Kaempferol improves glucose uptake in skeletal muscle via an AMPK-dependent mechanism

CDC (2021). Diabetes basics[EB/OL]. 〈https://www.cdc.gov/diabetes/basics/index.html〉. King, 1998, Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections, Diabetes Care, 21, 1414, 10.2337/diacare.21.9.1414 Stoffers, 2004, The development of beta-cell mass: recent progress and potential role of GLP-1, Horm. Metab. Res., 36, 811, 10.1055/s-2004-826168 Cozar-Castellano, 2006, Molecular control of cell cycle progression in the pancreatic beta-cell, Endocr. Rev., 27, 356, 10.1210/er.2006-0004 Butler, 2003, Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes, Diabetes, 52, 102, 10.2337/diabetes.52.1.102 DeFronzo, 2009, skeletal muscle insulin resistance is the primary defect in type 2 diabetes, Diabetes Care, 32, S157, 10.2337/dc09-S302 Barlow, 2018, Do skeletal muscle-secreted factors influence the function of pancreatic beta-cells?, Am. J. Physiol. Endocrinol. Metab., 314, E297-, 10.1152/ajpendo.00353.2017 Bouzakri, 2005, Molecular mechanisms of skeletal muscle insulin resistance in type 2 diabetes, Curr. Diabetes. Rev., 1, 167, 10.2174/1573399054022785 DeFronzo, 1981, The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization, Diabetes, 30, 1000, 10.2337/diab.30.12.1000 Thiebaud, 1982, The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man, Diabetes, 31, 957, 10.2337/diacare.31.11.957 Zamora-Ros, 2013, Impact of thearubigins on the estimation of total dietary flavonoids in the European Prospective Investigation into Cancer and Nutrition (EPIC) study, Eur. J. Clin. Nutr., 67, 779, 10.1038/ejcn.2013.89 Calderón-Montaño, 2011, A review on the dietary flavonoid kaempferol, Mini Rev. Med. Chem., 11, 298, 10.2174/138955711795305335 Hakkinen, 1999, Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries, J. Agric. Food Chem., 47, 2274, 10.1021/jf9811065 Wang, 2018, Interaction of two flavonols with fat mass and obesity-associated protein investigated by fluorescence quenching and molecular docking, J. Biomol. Struct. Dyn., 36, 3388, 10.1080/07391102.2017.1388287 Fan, 2013, Berry and citrus phenolic compounds inhibit dipeptidyl peptidase IV: implications in diabetes management, Evid. Based. Complement Alternat. Med., 2013, 10.1155/2013/479505 Suh, 2009, Kaempferol attenuates 2-deoxy-d-ribose- induced oxidative cell damage in MC3T3-E1 osteoblastic cells, Biol. Pharm. Bull., 32, 746, 10.1248/bpb.32.746 Zhang, 2013, Small molecule kaempferol modulates PDX-1 protein expression and subsequently promotes pancreatic β-cell survival and function via CREB, The J. of Nutr. Biochem., 24, 638, 10.1016/j.jnutbio.2012.03.008 Crespo, 2008, A comparison of the effects of kaempferol and quercetin on cytokine-induced pro-inflammatory status of cultured human endothelial cells, Br. J. Nutr., 100, 968, 10.1017/S0007114508966083 Torres-Villarreal, 2019, Anti-obesity effects of kaempferol by inhibiting adipogenesis and increasing lipolysis in 3T3-L1 cells, J. Physiol. Biochem., 75, 83, 10.1007/s13105-018-0659-4 Olszanecki, 2008, Kaempferol, but not resveratrol inhibits angiotensin converting enzyme, J. Physiol. Pharmacol., 59, 387 Loizzo, 2007, Inhibition of angiotensin converting enzyme (ACE) by flavonoids isolated from Ailanthus excelsa (Roxb) (Simaroubaceae), Phytother. Res., 21, 32, 10.1002/ptr.2008 Zhang, 2008, Ginkgo biloba extract kaempferol inhibits cell proliferation and induces apoptosis in pancreatic cancer cells, J. Surg. Res., 148, 17, 10.1016/j.jss.2008.02.036 Mylonis, 2010, The dietary flavonoid kaempferol effectively inhibits HIF-1 activity and hepatoma cancer cell viability under hypoxic conditions., Biochem. Biophys. Res. Commun., 398, 74, 10.1016/j.bbrc.2010.06.038 da-Silva, 2007, The small polyphenolic molecule kaempferol increases cellular energy expenditure and thyroid hormone activation, Diabetes, 56, 767, 10.2337/db06-1488 Alkhalidy, 2018, Kaempferol ameliorates hyperglycemia through suppressing hepatic gluconeogenesis and enhancing hepatic insulin sensitivity in diet-induced obese mice, J. Nutr. Biochem., 58, 90, 10.1016/j.jnutbio.2018.04.014 Alkhalidy, 2015, Small molecule kaempferol promotes insulin sensitivity and preserved pancreatic beta -cell mass in middle-aged obese diabetic mice, J. Diabetes Res., 2015, 10.1155/2015/532984 Chen, 2010, Flavonoids and isoflavonoids from Sophorae Flos improve glucose uptake in vitro, Planta Med., 76, 79, 10.1055/s-0029-1185944 Boden, 1994, Mechanisms of fatty acid- induced inhibition of glucose uptake, J. Clin. Invest., 93, 2438, 10.1172/JCI117252 Roden, 1996, Mechanism of free fatty acid-induced insulin resistance in humans, J. Clin. Invest., 97, 2859, 10.1172/JCI118742 Roden, 1999, Rapid impairment of skeletal muscle glucose transport/phosphorylation by free fatty acids in humans, Diabetes, 48, 358, 10.2337/diabetes.48.2.358 Dresner, 1999, Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity, J. Clin. Invest, 103, 253, 10.1172/JCI5001 Shah, 2002, Effects of free fatty acids and glycerol on splanchnic glucose metabolism and insulin extraction in nondiabetic humans, Diabetes, 51, 301, 10.2337/diabetes.51.2.301 Sylow, 2014, Akt and Rac1 signaling are jointly required for insulin-stimulated glucose uptake in skeletal muscle and downregulated in insulin resistance., Cell Signal., 26, 323, 10.1016/j.cellsig.2013.11.007 Bernal-Sore, 2018, Mifepristone enhances insulin-stimulated Akt phosphorylation and glucose uptake in skeletal muscle cells, Mol. Cell Endocrinol., 461, 277, 10.1016/j.mce.2017.09.028 Ijuin, 2012, Regulation of insulin signaling and glucose transporter 4 (GLUT4) exocytosis by phosphatidylinositol 3,4,5-trisphosphate (PIP3) phosphatase, skeletal muscle, and kidney enriched inositol polyphosphate phosphatase (SKIP), J. Biol. Chem., 287, 6991, 10.1074/jbc.M111.335539 Tao, 2010, AMPK exerts dual regulatory effects on the PI3K pathway, J. Mol. Signal., 5, 1, 10.1186/1750-2187-5-1 Sears, 2015, The role of fatty acids in insulin resistance, Lipids Health Dis, 14, 121, 10.1186/s12944-015-0123-1 Boden, 2006, Fatty acid-induced inflammation and insulin resistance in skeletal muscle and liver, Curr. Diab. Rep., 6, 177, 10.1007/s11892-006-0031-x Steinberg, 2009, AMPK in health and disease, Physiol. Rev., 89, 1025, 10.1152/physrev.00011.2008 Zhang, 2009, AMPK: an emerging drug target for diabetes and the metabolic syndrome, Cell Metab., 9, 407, 10.1016/j.cmet.2009.03.012 Bergeron, 2001, Effect of 5-aminoimidazole-4- carboxamide-1-beta-D-ribofuranoside infusion on in vivo glucose and lipid metabolism in lean and obese Zucker rats, Diabetes, 50, 1076, 10.2337/diabetes.50.5.1076 Jorgensen, 2005, Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle, FASEB J, 19, 1146, 10.1096/fj.04-3144fje Holmes, 1999, Chronic activation of 5'-AMP- activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle, J. Appl. Physiol., 87, 1990, 10.1152/jappl.1999.87.5.1990 Ploug, 1998, Analysis of GLUT4 distribution in whole skeletal muscle fibers: identification of distinct storage compartments that are recruited by insulin and muscle contractions, J. Cell Biol., 142(, 1429, 10.1083/jcb.142.6.1429 Foran, 1999, Protein kinase B stimulates the translocation of GLUT4 but not GLUT1 or transferrin receptors in 3T3-L1 adipocytes by a pathway involving SNAP-23, synaptobrevin-2, and/or cellubrevin, J. Biol. Chem., 274, 28087, 10.1074/jbc.274.40.28087 Zhou, 1999, Analysis of insulin signaling by RNAi- based gene silencing, Biochem. Soc. Trans., 32, 817, 10.1042/BST0320817 Cartee, 2015, AMPK-TBC1D4-dependent mechanism for increasing insulin sensitivity of skeletal muscle, Diabetes, 64, 1901, 10.2337/db15-0010 Kjobsted, 2017, Enhanced muscle insulin sensitivity after contraction/exercise is mediated by AMPK, Diabetes, 66, 598, 10.2337/db16-0530 Ouchi, 2004, Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells, J. Biol. Chem., 279, 1304, 10.1074/jbc.M310389200 Longnus, 2005, Insulin signaling downstream of protein kinase B is potentiated by 5'AMP-activated protein kinase in rat hearts in vivo, Diabetologia, 48, 2591, 10.1007/s00125-005-0016-3 Han, 2018, The critical role of AMPK in driving Akt activation under stress, tumorigenesis and drug resistance, Nat. Commun., 9, 4728, 10.1038/s41467-018-07188-9 Yamaguchi, 2005, Activators of AMP-activated protein kinase enhance GLUT4 translocation and its glucose transport activity in 3T3-L1 adipocytes, Am. J. Physiol. Endocrinol. Metab., 289, E643, 10.1152/ajpendo.00456.2004 Kurth-Kraczek, 1999, 5’ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle, Diabetes, 48, 1667, 10.2337/diabetes.48.8.1667 Klop, 2013, Dyslipidemia in obesity: mechanisms and potential targets, Nutrients, 5, 1218, 10.3390/nu5041218 Lee, 2010, Effects of Korean white ginseng extracts on obesity in high-fat diet-induced obese mice, Cytotechnology, 62, 367, 10.1007/s10616-010-9288-7 Kim, 2000, High-fat diet-induced muscle insulin resistance: relationship to visceral fat mass, Am. J. Physiol. Regul. Integr. Comp. Physiol., 279, R2057, 10.1152/ajpregu.2000.279.6.R2057 Trajcevski, 2013, Enhanced lipid oxidation and maintenance of muscle insulin sensitivity despite glucose intolerance in a diet-induced obesity mouse model, PLoS One, 8, 10.1371/journal.pone.0071747 Albers, 2015, Human muscle fiber type-specific insulin signaling: impact of obesity and type 2 diabetes, Diabetes, 64, 485, 10.2337/db14-0590 Murphy, 2001, Enhanced technique to measure proteins in single segments of human skeletal muscle fibers: fiber-type dependence of AMPK-alpha1 and -beta1, J. Appl. Physiol., 110, 820, 10.1152/japplphysiol.01082.2010 Hawley, 2005, Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase, Cell Metab., 2, 9, 10.1016/j.cmet.2005.05.009 Woods, 2005, Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells, Cell Metab., 2, 21, 10.1016/j.cmet.2005.06.005 Liu, 2017, Curcumin activates AMPK pathway and regulates lipid metabolism in rats following prolonged clozapine exposure, Front. Neurosci., 11, 558, 10.3389/fnins.2017.00558 Jimenez-Sanchez, 2017, AMPK modulatory activity of olive-tree leaves phenolic compounds: Bioassay-guided isolation on adipocyte model and in silico approach, PLoS One, 12, 10.1371/journal.pone.0173074 Hawley, 2010, Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation, Cell Metab., 11, 554, 10.1016/j.cmet.2010.04.001 Rigacci, 2015, Oleuropein aglycone induces autophagy via the AMPK/mTOR signalling pathway: a mechanistic insight, Oncotarget, 6, 35344, 10.18632/oncotarget.6119 Barve, 2009, Metabolism, oral bioavailability and pharmacokinetics of chemopreventive kaempferol in rats, Biopharm. Drug Dispos, 30, 356, 10.1002/bdd.677 DuPont, 2004, Absorption of kaempferol from endive, a source of kaempferol-3-glucuronide, in humans, Eur. J. Clin. Nutr., 58, 947, 10.1038/sj.ejcn.1601916