H.; Wanders, D.; Judd, R.L. Anti-inflammatory effects of the hydroxycarboxylic acid receptor 2. Metabolism, 2016, 65(2), 102-113.
[http://dx.doi.org/10.1016/j.metabol.2015.10.001] [PMID: 26773933]
[61]
Won, Y-J.; Lu, V.B.; Puhl, H.L., III; Ikeda, S.R. β-Hydroxybutyrate modulates N-type calcium channels in rat sympathetic neurons by acting as an agonist for the G-protein-coupled receptor FFA3. J. Neurosci., 2013, 33(49), 19314-19325.
[http://dx.doi.org/10.1523/JNEUROSCI.3102-13.2013] [PMID: 24305827]
[62]
Youm, Y-H.; Nguyen, K.Y.; Grant, R.W.; Goldberg, E.L.; Bodogai, M.; Kim, D.; D’Agostino, D.; Planavsky, N.; Lupfer, C.; Kanneganti, T.D.; Kang, S.; Horvath, T.L.; Fahmy, T.M.; Crawford, P.A.; Biragyn, A.; Alnemri, E.; Dixit, V.D. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat. Med., 2015, 21(3), 263-269.
[http://dx.doi.org/10.1038/nm.3804] [PMID: 25686106]
[63]
Thies, F.; Garry, J.M.C.; Yaqoob, P.; Rerkasem, K.; Williams, J.; Shearman, C.P.; Gallagher, P.J.; Calder, P.C.; Grimble, R.F. Association of n-3 polyunsaturated fatty acids with stability of atherosclerotic plaques: a randomised controlled trial. Lancet, 2003, 361(9356), 477-485.
[http://dx.doi.org/10.1016/S0140-6736(03)12468-3] [PMID: 12583947]
[64]
Valagussa, F.; Franzosi, M.G.; Geraci, E.; Mininni, N.; Nicolosi, G.L.; Santini, M. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell’Infarto miocardico. Lancet, 1999, 354(9177), 447-455.
[http://dx.doi.org/10.1016/S0140-6736(99)07072-5] [PMID: 10465168]
[65]
Akinkuolie, A.O.; Ngwa, J.S.; Meigs, J.B.; Djoussé, L. Omega-3 polyunsaturated fatty acid and insulin sensitivity: a meta-analysis of randomized controlled trials. Clin. Nutr., 2011, 30(6), 702-707.
[http://dx.doi.org/10.1016/j.clnu.2011.08.013] [PMID: 21959352]
[66]
MacIntosh, C.G.; Holt, S.H.A.; Brand-Miller, J.C. The degree of fat saturation does not alter glycemic, insulinemic or satiety responses to a starchy staple in healthy men. J. Nutr., 2003, 133(8), 2577-2580.
[http://dx.doi.org/10.1093/jn/133.8.2577] [PMID: 12888640]
[67]
Xiao, C.; Giacca, A.; Carpentier, A.; Lewis, G.F. Differential effects of monounsaturated, polyunsaturated and saturated fat ingestion on glucose-stimulated insulin secretion, sensitivity and clearance in overweight and obese, non-diabetic humans. Diabetologia, 2006, 49(6), 1371-1379.
[http://dx.doi.org/10.1007/s00125-006-0211-x] [PMID: 16596361]
[68]
Jans, A.; Konings, E.; Goossens, G.H.; Bouwman, F.G.; Moors, C.C.; Boekschoten, M.V.; Afman, L.A.; Müller, M.; Mariman, E.C.; Blaak, E.E. PUFAs acutely affect triacylglycerol-derived skeletal muscle fatty acid uptake and increase postprandial insulin sensitivity. Am. J. Clin. Nutr., 2012, 95(4), 825-836.
[http://dx.doi.org/10.3945/ajcn.111.028787] [PMID: 22338035]
[69]
Razny, U.; Kiec-Wilk, B.; Polus, A.; Goralska, J.; Malczewska-Malec, M.; Wnek, D.; Zdzienicka, A.; Gruca, A.; Childs, C.E.; Kapusta, M.; Slowinska-Solnica, K.; Calder, P.C.; Dembinska-Kiec, A. Effect of caloric restriction with or without n-3 polyunsaturated fatty acids on insulin sensitivity in obese subjects: A randomized placebo controlled trial. BBA Clin., 2015, 4, 7-13.
[http://dx.doi.org/10.1016/j.bbacli.2015.05.001] [PMID: 26925376]
[70]
Ramel, A.; Martinéz, A.; Kiely, M.; Morais, G.; Bandarra, N.M.; Thorsdottir, I. Beneficial effects of long-chain n-3 fatty acids included in an energy-restricted diet on insulin resistance in overweight and obese European young adults. Diabetologia, 2008, 51(7), 1261-1268.
[http://dx.doi.org/10.1007/s00125-008-1035-7] [PMID: 18491071]
[71]
Boss, A.; Lecoultre, V.; Ruffieux, C.; Tappy, L.; Schneiter, P. Combined effects of endurance training and dietary unsaturated fatty acids on physical performance, fat oxidation and insulin sensitivity. Br. J. Nutr., 2010, 103(8), 1151-1159.
[http://dx.doi.org/10.1017/S000711450999287X] [PMID: 19948079]
[72]
Somova, L.; Moodley, K.; Channa, M.L.; Nadar, A. Dose-dependent effect of dietary fish-oil (n-3) polyunsaturated fatty acids on in vivo insulin sensitivity in rat. Methods Find. Exp. Clin. Pharmacol., 1999, 21(4), 275-278.
[http://dx.doi.org/10.1358/mf.1999.21.4.538178] [PMID: 10399135]
[73]
Winzell, M.S.; Pacini, G.; Ahrén, B. Insulin secretion after dietary supplementation with conjugated linoleic acids and n-3 polyunsaturated fatty acids in normal and insulin-resistant mice. Am. J. Physiol. Endocrinol. Metab., 2006, 290(2), E347-E354.
[http://dx.doi.org/10.1152/ajpendo.00163.2005] [PMID: 16188912]
[74]
Flachs, P.; Mohamed-Ali, V.; Horakova, O.; Rossmeisl, M.; Hosseinzadeh-Attar, M.J.; Hensler, M.; Ruzickova, J.; Kopecky, J. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed a high-fat diet. Diabetologia, 2006, 49(2), 394-397.
[http://dx.doi.org/10.1007/s00125-005-0053-y] [PMID: 16397791]
[75]
Todoric, J.; Löffler, M.; Huber, J.; Bilban, M.; Reimers, M.; Kadl, A.; Zeyda, M.; Waldhäusl, W.; Stulnig, T.M. Adipose tissue inflammation induced by high-fat diet in obese diabetic mice is prevented by n-3 polyunsaturated fatty acids. Diabetologia, 2006, 49(9), 2109-2119.
[http://dx.doi.org/10.1007/s00125-006-0300-x] [PMID: 16783472]
[76]
Tishinsky, J.M.; Ma, D.W.L.; Robinson, L.E. Eicosapentaenoic acid and rosiglitazone increase adiponectin in an additive and PPARγ-dependent manner in human adipocytes. Obesity (Silver Spring), 2011, 19(2), 262-268.
[http://dx.doi.org/10.1038/oby.2010.186] [PMID: 20814411]
[77]
Oh, D.Y.; Talukdar, S.; Bae, E.J.; Imamura, T.; Morinaga, H.; Fan, W.; Li, P.; Lu, W.J.; Watkins, S.M.; Olefsky, J.M. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell, 2010, 142(5), 687-698.
[http://dx.doi.org/10.1016/j.cell.2010.07.041] [PMID: 20813258]
[78]
Cavaliere, G.; Trinchese, G.; Bergamo, P.; De Filippo, C.; Mattace Raso, G.; Gifuni, G.; Putti, R.; Moni, B.H.; Canani, R.B.; Meli, R.; Mollica, M.P. Polyunsaturated fatty acids attenuate diet induced obesity and insulin resistance, modulating mitochondrial respiratory uncoupling in rat skeletal muscle. PLoS One, 2016, 11(2)e0149033
[http://dx.doi.org/10.1371/journal.pone.0149033] [PMID: 26901315]
[79]
Sohet, F.M.; Neyrinck, A.M.; Dewulf, E.M.; Bindels, L.B.; Portois, L.; Malaisse, W.J.; Carpentier, Y.A.; Cani, P.D.; Delzenne, N.M. Lipid peroxidation is not a prerequisite for the development of obesity and diabetes in high-fat-fed mice. Br. J. Nutr., 2009, 102(3), 462-469.
[http://dx.doi.org/10.1017/S0007114508191243] [PMID: 19161640]
[80]
Moreno, J.A.; Hong, E. A single oral dose of fructose induces some features of metabolic syndrome in rats: role of oxidative stress. Nutr. Metab. Cardiovasc. Dis., 2013, 23(6), 536-542.
[http://dx.doi.org/10.1016/j.numecd.2011.10.008] [PMID: 22386006]
[81]
Francini, F.; Castro, M.C.; Schinella, G.; García, M.E.; Maiztegui, B.; Raschia, M.A.; Gagliardino, J.J.; Massa, M.L. Changes induced by a fructose-rich diet on hepatic metabolism and the antioxidant system. Life Sci., 2010, 86(25-26), 965-971.
[http://dx.doi.org/10.1016/j.lfs.2010.05.005] [PMID: 20470786]
[82]
Kopprasch, S.; Srirangan, D.; Bergmann, S.; Graessler, J.; Schwarz, P.E.H.; Bornstein, S.R. Association between systemic oxidative stress and insulin resistance/sensitivity indices - the PREDIAS study. Clin. Endocrinol. (Oxf.), 2016, 84(1), 48-54.
[http://dx.doi.org/10.1111/cen.12811] [PMID: 25940301]
[83]
Yun, J.; Finkel, T. Mitohormesis. Cell Metab., 2014, 19(5), 757-766.
[http://dx.doi.org/10.1016/j.cmet.2014.01.011] [PMID: 24561260]
[84]
Ristow, M. Unraveling the truth about antioxidants: mitohormesis explains ROS-induced health benefits. Nat. Med., 2014, 20(7), 709-711.
[http://dx.doi.org/10.1038/nm.3624] [PMID: 24999941]
[85]
Ristow, M.; Zarse, K.; Oberbach, A.; Klöting, N.; Birringer, M.; Kiehntopf, M.; Stumvoll, M.; Kahn, C.R.; Blüher, M. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. USA, 2009, 106(21), 8665-8670.
[http://dx.doi.org/10.1073/pnas.0903485106] [PMID: 19433800]
[86]
Hokayem, M.; Blond, E.; Vidal, H.; Lambert, K.; Meugnier, E.; Feillet-Coudray, C.; Coudray, C.; Pesenti, S.; Luyton, C.; Lambert-Porcheron, S.; Sauvinet, V.; Fedou, C.; Brun, J.F.; Rieusset, J.; Bisbal, C.; Sultan, A.; Mercier, J.; Goudable, J.; Dupuy, A.M.; Cristol, J.P.; Laville, M.; Avignon, A. Grape polyphenols prevent fructose-induced oxidative stress and insulin resistance in first-degree relatives of type 2 diabetic patients. Diabetes Care, 2013, 36(6), 1454-1461.
[http://dx.doi.org/10.2337/dc12-1652] [PMID: 23275372]
[87]
Montonen, J.; Knekt, P.; Järvinen, R.; Reunanen, A. Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care, 2004, 27(2), 362-366.
[http://dx.doi.org/10.2337/diacare.27.2.362] [PMID: 14747214]
[88]
Mason, S.A.; Della Gatta, P.A.; Snow, R.J.; Russell, A.P.; Wadley, G.D. Ascorbic acid supplementation improves skeletal muscle oxidative stress and insulin sensitivity in people with type 2 diabetes: Findings of a randomized controlled study. Free Radic. Biol. Med., 2016, 93, 227-238.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.01.006] [PMID: 26774673]
[89]
Arnlöv, J.; Zethelius, B.; Risérus, U.; Basu, S.; Berne, C.; Vessby, B.; Alfthan, G.; Helmersson, J. Serum and dietary beta-carotene and alpha-tocopherol and incidence of type 2 diabetes mellitus in a community-based study of Swedish men: report from the Uppsala Longitudinal Study of Adult Men (ULSAM) study. Diabetologia, 2009, 52(1), 97-105.
[http://dx.doi.org/10.1007/s00125-008-1189-3] [PMID: 18985315]
[90]
Poulsen, M.M.; Vestergaard, P.F.; Clasen, B.F.; Radko, Y.; Christensen, L.P.; Stødkilde-Jørgensen, H.; Møller, N.; Jessen, N.; Pedersen, S.B.; Jørgensen, J.O. High-dose resveratrol supplementation in obese men: an investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition. Diabetes, 2013, 62(4), 1186-1195.
[http://dx.doi.org/10.2337/db12-0975] [PMID: 23193181]
[91]
Yoshino, J.; Conte, C.; Fontana, L.; Mittendorfer, B.; Imai, S.; Schechtman, K.B.; Gu, C.; Kunz, I.; Rossi Fanelli, F.; Patterson, B.W.; Klein, S. Resveratrol supplementation does not improve metabolic function in nonobese women with normal glucose tolerance. Cell Metab., 2012, 16(5), 658-664.
[http://dx.doi.org/10.1016/j.cmet.2012.09.015] [PMID: 23102619]
[92]
Liu, K.; Zhou, R.; Wang, B.; Mi, M-T. Effect of resveratrol on glucose control and insulin sensitivity: a meta-analysis of 11 randomized controlled trials. Am. J. Clin. Nutr., 2014, 99(6), 1510-1519.
[http://dx.doi.org/10.3945/ajcn.113.082024] [PMID: 24695890]
[93]
Sena, C.M.; Nunes, E.; Gomes, A.; Santos, M.S.; Proença, T.; Martins, M.I.; Seiça, R.M. Supplementation of coenzyme Q10 and alpha-tocopherol lowers glycated hemoglobin level and lipid peroxidation in pancreas of diabetic rats. Nutr. Res., 2008, 28(2), 113-121.
[http://dx.doi.org/10.1016/j.nutres.2007.12.005] [PMID: 19083397]
[94]
Takikawa, M.; Inoue, S.; Horio, F.; Tsuda, T. Dietary anthocyanin-rich bilberry extract ameliorates hyperglycemia and insulin sensitivity via activation of AMP-activated protein kinase in diabetic mice. J. Nutr., 2010, 140(3), 527-533.
[http://dx.doi.org/10.3945/jn.109.118216] [PMID: 20089785]
[95]
Haohao, Z.; Guijun, Q.; Juan, Z.; Wen, K.; Lulu, C. Resveratrol improves high-fat diet induced insulin resistance by rebalancing subsarcolemmal mitochondrial oxidation and antioxidantion. J. Physiol. Biochem., 2015, 71(1), 121-131.
[http://dx.doi.org/10.1007/s13105-015-0392-1] [PMID: 25686565]
[96]
de Ligt, M.; Timmers, S.; Schrauwen, P. Resveratrol and obesity: Can resveratrol relieve metabolic disturbances? Biochim. Biophys. Acta, 2015, 1852(6), 1137-1144.
[http://dx.doi.org/10.1016/j.bbadis.2014.11.012] [PMID: 25446988]
[97]
Leibiger, I.B.; Berggren, P.O. Sirt1: a metabolic master switch that modulates lifespan. Nat. Med., 2006, 12(1), 34-36.
[http://dx.doi.org/10.1038/nm0106-34] [PMID: 16397557]
[98]
Rodgers, J.T.; Lerin, C.; Haas, W.; Gygi, S.P.; Spiegelman, B.M.; Puigserver, P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature, 2005, 434(7029), 113-118.
[http://dx.doi.org/10.1038/nature03354] [PMID: 15744310]
[99]
González-Rodríguez, Á.; Santamaría, B.; Mas-Gutierrez, J.A.; Rada, P.; Fernández-Millán, E.; Pardo, V.; Álvarez, C.; Cuadrado, A.; Ros, M.; Serrano, M.; Valverde, Á.M. Resveratrol treatment restores peripheral insulin sensitivity in diabetic mice in a sirt1-independent manner. Mol. Nutr. Food Res., 2015, 59(8), 1431-1442.
[http://dx.doi.org/10.1002/mnfr.201400933] [PMID: 25808216]
[100]
de Santi, C.; Pietrabissa, A.; Mosca, F.; Pacifici, G.M. Glucuronidation of resveratrol, a natural product present in grape and wine, in the human liver. Xenobiotica, 2000, 30(11), 1047-1054.
[http://dx.doi.org/10.1080/00498250010002487] [PMID: 11197066]
[101]
Walle, T. Bioavailability of resveratrol. Ann. N. Y. Acad. Sci., 2011, 1215, 9-15.
[http://dx.doi.org/10.1111/j.1749-6632.2010.05842.x] [PMID: 21261636]
[102]
Ortuno, J.; Covas, M-I.; Farre, M.; Pujadas, M.; Fito, M.; Khymenets, O. Matrix effects on the bioavailability of resveratrol in humans. Food Chem., 2010, 120(4), 1123-1130.
[http://dx.doi.org/10.1016/j.foodchem.2009.11.032]
[103]
Côté, C.D.; Rasmussen, B.A.; Duca, F.A.; Zadeh-Tahmasebi, M.; Baur, J.A.; Daljeet, M.; Breen, D.M.; Filippi, B.M.; Lam, T.K. Resveratrol activates duodenal Sirt1 to reverse insulin resistance in rats through a neuronal network. Nat. Med., 2015, 21(5), 498-505.
[http://dx.doi.org/10.1038/nm.3821] [PMID: 25849131]
[104]
Tomé-Carneiro, J.; Larrosa, M.; González-Sarrías, A.; Tomás-Barberán, F.A.; García-Conesa, M.T.; Espín, J.C. Resveratrol and clinical trials: the crossroad from in vitro studies to human evidence. Curr. Pharm. Des., 2013, 19(34), 6064-6093.
[http://dx.doi.org/10.2174/13816128113199990407] [PMID: 23448440]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 19
Year: 2019
Page: [3424 - 3438]
Pages: 15
DOI: 10.2174/0929867324666170523130123
Price: $65

Article Metrics

PDF: 59
HTML: 11