Glucagon-like peptide-1 receptor agonist treatment of high carbohydrate intake-induced metabolic syndrome provides pleiotropic effects on cardiac dysfunction through alleviations in electrical and intracellular Ca
arrhythmia
electrical activity
insulin resistance
ion-homeostasis
sodium-calcium exchanger
Journal
Clinical and experimental pharmacology & physiology
ISSN: 1440-1681
Titre abrégé: Clin Exp Pharmacol Physiol
Pays: Australia
ID NLM: 0425076
Informations de publication
Date de publication:
01 2022
01 2022
Historique:
revised:
07
09
2021
received:
08
07
2021
accepted:
10
09
2021
pubmed:
15
9
2021
medline:
30
3
2022
entrez:
14
9
2021
Statut:
ppublish
Résumé
The pleiotropic effects of glucagon-like peptide-1 receptor (GLP-1R) agonists on the heart have been recognised in obese or diabetic patients. However, little is known regarding the molecular mechanisms of these agonists in cardioprotective actions under metabolic disturbances. We evaluated the effects of GLP-1R agonist liraglutide treatment on left ventricular cardiomyocytes from high-carbohydrate induced metabolic syndrome rats (MetS rats), characterised with insulin resistance and cardiac dysfunction with a long-QT. Liraglutide (0.3 mg/kg for 4 weeks) treatment of MetS rats significantly reversed long-QT, through a shortening the prolonged action potential duration and recovering inhibited K
Identifiants
pubmed: 34519087
doi: 10.1111/1440-1681.13590
doi:
Substances chimiques
Dietary Carbohydrates
0
Glucagon-Like Peptide-1 Receptor
0
Liraglutide
839I73S42A
Glucose
IY9XDZ35W2
Calcium
SY7Q814VUP
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
46-59Subventions
Organisme : The Scientific and Technological Research Council of Turkey
ID : SBAG216S979
Informations de copyright
© 2021 John Wiley & Sons Australia, Ltd.
Références
Muller TD, Finan B, Bloom SR, et al. Glucagon-like peptide 1 (GLP-1). Mol Metab. 2019;30:72-130.
Chen J, Wang D, Wang F, et al. Exendin-4 inhibits structural remodeling and improves Ca(2+) homeostasis in rats with heart failure via the GLP-1 receptor through the eNOS/cGMP/PKG pathway. Peptides. 2017;90:69-77.
Nauck MA, Meier JJ, Cavender MA, Abd El Aziz M, Drucker DJ. Cardiovascular actions and clinical outcomes with glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors. Circulation. 2017;136(9):849-870.
Yamaoka-Tojo M, Tojo T, Takahira N, et al. Elevated circulating levels of an incretin hormone, glucagon-like peptide-1, are associated with metabolic components in high-risk patients with cardiovascular disease. Cardiovasc Diabetol. 2010;9:17.
Bahtiyar G, Pujals-Kury J, Sacerdote A. Cardiovascular effects of different GLP-1 receptor agonists in patients with type 2 diabetes. Curr Diab Rep. 2018;18(10):92.
Zhang L, Tian J, Diao S, Zhang G, Xiao M, Chang D. GLP-1 receptor agonist liraglutide protects cardiomyocytes from IL-1beta-induced metabolic disturbance and mitochondrial dysfunction. Chem Biol Interact. 2020;332:109252.
Huang JH, Chen YC, Lee TI, et al. Glucagon-like peptide-1 regulates calcium homeostasis and electrophysiological activities of HL-1 cardiomyocytes. Peptides. 2016;78:91-98.
Ang R, Mastitskaya S, Hosford PS, et al. Modulation of cardiac ventricular excitability by GLP-1 (glucagon-like peptide-1). Circ Arrhythm Electrophysiol. 2018;11(10):e006740.
Bai XJ, Hao JT, Zheng RH, et al. Glucagon-like peptide-1 analog liraglutide attenuates pressure-overload induced cardiac hypertrophy and apoptosis through activating ATP sensitive potassium channels. Cardiovasc Drugs Ther. 2021;35(1):87-101.
Marso SP, Daniels GH, Brown-Frandsen K, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375(4):311-322.
Du Q, Wang YJ, Yang S, Zhao YY, Han P. Liraglutide for the treatment of type 2 diabetes mellitus: a meta-analysis of randomized placebo-controlled trials. Adv Ther. 2014;31(11):1182-1195.
Tougaard RS, Jorsal A, Tarnow L, et al. Heart rate increases in liraglutide treated chronic heart failure patients: association with clinical parameters and adverse events. Scand Cardiovasc J. 2020;54(5):294-299.
Bizino MB, Jazet IM, Westenberg JJM, et al. Effect of liraglutide on cardiac function in patients with type 2 diabetes mellitus: randomized placebo-controlled trial. Cardiovasc Diabetol. 2019;18(1):55.
Chen WR, Shen XQ, Zhang Y, et al. Effects of liraglutide on left ventricular function in patients with non-ST-segment elevation myocardial infarction. Endocrine. 2016;52(3):516-526.
Jorsal A, Kistorp C, Holmager P, et al. Effect of liraglutide, a glucagon-like peptide-1 analogue, on left ventricular function in stable chronic heart failure patients with and without diabetes (LIVE)-a multicentre, double-blind, randomised, placebo-controlled trial. Eur J Heart Fail. 2017;19(1):69-77.
Shiraki A, Oyama JI, Nishikido T, Node K. GLP-1 analog liraglutide-induced cardiac dysfunction due to energetic starvation in heart failure with non-diabetic dilated cardiomyopathy. Cardiovasc Diabetol. 2019;18(1):164.
Xiong QF, Fan SH, Li XW, et al. GLP-1 relaxes rat coronary arteries by enhancing ATP-sensitive potassium channel currents. Cardiol Res Pract. 2019;2019:1968785.
Li PC, Liu LF, Jou MJ, Wang HK. The GLP-1 receptor agonists exendin-4 and liraglutide alleviate oxidative stress and cognitive and micturition deficits induced by middle cerebral artery occlusion in diabetic mice. BMC Neurosci. 2016;17(1):37.
Zheng RH, Bai XJ, Zhang WW, et al. Liraglutide attenuates cardiac remodeling and improves heart function after abdominal aortic constriction through blocking angiotensin II type 1 receptor in rats. Drug Des Devel Ther. 2019;13:2745-2757.
Luconi M, Cantini G, Ceriello A, Mannucci E. Perspectives on cardiovascular effects of incretin-based drugs: from bedside to bench, return trip. Int J Cardiol. 2017;241:302-310.
FDA. FDA approves weight management drug for patients. 2020. aged 12 and older 2020.
Mells JE, Fu PP, Sharma S, et al. Glp-1 analog, liraglutide, ameliorates hepatic steatosis and cardiac hypertrophy in C57BL/6J mice fed a Western diet. Am J Physiol Gastrointest Liver Physiol. 2012;302(2):G225-G235.
Chang G, Liu J, Qin S, et al. Cardioprotection by exenatide: a novel mechanism via improving mitochondrial function involving the GLP-1 receptor/cAMP/PKA pathway. Int J Mol Med. 2018;41(3):1693-1703.
Lambadiari V, Pavlidis G, Kousathana F, et al. Effects of 6-month treatment with the glucagon like peptide-1 analogue liraglutide on arterial stiffness, left ventricular myocardial deformation and oxidative stress in subjects with newly diagnosed type 2 diabetes. Cardiovasc Diabetol. 2018;17(1):8.
Margulies KB, Hernandez AF, Redfield MM, et al. Effects of liraglutide on clinical stability among patients with advanced heart failure and reduced ejection fraction: a randomized clinical trial. JAMA. 2016;316(5):500-508.
Saponaro F, Sonaglioni A, Rossi A, et al. Improved diastolic function in type 2 diabetes after a six month liraglutide treatment. Diabetes Res Clin Pract. 2016;118:21-28.
Abel ED, Litwin SE, Sweeney G. Cardiac remodeling in obesity. Physiol Rev. 2008;88(2):389-419.
Durak A, Olgar Y, Tuncay E, et al. Onset of decreased heart work is correlated with increased heart rate and shortened QT interval in high-carbohydrate fed overweight rats. Can J Physiol Pharmacol. 2017;95(11):1335-1342.
Durak A, Olgar Y, Degirmenci S, Akkus E, Tuncay E, Turan B. A SGLT2 inhibitor dapagliflozin suppresses prolonged ventricular-repolarization through augmentation of mitochondrial function in insulin-resistant metabolic syndrome rats. Cardiovasc Diabetol. 2018;17(1):1-17.
Marx SO, Reiken S, Hisamatsu Y, et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell. 2000;101(4):365-376.
Wehrens XH, Lehnart SE, Reiken S, Vest JA, Wronska A, Marks AR. Ryanodine receptor/calcium release channel PKA phosphorylation: a critical mediator of heart failure progression. Proc Natl Acad Sci USA. 2006;103(3):511-518.
Khan R, Tomas A, Rutter GA. Effects on pancreatic beta and other Islet cells of the glucose-dependent insulinotropic polypeptide. Peptides. 2020;125:170201.
Yu W, Zha W, Ren J. Exendin-4 and liraglutide attenuate glucose toxicity-induced cardiac injury through mTOR/ULK1-dependent autophagy. Oxid Med Cell Longev. 2018;2018:5396806.
McCormick LM, Heck PM, Ring LS, et al. Glucagon-like peptide-1 protects against ischemic left ventricular dysfunction during hyperglycemia in patients with coronary artery disease and type 2 diabetes mellitus. Cardiovasc Diabetol. 2015;14:102.
Dineen SL, McKenney ML, Bell LN, et al. Metabolic syndrome abolishes glucagon-like peptide 1 receptor agonist stimulation of SERCA in coronary smooth muscle. Diabetes. 2015;64(9):3321-3327.
Bao W, Holt LJ, Prince RD, et al. Novel fusion of GLP-1 with a domain antibody to serum albumin prolongs protection against myocardial ischemia/reperfusion injury in the rat. Cardiovasc Diabetol. 2013;12:148.
MacDonald PE, Salapatek AMF, Wheeler MB. Glucagon-Like Peptide-1 Receptor Activation Antagonizes Voltage-Dependent Repolarizing K+ Currents in -Cells: A Possible Glucose-Dependent Insulinotropic Mechanism. Diabetes. 2002;51(Supplement 3):S443-S447. http://dx.doi.org/10.2337/diabetes.51.2007.s443
Gaisano GG, Park SJ, Daly DM, Beyak MJ. Glucagon-like peptide-1 inhibits voltage-gated potassium currents in mouse nodose ganglion neurons. Neurogastroenterol Motil. 2010;22(4):470-479, e111.
Gill A, Hoogwerf BJ, Burger J, et al. Effect of exenatide on heart rate and blood pressure in subjects with type 2 diabetes mellitus: a double-blind, placebo-controlled, randomized pilot study. Cardiovasc Diabetol. 2010;9:6.
Kristensen J, Mortensen UM, Schmidt M, Nielsen PH, Nielsen TT, Maeng M. Lack of cardioprotection from subcutaneously and preischemic administered liraglutide in a closed chest porcine ischemia reperfusion model. BMC Cardiovasc Disord. 2009;9:31.
Yaras N, Ugur M, Ozdemir S, et al. Effects of Diabetes on Ryanodine Receptor Ca Release Channel (RyR2) and Ca2+ Homeostasis in Rat Heart. Diabetes. 2005;54(11):3082-3088. http://dx.doi.org/10.2337/diabetes.54.11.3082
Tuncay E, Bitirim VC, Durak A, et al. Hyperglycemia-induced changes in ZIP7 and ZnT7 expression cause Zn(2+) release from the sarco(endo)plasmic reticulum and mediate ER stress in the heart. Diabetes. 2017;66(5):1346-1358.
Bovo E, Huke S, Blatter LA, Zima AV. The effect of PKA-mediated phosphorylation of ryanodine receptor on SR Ca(2+) leak in ventricular myocytes. J Mol Cell Cardiol. 2017;104:9-16.
Ly LD, Xu S, Choi SK, et al. Oxidative stress and calcium dysregulation by palmitate in type 2 diabetes. Exp Mol Med. 2017;49(2):e291.
Potenza DM, Janicek R, Fernandez-Tenorio M, et al. Phosphorylation of the ryanodine receptor 2 at serine 2030 is required for a complete beta-adrenergic response. J Gen Physiol. 2019;151(2):131-145.
Burgos-Moron E, Abad-Jimenez Z, Maranon AM, et al. Relationship between oxidative stress, er stress, and inflammation in type 2 diabetes: the battle continues. J Clin Med. 2019;8(9):1385.
Yan LJ. Positive oxidative stress in aging and aging-related disease tolerance. Redox Biol. 2014;2:165-169.
Busik JV, Mohr S, Grant MB. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes. 2008;57(7):1952-1965.
Gorlach A, Bertram K, Hudecova S, Krizanova O. Calcium and ROS: a mutual interplay. Redox Biol. 2015;6:260-271.
Contreras-Ferrat A, Lavandero S, Jaimovich E, Klip A. Calcium signaling in insulin action on striated muscle. Cell Calcium. 2014;56(5):390-396.
Rowlands J, Heng J, Newsholme P, Carlessi R. Pleiotropic effects of GLP-1 and analogs on cell signaling, metabolism, and function. Front Endocrinol. 2018;9:672.
Skov J, Holst JJ, Gotze JP, Frokiaer J, Christiansen JS. Glucagon-like peptide-1: effect on pro-atrial natriuretic peptide in healthy males. Endocr Connect. 2014;3(1):11-16.
Kim M, Platt MJ, Shibasaki T, et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nat Med. 2013;19(5):567-575.
Rudovich N, Pivovarova O, Gögebakan Ö, et al. Effect of Exogenous Intravenous Administrations of GLP-1 and/or GIP on Circulating Pro-Atrial Natriuretic Peptide in Subjects With Different Stages of Glucose Tolerance: Figure 1. Diabetes Care. 2015;38(1):e7-e8. http://dx.doi.org/10.2337/dc14-1452
Ussher JR, Baggio LL, Campbell JE, et al. Inactivation of the cardiomyocyte glucagon-like peptide-1 receptor (GLP-1R) unmasks cardiomyocyte-independent GLP-1R-mediated cardioprotection. Mol Metab. 2014;3(5):507-517.
Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, Husain M. Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptor-dependent and -independent pathways. Circulation. 2008;117(18):2340-2350.
Noyan-Ashraf MH, Shikatani EA, Schuiki I, et al. A glucagon-like peptide-1 analog reverses the molecular pathology and cardiac dysfunction of a mouse model of obesity. Circulation. 2013;127(1):74-85.
Nikolaidis LA, Doverspike A, Hentosz T, et al. Glucagon-like peptide-1 limits myocardial stunning following brief coronary occlusion and reperfusion in conscious canines. J Pharmacol Exp Ther. 2005;312(1):303-308.
Nikolaidis LA, Elahi D, Hentosz T, et al. Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation. 2004;110(8):955-961.
Durak A, Bitirim CV, Turan B. Titin and CK2alpha are new intracellular targets in acute insulin application-associated benefits on electrophysiological parameters of left ventricular cardiomyocytes from insulin-resistant metabolic syndrome rats. Cardiovasc Drugs Ther. 2020;34(4):487-501.
Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC-delta activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab. 2003;285(2):E295-E302.
Dincer D, Besisik F, Sahin E, et al. Intestinal metaplasia of the gastric cardia: a study from Turkey. Hepatogastroenterology. 2002;49(46):1153-1156.
Okatan EN, Tuncay E, Hafez G, Turan B. Profiling of cardiac beta-adrenoceptor subtypes in the cardiac left ventricle of rats with metabolic syndrome: comparison with streptozotocin-induced diabetic rats. Can J Physiol Pharmacol. 2015;93(7):517-525.
Wang D, Luo P, Wang Y, et al. Glucagon-like peptide-1 protects against cardiac microvascular injury in diabetes via a cAMP/PKA/Rho-dependent mechanism. Diabetes. 2013;62(5):1697-1708.
Yi B, Hu X, Wen Z, Zhang T, Cai Y. Exendin-4, a glucagon-like peptide-1 receptor agonist, inhibits hyperglycemia-induced apoptosis in myocytes by suppressing receptor for advanced glycation end products expression. Exp Ther Med. 2014;8(4):1185-1190.
Tsuboi T, da Silva XG, Holz GG, Jouaville LS, Thomas AP, Rutter GA. Glucagon-like peptide-1 mobilizes intracellular Ca2+ and stimulates mitochondrial ATP synthesis in pancreatic MIN6 beta-cells. Biochem J. 2003;369(Pt 2):287-299.
Monji A, Mitsui T, Bando YK, Aoyama M, Shigeta T, Murohara T. Glucagon-like peptide-1 receptor activation reverses cardiac remodeling via normalizing cardiac steatosis and oxidative stress in type 2 diabetes. Am J Physiol Heart Circ Physiol. 2013;305(3):H295-H304.
Al Kury LT. Calcium homeostasis in ventricular myocytes of diabetic cardiomyopathy. J Diabetes Res. 2020;2020:1942086.
Hu SY, Zhang Y, Zhu PJ, Zhou H, Chen YD. Liraglutide directly protects cardiomyocytes against reperfusion injury possibly via modulation of intracellular calcium homeostasis. J Geriatr Cardiol. 2017;14(1):57-66.
Riedel MJ, Baczkó I, Searle GJ, et al. Metabolic regulation of sodium-calcium exchange by intracellular acyl CoAs. EMBO J. 2006;25(19):4605-4614. http://dx.doi.org/10.1038/sj.emboj.7601321
Ricci E, Smallwood S, Chouabe C, et al. Electrophysiological characterization of left ventricular myocytes from obese Sprague-Dawley rat. Obesity. 2006;14(5):778-786.
Ashrafi R, Modi P, Oo AY, et al. Arrhythmogenic gene remodelling in elderly patients with type 2 diabetes with aortic stenosis and normal left ventricular ejection fraction. Exp Physiol. 2017;102(11):1424-1434.
Jeon JY, Choi SE, Ha ES, et al. GLP1 improves palmitateinduced insulin resistance in human skeletal muscle via SIRT1 activity. Int J Mol Med. 2019;44(3):1161-1171.
Andreozzi F, Raciti GA, Nigro C, et al. The GLP-1 receptor agonists exenatide and liraglutide activate glucose transport by an AMPK-dependent mechanism. J Transl Med. 2016;14(1):229.
Wittenberg BA, White RL, Ginzberg RD, Spray DC. Effect of calcium on the dissociation of the mature rat heart into individual and paired myocytes: electrical properties of cell pairs. Circ Res. 1986;59(2):143-150.
Turan B, Desilets M, Acan LN, Hotomaroglu O, Vannier C, Vassort G. Oxidative effects of selenite on rat ventricular contractility and Ca movements. Cardiovasc Res. 1996;32(2):351-361.
Ozdemir S, Bito V, Holemans P, et al. Pharmacological inhibition of na/ca exchange results in increased cellular Ca2+ load attributable to the predominance of forward mode block. Circ Res. 2008;102(11):1398-1405.
Okatan EN, Durak AT, Turan B. Electrophysiological basis of metabolic-syndrome-induced cardiac dysfunction. Can J Physiol Pharmacol. 2016;94(10):1064-1073.