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Research Paper

Impaired autophagy flux contributes to enhanced ischemia reperfusion injury in the diabetic heart

, , , , , , , , , , , , , , & ORCID Icon show all
Article: 2330327 | Received 27 Aug 2023, Accepted 05 Mar 2024, Published online: 21 Mar 2024

References

  • Dunlay SM, Givertz MM, Aguilar D, et al. Type 2 Diabetes Mellitus and Heart Failure: A Scientific Statement From the American Heart Association and the Heart Failure Society of America: This statement does not represent an update of the 2017 ACC/AHA/HFSA heart failure guideline update. Circulation. 2019 Aug 13;140(7):e294–28.
  • Rawshani A, Rawshani A, Franzén S, et al. Range of Risk Factor Levels: Control, Mortality, and Cardiovascular Outcomes in Type 1 Diabetes Mellitus. Circulation. 2017 Apr 18;135(16):1522–1531.
  • Sousa GR, Pober D, Galderisi A, et al. Glycemic Control, Cardiac Autoimmunity, and Long-Term Risk of Cardiovascular Disease in Type 1 Diabetes Mellitus. Circulation. 2019 Feb 5;139(6):730–743.
  • Figtree GA, Rådholm K, Barrett TD, et al. Effects of Canagliflozin on Heart Failure Outcomes Associated With Preserved and Reduced Ejection Fraction in Type 2 Diabetes Mellitus. Circulation. 2019 May 28;139(22):2591–2593.
  • Cosentino F, Cannon CP, Cherney DZI, et al. Efficacy of Ertugliflozin on Heart Failure-Related Events in Patients With Type 2 Diabetes Mellitus and Established Atherosclerotic Cardiovascular Disease: Results of the VERTIS CV Trial. Circulation. 2020 Dec 8;142(23):2205–2215.
  • Rådholm K, Figtree G, Perkovic V, et al. Canagliflozin and Heart Failure in Type 2 Diabetes Mellitus: Results From the CANVAS Program. Circulation. 2018 Jul 31;138(5):458–468.
  • Mapanga RF, Joseph D, Symington B, et al. Detrimental effects of acute hyperglycaemia on the rat heart. Acta Physiol (Oxf). 2014 Mar;210(3):546–64.
  • Di Filippo C, Cuzzocrea S, Marfella R, et al. M40403 prevents myocardial injury induced by acute hyperglycaemia in perfused rat heart. Eur J Pharmacol. 2004 Aug 16;497(1):65–74.
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011 Nov 11;147(4):728–41.
  • Schiattarella GG, Hill JA. Therapeutic targeting of autophagy in cardiovascular disease [Review]. J Mol Cell Cardiol. 2016 Jun;95:86–93.
  • Ikeda S, Zablocki D, Sadoshima J. The role of autophagy in death of cardiomyocytes. J Mol Cell Cardiol. 2022 Apr;165:1–8.
  • Hariharan N, Ikeda Y, Hong C, et al. Autophagy plays an essential role in mediating regression of hypertrophy during unloading of the heart. PLoS One. 2013;8(1):e51632.
  • Cao DJ, Jiang N, Blagg A, et al. Mechanical unloading activates FoxO3 to trigger Bnip3-dependent cardiomyocyte atrophy. J Am Heart Assoc. 2013 Apr 8;2(2): e000016.
  • Wellnitz K, Taegtmeyer H. Mechanical unloading of the failing heart exposes the dynamic nature of autophagy. Autophagy. 2010 Jan;6(1):155–6.
  • Delbridge LMD, Mellor KM, Taylor DJ, et al. Myocardial stress and autophagy: mechanisms and potential therapies. Nat Rev Cardiol. 2017 Jul;14(7):412–425.
  • Nakai A, Yamaguchi O, Takeda T, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007 May;13(5):619–24.
  • Shirakabe A, Zhai P, Ikeda Y, et al. Drp1-Dependent Mitochondrial Autophagy Plays a Protective Role Against Pressure Overload-Induced Mitochondrial Dysfunction and Heart Failure. Circulation. 2016 Mar 29;133(13):1249–63.
  • Mariño G, Pietrocola F, Kong Y, et al. Dimethyl α-ketoglutarate inhibits maladaptive autophagy in pressure overload-induced cardiomyopathy. Autophagy. 2014 May;10(5):930–2.
  • Taneike M, Yamaguchi O, Nakai A, et al. Inhibition of autophagy in the heart induces age-related cardiomyopathy [Research Support, Non-U.S. Gov’t]. Autophagy. 2010 Jul;6(5):600–6.
  • Nah J, Fernández Á F, Kitsis RN, et al. Does Autophagy Mediate Cardiac Myocyte Death During Stress? Circ Res. 2016 Sep 30;119(8):893–5.
  • Zhang M, Sui W, Xing Y, et al. Angiotensin IV attenuates diabetic cardiomyopathy via suppressing FoxO1-induced excessive autophagy, apoptosis and fibrosis. Theranostics. 2021;11(18):8624–8639.
  • Moe GW, Marin-Garcia J. Role of cell death in the progression of heart failure. Heart Fail Rev. 2016 Mar;21(2):157–67.
  • Lavandero S, Chiong M, Rothermel BA, et al. Autophagy in cardiovascular biology. J Clin Invest. 2015 Jan;125(1):55–64.
  • Xing Y, Sui Z, Liu Y, et al. Blunting TRPML1 channels protects myocardial ischemia/reperfusion injury by restoring impaired cardiomyocyte autophagy. Basic Res Cardiol. 2022 Apr 7;117(1):20.
  • Xie M, Cho GW, Kong Y, et al. Activation of Autophagic Flux Blunts Cardiac Ischemia/Reperfusion Injury. Circ Res. 2021 Jul 23;129(3):435–450.
  • Xie M, Kong Y, Tan W, et al. Histone deacetylase inhibition blunts ischemia/reperfusion injury by inducing cardiomyocyte autophagy. Circulation. 2014 Mar 11;129(10):1139–51.
  • Li Y, Liang P, Jiang B, et al. CARD9 promotes autophagy in cardiomyocytes in myocardial ischemia/reperfusion injury via interacting with Rubicon directly. Basic Res Cardiol. 2020 Apr 4;115(3):29.
  • Gu S, Tan J, Li Q, et al. Downregulation of LAPTM4B Contributes to the Impairment of the Autophagic Flux via Unopposed Activation of mTORC1 Signaling During Myocardial Ischemia/Reperfusion Injury. Circ Res. 2020 Sep 11;127(7):e148–e165.
  • Maejima Y, Kyoi S, Zhai P, et al. Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2. Nat Med. 2013 Nov;19(11):1478–88.
  • Ma X, Liu H, Foyil SR, et al. Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation. 2012 Jun 26;125(25):3170–81.
  • Buse JB, Ginsberg HN, Bakris GL, et al. Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care. 2007 Jan;30(1):162–72.
  • Yun JS, Ko SH. Current trends in epidemiology of cardiovascular disease and cardiovascular risk management in type 2 diabetes. Metabolism. 2021 Oct;123:154838.
  • Jia G, Whaley-Connell A, Sowers JR. Diabetic cardiomyopathy: a hyperglycaemia- and insulin-resistance-induced heart disease. Diabetologia. 2018 Jan;61(1):21–28.
  • Laakso M, Kuusisto J. Insulin resistance and hyperglycaemia in cardiovascular disease development. Nat Rev Endocrinol. 2014 May;10(5):293–302.
  • Forrester SJ, Kikuchi DS, Hernandes MS, et al. Reactive Oxygen Species in Metabolic and Inflammatory Signaling. Circ Res. 2018 Mar 16;122(6):877–902.
  • Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 2015 Mar;22(3):377–88.
  • Kenny HC, Abel ED. Heart Failure in Type 2 Diabetes Mellitus. Circ Res. 2019 Jan 4;124(1):121–141.
  • Uchiyama Y. Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol. 2001 Aug;64(3):233–46.
  • Man SM, Kanneganti TD. Regulation of lysosomal dynamics and autophagy by CTSB/cathepsin B. Autophagy. 2016 Dec;12(12):2504–2505.
  • Wu P, Yuan X, Li F, et al. Myocardial Upregulation of Cathepsin D by Ischemic Heart Disease Promotes Autophagic Flux and Protects Against Cardiac Remodeling and Heart Failure. Circ Heart Fail. 2017 Jul;10(7).
  • Chen HH, Khatun Z, Wei L, et al. A nanoparticle probe for the imaging of autophagic flux in live mice via magnetic resonance and near-infrared fluorescence. Nat Biomed Eng. 2022 Sep;6(9):1045–1056.
  • Davidson MD, Ballinger KR, Khetani SR. Long-term exposure to abnormal glucose levels alters drug metabolism pathways and insulin sensitivity in primary human hepatocytes. Sci Rep. 2016 Jun 17;6:28178.
  • Zhang J, Wang X, Cui W, et al. Visualization of caspase-3-like activity in cells using a genetically encoded fluorescent biosensor activated by protein cleavage. Nat Commun. 2013;4:2157.
  • Lebek S, Chemello F, Caravia XM, et al. Ablation of CaMKIIdelta oxidation by CRISPR-Cas9 base editing as a therapy for cardiac disease. Science. 2023 Jan 13;379(6628):179-185.
  • Xiao H, Zhang M, Wu H, et al. CIRKIL Exacerbates Cardiac Ischemia/Reperfusion Injury by Interacting With Ku70. Circ Res. 2022 Mar 4;130(5):e3–e17.
  • Fang H, Geng S, Hao M, et al. Simultaneous Zn(2+) tracking in multiple organelles using super-resolution morphology-correlated organelle identification in living cells. Nat Commun. 2021 Jan 4;12(1):109.
  • Chen Q, Hao M, Wang L, et al. Prefused lysosomes cluster on autophagosomes regulated by VAMP8. Cell Death Dis. 2021 Oct 13;12(10):939.
  • Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007 Sep-Oct;3(5):452–60.
  • Aghaei M, Motallebnezhad M, Ghorghanlu S, et al. Targeting autophagy in cardiac ischemia/reperfusion injury: A novel therapeutic strategy. J Cell Physiol. 2019 Aug;234(10):16768–16778.
  • Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circulation research. 2009 Jan 30;104(2):150–8.
  • Przyklenk K, Dong Y, Undyala VV, et al. Autophagy as a therapeutic target for ischaemia /reperfusion injury? Concepts, controversies, and challenges. Cardiovascular research. 2012 May 1;94(2):197–205.
  • Sciarretta S, Boppana VS, Umapathi M, et al. Boosting autophagy in the diabetic heart: a translational perspective. Cardiovasc Diagn Ther. 2015 Oct;5(5):394–402.
  • Murase H, Kuno A, Miki T, et al. Inhibition of DPP-4 reduces acute mortality after myocardial infarction with restoration of autophagic response in type 2 diabetic rats. Cardiovasc Diabetol. 2015 Aug 11;14:103.
  • Matsui Y, Takagi H, Qu X, et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res. 2007 Mar 30;100(6):914–22.
  • Bugger H, Abel ED. Molecular mechanisms of diabetic cardiomyopathy [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Review]. Diabetologia. 2014 Apr;57(4):660–71.
  • Xu X, Kobayashi S, Chen K, et al. Diminished autophagy limits cardiac injury in mouse models of type 1 diabetes [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. J Biol Chem. 2013 Jun 21;288(25):18077–92.
  • Zhao Y, Zhang L, Qiao Y, et al. Heme oxygenase-1 prevents cardiac dysfunction in streptozotocin-diabetic mice by reducing inflammation, oxidative stress, apoptosis and enhancing autophagy [Research Support, Non-U.S. Gov’t]. PLoS One. 2013;8(9):e75927.
  • Zhang J, Cheng Y, Gu J, et al. Fenofibrate increases cardiac autophagy via FGF21/SIRT1 and prevents fibrosis and inflammation in the hearts of Type 1 diabetic mice [Research Support, Non-U.S. Gov’t]. Clin Sci (Lond). 2016 Apr;130(8):625–41.
  • Wang B, Yang Q, Sun YY, et al. Resveratrol-enhanced autophagic flux ameliorates myocardial oxidative stress injury in diabetic mice [Research Support, Non-U.S. Gov’t]. J Cell Mol Med. 2014 Aug;18(8):1599–611.
  • Guo Y, Yu W, Sun D, et al. A novel protective mechanism for mitochondrial aldehyde dehydrogenase (ALDH2) in type i diabetes-induced cardiac dysfunction: role of AMPK-regulated autophagy [Research Support, Non-U.S. Gov’t]. Biochim Biophys Acta. 2015 Feb;1852(2):319–31.
  • Kanamori H, Takemura G, Goto K, et al. Autophagic adaptations in diabetic cardiomyopathy differ between type 1 and type 2 diabetes. Autophagy. 2015;11(7):1146–60.
  • Eguchi M, Kim YH, Kang KW, et al. Ischemia-reperfusion injury leads to distinct temporal cardiac remodeling in normal versus diabetic mice [Research Support, Non-U.S. Gov’t]. PLoS One. 2012;7(2):e30450.
  • Guo J, Mihic A, Wu J, et al. Canopy 2 attenuates the transition from compensatory hypertrophy to dilated heart failure in hypertrophic cardiomyopathy. Eur Heart J. 2015 Oct 1;36(37):2530–40.
  • Traister A, Li M, Aafaqi S, et al. Integrin-linked kinase mediates force transduction in cardiomyocytes by modulating SERCA2a/PLN function. Nat Commun. 2014 Sep 11;5:4533.
  • Drawnel FM, Boccardo S, Prummer M, et al. Disease modeling and phenotypic drug screening for diabetic cardiomyopathy using human induced pluripotent stem cells. Cell Rep. 2014 Nov 6;9(3):810–21.
  • Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013 Nov;8(11):2281–2308.
  • Velagapudi R, Lepiarz I, El-Bakoush A, et al. Induction of Autophagy and Activation of SIRT-1 Deacetylation Mechanisms Mediate Neuroprotection by the Pomegranate Metabolite Urolithin A in BV2 Microglia and Differentiated 3D Human Neural Progenitor Cells. Mol Nutr Food Res. 2019 May;63(10):e1801237.
  • Jahng JWS, Alsaadi RM, Palanivel R, et al. Iron overload inhibits late stage autophagic flux leading to insulin resistance. EMBO Rep. 2019 Oct 4;20(10):e47911.
  • Haslam G, Wyatt D, Kitos PA. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology. 2000 Jan;32(1):63–75.
  • Lazar DF, Gillette AA, Lewis SR, et al. Multimodal assessment of autophagy in mammalian cells with a novel, LC3-based tandem reporter. Methods Cell Biol. 2021;165:39–57.