Cardioprotection resulting from glucagon-like peptide-1 administration involves shifting metabolic substrate utilization to increase energy efficiency in the rat heart

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Aravindhan, Karpagam ^a   Bao, Weike ^a   Harpel, Mark R ^a   Willette, Robert N ^a   Lepore, John J ^a   Jucker, Beat M ^a  

^a GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; GLYCOGEN; CARBON; CARDIOTONIC AGENT; FATTY ACID; GLUCOSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY ACID METABOLISM; GLUCOSE CLAMP TECHNIQUE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HEART HEMODYNAMICS; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION; RAT; REPERFUSION INJURY; TISSUE OXYGENATION; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGEN CONSUMPTION; PH; PHYSIOLOGY;

RATTUS;

ANIMALS; CARBON ISOTOPES; CARDIOTONIC AGENTS; CYCLIC AMP; ENERGY METABOLISM; FATTY ACIDS; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MYOCARDIUM; MYOCYTES, CARDIAC; OXYGEN CONSUMPTION; RATS; REPERFUSION INJURY;

EID: 84939540746     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130894     Document Type: Article

References (44)

1. Bose AK, Mocanu MM, Carr RD, Brand CL, Yellon DM. (2005) Glucagon-like peptide 1 can directly protect the heart against ischemia/reperfusion injury. Diabetes. 54:146-151. PMID: 15616022
2. Hausenloy DJ, Yellon DM. (2008) GLP-1 therapy beyond glucose control. Circ Heart Fail. 1: 147-149. doi: 10.1161/CIRCHEARTFAILURE.108.810887 PMID: 19808284
3. Nikolaidis LA, Mankad S, Sokos GG, Miske G, Shah A, Elahi D, et al. (2004) Effects of glucagon-like peptide-1 in patients with acute myocardial infarction and left ventricular dysfunction after successful reperfusion. Circulation. 109: 962-965. PMID: 14981009
4. Sokos GG, Nikolaidi LA, Mankad S, Elahi D, Shannon RP. (2006) Glucagon-like peptide-1 infusion improves left ventricular ejection fraction and functional status in patients with chronic heart failure. J. Card. Fail. 12:694-699. PMID: 17174230
5. Sokos GG, Bolukoglu H, German J, Hentosz T, Magovern GJ Jr, Maher TD, et al. (2007) Effect of glucagon-like peptide-1 (GLP-1) on glycemic control and left ventricular function in patients undergoing coronary artery bypass grafting. Am. J. Cardiol. 100: 824-829. PMID: 17719327
6. Nikolaidis LA, Elahi D, Hentosz T, Doverspike A, Huerbin R, Zourelias L, et al. (2004) Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation. 110:955-961. PMID: 15313949
7. Nikolaidis LA, Doverspike A, Hentosz T, Zourelias L, Shen YT, Elahi D, et al. (2005) Glucagon-like peptide-1 limits myocardial stunning following brief coronary occlusion and reperfusion in conscious canines. J. Pharmacol. Exp. Ther. 312:303-308. PMID: 15356213
8. Bose AK, Mocanu MM, Carr RD, Yellon DM. (2005) Glucagon like peptide-1 is protective against myocardial ischemia/reperfusion injury when given either as a preconditioning mimetic or at reperfusion in an isolated rat heart model. Cardiovasc. Drugs Ther. 19:9-11. PMID: 15883751
9. Bao W, Aravindhan A, Alsaid H, Chendrimada T, Szapacs M, Citerone DR, et al. (2011) Albiglutide, a long lasting glucagon-like peptide-1 analog, protects the rat heart against ischemia/reperfusion injury: evidence for improving cardiac metabolic efficiency. PLoS One. 6:e23570. doi: 10.1371/journal.pone. 0023570 PMID: 21887274
10. Bao W, Holt LJ, Prince RD, Jones GX, Aravindhan K, Szapacs M, et al. (2013) Novel fusion of GLP-1 with a domain antibody to serum albumin prolongs protection against myocardial ischemia/reperfusion injury in the rat. Cardiovasc. Diabetol. 12:148. doi: 10.1186/1475-2840-12-148 PMID: 24125539
11. Chang G, Zhang D, Yu H, Zhang P, Wang Y, Zheng A, et al. (2013) Cardioprotective effect of exenatide against oxidative stress-induced injury. Int. J. Mol. Med. 32:1011-20. doi: 10.3892/ijmm.2013.1475 PMID: 23982489
12. Noyan-Ashraf MH, Momen MA, Ban K, Sadi AM, Zhou YQ, Riazi AM, et al. (2009) GLP-1R agonist liraglutide activates cytoprotective pathways and improves outcomes after experimental myocardial infarction in mice. Diabetes. 58:975-983. doi: 10.2337/db08-1193 PMID: 19151200
13. Bose AK., Mocanu MM, Carr RD, Yellon DM. (2007) Myocardial ischaemia-reperfusion injury is attenuated by intact glucagon like peptide-1 (GLP-1) in the in vitro rat heart and may involve the p70s6K pathway. Cardiovasc. Drugs Ther. 21:253-256. PMID: 17541736
14. Nguyen TD, Doenst T. (2009) Letter by Nguyen and Doenst regarding article "Chronic glucagon-like peptide-1 infusion sustains left ventricular systolic function and prolongs survival in the spontaneously hypertensive, heart-failure prone rat". Circ. Heart Fail. 2:e1. doi: 10.1161/CIRCHEARTFAILURE.108.832162 PMID: 19808332
15. Poornima I, Brown SB, Bhashyam S, Parikh P, Bolukoglu H, Shannon RP. (2008) Chronic glucagonlike peptide-1 infusion sustains left ventricular systolic function and prolongs survival in the spontaneously hypertensive, heart failure-prone rat. Circ. Heart Fail. 1:153-160. doi: 10.1161/CIRCHEARTFAILURE.108.766402 PMID: 19727407
16. Grieve DJ, Cassidy RS, Green BD. (2009) Emerging cardiovascular actions of the incretin hormone glucagon-like peptide-1: potential therapeutic benefits beyond glycaemic control. Br. J. Pharmacol. 157:1340-1351. doi: 10.1111/j.1476-5381.2009.00376.x PMID: 19681866
17. Neubauer S. (2007) The failing heart-an engine out of fuel. N. Engl. J. Med. 356:1140-1151. PMID: 17360992
18. Zhao T, Parikh P, Bhashyam S, Bolukoglu H, Poornima I, Shen YT, et al. (2006) Direct effects of glucagon-like peptide-1 on myocardial contractility and glucose uptake in normal and postischemic isolated rat hearts. J. Pharmacol. Exp. Ther. 317:1106-1113. PMID: 16489128
19. Huisamen B, Genade S, Lochner A. (2008) Signalling pathways activated by glucagon-like peptide-1 (7-36) amide in the rat heart and their role in protection against ischaemia. Cardiovasc. J. Afr. 19:77-83. PMID: 18516352
20. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, Husain M. (2008) Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptor-dependent and-independent pathways. Circulation 117:2340-2350. doi: 10.1161/CIRCULATIONAHA.107.739938 PMID: 18427132
21. Bhashyam S, Fields AV, Patterson B, Testani JM, Chen L, Shen YT, et al. (2010) Glucagon-like peptide-1 increases myocardial glucose uptake via p38alpha MAP kinase-mediated, nitric oxide-dependent mechanisms in conscious dogs with dilated cardiomyopathy. Circ. Heart Fail. 3:512-521. doi: 10.1161/CIRCHEARTFAILURE.109.900282 PMID: 20466848
22. Bao W, Hu E, Tao L, Boyce R, Mirabile R., Thudium, et al. (2004) Inhibition of Rho-kinase protects the heart against ischemia/reperfusion injury. Cardiovasc. Res. 61:548-558. PMID: 14962485
23. Yue TL, Nerurkar SS, Bao W, Jucker BM, Sarov-Blat L, Steplewski K, et al. (2008) In vivo activation of peroxisome proliferator-activated receptor-delta protects the heart from ischemia/reperfusion injury in Zucker fatty rats. J. Pharmacol. Exp. Ther. 325:466-474. doi: 10.1124/jpet.107.135327 PMID: 18287212
24. Wetter TJ, Gazdag AC, Dean DJ, Cartee GD. (1999) Effect of calorie restriction on in vivo glucose metabolism by individual tissues in rats. Am. J. Physiol. 276:E728-E738. PMID: 10198310
25. Kraegen EW, James DE, Jenkins AB, Chisholm DJ. (1985). Dose-response curves for in vivo insulin sensitivity in individual tissues in rats. Am. J. Physiol. 248:E353-E362. PMID: 3883806
26. Jucker BM, Rennings AJ, Cline GW, Petersen KF, Shulman GI. (1997) In vivo NMR investigation of intramuscular glucose metabolism in conscious rats. Am. J. Physiol. 273: E139-E148. PMID: 9252490
27. Jucker BM, Rennings AJ, Cline GW, Shulman GI. (1997) 13C and 31P NMR studies on the effects of increased plasma free fatty acids on intramuscular glucose metabolism in the awake rat. J. Biol. Chem. 272:10464-10473.
28. Willette RN, Bao W, Nerurkar S, Yue TL, Doe CP, Stankus G, et al. (2008) Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse. Part 2. J. Pharmacol. Exp.Ther. 326:443-452. doi: 10.1124/jpet.107.134551 PMID: 18499744
29. Perrone CE, Mattocks DA, Hristopoulos G, Plummer JD, Krajcik RA, Orentreich N. (2008) Methionine restriction effects on 11-HSD1 activity and lipogenic/lipolytic balance in F344 rat adipose tissue. J. Lipid Res. 49:12-23.
30. Bloch G, Chase JR, Meyer DB, Avison MJ, Shulman GI, Shulman RG. (1994) In vivo regulation of rat muscle glycogen resynthesis after intense exercise. Am. J. Physiol. 266:E85-E91.
31. Snabaitism AK, Muntendrof A, Thomas Wielan T, Avkiran M. (2005) Regulation of the extracellular signal-regulated kinse pathway in adult myocardium: differential roles of Gg/11, Gi and G12/13 proteins in signalling by i-adrenergic, endothelin-1 and thrombin-sensitive protease-activated receptors. Cellular signalling. 17:655-664. PMID: 15683740
32. Dranka BP, Hill BG, Hurley-Usmar VM. (2010) Mitochondrial reserve capacity in endothelial cells: The impact of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 48:905-914. doi: 10.1016/j.freeradbiomed.2010.01.015 PMID: 20093177
33. Parkes DG, Pittner R, Jodka C, Smith P, Young A. (2001) Insulinotropic actions of exendin-4 and glucagon-like peptide-1 in vivo. Metabolism. 50:583-589. PMID: 11319721
34. Depre C, Vanoverschelde J-LJ, Taegtmeyer H. (1999) Glucose for the heart. Circulation 99:578-588. PMID: 9927407
35. Ferrick DA, Neilson A, Beeson C. (2008) Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov. Today. 13:268-274. doi: 10.1016/j.drudis.2007.12.008 PMID: 18342804
36. Liu Q, Anderson C, Broyde A, Polizzi C, Fernandez R, Baron A, et al. (2010) Glucagon-like peptide-1 and the exenatide analogue AC3174 improve cardiac function, cardiac remodeling, and survival in rats with chronic heart failure Cardiovascular. Diabetology 9:76.
37. Jia G, Yun-fei B, Li W, Hui-yu Y, Chuan-shi X. (2012) Effects of glucagon-like peptide-1 on myocardial ischemia-reperfusion/hypoxia-reoxygenation injury in rats. Chin. J. Pathophysiol. 28:858-864.
38. Nguyen TD, Shingu Y, Amorim PA, Schwarzer M, Doenst T. (2013) Glucagon-like peptide-1 reduces contractile function and fails to boost glucose utilization in normal hearts in the presence of fatty acids. See comment in PubMed Commons belowInt J Cardiol. 168:4085-92. doi: 10.1016/j.ijcard.2013.07.018 PMID: 23890859
39. Balteau M, Van Steenbergen A, Timmermans AD, Dessy C, Behets-Wydemans G, Tajeddine N, et al. (2014) AMPK activation by glucagon-like peptide-1 prevents NADPH oxidase activation induced by hyperglycemia in adult cardiomyocytes. Am J Physiol Heart Circ Physiol. 307(8):H1120-33. doi: 10.1152/ajpheart.00210.2014 PMID: 25128166
40. Abozguia K, Clarke K, Lee L, Frenneaux M. (2006) Modification of myocardial substrate use as a therapy for heart failure. Nat Clin Pract Cardiovasc Med. 3:490-498. PMID: 16932766
41. Tomas E, Habener JF. (2010) Insulin-like actions of glucagon-like peptide-1: a dual receptor hypothesis. Trends Endocrinol Metab. 21:59-67. doi: 10.1016/j.tem.2009.11.007 PMID: 20018525
42. Park TS, Yamashita H, Blaner WS, Goldberg IJ. (2007) Lipids in the heart: a source of fuel and a source of toxins. Curr. Opin. Lipidol. 18:277-282. PMID: 17495601
43. Hue L, Taegtmeyer H. (2009) The Randle cycle revisited: a new head for an old hat. Am J Physiol Endocrinol Metab. 297: E578-E591.
44. Ravassa S, Zudaire A, Díez J. (2012) GLP-1 and cardioprotection: from bench to bedside. Cardiovasc. Res. 94:316-323. doi: 10.1093/cvr/cvs123 PMID: 22419668