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ORIGINAL RESEARCH

Resveratrol Regulates Glucose and Lipid Metabolism in Diabetic Rats by Inhibition of PDK1/AKT Phosphorylation and HIF-1α Expression

ORCID Icon, &
Pages 1063-1074 | Received 06 Jan 2023, Accepted 07 Apr 2023, Published online: 15 Apr 2023

References

  • James DE, Stockli J, Birnbaum MJ. The aetiology and molecular landscape of insulin resistance. Nat Rev Mol Cell Biol. 2021;22(11):751–771. doi:10.1038/s41580-021-00390-6
  • Cheng Z, Qiao D, Zhao S, Zhang B, Lin Q, Xie F. Whole grain rice: updated understanding of starch digestibility and the regulation of glucose and lipid metabolism. Compr Rev Food Sci Food Saf. 2022;21(4):3244–3273. doi:10.1111/1541-4337.12985
  • Li KX, Ji MJ, Sun HJ. An updated pharmacological insight of resveratrol in the treatment of diabetic nephropathy. Gene. 2021;780:145532. doi:10.1016/j.gene.2021.145532
  • Miao R, Fang X, Wei J, et al. Target for Metabolic Syndrome. Front Physiol. 2022;13:822333. doi:10.3389/fphys.2022.822333
  • Di Blasio L, Gagliardi PA, Puliafito A, Primo L. Serine/Threonine Kinase 3-Phosphoinositide-Dependent Protein Kinase-1 (PDK1) as a key regulator of cell migration and cancer dissemination. Cancers. 2017;9(3):25. doi:10.3390/cancers9030025
  • Gonzalez FJ, Xie C, Jiang C. The role of hypoxia-inducible factors in metabolic diseases. Nat Rev Endocrinol. 2018;15(1):21–32. doi:10.1038/s41574-018-0096-z
  • LaGory EL, Giaccia AJ. The ever-expanding role of HIF in tumour and stromal biology. Nat Cell Biol. 2016;18(4):356–365. doi:10.1038/ncb3330
  • Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol. 2001;21(12):3995–4004. doi:10.1128/MCB.21.12.3995-4004.2001
  • Lee YS, Kim JW, Osborne O, et al. Increased adipocyte O2 consumption triggers HIF-1alpha, causing inflammation and insulin resistance in obesity. Cell. 2014;157(6):1339–1352. doi:10.1016/j.cell.2014.05.012
  • Mesarwi OA, Moya EA, Zhen X, et al. Hepatocyte HIF-1 and intermittent hypoxia independently impact liver fibrosis in murine nonalcoholic fatty liver disease. Am J Respir Cell Mol Biol. 2021;65(4):390–402. doi:10.1165/rcmb.2020-0492OC
  • Dodd MS, Sousa Fialho MDL, Montes Aparicio CN, et al. Fatty acids prevent hypoxia-inducible factor-1alpha signaling through decreased succinate in diabetes. JACC Basic Transl Sci. 2018;3(4):485–498. doi:10.1016/j.jacbts.2018.04.005
  • Halberg N, Khan T, Trujillo ME, et al. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol. 2009;29(16):4467–4483. doi:10.1128/MCB.00192-09
  • Ochiai D, Goda N, Hishiki T, et al. Disruption of HIF-1alpha in hepatocytes impairs glucose metabolism in diet-induced obesity mice. Biochem Biophys Res Commun. 2011;415(3):445–449. doi:10.1016/j.bbrc.2011.10.089
  • Jardim FR, de Rossi FT, Nascimento MX, et al. Resveratrol and brain mitochondria: a review. Mol Neurobiol. 2018;55(3):2085–2101. doi:10.1007/s12035-017-0448-z
  • Bhatt JK, Thomas S, Nanjan MJ. Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus. Nutr Res. 2012;32(7):537–541. doi:10.1016/j.nutres.2012.06.003
  • Ding S, Jiang J, Wang Z, et al. Resveratrol reduces the inflammatory response in adipose tissue and improves adipose insulin signaling in high-fat diet-fed mice. PeerJ. 2018;6:e5173. doi:10.7717/peerj.5173
  • Wang XL, Wu LY, Zhao L, et al. SIRT1 activator ameliorates the renal tubular injury induced by hyperglycemia in vivo and in vitro via inhibiting apoptosis. Bio Pharm. 2016;83:41–50. doi:10.1016/j.biopha.2016.06.009
  • Wang X, Meng L, Zhao L, et al. Resveratrol ameliorates hyperglycemia-induced renal tubular oxidative stress damage via modulating the SIRT1/FOXO3a pathway. Diabetes Res Clin Pract. 2017;126:172–181. doi:10.1016/j.diabres.2016.12.005
  • Gheibi S, Kashfi K, Ghasemi A. A practical guide for induction of type-2 diabetes in rat: incorporating a high-fat diet and streptozotocin. Bio Pharm. 2017;95:605–613. doi:10.1016/j.biopha.2017.08.098
  • Den Hartogh DJ, Tsiani E. Health benefits of resveratrol in kidney disease: evidence from in vitro and in vivo studies. Nutrients. 2019;11(7):1624. doi:10.3390/nu11071624
  • Nair AB, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7(2):27–31. doi:10.4103/0976-0105.177703
  • Di Angelantonio E, Sarwar N, Perry PL, et al.; Emerging Risk Factors C. Major lipids, apolipoproteins, and risk of vascular disease. JAMA. 2009;302(18):1993–2000. doi:10.1001/jama.2009.1619
  • Zhao L, Chen Y, Tang R, et al. Inflammatory stress exacerbates hepatic cholesterol accumulation via increasing cholesterol uptake and de novo synthesis. J Gastroenterol Hepatol. 2011;26(5):875–883. doi:10.1111/j.1440-1746.2010.06560.x
  • Barcat D, Amadio A, Palos-Pinto A, et al. Combined hyperlipidemia/hyperalphalipoproteinemia associated with premature spontaneous atherosclerosis in mice lacking hepatic lipase and low density lipoprotein receptor. Atherosclerosis. 2006;188(2):347–355. doi:10.1016/j.atherosclerosis.2005.11.022
  • Giammanco A, Noto D, Barbagallo CM, et al. Hyperalphalipoproteinemia and Beyond: the role of HDL in cardiovascular diseases. Life. 2021;11(6):581. doi:10.3390/life11060581
  • Catrina SB, Zheng X. Hypoxia and hypoxia-inducible factors in diabetes and its complications. Diabetologia. 2021;64(4):709–716. doi:10.1007/s00125-021-05380-z
  • Girgis CM, Cheng K, Scott CH, Gunton JE. Novel links between HIFs, type 2 diabetes, and metabolic syndrome. Trends Endocrinol Metab. 2012;23(8):372–380. doi:10.1016/j.tem.2012.05.003
  • Botusan IR, Sunkari VG, Savu O, et al. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci U S A. 2008;105(49):19426–19431. doi:10.1073/pnas.0805230105
  • Cheng K, Ho K, Stokes R, et al. Hypoxia-inducible factor-1alpha regulates beta cell function in mouse and human islets. J Clin Invest. 2010;120(6):2171–2183. doi:10.1172/JCI35846
  • Gu HF, Zheng X, Abu Seman N, et al. Impact of the hypoxia-inducible factor-1 alpha (HIF1A) Pro582Ser polymorphism on diabetes nephropathy. Diabetes Care. 2013;36(2):415–421. doi:10.2337/dc12-1125
  • Michailidou Z, Morton NM, Moreno Navarrete JM, et al. Adipocyte pseudohypoxia suppresses lipolysis and facilitates benign adipose tissue expansion. Diabetes. 2015;64(3):733–745. doi:10.2337/db14-0233
  • Rahtu-Korpela L, Karsikas S, Horkko S, et al. HIF prolyl 4-hydroxylase-2 inhibition improves glucose and lipid metabolism and protects against obesity and metabolic dysfunction. Diabetes. 2014;63(10):3324–3333. doi:10.2337/db14-0472
  • Li X, Li J, Wang L, et al. The role of metformin and resveratrol in the prevention of hypoxia-inducible factor 1alpha accumulation and fibrosis in hypoxic adipose tissue. Br J Pharmacol. 2016;173(12):2001–2015. doi:10.1111/bph.13493
  • Ma Z, Zhang Y, Li Q, Xu M, Bai J, Wu S. Resveratrol improves alcoholic fatty liver disease by downregulating HIF-1alpha expression and mitochondrial ROS production. PLoS One. 2017;12(8):e0183426. doi:10.1371/journal.pone.0183426
  • Sha W, Liu M, Sun D, et al. Resveratrol ameliorated endothelial injury of thoracic aorta in diabetic mice and Gly-LDL-induced HUVECs through inhibiting TLR4/HIF-1alpha. J Cell Mol Med. 2021;25(13):6258–6270. doi:10.1111/jcmm.16584
  • Lebeau PF, Byun JH, Platko K, et al. Caffeine blocks SREBP2-induced hepatic PCSK9 expression to enhance LDLR-mediated cholesterol clearance. Nat Commun. 2022;13(1):770. doi:10.1038/s41467-022-28240-9
  • Kucejova B, Sunny NE, Nguyen AD, et al. Uncoupling hypoxia signaling from oxygen sensing in the liver results in hypoketotic hypoglycemic death. Oncogene. 2011;30(18):2147–2160. doi:10.1038/onc.2010.587
  • Wang XL, Suzuki R, Lee K, et al. Ablation of ARNT/HIF1beta in liver alters gluconeogenesis, lipogenic gene expression, and serum ketones. Cell Metab. 2009;9(5):428–439. doi:10.1016/j.cmet.2009.04.001
  • Pez F, Dayan F, Durivault J, et al. The HIF-1-inducible lysyl oxidase activates HIF-1 via the Akt pathway in a positive regulation loop and synergizes with HIF-1 in promoting tumor cell growth. Cancer Res. 2011;71(5):1647–1657. doi:10.1158/0008-5472.CAN-10-1516
  • Vasudevan KM, Garraway LA. AKT signaling in physiology and disease. Curr Top Microbiol Immunol. 2010;347:105–133. doi:10.1007/82_2010_66
  • Brito PM, Devillard R, Negre-Salvayre A, et al. Resveratrol inhibits the mTOR mitogenic signaling evoked by oxidized LDL in smooth muscle cells. Atherosclerosis. 2009;205(1):126–134. doi:10.1016/j.atherosclerosis.2008.11.011
  • Xu F, Wang Y, Cui W, et al. Resveratrol prevention of diabetic nephropathy is associated with the suppression of renal inflammation and mesangial cell proliferation: possible roles of Akt/NF-kappaB pathway. Int J Endocrinol. 2014;2014:289327. doi:10.1155/2014/289327
  • Taha C, Liu Z, Jin J, Al-Hasani H, Sonenberg N, Klip A. Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase b, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation. J Biol Chem. 1999;274(46):33085–33091. doi:10.1074/jbc.274.46.33085
  • Zelzer E, Levy Y, Kahana C, Shilo BZ, Rubinstein M, Cohen B. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J. 1998;17(17):5085–5094. doi:10.1093/emboj/17.17.5085
  • Li RL, He LY, Zhang Q, et al. HIF-1alpha is a potential molecular target for herbal medicine to treat diseases. Drug Des Devel Ther. 2020;14:4915–4949. doi:10.2147/DDDT.S274980
  • Naito K, Kanki K. Glycolytic inhibition by resveratrol prevents myoblast cell death caused by glucose deprivation and hypoxia; a possible application to the three-dimensional tissue construction. J Biosci Bioeng. 2021;131(1):90–97. doi:10.1016/j.jbiosc.2020.08.010
  • Chandra NC. A comprehensive account of insulin and LDL receptor activity over the years: a highlight on their signaling and functional role. J Biochem Mol Toxicol. 2021;35(9):e22840. doi:10.1002/jbt.22840
  • Jing Y, Hu T, Lin C, et al. Resveratrol downregulates PCSK9 expression and attenuates steatosis through estrogen receptor alpha-mediated pathway in L02cells. Eur J Pharmacol. 2019;855:216–226. doi:10.1016/j.ejphar.2019.05.019
  • Hwang S, Nguyen AD, Jo Y, Engelking LJ, Brugarolas J, DeBose-Boyd RA. Hypoxia-inducible factor 1alpha activates insulin-induced gene 2 (Insig-2) transcription for degradation of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase in the liver. J Biol Chem. 2017;292(22):9382–9393. doi:10.1074/jbc.M117.788562
  • Bjune K, Wierod L, Naderi S. Inhibitors of AKT kinase increase LDL receptor mRNA expression by two different mechanisms. PLoS One. 2019;14(6):e0218537. doi:10.1371/journal.pone.0218537
  • He Y, Yang W, Gan L, et al. Silencing HIF-1alpha aggravates non-alcoholic fatty liver disease in vitro through inhibiting PPAR-alpha/ANGPTL4 singling pathway. Gastroenterol Hepatol. 2021;44(5):355–365. doi:10.1016/j.gastrohep.2020.09.014