Exenatide exerts a PKA-dependent positive inotropic effect in human atrial myocardium: GLP-1R mediated effects in human myocardium

Journal of Molecular and Cellular Cardiology

Volumn 89, Issue , 2015, Pages 365-375

  Wallner, Markus ^a   Kolesnik, Ewald ^a   Ablasser, Klemens ^a   Khafaga, Mounir ^a,b   Wakula, Paulina ^c   Ljubojevic, Senka ^a   Thon Gutschi, Eva Maria ^a   Sourij, Harald ^a   Kapl, Martin ^a   Edmunds, Nicholas J ^d   Kuzmiski, J Brent ^d   Griffith, David A ^d   Knez, Igor ^a   Pieske, Burkert ^a,c   Von Lewinski, Dirk ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d PFIZER INC   (United States)

Author keywords

Diabetes mellitus; GLP 1; Inotropic agents; Myocardial contraction; Signal transduction

Indexed keywords

BETA ARRESTIN; CAMP ACTIVATED GUANINE NUCLEOTIDE EXCHANGE FACTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; GLUCAGON LIKE PEPTIDE 1 [7-36] AMIDE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 4; GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CARDIOTONIC AGENT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PEPTIDE; RAPGEF4 PROTEIN, HUMAN; VENOM;

ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; GLUCOSE TRANSPORT; HEART ATRIUM MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE CONTRACTILITY; HEART TRABECULAR MUSCLE; HEART VENTRICLE MUSCLE; HUMAN; HUMAN TISSUE; INOTROPISM; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; AGONISTS; CARDIAC MUSCLE; DRUG EFFECTS; HEART ATRIUM; HEART CONTRACTION; HEART VENTRICLE; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT;

CALCIUM-BINDING PROTEINS; CARDIOTONIC AGENTS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 4; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEART ATRIA; HEART VENTRICLES; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIUM; PEPTIDES; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VENOMS;

EID: 84952655093     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.09.018     Document Type: Article

References (54)

1. Stamler J., Vaccaro O., Neaton J.D., Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 1993, 16:434-444.
2. Emerging Risk Factors C, Sarwar N., Gao P., Seshasai S.R., Gobin R., Kaptoge S., et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet 2010, 375:2215-2222.
3. Nasir S., Aguilar D. Congestive heart failure and diabetes mellitus: balancing glycemic control with heart failure improvement. Am. J. Cardiol. 2012, 110:50B-57B.
4. MacIntyre K., Capewell S., Stewart S., Chalmers J.W., Boyd J., Finlayson A., et al. Evidence of improving prognosis in heart failure: trends in case fatality in 66 547 patients hospitalized between 1986 and 1995. Circulation 2000, 102:1126-1131.
5. From A.M., Leibson C.L., Bursi F., Redfield M.M., Weston S.A., Jacobsen S.J., et al. Diabetes in heart failure: prevalence and impact on outcome in the population. Am. J. Med. 2006, 119:591-599.
6. Dormandy J.A., Charbonnel B., Eckland D.J., Erdmann E., Massi-Benedetti M., Moules I.K., et al. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet 2005, 366:1279-1289.
7. Home P.D., Pocock S.J., Beck-Nielsen H., Curtis P.S., Gomis R., Hanefeld M., et al. Rosiglitazone evaluated for cardiovascular outcomes in oral agent combination therapy for type 2 diabetes (RECORD): a multicentre, randomised, open-label trial. Lancet 2009, 373:2125-2135.
8. Scirica B.M., Bhatt D.L., Braunwald E., Steg P.G., Davidson J., Hirshberg B., et al. Saxagliptin and cardiovascular outcomes in patients with type 2 diabetes mellitus. N. Engl. J. Med. 2013, 369:1317-1326.
9. Mojsov S., Heinrich G., Wilson I.B., Ravazzola M., Orci L., Habener J.F. Preproglucagon gene expression in pancreas and intestine diversifies at the level of post-translational processing. J. Biol. Chem. 1986, 261:11880-11889.
10. Kieffer T.J., McIntosh C.H., Pederson R.A. Degradation of glucose-dependent insulinotropic polypeptide and truncated glucagon-like peptide 1 in vitro and in vivo by dipeptidyl peptidase IV. Endocrinology 1995, 136:3585-3596.
11. Serre V., Dolci W., Schaerer E., Scrocchi L., Drucker D., Efrat S., et al. Exendin-(9-39) is an inverse agonist of the murine glucagon-like peptide-1 receptor: implications for basal intracellular cyclic adenosine 3',5'-monophosphate levels and beta-cell glucose competence. Endocrinology 1998, 139:4448-4454.
12. Drucker D.J., Nauck M.A. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006, 368:1696-1705.
13. Nikolaidis L.A., Mankad S., Sokos G.G., Miske G., Shah A., Elahi D., et al. Effects of glucagon-like peptide-1 in patients with acute myocardial infarction and left ventricular dysfunction after successful reperfusion. Circulation 2004, 109:962-965.
14. Koska J., Schwartz E.A., Mullin M.P., Schwenke D.C., Reaven P.D. Improvement of postprandial endothelial function after a single dose of exenatide in individuals with impaired glucose tolerance and recent-onset type 2 diabetes. Diabetes Care 2010, 33:1028-1030.
15. Lonborg J., Vejlstrup N., Kelbaek H., Botker H.E., Kim W.Y., Mathiasen A.B., et al. Exenatide reduces reperfusion injury in patients with ST-segment elevation myocardial infarction. Eur. Heart J. 2012, 33:1491-1499.
16. Tate M., Chong A., Robinson E., Green B.D., Grieve D.J. Selective targeting of glucagon-like peptide-1 signalling as a novel therapeutic approach for cardiovascular disease in diabetes. Br. J. Pharmacol. 2015, 172:721-736.
17. Bos J.L. Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 2006, 31:680-686.
18. Kim M., Platt M.J., Shibasaki T., Quaggin S.E., Backx P.H., Seino S., et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nat. Med. 2013, 19:567-575.
19. Tilley D.G. G protein-dependent and G protein-independent signaling pathways and their impact on cardiac function. Circ. Res. 2011, 109:217-230.
20. Mangmool S., Shukla A.K., Rockman H.A. Beta-arrestin-dependent activation of Ca(2+)/calmodulin kinase II after beta(1)-adrenergic receptor stimulation. J. Cell Biol. 2010, 189:573-587.
21. Tilley D.G., Nguyen A.D., Rockman H.A. Troglitazone stimulates beta-arrestin-dependent cardiomyocyte contractility via the angiotensin II type 1A receptor. Biochem. Biophys. Res. Commun. 2010, 396:921-926.
22. Ravier M.A., Leduc M., Richard J., Linck N., Varrault A., Pirot N., et al. Beta-arrestin2 plays a key role in the modulation of the pancreatic beta cell mass in mice. Diabetologia 2014, 57:532-541.
23. Sonoda N., Imamura T., Yoshizaki T., Babendure J.L., Lu J.C., Olefsky J.M. Beta-arrestin-1 mediates glucagon-like peptide-1 signaling to insulin secretion in cultured pancreatic beta cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6614-6619.
24. Bisping E., Tenderich G., Barckhausen P., Stumme B., Bruns S., von Lewinski D., et al. Atrial myocardium is the predominant inotropic target of adrenomedullin in the human heart. Am. J. Phys. Heart Circ. Phys. 2007, 293:H3001-H3007.
25. Ban K., Noyan-Ashraf M.H., Hoefer J., Bolz S.S., Drucker D.J., 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, 117:2340-2350.
26. Bers D.M. Calcium cycling and signaling in cardiac myocytes. Annu. Rev. Physiol. 2008, 70:23-49.
27. Zhao T., Parikh P., Bhashyam S., Bolukoglu H., Poornima I., Shen Y.T., et al. Direct effects of glucagon-like peptide-1 on myocardial contractility and glucose uptake in normal and postischemic isolated rat hearts. J. Pharmacol. Exp. Ther. 2006, 317:1106-1113.
28. Richards P., Parker H.E., Adriaenssens A.E., Hodgson J.M., Cork S.C., Trapp S., et al. Identification and characterization of GLP-1 receptor-expressing cells using a new transgenic mouse model. Diabetes 2014, 63:1224-1233.
29. Wohlfart P., Linz W., Hubschle T., Linz D., Huber J., Hess S., et al. Cardioprotective effects of lixisenatide in rat myocardial ischemia-reperfusion injury studies. J. Transl. Med. 2013, 11:84.
30. Panjwani N., Mulvihill E.E., Longuet C., Yusta B., Campbell J.E., Brown T.J., et al. GLP-1 receptor activation indirectly reduces hepatic lipid accumulation but does not attenuate development of atherosclerosis in diabetic male ApoE(-/-) mice. Endocrinology 2013, 154:127-139.
31. Pyke C., Heller R.S., Kirk R.K., Orskov C., Reedtz-Runge S., Kaastrup P., et al. GLP-1 receptor localization in monkey and human tissue: novel distribution revealed with extensively validated monoclonal antibody. Endocrinology 2014, 155:1280-1290.
32. von Lewinski D., Gasser R., Rainer P.P., Huber M.S., Wilhelm B., Roessl U., et al. Functional effects of glucose transporters in human ventricular myocardium. Eur. J. Heart Fail. 2010, 12:106-113.
33. Timmers L., Henriques J.P., de Kleijn D.P., Devries J.H., Kemperman H., Steendijk P., et al. Exenatide reduces infarct size and improves cardiac function in a porcine model of ischemia and reperfusion injury. J. Am. Coll. Cardiol. 2009, 53:501-510.
34. Noyan-Ashraf M.H., Momen M.A., Ban K., Sadi A.M., Zhou Y.Q., Riazi A.M., et al. GLP-1R agonist liraglutide activates cytoprotective pathways and improves outcomes after experimental myocardial infarction in mice. Diabetes 2009, 58:975-983.
35. Nikolaidis L.A., Elahi D., Hentosz T., Doverspike A., Huerbin R., Zourelias L., 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, 110:955-961.
36. Poornima I., Brown S.B., Bhashyam S., Parikh P., Bolukoglu H., Shannon R.P. 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. 2008, 1:153-160.
37. Janssen P.M., Datz N., Zeitz O., Hasenfuss G. Levosimendan improves diastolic and systolic function in failing human myocardium. Eur. J. Pharmacol. 2000, 404:191-199.
38. Pieske B., Beyermann B., Breu V., Loffler B.M., Schlotthauer K., Maier L.S., et al. Functional effects of endothelin and regulation of endothelin receptors in isolated human nonfailing and failing myocardium. Circulation 1999, 99:1802-1809.
39. Jonsson E.N., Antila S., McFadyen L., Lehtonen L., Karlsson M.O. Population pharmacokinetics of levosimendan in patients with congestive heart failure. Br. J. Clin. Pharmacol. 2003, 55:544-551.
40. Melenovsky V., Hwang S.J., Redfield M.M., Zakeri R., Lin G., Borlaug B.A. Left atrial remodeling and function in advanced heart failure with preserved or reduced ejection fraction. Circ. Heart Fail. 2015, 8:295-303.
41. Deedwania P.C., Lardizabal J.A. Atrial fibrillation in heart failure: a comprehensive review. Am. J. Med. 2010, 123:198-204.
42. Zinman B., Wanner C., Lachin J.M., Fitchett D., Bluhmki E., Hantel S., et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N. Engl. J. Med. 2015.
43. Nikolaidis L.A., Elahi D., Shen Y.T., Shannon R.P. Active metabolite of GLP-1 mediates myocardial glucose uptake and improves left ventricular performance in conscious dogs with dilated cardiomyopathy. Am. J. Phys. Heart Circ. Phys. 2005, 289:H2401-H2408.
44. Ban K., Kim K.H., Cho C.K., Sauve M., Diamandis E.P., Backx P.H., et al. Glucagon-like peptide (GLP)-1(9-36)amide-mediated cytoprotection is blocked by exendin(9-39) yet does not require the known GLP-1 receptor. Endocrinology 2010, 151:1520-1531.
45. Ussher J.R. Deciphering ventricular GLP-1 action: time for a change of heart. Am. J. Phys. Heart Circ. Phys. 2014, 307:H1390-H1392.
46. Freedman N.J., Liggett S.B., Drachman D.E., Pei G., Caron M.G., Lefkowitz R.J. Phosphorylation and desensitization of the human beta 1-adrenergic receptor. Involvement of G protein-coupled receptor kinases and cAMP-dependent protein kinase. J. Biol. Chem. 1995, 270:17953-17961.
47. Drucker D.J., Philippe J., Mojsov S., Chick W.L., Habener J.F. Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:3434-3438.
48. Vila Petroff M.G., Egan J.M., Wang X., Sollott S.J. Glucagon-like peptide-1 increases cAMP but fails to augment contraction in adult rat cardiac myocytes. Circ. Res. 2001, 89:445-452.
49. Cazorla O., Lucas A., Poirier F., Lacampagne A., Lezoualc'h F. The cAMP binding protein Epac regulates cardiac myofilament function. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14144-14149.
50. von Lewinski D., Rainer P.P., Gasser R., Huber M.S., Khafaga M., Wilhelm B., et al. Glucose-transporter-mediated positive inotropic effects in human myocardium of diabetic and nondiabetic patients. Metab. Clin. Exp. 2010, 59:1020-1028.
51. Buchanan J., Mazumder P.K., Hu P., Chakrabarti G., Roberts M.W., Yun U.J., et al. Reduced cardiac efficiency and altered substrate metabolism precedes the onset of hyperglycemia and contractile dysfunction in two mouse models of insulin resistance and obesity. Endocrinology 2005, 146:5341-5349.
52. Desrois M., Sidell R.J., Gauguier D., King L.M., Radda G.K., Clarke K. Initial steps of insulin signaling and glucose transport are defective in the type 2 diabetic rat heart. Cardiovasc. Res. 2004, 61:288-296.
53. Kantor P.F., Lucien A., Kozak R., Lopaschuk G.D. The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ. Res. 2000, 86:580-588.
54. Cha Y.M., Dzeja P.P., Shen W.K., Jahangir A., Hart C.Y., Terzic A., et al. Failing atrial myocardium: energetic deficits accompany structural remodeling and electrical instability. Am. J. Phys. Heart Circ. Phys. 2003, 284:H1313-H1320.