Pharmacological preconditioning protects from ischemia/reperfusion-induced apoptosis by modulating Bcl-xL expression through a ROS-dependent mechanism.


Journal

The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646

Informations de publication

Date de publication:
06 2021
Historique:
revised: 02 12 2020
received: 06 07 2020
accepted: 16 12 2020
pubmed: 20 12 2020
medline: 23 7 2021
entrez: 19 12 2020
Statut: ppublish

Résumé

Myocardial ischemia/reperfusion (I/R) injury is a frequent perioperative threat, with numerous strategies developed to limit and/or prevent it. One interesting axis of research is the anesthetic preconditioning (APc) agent's hypothesis (such as sevoflurane, SEV). However, APc's mode of action is still poorly understood and volatile anesthetics used as preconditioning agents are often not well suited in clinical practice. Here, in vitro using H9C2 cells lines (in myeloblast state or differentiated toward cardiomyocytes) and in vivo in mice, we identified that SEV-induced APc is mediated by a mild induction of reactive oxygen species (ROS) that activates Akt and induces the expression of the anti-apoptotic protein B-cell lymphoma-extra large (Bcl-xL), therefore protecting cardiomyocytes from I/R-induced death. Furthermore, we extended these results to human cardiomyocytes (derived from induced pluripotent stem - IPS - cells). Importantly, we demonstrated that this protective signaling pathway induced by SEV could be stimulated using the antidiabetic agent metformin (MET), suggesting the preconditioning properties of MET. Altogether, our study identified a signaling pathway allowing APc of cardiac injuries as well as a rational for the use of MET as a pharmacological preconditioning agent to prevent I/R injuries.

Identifiants

pubmed: 33340237
doi: 10.1111/febs.15675
doi:

Substances chimiques

Hypoglycemic Agents 0
Reactive Oxygen Species 0
bcl-X Protein 0
Sevoflurane 38LVP0K73A
Metformin 9100L32L2N

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3547-3569

Informations de copyright

© 2020 Federation of European Biochemical Societies.

Références

Devereaux PJ & Szczeklik W (2019) Myocardial injury after non-cardiac surgery: diagnosis and management. Eur Heart J 41, 3083-3091.
Botto F, Alonso-Coello P, Chan MT, Villar JC, Xavier D, Srinathan S, Guyatt G, Cruz P, Graham M, Wang CY et al. (2014) Myocardial injury after noncardiac surgery: a large, international, prospective cohort study establishing diagnostic criteria, characteristics, predictors, and 30-day outcomes. Anesthesiology 120, 564-578.
Lienhart A, Auroy Y, Pequignot F, Benhamou D, Warszawski J, Bovet M & Jougla E (2006) Survey of anesthesia-related mortality in France. Anesthesiology 105, 1087-1097.
Eltzschig HK & Eckle T (2011) Ischemia and reperfusion-from mechanism to translation. Nat Med 17, 1391-1401.
Zweier JL, Flaherty JT & Weisfeldt ML (1987) Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84, 1404-1407.
Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417, 1-13.
McCully JD, Wakiyama H, Hsieh YJ, Jones M & Levitsky S (2004) Differential contribution of necrosis and apoptosis in myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 286, H1923-H1935.
Wu MY, Yiang GT, Liao WT, Tsai AP, Cheng YL, Cheng PW, Li CY & Li CJ (2018) Current mechanistic concepts in ischemia and reperfusion injury. Cell Physiol Biochem 46, 1650-1667.
Gottlieb RA (2011) Cell death pathways in acute ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther 16, 233-238.
Eefting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ & Doevendans PA (2004) Role of apoptosis in reperfusion injury. Cardiovasc Res 61, 414-426.
Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW et al. (2018) Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ 25, 486-541.
Imahashi K, Schneider MD, Steenbergen C & Murphy E (2004) Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ Res 95, 734-741.
Chen M, Won DJ, Krajewski S & Gottlieb RA (2002) Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 277, 29181-29186.
MacFarlane M, Merrison W, Bratton SB & Cohen GM (2002) Proteasome-mediated degradation of Smac during apoptosis: XIAP promotes Smac ubiquitination in vitro. J Biol Chem 277, 36611-36616.
Davidson SM, Adameova A, Barile L, Cabrera-Fuentes HA, Lazou A, Pagliaro P, Stenslokken KO, Garcia-Dorado D & Action E-CC (2020) Mitochondrial and mitochondrial-independent pathways of myocardial cell death during ischaemia and reperfusion injury. J Cell Mol Med 24, 3795-3806.
Andreadou I, Schulz R, Papapetropoulos A, Turan B, Ytrehus K, Ferdinandy P, Daiber A & Di Lisa F (2020) The role of mitochondrial reactive oxygen species, NO and H2 S in ischaemia/reperfusion injury and cardioprotection. J Cell Mol Med 24, 6510-6522.
Xia Z, Li H & Irwin MG (2016) Myocardial ischaemia reperfusion injury: the challenge of translating ischaemic and anaesthetic protection from animal models to humans. Br J Anaesth 117(Suppl 2), ii44-ii62.
Chouchani ET, Pell VR, James AM, Work LM, Saeb-Parsy K, Frezza C, Krieg T & Murphy MP (2016) A unifying mechanism for mitochondrial superoxide production during ischemia-reperfusion injury. Cell Metab 23, 254-263.
Pagel PS & Crystal GJ (2018) The discovery of myocardial preconditioning using volatile anesthetics: a history and contemporary clinical perspective. J Cardiothorac Vasc Anesth 32, 1112-1134.
Kevin LG, Novalija E, Riess ML, Camara AK, Rhodes SS & Stowe DF (2003) Sevoflurane exposure generates superoxide but leads to decreased superoxide during ischemia and reperfusion in isolated hearts. Anesth Analg 96, 949-955, table of contents.
Hirata N, Shim YH, Pravdic D, Lohr NL, Pratt PF Jr, Weihrauch D, Kersten JR, Warltier DC, Bosnjak ZJ & Bienengraeber M (2011) Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward versus reverse electron transport flow: implications for preconditioning. Anesthesiology 115, 531-540.
Hescheler J, Meyer R, Plant S, Krautwurst D, Rosenthal W & Schultz G (1991) Morphological, biochemical, and electrophysiological characterization of a clonal cell (H9c2) line from rat heart. Circ Res 69, 1476-1486.
Zitta K, Meybohm P, Bein B, Ohnesorge H, Steinfath M, Scholz J & Albrecht M (2010) Cytoprotective effects of the volatile anesthetic sevoflurane are highly dependent on timing and duration of sevoflurane conditioning: findings from a human, in-vitro hypoxia model. Eur J Pharmacol 645, 39-46.
van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, Willis SN, Scott CL, Day CL, Cory S et al. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399.
Colell A, Ricci JE, Tait S, Milasta S, Maurer U, Bouchier-Hayes L, Fitzgerald P, Guio-Carrion A, Waterhouse NJ, Li CW et al. (2007) GAPDH and autophagy preserve survival after apoptotic cytochrome C release in the absence of caspase activation. Cell 129, 983-997.
Lessene G, Czabotar PE, Sleebs BE, Zobel K, Lowes KN, Adams JM, Baell JB, Colman PM, Deshayes K, Fairbrother WJ et al. (2013) Structure-guided design of a selective BCL-X(L) inhibitor. Nat Chem Biol 9, 390-397.
Ogata Y & Takahashi M (2003) Bcl-xL as an antiapoptotic molecule for cardiomyocytes. Drug News Perspect 16, 446-452.
Lamberts RR, Onderwater G, Hamdani N, Vreden MJ, Steenhuisen J, Eringa EC, Loer SA, Stienen GJ & Bouwman RA (2009) Reactive oxygen species-induced stimulation of 5'AMP-activated protein kinase mediates sevoflurane-induced cardioprotection. Circulation 120, S10-S15.
Zhao J, Wang F, Zhang Y, Jiao L, Lau WB, Wang L, Liu B, Gao E, Koch WJ, Ma XL et al. (2013) Sevoflurane preconditioning attenuates myocardial ischemia/reperfusion injury via caveolin-3-dependent cyclooxygenase-2 inhibition. Circulation 128, S121-S129.
Collodet C, Foretz M, Deak M, Bultot L, Metairon S, Viollet B, Lefebvre G, Raymond F, Parisi A, Civiletto G et al. (2019) AMPK promotes induction of the tumor suppressor FLCN through activation of TFEB independently of mTOR. FASEB J 33, 12374-12391.
Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, Foretz M & Viollet B (2006) 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 26, 5336-5347.
Zhang J, Wang C, Yu S, Luo Z, Chen Y, Liu Q, Hua F, Xu G & Yu P (2014) Sevoflurane postconditioning protects rat hearts against ischemia-reperfusion injury via the activation of PI3K/AKT/mTOR signaling. Sci Rep 4, 7317.
Jacquin MA, Chiche J, Zunino B, Beneteau M, Meynet O, Pradelli LA, Marchetti S, Cornille A, Carles M & Ricci JE (2013) GAPDH binds to active Akt, leading to Bcl-xL increase and escape from caspase-independent cell death. Cell Death Differ 20, 1043-1054.
Lu Z, Yang H, Sutton MN, Yang M, Clarke CH, Liao WS & Bast RC Jr (2014) ARHI (DIRAS3) induces autophagy in ovarian cancer cells by downregulating the epidermal growth factor receptor, inhibiting PI3K and Ras/MAP signaling and activating the FOXo3a-mediated induction of Rab7. Cell Death Differ 21, 1275-1289.
Wang X, McCullough KD, Franke TF & Holbrook NJ (2000) Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 275, 14624-14631.
Song J, Liu Q, Tang H, Tao A, Wang H, Kao R & Rui T (2016) Activation of PI3Kgamma/Akt pathway increases cardiomyocyte HMGB1 expression in diabetic environment. Oncotarget 7, 80803-80810.
Pasupathy S, Tavella R, Grover S, Raman B, Procter NEK, Du YT, Mahadavan G, Stafford I, Heresztyn T, Holmes A et al. (2017) Early use of N-acetylcysteine with nitrate therapy in patients undergoing primary percutaneous coronary intervention for ST-segment-elevation myocardial infarction reduces myocardial infarct size (the NACIAM Trial [N-acetylcysteine in Acute Myocardial Infarction]). Circulation 136, 894-903.
Varjabedian L, Bourji M, Pourafkari L & Nader ND (2018) Cardioprotection by metformin: beneficial effects beyond glucose reduction. Am J Cardiovasc Drugs 18, 181-193.
Bost F, Decoux-Poullot AG, Tanti JF & Clavel S (2016) Energy disruptors: rising stars in anticancer therapy? Oncogenesis 5, e188.
Riess ML, Kevin LG, Camara AK, Heisner JS & Stowe DF (2004) Dual exposure to sevoflurane improves anesthetic preconditioning in intact hearts. Anesthesiology 100, 569-574.
De Hert SG, ten Broecke PW, Mertens E, Van Sommeren EW, De Blier IG, Stockman BA & Rodrigus IE (2002) Sevoflurane but not propofol preserves myocardial function in coronary surgery patients. Anesthesiology 97, 42-49.
Claroni C, Torregiani G, Covotta M, Sofra M, Scotto Di Uccio A, Marcelli ME, Naccarato A & Forastiere E (2016) Protective effect of sevoflurane preconditioning on ischemia-reperfusion injury in patients undergoing reconstructive plastic surgery with microsurgical flap, a randomized controlled trial. BMC Anesthesiol 16, 66.
Zhao ZQ & Vinten-Johansen J (2002) Myocardial apoptosis and ischemic preconditioning. Cardiovasc Res 55, 438-455.
Kroemer G, Galluzzi L & Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87, 99-163.
Gallogly MM, Shelton MD, Qanungo S, Pai HV, Starke DW, Hoppel CL, Lesnefsky EJ & Mieyal JJ (2010) Glutaredoxin regulates apoptosis in cardiomyocytes via NFkappaB targets Bcl-2 and Bcl-xL: implications for cardiac aging. Antioxid Redox Signal 12, 1339-1353.
Cao Y, Li H, Liu H, Zheng C, Ji H & Liu X (2010) The serine/threonine kinase LKB1 controls thymocyte survival through regulation of AMPK activation and Bcl-XL expression. Cell Res 20, 99-108.
Dimmeler S, Breitschopf K, Haendeler J & Zeiher AM (1999) Dephosphorylation targets Bcl-2 for ubiquitin-dependent degradation: a link between the apoptosome and the proteasome pathway. J Exp Med 189, 1815-1822.
Johansson JS, Zou H & Tanner JW (1999) Bound volatile general anesthetics alter both local protein dynamics and global protein stability. Anesthesiology 90, 235-245.
Matsuyama N, Leavens JE, McKinnon D, Gaudette GR, Aksehirli TO & Krukenkamp IB (2000) Ischemic but not pharmacological preconditioning requires protein synthesis. Circulation 102, III312-III318.
Bienengraeber M, Pellitteri-Hahn M, Hirata N, Baye TM, Bosnjak ZJ & Olivier M (2013) Quantitative characterization of changes in the cardiac mitochondrial proteome during anesthetic preconditioning and ischemia. Physiol Genomics 45, 163-170.
Sussman MA, Volkers M, Fischer K, Bailey B, Cottage CT, Din S, Gude N, Avitabile D, Alvarez R, Sundararaman B et al. (2011) Myocardial AKT: the omnipresent nexus. Physiol Rev 91, 1023-1070.
Rossello X & Yellon DM (2018) The RISK pathway and beyond. Basic Res Cardiol 113, 2.
Yu X, Mao W, Zhai Y, Tong C, Liu M, Ma L, Yu X & Li S (2017) Anti-tumor activity of metformin: from metabolic and epigenetic perspectives. Oncotarget 8, 5619-5628.
Rotermund C, Machetanz G & Fitzgerald JC (2018) The therapeutic potential of metformin in neurodegenerative diseases. Front Endocrinol 9, 400.
Fontaine E (2018) Metformin-induced mitochondrial complex I inhibition: facts, uncertainties, and consequences. Front Endocrinol 9, 753.
Zaugg M, Lucchinetti E, Behmanesh S & Clanachan AS (2014) Anesthetic cardioprotection in clinical practice from proof-of-concept to clinical applications. Curr Pharm Des 20, 5706-5726.
Reitz KM, Marroquin OC, Zenati MS, Kennedy J, Korytkowski M, Tzeng E, Koscum S, Newhouse D, Garcia RM, Vates J et al. (2020) Association between preoperative metformin exposure and postoperative outcomes in adults with type 2 diabetes. JAMA Surg 155, e200416.
Whittington HJ, Hall AR, McLaughlin CP, Hausenloy DJ, Yellon DM & Mocanu MM (2013) Chronic metformin associated cardioprotection against infarction: not just a glucose lowering phenomenon. Cardiovasc Drugs Ther 27, 5-16.
Techiryan G, Weil BR, Palka BA & Canty JM Jr (2018) Effect of intracoronary metformin on myocardial infarct size in swine. Circ Res 123, 986-995.
Mohsin AA, Chen Q, Quan N, Rousselle T, Maceyka MW, Samidurai A, Thompson J, Hu Y, Li J & Lesnefsky EJ (2019) Mitochondrial complex I inhibition by metformin limits reperfusion injury. J Pharmacol Exp Ther 369, 282-290.
Sauve M, Ban K, Momen MA, Zhou YQ, Henkelman RM, Husain M & Drucker DJ (2010) Genetic deletion or pharmacological inhibition of dipeptidyl peptidase-4 improves cardiovascular outcomes after myocardial infarction in mice. Diabetes 59, 1063-1073.
Lexis CP, van der Horst IC, Lipsic E, Wieringa WG, de Boer RA, van den Heuvel AF, van der Werf HW, Schurer RA, Pundziute G, Tan ES et al. (2014) Effect of metformin on left ventricular function after acute myocardial infarction in patients without diabetes: the GIPS-III randomized clinical trial. JAMA 311, 1526-1535.
El Messaoudi S, Nederlof R, Zuurbier CJ, van Swieten HA, Pickkers P, Noyez L, Dieker HJ, Coenen MJ, Donders AR, Vos A et al. (2015) Effect of metformin pretreatment on myocardial injury during coronary artery bypass surgery in patients without diabetes (MetCAB): a double-blind, randomised controlled trial. Lancet Diabetes Endocrinol 3, 615-623.
Lexis CP, Wieringa WG, Hiemstra B, van Deursen VM, Lipsic E, van der Harst P, van Veldhuisen DJ & van der Horst IC (2014) Chronic metformin treatment is associated with reduced myocardial infarct size in diabetic patients with ST-segment elevation myocardial infarction. Cardiovasc Drugs Ther 28, 163-171.
Chiari P, Durand M, Desebbe O, Fischer MO, Lena-Quintard D, Palao JC, Mercier C, Samson G, Varillon Y, Pozzi M et al. (2019) Multimodal cardioprotective strategy in cardiac surgery (the ProCCard trial): Study protocol for a multicenter randomized controlled trial. Trials 20, 560.
Branco AF, Pereira SP, Gonzalez S, Gusev O, Rizvanov AA & Oliveira PJ (2015) Gene expression profiling of H9c2 myoblast differentiation towards a cardiac-like phenotype. PLoS One 10, e0129303.
Genin EC, Madji Hounoum B, Bannwarth S, Fragaki K, Lacas-Gervais S, Mauri-Crouzet A, Lespinasse F, Neveu J, Ropert B, Auge G et al. (2019) Mitochondrial defect in muscle precedes neuromuscular junction degeneration and motor neuron death in CHCHD10(S59L/+) mouse. Acta Neuropathol 138, 123-145.
Lian X, Zhang J, Azarin SM, Zhu K, Hazeltine LB, Bao X, Hsiao C, Kamp TJ & Palecek SP (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions. Nat Protoc 8, 162-175.
Ronnback A, Dahlqvist P, Bergstrom SA & Olsson T (2005) Diurnal effects of enriched environment on immediate early gene expression in the rat brain. Brain Res 1046, 137-144.

Auteurs

Romain Rozier (R)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Rachel Paul (R)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Blandine Madji Hounoum (B)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Elodie Villa (E)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Rana Mhaidly (R)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Johanna Chiche (J)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Els Verhoeyen (E)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Sandrine Marchetti (S)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Ashaina Vandenberghe (A)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Marc Raucoules (M)

Anesthésie Réanimation, Centre Hospitalier Universitaire, Nice, France.

Michel Carles (M)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.
Anesthésie Réanimation, Centre Hospitalier Universitaire, Nice, France.
Réanimation, Faculté des Antilles, Centre Hospitalier Universitaire, Guadeloupe, France.

Jean-Ehrland Ricci (JE)

INSERM, C3M, Université Côte d'Azur, Nice, France.
Equipe labellisée Ligue Contre le Cancer, Nice, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH