303
Views
0
CrossRef citations to date
0
Altmetric
Research paper

(-)-Epigallocatechin 3-gallate protects pancreatic β-cell against excessive autophagy-induced injury through promoting FTO degradation

, , , , , , , , , , , & show all
Received 09 Nov 2023, Accepted 17 Jun 2024, Published online: 03 Jul 2024

References

  • Chen ZF, Li YB, Han JY, et al. The double-edged effect of autophagy in pancreatic beta cells and diabetes. Autophagy. 2011;7(1):12–16. doi: 10.4161/auto.7.1.13607
  • Tanemura M, Ohmura Y, Deguchi T, et al. Rapamycin causes upregulation of autophagy and impairs islets function both in vitro and in vivo. Am J Transplant. 2012;12(1):102–114. doi: 10.1111/j.1600-6143.2011.03771.x
  • Lee YH, Kim J, Park K, et al. beta-cell autophagy: mechanism and role in beta-cell dysfunction. Mol Metab. 2019;27S:S92–S103. doi: 10.1016/j.molmet.2019.06.014
  • Israeli T, Riahi Y, Garzon P, et al. Nutrient sensor mTORC1 regulates insulin secretion by modulating beta-cell autophagy. Diabetes. 2022;71(3):453–469. doi: 10.2337/db21-0281
  • Li S, Du L, Zhang L, et al. Cathepsin B contributes to autophagy-related 7 (Atg7)-induced nod-like receptor 3 (NLRP3)-dependent proinflammatory response and aggravates lipotoxicity in rat insulinoma cell line. J Biol Chem. 2013;288(42):30094–30104. doi: 10.1074/jbc.M113.494286
  • Yamamoto S, Kuramoto K, Wang N, et al. Autophagy differentially regulates insulin production and insulin sensitivity. Cell Rep. 2018;23(11):3286–3299. doi: 10.1016/j.celrep.2018.05.032
  • Wu T, Shao Y, Li X, et al. NR3C1/Glucocorticoid receptor activation promotes pancreatic beta-cell autophagy overload in response to glucolipotoxicity. Autophagy. 2023;19(9):2538–2557. doi: 10.1080/15548627.2023.2200625
  • Xing QC, Liu X, Li W, et al. Sangguayin preparation prevents palmitate-induced apoptosis by suppressing endoplasmic reticulum stress and autophagy in db/db mice and MIN6 pancreatic beta-cells. Chin J Nat Med. 2020;18(6):472–480. doi: 10.1016/S1875-5364(20)30054-6
  • Chu KY, Mellet N, Thai LM, et al. Short-term inhibition of autophagy benefits pancreatic beta-cells by augmenting ether lipids and peroxisomal function, and by countering depletion of n-3 polyunsaturated fatty acids after fat-feeding. Mol Metab. 2020;40:101023. doi: 10.1016/j.molmet.2020.101023
  • Jin W, Fan M, Zhang Y, et al. Polydatin prevents lipotoxicity-induced dysfunction in pancreatic beta-cells by inhibiting endoplasmic reticulum stress and excessive autophagy. Phytomedicine. 2022;106:154410. doi: 10.1016/j.phymed.2022.154410
  • Cai EP, Lin JK. Epigallocatechin gallate (EGCG) and rutin suppress the glucotoxicity through activating IRS2 and AMPK signaling in rat pancreatic beta cells. J Agric Food Chem. 2009;57(20):9817–9827. doi: 10.1021/jf902618v
  • Martino L, Masini M, Novelli M, et al. The aryl receptor inhibitor epigallocatechin-3-gallate protects INS-1E beta-cell line against acute dioxin toxicity. Chemosphere. 2013;93(8):1447–1455. doi: 10.1016/j.chemosphere.2013.06.026
  • Hintzpeter J, Stapelfeld C, Loerz C, et al. Green tea and one of its constituents, epigallocatechine-3-gallate, are potent inhibitors of human 11β-hydroxysteroid dehydrogenase type 1. PLOS ONE. 2014;9(1):e84468. doi: 10.1371/journal.pone.0084468
  • Wu T, Xiang J, Shan W, et al. Epigallocatechin-3-gallate inhibits ethanol-induced apoptosis through neurod1 regulating CHOP expression in pancreatic beta-cells. Anat Rec (Hoboken). 2016;299(5):573–582. doi: 10.1002/ar.23332
  • Kose T, Vera-Aviles M, Sharp PA, et al. Curcumin and (−)- Epigallocatechin-3-gallate protect murine MIN6 pancreatic beta-cells against iron toxicity and Erastin-Induced Ferroptosis. Pharmaceuticals (Basel). 2019;12(1):26. doi: 10.3390/ph12010026
  • Jia X, Luo Z, Gao Y, et al. EGCG Upregulates UCP(3) levels to protect MIN(6) pancreatic islet cells from interleukin-1beta-induced apoptosis. Drug Des Devel Ther. 2020;14:4251–4261. doi: 10.2147/DDDT.S270345
  • Ortsater H, Grankvist N, Wolfram S, et al. Diet supplementation with green tea extract epigallocatechin gallate prevents progression to glucose intolerance in db/db mice. Nutr Metab (Lond). 2012;9(1):11. doi: 10.1186/1743-7075-9-11
  • Pathak NM, Millar PJB, Pathak V, et al. Beneficial metabolic effects of dietary epigallocatechin gallate alone and in combination with exendin-4 in high fat diabetic mice. Mol Cell Endocrinol. 2018;460:200–208. doi: 10.1016/j.mce.2017.07.024
  • Zhu T, Li M, Zhu M, et al. Epigallocatechin-3-gallate alleviates type 2 diabetes mellitus via beta-cell function improvement and insulin resistance reduction. Iran J Basic Med Sci. 2022;25(4):483–488. doi: 10.22038/IJBMS.2022.58591.13016
  • Zhang ZF, Li Q, Liang J, et al. Epigallocatechin-3-O-gallate (EGCG) protects the insulin sensitivity in rat L6 muscle cells exposed to dexamethasone condition. Phytomedicine. 2010;17(1):14–18. doi: 10.1016/j.phymed.2009.09.007
  • Yan J, Feng Z, Liu J, et al. Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate. J Nutr Biochem. 2012;23(7):716–724. doi: 10.1016/j.jnutbio.2011.03.014
  • Loos RJ, Bouchard C. FTO: the first gene contributing to common forms of human obesity. Obes Rev. 2008;9(3):246–250. doi: 10.1111/j.1467-789X.2008.00481.x
  • Yang Z, Yu GL, Zhu X, et al. Critical roles of FTO-mediated mRNA m6A demethylation in regulating adipogenesis and lipid metabolism: implications in lipid metabolic disorders. Genes Dis. 2022;9(1):51–61. doi: 10.1016/j.gendis.2021.01.005
  • Yin D, Li Y, Liao X, et al. FTO: a critical role in obesity and obesity-related diseases. Br J Nutr. 2023;130(10):1657–1664. doi: 10.1017/S0007114523000764
  • Shen F, Huang W, Huang JT, et al. Decreased N 6 -methyladenosine in peripheral blood RNA from diabetic patients is associated with FTO expression rather than ALKBH5. J Clin Endocrinol Metab. 2015;100(1):E148–E154. doi: 10.1210/jc.2014-1893
  • Yang Y, Shen F, Huang W, et al. Glucose is involved in the dynamic regulation of m6A in patients with type 2 diabetes. J Clin Endocrinol Metab. 2019;104(3):665–673. doi: 10.1210/jc.2018-00619
  • Russell MA, Morgan NG. Conditional expression of the FTO gene product in rat INS-1 cells reveals its rapid turnover and a role in the profile of glucose-induced insulin secretion. Clin Sci (Lond). 2011;120(9):403–413. doi: 10.1042/CS20100416
  • Taneera J, Prasad RB, Dhaiban S, et al. Silencing of the FTO gene inhibits insulin secretion: an in vitro study using GRINCH cells. Mol Cell Endocrinol. 2018;472:10–17. doi: 10.1016/j.mce.2018.06.003
  • Fan HQ, He W, Xu KF, et al. FTO inhibits insulin secretion and promotes NF-κB Activation through positively regulating ROS production in pancreatic β cells. PLOS ONE. 2015;10(5):e0127705. doi: 10.1371/journal.pone.0127705
  • Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 2015;22(3):377–388. doi: 10.1038/cdd.2014.150
  • Qi Z, He Q, Ji L, et al. Antioxidant supplement inhibits skeletal muscle constitutive autophagy rather than fasting-induced autophagy in mice. Oxid Med Cell Longev. 2014;2014:1–10. doi: 10.1155/2014/315896
  • Wang S, Wang C, Yan F, et al. N-Acetylcysteine attenuates diabetic myocardial ischemia reperfusion injury through inhibiting excessive autophagy. Mediators Inflamm. 2017;2017:1–10. doi: 10.1155/2017/9257291
  • !!! INVALID CITATION! [4].
  • Wu R, Yao Y, Jiang Q, et al. Epigallocatechin gallate targets FTO and inhibits adipogenesis in an mRNA m(6)A-YTHDF2-dependent manner. Int J Obes (Lond). 2018;42(7):1378–1388. doi: 10.1038/s41366-018-0082-5
  • Zhu T, Yong XLH, Xia D, et al. Ubiquitination regulates the proteasomal degradation and nuclear translocation of the fat Mass and obesity-associated (FTO) protein. J Mol Biol. 2018;430(3):363–371. doi: 10.1016/j.jmb.2017.12.003
  • Cui YH, Yang S, Wei J, et al. Autophagy of the m(6)A mRNA demethylase FTO is impaired by low-level arsenic exposure to promote tumorigenesis. Nat Commun. 2021;12(1):2183. doi: 10.1038/s41467-021-22469-6
  • Li W, Zhu C, Liu T, et al. Epigallocatechin-3-gallate ameliorates glucolipid metabolism and oxidative stress in type 2 diabetic rats. Diab Vasc Dis Res. 2020;17(6):1479164120966998. doi: 10.1177/1479164120966998
  • Mukai E, Fujimoto S, Sato H, et al. Exendin-4 suppresses SRC activation and reactive oxygen species production in diabetic Goto-Kakizaki rat islets in an epac-dependent manner. Diabetes. 2011;60(1):218–226. doi: 10.2337/db10-0021
  • Vivot K, Langlois A, Bietiger W, et al. Pro-inflammatory and pro-oxidant status of pancreatic islet in vitro is controlled by TLR-4 and HO-1 pathways. PLOS ONE. 2014;9(10):e107656. doi: 10.1371/journal.pone.0107656
  • Wang X, Ge QM, Bian F, et al. Inhibition of TLR4 protects rat islets against lipopolysaccharide-induced dysfunction. Mol Med Rep. 2017;15(2):805–812. doi: 10.3892/mmr.2016.6097
  • Blair LA, Heitmeier MR, Scarim AL, et al. Double-stranded RNA-dependent protein kinase is not required for double-stranded RNA-induced nitric oxide synthase expression or nuclear factor-kappaB activation by islets. Diabetes. 2001;50(2):283–290. doi: 10.2337/diabetes.50.2.283
  • Kominato R, Fujimoto S, Mukai E, et al. Src activation generates reactive oxygen species and impairs metabolism-secretion coupling in diabetic Goto-Kakizaki and ouabain-treated rat pancreatic islets. Diabetologia. 2008;51(7):1226–1235. doi: 10.1007/s00125-008-1008-x
  • Li X, Li S, Chen M, et al. (-)-Epigallocatechin-3-gallate (EGCG) inhibits starch digestion and improves glucose homeostasis through direct or indirect activation of PXR/CAR-mediated phase II metabolism in diabetic mice. Food Funct. 2018;9(9):4651–4663. doi: 10.1039/C8FO01293H
  • Park JM, Shin Y, Kim SH, et al. Dietary Epigallocatechin-3-gallate alters the gut microbiota of obese diabetic db/db mice: lactobacillus is a putative target. J Med Food. 2020;23(10):1033–1042. doi: 10.1089/jmf.2020.4700
  • Darwish MA, Abdel-Bakky MS, Messiha BAS, et al. Resveratrol mitigates pancreatic TF activation and autophagy-mediated beta cell death via inhibition of CXCL16/ox-LDL pathway: a novel protective mechanism against type 1 diabetes mellitus in mice. Eur J Pharmacol. 2021;901:174059. doi: 10.1016/j.ejphar.2021.174059
  • Zummo FP, Krishnanda SI, Georgiou M, et al. Exendin-4 stimulates autophagy in pancreatic β-cells via the RAPGEF/EPAC-Ca 2+ -PPP3/calcineurin-TFEB axis. Autophagy. 2022;18(4):799–815. doi: 10.1080/15548627.2021.1956123
  • Zummo FP, Cullen KS, Honkanen-Scott M, et al. Glucagon-like peptide 1 protects pancreatic beta-cells from death by increasing autophagic flux and restoring lysosomal function. Diabetes. 2017;66(5):1272–1285. doi: 10.2337/db16-1009
  • Liu J, Tang Y, Feng Z, et al. (-)-Epigallocatechin-3-gallate attenuated myocardial mitochondrial dysfunction and autophagy in diabetic Goto-Kakizaki rats. Free Radic Res. 2014;48(8):898–906. doi: 10.3109/10715762.2014.920955
  • Wang L, Sun X, Zhu M, et al. Epigallocatechin-3-gallate stimulates autophagy and reduces apoptosis levels in retinal Muller cells under high-glucose conditions. Exp Cell Res. 2019;380(2):149–158. doi: 10.1016/j.yexcr.2019.04.014
  • Kim HS, Montana V, Jang HJ, et al. Epigallocatechin gallate (EGCG) stimulates autophagy in vascular endothelial cells: a potential role for reducing lipid accumulation. J Biol Chem. 2013;288(31):22693–22705. doi: 10.1074/jbc.M113.477505
  • Kim HS, Quon MJ, Kim JA. New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol. 2014;2:187–195. doi: 10.1016/j.redox.2013.12.022
  • Zhao J, Blayney A, Liu X, et al. EGCG binds intrinsically disordered N-terminal domain of p53 and disrupts p53-MDM2 interaction. Nat Commun. 2021;12(1):986. doi: 10.1038/s41467-021-21258-5
  • Quan Y, Li L, Dong L, et al. Epigallocatechin-3-gallate (EGCG) inhibits aggregation of pulmonary fibrosis associated mutant surfactant protein A2 via a proteasomal degradation pathway. Int J Biochem Cell Biol. 2019;116:105612. doi: 10.1016/j.biocel.2019.105612
  • Chen CY, Lin YJ, Wang CCN, et al. Epigallocatechin-3-gallate inhibits tumor angiogenesis: involvement of endoglin/Smad1 signaling in human umbilical vein endothelium cells. Biomed Pharmacother. 2019;120:109491. doi: 10.1016/j.biopha.2019.109491
  • Hou H, Wang Y, Li C, et al. Dipeptidyl Peptidase-4 Is a Target Protein of Epigallocatechin-3-Gallate. Biomed Res Int. 2020;2020:1–9. doi: 10.1155/2020/5370759
  • Tai H, Wang X, Zhou J, et al. Protein kinase Cbeta activates fat mass and obesity-associated protein by influencing its ubiquitin/proteasome degradation. Faseb J. 2017;31(10):4396–4406. doi: 10.1096/fj.201601159RR
  • Song X, Hu Q, Xu X, et al. Protein kinase C beta relieves autism-like behavior in EN2 knockout mice via upregulation of the FTO/PGC-1alpha/UCP1 axis. J Biochem Mol Toxicol. 2023;37(1):e23236. doi: 10.1002/jbt.23236
  • Li YF, Wang H, Fan Y, et al. Epigallocatechin-3-gallate inhibits matrix metalloproteinase-9 and monocyte chemotactic protein-1 expression through the 67-kappaDa laminin receptor and the TLR4/MAPK/NF-kappaB signalling Pathway in Lipopolysaccharide-Induced Macrophages. Cell Physiol Biochem. 2017;43(3):926–936. doi: 10.1159/000481643
  • Won HR, Lee P, Oh SR, et al. Epigallocatechin-3-gallate suppresses the expression of TNF-alpha-induced MMP-1 via MAPK/ERK signaling pathways in human dermal fibroblasts. Biol Pharm Bull. 2021;44(1):18–24. doi: 10.1248/bpb.b20-00304
  • Qu Z, Jia L, Xie T, et al. (-)-Epigallocatechin-3-gallate protects against lithium-pilocarpine-induced epilepsy by inhibiting the toll-like receptor 4 (TLR4)/nuclear factor-kappaB (NF-kappaB) signaling pathway. Med Sci Monit. 2019;25:1749–1758. doi: 10.12659/MSM.915025
  • Mahmoud MF, Abdelaal S, Mohammed HO, et al. Syzygium aqueum (Burm.F.) alston prevents streptozotocin-induced pancreatic beta cells damage via the TLR-4 signaling pathway. Front Pharmacol. 2021;12:769244. doi: 10.3389/fphar.2021.769244
  • Sarparanta J, Garcia-Macia M, Singh R. Autophagy and mitochondria in obesity and type 2 diabetes. Curr Diabetes Rev. 2017;13(4):352–369. doi: 10.2174/1573399812666160217122530
  • Marasco MR, Conteh AM, Reissaus CA, et al. Interleukin-6 reduces β-Cell oxidative stress by linking autophagy with the antioxidant response. Diabetes. 2018;67(8):1576–1588. doi: 10.2337/db17-1280
  • Liu J, Tang Y, Feng Z, et al. Acetylated FoxO1 mediates high-glucose induced autophagy in H9c2 cardiomyoblasts: regulation by a polyphenol -(-)-epigallocatechin-3-gallate. Metabolism. 2014;63(10):1314–1323. doi: 10.1016/j.metabol.2014.06.012
  • Wu T, Zhang S, Xu J, et al. HRD1, an important player in pancreatic beta-cell failure and therapeutic target for type 2 diabetic mice. Diabetes. 2020;69(5):940–953. doi: 10.2337/db19-1060
  • Wang X, Wu R, Liu Y, et al. Wang Y: m(6)A mRNA methylation controls autophagy and adipogenesis by targeting Atg5 and Atg7. Autophagy. 2020;16(7):1221–1235. doi: 10.1080/15548627.2019.1659617

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.