Influence of GLP-1 on myocardial glucose metabolism in healthy men during normo- or hypoglycemia

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Gejl, Michael ^a   Lerche, Susanne ^a   Mengel, Annette ^b   Mløler, Niels ^b   Bibby, Bo Martin ^a   Smidt, Kamille ^a   Brock, Birgitte ^a,b   Snødergaard, Hanne ^d   Bøtker, Hans Erik ^b   Gjedde, Albert ^b,c   Holst, Jens Juul ^c   Hansen, Søren Baarsgaard ^b   Rungby, Jørgen ^a,b,e  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d VIBORG HOSPITAL   (Denmark)

^e Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; FATTY ACID; FLUORODEOXYGLUCOSE F 18; GLUCAGON; GLUCAGON LIKE PEPTIDE 1 [7-36] AMIDE; GLUCOSE; HYDROCORTISONE; INSULIN; PLACEBO;

ADULT; ARTICLE; BODY MASS; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; GLUCOSE BLOOD LEVEL; GLUCOSE INFUSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; HEART MUSCLE METABOLISM; HUMAN; HUMAN EXPERIMENT; HYPOGLYCEMIA; INSULIN RESISTANCE; MALE; NAUSEA; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; RANDOMIZED CONTROLLED TRIAL; VOMITING;

ADULT; BLOOD GLUCOSE; CROSS-OVER STUDIES; FLUORODEOXYGLUCOSE F18; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HEART; HORMONES; HUMANS; HYPOGLYCEMIA; MALE; METABOLOME; MYOCARDIUM; POSITRON-EMISSION TOMOGRAPHY; YOUNG ADULT;

EID: 84896467624     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083758     Document Type: Article

References (57)

1. Smyth S, Heron A (2006) Diabetes and obesity: the twin epidemics. Nat Med 12: 75-80. nm0106-75 [pii];10.1038/nm0106-75 [doi].
2. DeFronzo RA (2004) Pathogenesis of type 2 diabetes mellitus. Med Clin North Am 88: 787-835, ix.
3. Guz Y, Nasir I, Teitelman G (2001) Regeneration of pancreatic beta cells from intra-islet precursor cells in an experimental model of diabetes. Endocrinology 142: 4956-4968. (Pubitemid 33022372)
4. Nauck MA, Vardarli I, Deacon CF, Holst JJ, Meier JJ (2011) Secretion of glucagon-like peptide-1 (GLP-1) in type 2 diabetes: what is up, what is down? Diabetologia 54: 10-18. 10.1007/s00125-010-1896-4 [doi].
5. van den Brom CE, Bulte CS, Loer SA, Bouwman RA, Boer C (2013) Diabetes, perioperative ischaemia and volatile anaesthetics: consequences of derangements in myocardial substrate metabolism. Cardiovasc Diabetol 12: 42. 1475-2840-12-42 [pii];10.1186/1475-2840-12-42 [doi].
6. Taegtmeyer H, McNulty P, Young ME (2002) Adaptation and maladaptation of the heart in diabetes: Part I: general concepts. Circulation 105: 1727-1733. (Pubitemid 34298619)
7. Holst JJ (2004) On the Physiology of GIP and GLP-1. Horm Metab Res 36: 747-754.
8. Lonborg J, Vejlstrup N, Kelbaek H, Botker HE, Kim WY, et al. (2012) Exenatide reduces reperfusion injury in patients with ST-segment elevation myocardial infarction. Eur Heart J 33: 1491-1499. ehr309 [pii];10.1093/ eurheartj/ehr309 [doi].
9. Ravassa S, Zudaire A, Diez J (2012) GLP-1 and cardioprotection: from bench to bedside. Cardiovasc Res 94: 316-323. cvs123 [pii];10.1093/cvr/cvs123 [doi].
10. Degn KB, Brock B, Juhl CB, Djurhuus CB, Grubert J, et al. (2004) Effect of intravenous infusion of exenatide (synthetic exendin-4) on glucose-dependent insulin secretion and counterregulation during hypoglycemia. Diabetes 53: 2397-2403. 53/9/2397 [pii].
11. Gejl M, Sondergaard HM, Stecher C, Bibby BM, Moller N, et al. (2012) Exenatide alters myocardial glucose transport and uptake depending on insulin resistance and increases myocardial blood flow in patients with type 2 diabetes. J Clin Endocrinol Metab 97: E1165-E1169. jc.2011-3456 [pii];10.1210/jc.2011- 3456 [doi].
12. Toft-Nielsen MB, Madsbad S, Holst JJ (1999) Continuous subcutaneous infusion of glucagon-like peptide 1 lowers plasma glucose and reduces appetite in type 2 diabetic patients. Diabetes Care 22: 1137-1143. (Pubitemid 29293967)
13. Espelund U, Hansen TK, Hojlund K, Beck-Nielsen H, Clausen JT, et al. (2005) Fasting unmasks a strong inverse association between ghrelin and cortisol in serum: studies in obese and normal-weight subjects. J Clin Endocrinol Metab 90: 741-746. jc.2004-0604 [pii];10.1210/jc.2004-0604 [doi].
14. Eriksson BM, Persson BA (1982) Determination of catecholamines in rat heart tissue and plasma samples by liquid chromatography with electrochemical detection. J Chromatogr 228: 143-154. (Pubitemid 12075991)
15. Orskov H, Thomsen HG, Yde H (1968) Wick chromatography for rapid and reliable immunoassay of insulin, glucagon and growth hormone. Nature 219: 193-195.
16. Wilken M, Larsen FS, Buckley D, Holst JJ (1999) New highly specific immunoassays for glucacon-like peptide 1 (GLP-1). Diabetologia 42: A196.
17. Orskov C, Rabenhoj L, Wettergren A, Kofod H, Holst JJ (1994) Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes 43: 535-539. (Pubitemid 24096293)
18. Gjedde A (1981) High- and low-affinity transport of D-glucose from blood to brain. J Neurochem 36: 1463-1471.
19. Gjedde A (1982) Calculation of cerebral glucose phosphorylation from brain uptake of glucose analogs in vivo: a re-examination. Brain Res 257: 237-274.
20. Lerche S, Brock B, Rungby J, Botker HE, Moller N, et al. (2008) Glucagon-like peptide-1 inhibits blood-brain glucose transfer in humans. Diabetes 57: 325-331. db07-1162 [pii];10.2337/db07-1162 [doi].
21. Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27: 1487-1495. 27/6/1487 [pii].
22. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC (2010) Myocardial fatty acid metabolism in health and disease. Physiol Rev 90: 207-258. 90/1/207 [pii];10.1152/physrev.00015.2009 [doi].
23. Owen P, Dennis S, Opie LH (1990) Glucose flux rate regulates onset of ischemic contracture in globally underperfused rat hearts. Circ Res 66: 344-354. (Pubitemid 20041166)
24. Mallet RT, Hartman DA, Bunger R (1990) Glucose requirement for postischemic recovery of perfused working heart. Eur J Biochem 188: 481-493. (Pubitemid 20106264)
25. Finfer S, Chittock DR, Su SY, Blair D, Foster D, et al. (2009) Intensive versus conventional glucose control in critically ill patients. N Engl J Med 360: 1283-1297. NEJMoa0810625 [pii];10.1056/NEJMoa0810625 [doi].
26. Sokos GG, Nikolaidis 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. S1071-9164(06)01109-2 [pii];10.1016/j.cardfail.2006.08.211 [doi].
27. Nielsen R, Wiggers H, Halbirk M, Botker H, Holst JJ, et al. (2012) Metabolic effects of short-term GLP-1 treatment in insulin resistant heart failure patients. Exp Clin Endocrinol Diabetes 120: 266-272. 10.1055/s-0032-1304605 [doi].
28. Nauck MA, Heimesaat MM, Behle K, Holst JJ, Nauck MS, et al (2002) Effects of glucagon-like peptide 1 on counterregulatory hormone responses, cognitive functions, and insulin secretion during hyperinsulinemic, stepped hypoglycemic clamp experiments in healthy volunteers. J Clin Endocrinol Metab 87: 1239-1246. (Pubitemid 36121094)
29. Gejl M, Lerche S, Egefjord L, Brock B, Moller N, et al. (2013) Glucagon-like peptide-1 (GLP-1) raises blood-brain glucose transfer capacity and hexokinase activity in human brain. Front Neuroenergetics 5: 2. 10.3389/fnene.2013.00002 [doi].
30. Ahren B, Schweizer A, Dejager S, Dunning BE, Nilsson PM, et al. (2009) Vildagliptin enhances islet responsiveness to both hyper- and hypoglycemia in patients with type 2 diabetes. J Clin Endocrinol Metab 94: 1236-1243. jc.2008-2152 [pii];10.1210/jc.2008-2152 [doi].
31. Vella A, Shah P, Basu R, Basu A, Camilleri M, et al. (2001) Effect of glucagon-like peptide-1(7-36)-amide on initial splanchnic glucose uptake and insulin action in humans with type 1 diabetes. Diabetes 50: 565-572. (Pubitemid 32195221)
32. Vella A, Shah P, Reed AS, Adkins AS, Basu R, et al. (2002) Lack of effect of exendin-4 and glucagon-like peptide-1-(7,36)-amide on insulin action in nondiabetic humans. Diabetologia 45: 1410-1415. (Pubitemid 35244894)
33. Ryan AS, Egan JM, Habener JF, Elahi D (1998) Insulinotropic hormone glucagon-like peptide-1-(7-37) appears not to augment insulin-mediated glucose uptake in young men during euglycemia. J Clin Endocrinol Metab 83: 2399-2404. (Pubitemid 28503037)
34. Larsen PJ, Tang-Christensen M, Jessop DS (1997) Central administration of glucagon-like peptide-1 activates hypothalamic neuroendocrine neurons in the rat. Endocrinology 138: 4445-4455. (Pubitemid 27408493)
35. Choi Y, Brunken RC, Hawkins RA, Huang SC, Buxton DB, et al. (1993) Factors affecting myocardial 2-[F-18]fluoro-2-deoxy-D-glucose uptake in positron emission tomography studies of normal humans. Eur J Nucl Med 20: 308-318. (Pubitemid 23234002)
36. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, et al. (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. CIRCULATIONAHA.107.739938 [pii];10.1161/CIRCULATIONAHA.107.739938 [doi].
37. Bhashyam S, Fields AV, Patterson B, Testani JM, Chen L, 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. CIRCHEARTFAILURE. 109.900282 [pii];10.1161/CIRCHEARTFAILURE.109.900282 [doi].
38. Panjwani N, Mulvihill EE, Longuet C, Yusta B, Campbell JE, et al. (2013) GLP-1 receptor activation indirectly reduces hepatic lipid accumulation but does not attenuate development of atherosclerosis in diabetic male ApoE(-/-) mice. Endocrinology 154: 127-139. en.2012-1937 [pii];10.1210/en.2012-1937 [doi].
39. Kim M, Platt MJ, Shibasaki T, Quaggin SE, Backx PH, et al. (2013) GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nat Med. nm.3128 [pii];10.1038/nm.3128 [doi].
40. Pyke C, Knudsen LB (2013) The glucagon-like peptide-1 receptor-or not? Endocrinology 154: 4-8. 154/1/4 [pii];10.1210/en.2012-2124 [doi].
41. Chinda K, Chattipakorn S, Chattipakorn N (2012) Cardioprotective effects of incretin during ischaemia-reperfusion. Diab Vasc Dis Res 9: 256-269. 1479164112440816 [pii];10.1177/1479164112440816 [doi].
42. Best JH, Hoogwerf BJ, Herman WH, Pelletier EM, Smith DB, et al. (2011) Risk of cardiovascular disease events in patients with type 2 diabetes prescribed the glucagon-like peptide 1 (GLP-1) receptor agonist exenatide twice daily or other glucose-lowering therapies: a retrospective analysis of the LifeLink database. Diabetes Care 34: 90-95. dc10-1393 [pii];10.2337/dc10-1393 [doi].
43. Sun F, Yu K, Wu S, Zhang Y, Yang Z, et al. (2012) Cardiovascular safety and glycemic control of glucagon-like peptide-1 receptor agonists for type 2 diabetes mellitus: A pairwise and network meta-analysis. Diabetes Res Clin Pract. S0168-8227(12)00308-7 [pii];10.1016/j.diabres.2012.09.004 [doi].
44. Sivertsen J, Rosenmeier J, Holst JJ, Vilsboll T (2012) The effect of glucagon-like peptide 1 on cardiovascular risk. Nat Rev Cardiol 9: 209-222. nrcardio. 2011.211 [pii];10.1038/nrcardio.2011.211 [doi].
45. Kudoh A, Katagai H, Takazawa T (2002) Atrial natriuretic peptide increases glucose uptake during hypoxia in cardiomyocytes. J Cardiovasc Pharmacol 40: 601-610.
46. Moberly SP, Mather KJ, Berwick ZC, Owen MK, Goodwill AG, et al. (2013) Impaired cardiometabolic responses to glucagon-like peptide 1 in obesity and type 2 diabetes mellitus. Basic Res Cardiol 108: 365. 10.1007/s00395-013-0365-x [doi].
47. Nishino Y, Miura T, Miki T, Sakamoto J, Nakamura Y, et al. (2004) Ischemic preconditioning activates AMPK in a PKC-dependent manner and induces GLUT4 up-regulation in the late phase of cardioprotection. Cardiovasc Res 61: 610-619. 10.1016/j.cardiores.2003.10.022 [doi];S0008636303006874 [pii].
48. Kainulainen H, Breiner M, Schurmann A, Marttinen A, Virjo A, et al. (1994) In vivo glucose uptake and glucose transporter proteins GLUT1 and GLUT4 in heart and various types of skeletal muscle from streptozotocin-diabetic rats. Biochim Biophys Acta 1225: 275-282. (Pubitemid 24066578)
49. Hall JL, Sexton WL, Stanley WC (1995) Exercise training attenuates the reduction in myocardial GLUT-4 in diabetic rats. J Appl Physiol (1985) 78: 76-81.
50. Vyas AK, Yang KC, Woo D, Tzekov A, Kovacs A, et al. (2011) Exenatide improves glucose homeostasis and prolongs survival in a murine model of dilated cardiomyopathy. PLoS One 6: e17178. 10.1371/journal.pone.0017178 [doi].
51. Zhao T, Parikh P, Bhashyam S, Bolukoglu H, Poornima I, 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. jpet.106.100982 [pii];10.1124/jpet.106.100982 [doi].
52. Ding SY, Nkobena A, Kraft CA, Markwardt ML, Rizzo MA (2011) Glucagon-like peptide 1 stimulates post-translational activation of glucokinase in pancreatic beta cells. J Biol Chem 286: 16768-16774. M110.192799 [pii];10.1074/jbc.M110. 192799 [doi].
53. Van Dyke DA, Walters L, Frieswyk D, Kokmeyer D, Louters LL (2003) Acute effects of troglitazone and nitric oxide on glucose uptake in L929 fibroblast cells. Life Sci 72: 2321-2327. S002432050300119X [pii].
54. Etgen GJ Jr, Fryburg DA, Gibbs EM (1997) Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway. Diabetes 46: 1915-1919. (Pubitemid 27456433)
55. Gejl M, Egefjord L, Lerche S, Vang K, Bibby BM, et al. (2012) Glucagon-like peptide-1 decreases intracerebral glucose content by activating hexokinase and changing glucose clearance during hyperglycemia. J Cereb Blood Flow Metab. jcbfm2012118 [pii];10.1038/jcbfm.2012.118 [doi].
56. Botker HE, Bottcher M, Schmitz O, Gee A, Hansen SB, et al. (1997) Glucose uptake and lumped constant variability in normal human hearts determined with [18F]fluorodeoxyglucose. J Nucl Cardiol 4: 125-132.
57. Botker HE, Goodwin GW, Holden JE, Doenst T, Gjedde A, et al. (1999) Myocardial glucose uptake measured with fluorodeoxyglucose: a proposed method to account for variable lumped constants. J Nucl Med 40: 1186-1196. (Pubitemid 29315512)