Cardiomyocyte glucagon receptor signaling modulates outcomes in mice with experimental myocardial infarction

Molecular Metabolism

Volumn 4, Issue 2, 2015, Pages 132-143

  Ali, Safina ^a,b   Ussher, John R ^b   Baggio, Laurie L ^b   Kabir, M Golam ^b   Charron, Maureen J ^d   Ilkayeva, Olga ^c   Newgard, Christopher B ^c   Drucker, Daniel J ^a,b,e  

^a Department of Medicine ^*  (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cardiomyocytes; Diabetes; Fatty acid metabolism; Glucagon; Glucagon receptor; Heart; Myocardial infarction

Indexed keywords

ACYLCARNITINE; FATTY ACID; GLUCAGON; GLUCAGON RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CORONARY ARTERY LIGATION; EX VIVO STUDY; EXPERIMENTAL MYOCARDIAL INFARCTION; FATTY ACID METABOLISM; GENE DELETION; GENE EXPRESSION; HEART HYPERTROPHY; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART VENTRICLE PRESSURE; HEART VENTRICLE REMODELING; HISTOPATHOLOGY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LIPID DIET; MALE; MORTALITY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SURVIVAL RATE; WILD TYPE MOUSE;

MUS;

EID: 84921892213     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2014.11.005     Document Type: Article

References (57)

1. Unger R.H., Cherrington A.D. Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. Journal of Clinical Investigation 2012, 122(1):4-12.
2. Sinclair E.M., Yusta B., Streutker C., Baggio L.L., Koehler J., Charron M.J., et al. Glucagon receptor signaling is essential for control of murine hepatocyte survival. Gastroenterology 2008, 135(6):2096-2106.
3. Dunphy J.L., Taylor R.G., Fuller P.J. Tissue distribution of rat glucagon receptor and GLP-1 receptor gene expression. Molecular and Cellular Endocrinology 1998, 141(1-2):179-186.
4. Campos R.V., Lee Y.C., Drucker D.J. Divergent tissue-specific and developmental expression of receptors for glucagon and glucagon-like peptide-1 in the mouse. Endocrinology 1994, 134:2156-2164.
5. Ali S., Drucker D.J. Benefits and limitations of reducing glucagon action for the treatment of type 2 diabetes. American Journal of Physiology. Endocrinology and Metabolism 2009, 296(3):E415-E421.
6. Muller W.A., Faloona G.R., Aguilar-Parada E., Unger R.H. Abnormal alpha-cell function in diabetes. Response to carbohydrate and protein ingestion. New England Journal of Medicine 1970, 283(3):109-115.
7. Habegger K.M., Heppner K.M., Geary N., Bartness T.J., DiMarchi R., Tschop M.H. The metabolic actions of glucagon revisited. Nature Reviews Endocrinology 2010, 6(12):689-697.
8. Longuet C., Sinclair E.M., Maida A., Baggio L.L., Maziarz M., Charron M.J., et al. The glucagon receptor is required for the adaptive metabolic response to fasting. Cell Metabolism 2008, 8(5):359-371.
9. Day J.W., Gelfanov V., Smiley D., Carrington P.E., Chicchi G., Erion M.D., et al. Optimization of co-agonism at GLP-1 and glucagon receptors to safely maximize weight reduction in DIO-rodents. Biopolymers 2012, 98(5):443-450.
10. Sadry S.A., Drucker D.J. Emerging combinatorial hormone therapies for the treatment of obesity and T2DM. Nature Reviews Endocrinology 2013, 9(7):425-433.
11. Dakin C.L., Small C.J., Batterham R.L., Neary N.M., Cohen M.A., Patterson M., et al. Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 2004, 145(6):2687-2695.
12. Wynne K., Park A.J., Small C.J., Patterson M., Ellis S.M., Murphy K.G., et al. Subcutaneous oxyntomodulin reduces body weight in overweight and obese subjects: a double-blind, randomized, controlled trial. Diabetes 2005, 54(8):2390-2395.
13. Day J.W., Ottaway N., Patterson J.T., Gelfanov V., Smiley D., Gidda J., et al. Anew glucagon and GLP-1 co-agonist eliminates obesity in rodents. Nature Chemical Biology 2009, 5(10):749-757.
14. Glick G., Parmley W.W., Wechsler A.S., Sonnenblick E.H. Glucagon. Its enhancement of cardiac performance in the cat and dog and persistence of its inotropic action despite beta-receptor blockade with propranolol. Circulation Research 1968, 22(6):789-799.
15. Gonzalez-Munoz C., Nieto-Ceron S., Cabezas-Herrera J., Hernandez-Cascales J. Glucagon increases contractility in ventricle but not in atrium of the rat heart. European Journal of Pharmacology 2008, 587(1-3):243-247.
16. Goodwin G.W., Taegtmeyer H. Metabolic recovery of isolated working rat heart after brief global ischemia. American Journal of Physiology 1994, 267(2 Pt 2):H462-H470.
17. Maroko P.R., Kjekshus J.K., Sobel B.E., Watanabe T., Covell J.W., Ross J., et al. Factors influencing infarct size following experimental coronary artery occlusions. Circulation 1971, 43(1):67-82.
18. Sohal D.S., Nghiem M., Crackower M.A., Witt S.A., Kimball T.R., Tymitz K.M., et al. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circulation Research 2001, 89(1):20-25.
19. Longuet C., Robledo A.M., Dean E.D., Dai C., Ali S., McGuinness I., et al. Liver-specific disruption of the murine glucagon receptor produces alpha-cell hyperplasia: evidence for a circulating alpha-cell growth factor. Diabetes 2013, 62(4):1196-1205.
20. Ussher J.R., Baggio L.L., Campbell J.E., Mulvihill E.E., Kim M., Kabir M.G., et al. Inactivation of the cardiomyocyte Glucagon-Like Peptide-1 Receptor (GLP-1R) unmasks cardiomyocyte-independent GLP-1R-mediated cardioprotection. Molecular Metabolism 2014, 3(5):507-517.
21. Koitabashi N., Bedja D., Zaiman A.L., Pinto Y.M., Zhang M., Gabrielson K.L., et al. Avoidance of transient cardiomyopathy in cardiomyocyte-targeted tamoxifen-induced MerCreMer gene deletion models. Circulation Research 2009, 105(1):12-15.
22. Kim M., Platt M., Shibasaki T., Quaggin S., Backx P.H., Seino S., et al. GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nature Medicine 2013, 19(5):567-575.
23. 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(18):2340-2350.
24. Koves T.R., Ussher J.R., Noland R.C., Slentz D., Mosedale M., Ilkayeva O., et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metabolism 2008, 7(1):45-56.
25. Ussher J.R., Koves T.R., Jaswal J.S., Zhang L., Ilkayeva O., Dyck J.R., et al. Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes 2009, 58(8):1766-1775.
26. Ali S., Lamont B.J., Charron M.J., Drucker D.J. Dual elimination of the glucagon and GLP-1 receptors in mice reveals plasticity in the incretin axis. Journal of Clinical Investigation 2011, 121(5):1917-1929.
27. Koehler J.A., Drucker D.J. Activation of GLP-1 receptor signaling does not modify the growth or apoptosis of human pancreatic cancer cells. Diabetes 2006, 55:1369-1379.
28. Yusta B., Holland D., Koehler J.A., Maziarz M., Estall J.L., Higgins R., et al. ErbB signaling is required for the proliferative actions of GLP-2 in the murine gut. Gastroenterology 2009, 173(3):986-996.
29. Ban K., Kim H., Cho J., Diamandis E., Backx P.H., Drucker D.J., et al. GLP-1(9-36) protects cardiomyocytes and endothelial cells from ischemia-reperfusion injury via cytoprotective pathways independent of the GLP-1 receptor. Endocrinology 2010, 151(4):1520-1531.
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(1):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(4):1280-1290.
32. Moore-Morris T., Varrault A., Mangoni M.E., Le Digarcher A., Negre V., Dantec C., et al. Identification of potential pharmacological targets by analysis of the comprehensive G protein-coupled receptor repertoire in the four cardiac chambers. Molecular Pharmacology 2009, 75(5):1108-1116.
33. Gelling R.W., Du X.Q., Dichmann D.S., Romer J., Huang H., Cui L., et al. Lower blood glucose, hyperglucagonemia, and pancreatic {alpha} cell hyperplasia in glucagon receptor knockout mice. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:1438-1443.
34. Yang J., MacDougall M.L., McDowell M.T., Xi L., Wei R., Zavadoski W.J., et al. Polyomic profiling reveals significant hepatic metabolic alterations in glucagon-receptor (GCGR) knockout mice: implications on anti-glucagon therapies for diabetes. BMC Genomics 2011, 12:281.
35. Omar B.A., Andersen B., Hald J., Raun K., Nishimura E., Ahren B. Fibroblast growth factor 21 (FGF21) and glucagon-like peptide 1 contribute todiabetes resistance in glucagon receptor-deficient mice. Diabetes 2014, 63(1):101-110.
36. Ussher J.R., Drucker D.J. Cardiovascular actions of incretin-based therapies. Circulation Research 2014, 114(11):1788-1803.
37. Planavila A., Redondo I., Hondares E., Vinciguerra M., Munts C., Iglesias R., et al. Fibroblast growth factor 21 protects against cardiac hypertrophy in mice. Nature Communications 2013, 420:19.
38. Chang-Chretien K., Chew J.T., Judge D.P. Reversible dilated cardiomyopathy associated with glucagonoma. Heart 2004, 90(7):e44.
39. Puri P.S., Bing R.J. Effects of glucagon on myocardial contractility and hemodynamics in acute experimental myocardial infarction. Basis for its possible use in cardiogenic shock. American Heart Journal 1969, 78(5):660-668.
40. Eddy J.D., O'Brien E.T., Singh S.P. Glucagon and haemodynamics of acute myocardial infarction. British Medical Journal 1969, 4(5684):663-665.
41. Kumar R., Molokhia F.A., Norman J.C., Inamdar A.N., Messer J.V., Abelmann W.H., et al. Experimental myocardial infarction. X. Efficacy of glucagon in acute and healing phase in intact conscious dogs: effects on hemodynamics and myocardial oxygen consumption. Circulation 1972, 45(1):55-64.
42. Lai L., Leone T.C., Keller M.P., Martin O.J., Broman A.T., Nigro J., et al. Energy metabolic re-programming in the hypertrophied and early stage failing heart: a multi-systems approach. Circulation Heart Failure 2014 Nov, 7(6):1022-1031.
43. Muoio D.M., Noland R.C., Kovalik J.P., Seiler S.E., Davies M.N., DeBalsi K.L., et al. Muscle-specific deletion of carnitine acetyltransferase compromises glucose tolerance and metabolic flexibility. Cell Metabolism 2012, 15(5):764-777.
44. Campbell F.M., Kozak R., Wagner A., Altarejos J.Y., Dyck J.R., Belke D.D., et al. Arole for peroxisome proliferator-activated receptor alpha (PPARalpha ) in the control of cardiac malonyl-CoA levels: reduced fatty acid oxidation rates and increased glucose oxidation rates in the hearts of mice lacking PPARalpha are associated with higher concentrations of malonyl-CoA and reduced expression of malonyl-CoA decarboxylase. Journal of Biological Chemistry 2002, 277(6):4098-4103.
45. Finck B.N., Lehman J.J., Leone T.C., Welch M.J., Bennett M.J., Kovacs A., et al. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. Journal of Clinical Investigation 2002, 109(1):121-130.
46. Sambandam N., Morabito D., Wagg C., Finck B.N., Kelly D.P., Lopaschuk G.D. Chronic activation of PPARalpha is detrimental to cardiac recovery after ischemia. American Journal of Physiology. Heart and Circulatory Physiology 2006, 290(1):H87-H95.
47. Matsushima S., Kuroda J., Ago T., Zhai P., Ikeda Y., Oka S., et al. Broad suppression of NADPH oxidase activity exacerbates ischemia/reperfusion injury through inadvertent downregulation of hypoxia-inducible factor-1alpha and upregulation of peroxisome proliferator-activated receptor-alpha. Circulation Research 2013, 112(8):1135-1149.
48. Wu R., Chang H.C., Khechaduri A., Chawla K., Tran M., Chai X., et al. Cardiac-specific ablation of ARNT leads to lipotoxicity and cardiomyopathy. Journal of Clinical Investigation 2014, 124(11):4795-4806.
49. Finck B.N., Han X., Courtois M., Aimond F., Nerbonne J.M., Kovacs A., et al. Acritical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(3):1226-1231.
50. Yue T.L., Bao W., Jucker B.M., Gu J.L., Romanic A.M., Brown P.J., et al. Activation of peroxisome proliferator-activated receptor-alpha protects the heart from ischemia/reperfusion injury. Circulation 2003, 108(19):2393-2399.
51. Aasum E., Khalid A.M., Gudbrandsen O.A., How O.J., Berge R.K., Larsen T.S. Fenofibrate modulates cardiac and hepatic metabolism and increases ischemic tolerance in diet-induced obese mice. Journal of Molecular and Cellular Cardiology 2008, 44(1):201-209.
52. Omar M.A., Verma S., Clanachan A.S. Adenosine-mediated inhibition of 5'-AMP-activated protein kinase and p38 mitogen-activated protein kinase during reperfusion enhances recovery of left ventricular mechanical function. Journal of Molecular and Cellular Cardiology 2012, 52(6):1308-1318.
53. Fiedler B., Feil R., Hofmann F., Willenbockel C., Drexler H., Smolenski A., et al. cGMP-dependent protein kinase type I inhibits TAB1-p38 mitogen-activated protein kinase apoptosis signaling in cardiac myocytes. Journal of Biological Chemistry 2006, 281(43):32831-32840.
54. Sassi Y., Ahles A., Truong D.J., Baqi Y., Lee S.Y., Husse B., et al. Cardiac myocyte-secreted cAMP exerts paracrine action via adenosine receptor activation. Journal of Clinical Investigation 2014 Dec 1, 124(12):5385-5397.
55. Tschop M.H., DiMarchi R.D. Outstanding Scientific Achievement Award Lecture 2011: defeating diabesity: the case for personalized combinatorial therapies. Diabetes 2012, 61(6):1309-1314.
56. Axelsen L.N., Keung W., Pedersen H.D., Meier E., Riber D., Kjolbye A.L., et al. Glucagon and a glucagon-GLP-1 dual-agonist increases cardiac performance with different metabolic effects in insulin-resistant hearts. British Journal of Pharmacology 2012, 165(8):2736-2748.
57. Russell S.J., El-Khatib F.H., Sinha M., Magyar K.L., McKeon K., Goergen L.G., et al. Outpatient glycemic control with a bionic pancreas in type 1 diabetes. New England Journal of Medicine 2014, 371(4):313-325.