Phosphodiesterase-3 inhibition augments the myocardial infarct size-limiting effects of exenatide in mice with type 2 diabetes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 1, 2013, Pages

  Ye, Yumei ^a   Qian, Jinqiao ^a   Castillo, Alexander C ^a   Ling, Shukuan ^a   Ye, Hongmei ^b   Perez Polo, Jose R ^a   Bajaj, Mandeep ^c,d   Birnbaum, Yochai ^a,c,d  

^a University of Texas Medical Branch School of Medicine   (United States)

^b CHINA ASTRONAUT RESEARCH AND TRAINING CENTER   (China)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d TEXAS HEART INSTITUTE   (United States)

Author keywords

cAMP; Cilostazol; Glucagon like peptide 1; Infarct size; Phosphatase and tensin homolog on chromosome 10; Phosphdiesterase 3 inhibitor; Protein kinase A

Indexed keywords

CILOSTAZOL; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXENDIN 4; GLUCOSE; HEMOGLOBIN A1C; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHODIESTERASE III; PROTEIN KINASE B; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GLUCOSE BLOOD LEVEL; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE CELL; IN VITRO STUDY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WILD TYPE;

ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; CHOLESTEROL; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; HEMOGLOBIN A, GLYCOSYLATED; HYPOGLYCEMIC AGENTS; ISOQUINOLINES; LIPOXINS; MALE; MICE; MYOCARDIAL INFARCTION; MYOCARDIUM; PEPTIDES; PHOSPHODIESTERASE 3 INHIBITORS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PTEN PHOSPHOHYDROLASE; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION; SULFONAMIDES; TETRAZOLES; TRIGLYCERIDES; UP-REGULATION; VENOMS;

EID: 84871851596     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00609.2012     Document Type: Article

References (71)

1. Aasum E, Hafstad AD, Severson DL, Larsen TS. Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes 52: 434-441, 2003.
2. Anzawa R, Bernard M, Tamareille S, Baetz D, Confort-Gouny S, Gascard JP, Cozzone P, Feuvray D. Intracellular sodium increase and susceptibility to ischaemia in hearts from type 2 diabetic db/db mice. Diabetologia 49: 598-606, 2006.
3. Ban K, Kim KH, Cho CK, Sauve M, Diamandis EP, Backx PH, Drucker DJ, Husain M. Glucagon-like peptide (GLP)-1(9-36)amidemediated cytoprotection is blocked by exendin(9-39) yet does not require the known GLP-1 receptor. Endocrinology 151: 1520-1531, 2010.
4. 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 receptordependent and-independent pathways. Circulation 117: 2340-2350, 2008.
5. Bao W, Aravindhan K, Alsaid H, Chendrimada T, Szapacs M, Citerone DR, Harpel MR, Willette RN, Lepore JJ, Jucker BM. 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, 2011.
6. Bellis A, Castaldo D, Trimarco V, Monti MG, Chivasso P, Sadoshima J, Trimarco B, Morisco C. Cross-talk between PKA and Akt protects endothelial cells from apoptosis in the late ischemic preconditioning. Arterioscler Thromb Vasc Biol 29: 1207-1212, 2009.
7. Birnbaum Y, Castillo AC, Qian J, Shukuan Ling Hongmei Ye Perez-Polo JR, Bajaj M, Ye Y. Phosphodiesterase III inhibition increases cAMP levels and augments the infarct size limiting effect of a DPP-4 inhibitor in mice with type-2 diabetes mellitus. Cardiovasc Drug Ther In press.
8. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Nishi SP, Martinez JD, Huang MH, Uretsky BF, Perez-Polo JR. Augmentation of myocardial production of 15-epi-lipoxin-a4 by pioglitazone and atorvastatin in the rat. Circulation 114: 929-935, 2006.
9. Black SC, Huang JQ, Rezaiefar P, Radinovic S, Eberhart A, Nicholson DW, Rodger IW. Co-localization of the cysteine protease caspase-3 with apoptotic myocytes after in vivo myocardial ischemia and reperfusion in the rat. J Mol Cell Cardiol 30: 733-742, 1998.
10. Bose AK, Mocanu MM, Carr RD, Brand CL, Yellon DM. Glucagonlike peptide 1 can directly protect the heart against ischemia/reperfusion injury. Diabetes 54: 146-151, 2005.
11. Bose AK, Mocanu MM, Carr RD, Yellon DM. 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, 2005.
12. Bose AK, Mocanu MM, Carr RD, Yellon DM. Myocardial ischaemiareperfusion 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, 2007.
13. Calvert JW, Gundewar S, Jha S, Greer JJ, Bestermann WH, Tian R, Lefer DJ. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 57: 696-705, 2008.
14. Chen JX, Stinnett A. Disruption of Ang-1/Tie-2 signaling contributes to the impaired myocardial vascular maturation and angiogenesis in type II diabetic mice. Arterioscler Thromb Vasc Biol 28: 1606-1613, 2008.
15. Cosentino C, Di Domenico M, Porcellini A, Cuozzo C, De Gregorio G, Santillo MR, Agnese S, Di Stasio R, Feliciello A, Migliaccio A, Avvedimento EV. p85 regulatory subunit of PI3K mediates cAMP-PKA and estrogens biological effects on growth and survival. Oncogene 26: 2095-2103, 2007.
16. Das S, Cordis GA, Maulik N, Das DK. Pharmacological preconditioning with resveratrol: role of CREB-dependent Bcl-2 signaling via adenosine A3 receptor activation. Am J Physiol Heart Circ Physiol 288: H328-H335, 2005.
17. De Gregorio G, Coppa A, Cosentino C, Ucci S, Messina S, Nicolussi A, D'Inzeo S, Di Pardo A, Avvedimento EV, Porcellini A. The p85 regulatory subunit of PI3K mediates TSH-cAMP-PKA growth and survival signals. Oncogene 26: 2039-2047, 2007.
18. Dokken BB, La Bonte LR, Davis-Gorman G, Teachey MK, Seaver N, McDonagh PF. Glucagon-like peptide-1 (GLP-1), immediately prior to reperfusion, decreases neutrophil activation and reduces myocardial infarct size in rodents. Horm Metab Res 43: 300-305, 2011.
19. Doyle ME, Egan JM. Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol Ther 113: 546-593, 2007.
20. Eliseev RA, Vanwinkle B, Rosier RN, Gunter TE. Diazoxide-mediated preconditioning against apoptosis involves activation of cAMP-response element-binding protein (CREB) and NF B. J Biol Chem 279: 46748-46754, 2004.
21. Feliciello A, Gottesman ME, Avvedimento EV. cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell Signal 17: 279-287, 2005.
22. Greer JJ, Ware DP, Lefer DJ. Myocardial infarction and heart failure in the db/db diabetic mouse. Am J Physiol Heart Circ Physiol 290: H146-H153, 2006.
23. Gundewar S, Calvert JW, Elrod JW, Lefer DJ. Cytoprotective effects of N,N,N-trimethylsphingosine during ischemia-reperfusion injury are lost in the setting of obesity and diabetes. Am J Physiol Heart Circ Physiol 293: H2462-H2471, 2007.
24. Harris MB, Blackstone MA, Sood SG, Li C, Goolsby JM, Venema VJ, Kemp BE, Venema RC. Acute activation and phosphorylation of endothelial nitric oxide synthase by HMG-CoA reductase inhibitors. Am J Physiol Heart Circ Physiol 287: H560-H566, 2004.
25. Hausenloy DJ, Yellon DM. Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 70: 240-253, 2006.
26. Hilal-Dandan R, Kanter JR, Brunton LL. Characterization of G-protein signaling in ventricular myocytes from the adult mouse heart: differences from the rat. J Mol Cell Cardiol 32: 1211-1221, 2000.
27. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439, 2007.
28. Hong KW, Kim KY, Shin HK, Lee JH, Choi JM, Kwak YG, Kim CD, Lee WS, Rhim BY. Cilostazol prevents tumor necrosis factor-alphainduced cell death by suppression of phosphatase and tensin homolog deleted from chromosome 10 phosphorylation and activation of Akt/cyclic AMP response element-binding protein phosphorylation. J Pharmacol Exp Ther 306: 1182-1190, 2003.
29. How OJ, Larsen TS, Hafstad AD, Khalid A, Myhre ES, Murray AJ, Boardman NT, Cole M, Clarke K, Severson DL, Aasum E. Rosiglitazone treatment improves cardiac efficiency in hearts from diabetic mice. Arch Physiol Biochem 113: 211-220, 2007.
30. Huang MH, Wang HQ, Roeske WR, Birnbaum Y, Wu Y, Yang NP, Lin Y, Ye Y, McAdoo DJ, Hughes MG, Lick SD, Boor PJ, Lui CY, Uretsky BF. Mediating-opioid-initiated heart protection via the 2- adrenergic receptor: role of the intrinsic cardiac adrenergic cell. Am J Physiol Heart Circ Physiol 293: H376-H384, 2007.
31. Huisamen B, Genade S, Lochner A. 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, 2008.
32. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Agullo L, Pina P, Soler-Soler J. Ischemic preconditioning attenuates calpain-mediated degradation of structural proteins through a protein kinase A-dependent mechanism. Cardiovasc Res 64: 105-114, 2004.
33. Iwasa M, Yamada Y, Kobayashi H, Yasuda S, Kawamura I, Sumi S, Shiraki T, Yamaki T, Ushikoshi H, Hattori A, Aoyama T, Nishigaki K, Takemura G, Fujiwara H, Minatoguchi S. Both stimulation of GLP-1 receptors and inhibition of glycogenolysis additively contribute to a protective effect of oral miglitol against ischaemia-reperfusion injury in rabbits. Br J Pharmacol 164: 119-131, 2011.
34. Jones SP, Girod WG, Granger DN, Palazzo AJ, Lefer DJ. Reperfusion injury is not affected by blockade of P-selectin in the diabetic mouse heart. Am J Physiol Heart Circ Physiol 277: H763-H769, 1999.
35. Kambayashi J, Liu Y, Sun B, Shakur Y, Yoshitake M, Czerwiec F. Cilostazol as a unique antithrombotic agent. Curr Pharm Des 9: 2289-2302, 2003.
36. Keyes KT, Xu J, Long B, Zhang C, Hu Z, Ye Y. Pharmacological inhibition of PTEN limits myocardial infarct size and improves left ventricular function postinfarction. Am J Physiol Heart Circ Physiol 298: H1198-H1208, 2010.
37. Keyes KT, Ye Y, Lin Y, Zhang C, Perez-Polo JR, Gjorstrup P, Birnbaum Y. Resolvin E1 protects the rat heart against reperfusion injury. Am J Physiol Heart Circ Physiol 299: H153-H164, 2010.
38. Kim KY, Shin HK, Lee JH, Kim CD, Lee WS, Rhim BY, Shin YW, Hong KW. Cilostazol enhances casein kinase 2 phosphorylation and suppresses tumor necrosis factor--induced increased phosphatase and tensin homolog deleted from chromosome 10 phosphorylation and apoptotic cell death in SK-N-SH cells. J Pharmacol Exp Ther 308: 97-104, 2004.
39. Kobayashi K, Forte TM, Taniguchi S, Ishida BY, Oka K, Chan L. The db/db mouse, a model for diabetic dyslipidemia: molecular characterization and effects of Western diet feeding. Metabolism 49: 22-31, 2000.
40. Lee JH, Park SY, Lee WS, Hong KW. Lack of antiapoptotic effects of antiplatelet drug, aspirin and clopidogrel, and antioxidant, MCI-186, against focal ischemic brain damage in rats. Neurol Res 27: 483-492, 2005.
41. Lee SP, Bae JW, Park KW, Rha SW, Bae JH, Suh JW, Chae IH, Cho MC, Kim HS. Inhibitory interaction between calcium channel blocker and clopidogrel. Efficacy of cilostazol to overcome it. Circ J 75: 2581-2589, 2011.
42. Lonborg J, Vejlstrup N, Kelbaek H, Botker HE, Kim WY, Mathiasen AB, Jorgensen E, Helqvist S, Saunamaki K, Clemmensen P, Holmvang L, Thuesen L, Krusell LR, Jensen JS, Kober L, Treiman M, Holst JJ, Engstrom T. Exenatide reduces reperfusion injury in patients with ST-segment elevation myocardial infarction. Eur Heart J 33: 1491-1499, 2012.
43. Manickavasagam S, Ye Y, Lin Y, Perez-Polo RJ, Huang MH, Lui CY, Hughes MG, McAdoo DJ, Uretsky BF, Birnbaum Y. The cardioprotective effect of a statin and cilostazol combination: relationship to Akt and endothelial nitric oxide synthase activation. Cardiovasc Drugs Ther 21: 321-330, 2007.
44. Marais E, Genade S, Lochner A. CREB activation and ischaemic preconditioning. Cardiovasc Drugs Ther 22: 3-17, 2008.
45. Matsubara M, Kanemoto S, Leshnower BG, Albone EF, Hinmon R, Plappert T, Gorman JH 3rd, Gorman RC. Single dose GLP-1-Tf ameliorates myocardial ischemia/reperfusion injury. J Surg Res 165: 38-45, 2011.
46. Mensah K, Mocanu MM, Yellon DM. Failure to protect the myocardium against ischemia/reperfusion injury after chronic atorvastatin treatment is recaptured by acute atorvastatin treatment: a potential role for phosphatase and tensin homolog deleted on chromosome ten? J Am Coll Cardiol 45: 1287-1291, 2005.
47. Mocanu MM, Field DC, Yellon DM. A potential role for PTEN in the diabetic heart. Cardiovasc Drugs Ther 20: 319-321, 2006.
48. Nagy N, Shiroto K, Malik G, Huang CK, Gaestel M, Abdellatif M, Tosaki A, Maulik N, Das DK. Ischemic preconditioning involves dual cardio-protective axes with p38MAPK as upstream target. J Mol Cell Cardiol 42: 981-990, 2007.
49. Nakaya Y, Minami A, Sakamoto S, Niwa Y, Ohnaka M, Harada N, Nakamura T. Cilostazol, a phosphodiesterase inhibitor, improves insulin sensitivity in the Otsuka Long-Evans Tokushima Fatty Rat, a model of spontaneous NIDDM. Diabetes Obes Metab 1: 37-41, 1999.
50. Noyan-Ashraf MH, Momen MA, Ban K, Sadi AM, Zhou YQ, Riazi AM, Baggio LL, Henkelman RM, Husain M, Drucker DJ. GLP-1R agonist liraglutide activates cytoprotective pathways and improves outcomes after experimental myocardial infarction in mice. Diabetes 58: 975-983, 2009.
51. Ossum A, van Deurs U, Engstrom T, Jensen JS, Treiman M. The cardioprotective and inotropic components of the postconditioning effects of GLP-1 and GLP-1(9-36)a in an isolated rat heart. Pharmacol Res 60: 411-417, 2009.
52. Park SY, Lee JH, Kim KY, Kim EK, Yun SJ, Kim CD, Lee WS, Hong KW. Cilostazol increases 3T3-L1 preadipocyte differentiation with improved glucose uptake associated with activation of peroxisome proliferator-activated receptor-gamma transcription. Atherosclerosis 201: 258-265, 2008.
53. Park SY, Shin HK, Lee JH, Kim CD, Lee WS, Rhim BY, Hong KW. Cilostazol ameliorates metabolic abnormalities with suppression of proinflammatory markers in a db/db mouse model of type 2 diabetes via activation of peroxisome proliferator-activated receptor transcription. J Pharmacol Exp Ther 329: 571-579, 2009.
54. Preiss D, Seshasai SR, Welsh P, Murphy SA, Ho JE, Waters DD, DeMicco DA, Barter P, Cannon CP, Sabatine MS, Braunwald E, Kastelein JJ, de Lemos JA, Blazing MA, Pedersen TR, Tikkanen MJ, Sattar N, Ray KK. Risk of incident diabetes with intensive-dose compared with moderate-dose statin therapy: a meta-analysis. JAMA 305: 2556-2564, 2011.
55. Przyklenk K, Maynard M, Greiner DL, Whittaker P. Cardioprotection with postconditioning: loss of efficacy in murine models of type-2 and type-1 diabetes. Antioxid Redox Signal 14: 781-790, 2011.
56. Qian J, Ling S, Castillo AC, Long B, Birnbaum Y, Ye Y. Regulation of phosphatase and tensin homolog on chromosome 10 in response to hypoxia. Am J Physiol Heart Circ Physiol 302: H1806-H1817, 2012.
57. Rogers KC, Faircloth JM, Finks SW. Use of cilostazol in percutaneous coronary interventions. Ann Pharmacother 46: 839-850, 2012.
58. Sanada S, Asanuma H, Tsukamoto O, Minamino T, Node K, Takashima S, Fukushima T, Ogai A, Shinozaki Y, Fujita M, Hirata A, Okuda H, Shimokawa H, Tomoike H, Hori M, Kitakaze M. Protein kinase A as another mediator of ischemic preconditioning independent of protein kinase C. Circulation 110: 51-57, 2004.
59. Sanada S, Kitakaze M, Papst PJ, Asanuma H, Node K, Takashima S, Asakura M, Ogita H, Liao Y, Sakata Y, Ogai A, Fukushima T, Yamada J, Shinozaki Y, Kuzuya T, Mori H, Terada N, Hori M. Cardioprotective effect afforded by transient exposure to phosphodiesterase III inhibitors: the role of protein kinase A and p38 mitogen-activated protein kinase. Circulation 104: 705-710, 2001.
60. Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68: 821-861, 1999.
61. Sonne DP, Engstrom T, Treiman M. Protective effects of GLP-1 analogues exendin-4 and GLP-1(9-36) amide against ischemia-reperfusion injury in rat heart. Regul Pept 146: 243-249, 2008.
62. Tamhane U, Meier P, Chetcuti S, Chen KY, Rha SW, Grossman MP, Gurm H. Efficacy of cilostazol in reducing restenosis in patients undergoing contemporary stent based PCI: a meta-analysis of randomised controlled trials. EuroIntervention 5: 384-393, 2009.
63. Thakker GD, Frangogiannis NG, Bujak M, Zymek P, Gaubatz JW, Reddy AK, Taffet G, Michael LH, Entman ML, Ballantyne CM. Effects of diet-induced obesity on inflammation and remodeling after myocardial infarction. Am J Physiol Heart Circ Physiol 291: H2504-H2514, 2006.
64. Timmers L, Henriques JP, de Kleijn DP, Devries JH, Kemperman H, Steendijk P, Verlaan CW, Kerver M, Piek JJ, Doevendans PA, Pasterkamp G, Hoefer IE. Exenatide reduces infarct size and improves cardiac function in a porcine model of ischemia and reperfusion injury. J Am Coll Cardiol 53: 501-510, 2009.
65. Tsang A, Hausenloy DJ, Mocanu MM, Carr RD, Yellon DM. Preconditioning the diabetic heart: the importance of Akt phosphorylation. Diabetes 54: 2360-2364, 2005.
66. Vadas O, Burke JE, Zhang X, Berndt A, Williams RL. Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Sci Signal 4: re2, 2011.
67. Ye Y, Keyes KT, Zhang C, Perez-Polo JR, Lin Y, Birnbaum Y. The myocardial infarct size-limiting effect of sitagliptin is PKA-dependent, whereas the protective effect of pioglitazone is partially dependent on PKA. Am J Physiol Heart Circ Physiol 298: H1454-H1465, 2010.
68. Ye Y, Lin Y, Perez-Polo JR, Uretsky BF, Ye Z, Tieu BC, Birnbaum Y. Phosphorylation of 5-lipoxygenase at ser523 by protein kinase A determines whether pioglitazone and atorvastatin induce proinflammatory leukotriene B4 or anti-inflammatory 15-epi-lipoxin A4 production. J Immunol 181: 3515-3523, 2008.
69. Ye Y, Perez-Polo JR, Aguilar D, Birnbaum Y. The potential effects of anti-diabetic medications on myocardial ischemia-reperfusion injury. Basic Res Cardiol 106: 925-952, 2011.
70. Ye Y, Qian J, Castillo AC, Perez-Polo JR, Birnbaum Y. Aliskiren and valsartan reduce myocardial AT1 receptor expression and limit myocardial infarct size in diabetic mice. Cardiovasc Drugs Ther 25: 505-515, 2011.
71. Zhu SG, Xi L, Kukreja RC. Type 2 diabetic obese db/db mice are refractory to myocardial ischaemic post-conditioning in vivo: potential role for Hsp20, F1-ATPase delta and Echs1. J Cell Mol Med 16: 950-958, 2012.