Ghrelin ameliorates impaired angiogenesis of ischemic myocardium through GHSR1a-mediated AMPK/eNOS signal pathway in diabetic rats

Peptides

Volumn 73, Issue , 2015, Pages 77-87

  Wang, Li ^a   Chen, Qingwei ^a   Li, Guiqiong ^a   Ke, Dazhi ^a  

^a THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

Angiogenesis; Diabetes; Ghrelin; GHSR; Myocardial infarction

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GHRELIN; GHRELIN RECEPTOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; GHSR1A PROTEIN, RAT; NOS3 PROTEIN, RAT;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; ANIMAL; CARDIAC MUSCLE; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; METABOLISM; MYOCARDIAL ISCHEMIA; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; GHRELIN; MYOCARDIAL ISCHEMIA; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GHRELIN; SIGNAL TRANSDUCTION;

EID: 84941945893     PISSN: 01969781     EISSN: 18735169     Source Type: Journal    
DOI: 10.1016/j.peptides.2015.09.004     Document Type: Article

References (57)

1. M. Laakso, and J. Kuusisto Insulin resistance and hyperglycaemia in cardiovascular disease development Nat. Rev. Endocrinol. 10 5 2014 293 302
2. P.P. Toth Overview of saxagliptin efficacy and safety in patients with type 2 diabetes and cardiovascular disease or risk factors for cardiovascular disease Vasc. Health Risk Manage. 11 2014 9 23
3. M. Thirunavukkarasu, V. Selvaraju, N.R. Dunna, J.L. Foye, M. Joshi, H. Otani, and N. Maulik Simvastatin treatment inhibits hypoxia inducible factor 1-alpha-(HIF-1alpha)-prolyl-4-hydroxylase 3 (PHD-3) and increases angiogenesis after myocardial infarction in streptozotocin-induced diabetic rat Int. J. Cardiol. 168 3 2013 2474 2480
4. A. Ikeda, S. Matsushita, and Y. Sakakibara Inhibition of protein kinase C β ameliorates impaired angiogenesis in type I diabetic mice complicating myocardial infarction Circ. J. 76 4 2012 943 949
5. F.C. Sasso, D. Torella, O. Carbonara, G.M. Ellison, M. Torella, M. Scardone, C. Marra, R. Nasti, R. Marfella, D. Cozzolino, C. Indolfi, M. Cotrufo, R. Torella, and T. Salvatore Increased vascular endothelial growth factor expression but impaired vascular endothelial growth factor receptor signaling in the myocardium of type 2 diabetic patients with chronic coronary heart disease J. Am. Coll. Cardiol. 46 5 2005 827 834
6. M. Boodhwani, N.R. Sodha, S. Mieno, S.H. Xu, J. Feng, B. Ramlawi, R.T. Clements, and F.W. Sellke Functional, cellular, and molecular characterization of the angiogenic response to chronic myocardial ischemia in diabetes Circulation 116 11 Suppl 2007 I31 I37
7. M. Kojima, H. Hosoda, Y. Date, M. Nakazato, H. Matsuo, and K. Kangawa Ghrelin is a growth-hormone-releasing acylated peptide from stomach Nature 402 6762 1999 656 660
8. M.J. Kleinz, J.J. Maguire, J.N. Skepper, and A.P. Davenport Functional and immunocytochemical evidence for a role of ghrelin and des-octanoyl ghrelin in the regulation of vascular tone in man Cardiovasc. Res. 69 1 2006 227 235
9. S.D. Katugampola, Z. Pallikaros, and A.P. Davenport [125I-His(9)]-ghrelin, a novel radioligand for localizing GHS orphan receptors in human and rat tissue: up-regulation of receptors with athersclerosis Br J. Pharmacol. 134 1 2001 143 149
10. M. Tesauro, F. Schinzari, M. Caramanti, R. Lauro, and C. Cardillo Cardiovascular and metabolic effects of ghrelin Curr. Diabetes Rev. 6 4 2010 228 235
11. M. Tesauro, F. Schinzari, M. Iantorno, S. Rizza, D. Melina, D. Lauro, and C. Cardillo Ghrelin improves endothelial function in patients with metabolic syndrome Circulation 112 19 2005 2986 2992
12. M.J. Yuan, C.X. Huang, Y.H. Tang, X. Wang, H. Huang, Y.J. Chen, and T. Wang A novel peptide ghrelin inhibits neural remodeling after myocardial infarction in rats Eur. J. Pharmacol. 618 1-3 2009 52 57
13. C. Cheyuo, R. Wu, M. Zhou, A. Jacob, G. Coppa, and P. Wang Ghrelin suppresses inflammation and neuronal nitric oxide synthase in focal cerebral ischemia via the vagus nerve Shock 35 3 2011 258 265
14. H. Zhao, G. Liu, Q. Wang, L. Ding, H. Cai, H. Jiang, and Z. Xin Effect of ghrelin on human endothelial cells apoptosis induced by high glucose Biochem. Biophys. Res. Commun. 362 3 2007 677 681
15. Q.H. Liang, Y. Liu, S.S. Wu, R.R. Cui, L.Q. Yuan, and E.Y. Liao Ghrelin inhibits the apoptosis of MC3T3-E1 cells through ERK and AKT signaling pathway Toxicol. Appl. Pharmacol. 272 3 2013 591 597
16. M. Dincə, I.L. Dumitriu, M.B. Gurzu, S.M. Slətineanu, L. Foia, L. Vâţə, E. Cojocaru, and G. Petrescu Ghrelin and ang 1-7 have cumulative vasodilatory effects on pulmonary vessels Rev. Med. Chir. Soc. Med. Nat. Iasi. 114 3 2010 803 807
17. M. Zhang, W.Y. Fang, F. Yuan, X.K. Qu, H. Liu, Y.J. Xu, H. Chen, Y.F. Yu, Y. Shen, and Z.C. Zheng Plasma ghrelin levels are closely associated with severity and morphology of angiographically-detected coronary atherosclerosis in Chineses patients with diabetes mellitus Acta Pharmacol. Sin. 33 4 2012 452 458
18. M. Zhang, W.Y. Fang, X.K. Qu, F. Yuan, W.G. Wang, J. Fei, and Z.G. Wang AMPK activity is down-regulated in endothelial cells of GHS-R (-/-) mice Int. J. Clin. Exp. Pathol. 6 9 2013 1770 1780
19. Mahalaqua Nazli Khatib, Padam Simkhada, and Dilip Gode Cardioprotective effects of ghrelin in heart failure: from gut to heart Heart Views 15 3 2014 74 76
20. A. Ahluwalia, A. Li, G. Cheng, X. Deng, and A.S. Tarnawski Reduced ghrelin in endothelial cells plays important mechanistic role in aging-related impairment of angiogenesis J. Physiol. Pharmacol. 60 2 2009 29 34
21. A. Li, G. Cheng, G.H. Zhu, and A.S. Tarnawski Ghrelin stimulates angiogenesis in human microvascular endothelial cells: Implications beyond GH release Biochem. Biophys. Res. Commun. 353 2 2007 238 243
22. K. Zaniolo, P. Sapieha, Z. Shao, A. Stahl, T. Zhu, S. Tremblay, E. Picard, A. Madaan, M. Blais, P. Lachapelle, J. Mancini, P. Hardy, L.E. Smith, H. Ong, and S. Chemtob Ghrelin modulates physiologic and pathologic retinal angiogenesis through GHSR-1a Invest. Ophthalmol. Vis. Sci. 52 8 2011 5376 5386
23. M.J. Yuan, Huang He, H.Y. Hu, Quan Li, Jiang Hong, and C.X. Huang Myocardial angiogenesis after chronic ghrelin treatment in a rat myocardial infarction model Regul. Pept. 179 1-3 2012 39 42
24. L. Wang, Q. Chen, G. Li, and D. Ke Ghrelin stimulates angiogenesis via GHSR1a-dependent MEK/ERK and PI3K/Akt signal pathways in rat cardiac microvascular endothelial cells Peptides 33 1 2012 92 100
25. X. Chen, Q. Chen, L. Wang, and G. Li Ghrelin induces cell migration through GHSR1a-mediated PI3K/Akt/eNOS/NO signaling pathway in endothelial progenitor cells Metabolism 62 5 2013 743 752
26. F. Wang, D. Huang, W. Zhu, S. Li, M. Yan, M. Wei, and J. Li Selective inhibition of PKCβ2 preserves cardiac function after myocardial infarction and is associated with improved angiogenesis of ischemia myocardium in diabetic rats Int. J. Mol. Med. 32 5 2013 1037 1046
27. Kazuaki Nakajima, Jun Fujita, Makoto Matsui, Shugo Tohyama, Noriko Tamura, Hideaki Kanazawa, Tomohisa Seki, Yoshikazu Kishino, Akinori Hirano, Marina Okada, Ryota Tabei, Motoaki Sano, Shinya Goto, Yasuhiko Tabata, and Keiichi Fukuda Gelatin hydrogel enhances the engraftment of transplanted cardiomyocytes and angiogenesis to ameliorate cardiac function after myocardial infarction PLoS One 10 7 2015 e0133308
28. J. Takagawa, Y. Zhang, M.L. Wong, R.E. Sievers, N.K. Kapasi, Y. Wang, Y. Yeghiazarians, R.J. Lee, W. Grossman, and M.L. Springer Myocardial infarct size measurement in the mouse chronic infarction model: comparison of area- and length-based approaches J. Appl. Physiol. 102 6 1985 2104 2111
29. N. Ouchi, R. Shibata, and K. Walsh AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle Circ. Res. 96 8 2005 838 846
30. D. Nagata, M. Mogi, and K. Walsh AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress J. Biol. Chem. 278 33 2003 31000 31006
31. D. Huang, F.B. Wang, M. Guo, S. Li, M.L. Yan, T. Yu, M. Wei, and J.B. Li Effect of combined treatment with rosuvastatin and protein kinase Cβ2 inhibitor on angiogenesis following myocardial infarction in diabetic rats Int. J. Mol. Med. 35 3 2015 829 838
32. K. Ohashi, T. Enomoto, Y. Joki, R. Shibata, Y. Ogura, Y. Kataoka, Y. Shimizu, T. Kambara, Y. Uemura, D. Yuasa, K. Matsuo, S. Hayakawa, M. Hiramatsu-Ito, T. Murohara, and N. Ouchi Neuron-derived neurotrophic factor functions as a novel modulator that enhances endothelial cell function and revascularization processes J. Biol. Chem. 289 20 2014 14132 14144
33. M. Nakazato, N. Murakami, Y. Date, M. Kojima, H. Matsuo, K. Kangawa, and S. Matsukura A role for ghrelin in the central regulation of feeding Nature 409 6817 2001 194 198
34. M. Tschöp, D.L. Smiley, and M.L. Heiman Ghrelin induces adiposity in rodents Nature 407 6806 2000 908 913
35. P. Carmeliet Angiogenesis in health and disease Nat. Med. 9 6 2003 653 660
36. Y. Wang, K. Narsinh, L. Zhao, D. Sun, D. Wang, Z. Zhang, Z. Sun, R. Zhang, H. Wang, and F. Cao Effects and mechanisms of ghrelin on cardiac microvascular endothelial cells in rats Cell Biol. Int. 35 2 2011 135 140
37. A. Martin, M.R. Komada, and D.C. Sane Abnormal angiogenesis in diabetes mellitus Med. Res. Rev. 23 2 2003 117 145
38. K.Y. Howangyin, and J.S. Silvestre Diabetes mellitus and ischemic diseases: molecular mechanisms of vascular repair dysfunction Arterioscler. Thromb. Vasc. Biol. 34 6 2014 1126 1135
39. L.Y. Ma, D.M. Zhang, Y. Tang, Y. Lu, Y. Zhang, Y. Gao, L. Xia, K.X. Zhao, L.Y. Chai, and Q. Xiao Ghrelin-attenuated cognitive dysfunction in streptozotocin-induced diabetic rats Alzheimer Dis. Assoc. Disord. 25 October-December (4) 2011 352 363
40. V.P. Singh, A. Bali, N. Singh, and A.S. Jaggi Advanced glycation end products and diabetic complications Korean J. Physiol. Pharmacol. 18 1 2014 1 14
41. X. Xu, P. Luo, Y. Wang, Y. Cui, and L. Miao Nuclear factor (erythroid-derived 2)-like 2 (NFE2L2) is a novel therapeutic target for diabetic complications J. Int. Med. Res. 41 1 2013 13 19
42. M.A. Carrillo-Sepulveda, K. Spitler, D. Pandey, D.E. Berkowitz, and T. Matsumoto Inhibition of TLR4 attenuates vascular dysfunction and oxidative stress in diabetic rats J. Mol. Med. (Berl) 2015 10.1007/s00109-015-1318-7 [Epub ahead of print]
43. F. Wang, C. Pu, P. Zhou, P. Wang, D. Liang, Q. Wang, Y. Hu, B. Li, and X. Hao Cinnamaldehyde prevents endothelial dysfunction induced by high glucose by activating Nrf2 Cell Physiol. Biochem. 36 1 2015 315 324
44. T. Zhang, X. Hu, Y. Cai, B. Yi, and Z. Wen Metformin protects against hyperglycemia-induced cardiomyocytes injury by inhibiting the expressions of receptor for advanced glycation end products and high mobility group box 1 protein Mol. Biol. Rep. 41 3 2014 1335 1340
45. H. Chirag Mandavia, R. Annayya Aroor, G. Vincent DeMarco, and R. James Sowers Molecular and metabolic mechanisms of cardiac dysfunction in diabetes Life Sci. 92 11 2013 601 608
46. J.Y. Li, G.Q. Zhong, Z. Wei, W.Y. Xu, H.H. Ke, Z. Ning, and Z.F. Wu Establishment of a rat model of myocardial infarction and the post-infarction changes in electrophysiology and left ventricular function Acta Laboratorium Anim. Sci. Sin. 17 6 2009 419 423
47. M. Zhang, X. Gao, S.J. Bai, X.M. Ye, and J. Zhang Effect of pioglitazone on expression of hypoxia-inducible factor 1α and vascular endothelial growth factor in ischemic hindlimb of diabetic rats Eur. Rev. Med. Pharmacol. Sci. 18 9 2014 1307 1314
48. Randolph Hutter, Walter S. Speidl, Carolina Valdiviezo, Bernhard Sauter, Roberto Corti, Valentin Fuster, and Juan J. Badimon Badimon Macrophages Transmit potent proangiogenic effects of oxldl in vitro and in vivo involving hif-1α activation: a novel aspect of angiogenesis in atherosclerosis J. Cardiovasc. Transl. Res. 6 4 2013 558 569
49. A. Vink, A.H. Schoneveld, D. Lamers, A.J. Houben, P. van der Groep, P.J. van Diest, and G. Pasterkamp HIF-1 alpha expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages Atherosclerosis 195 2 2007 e69 75
50. X.H. Wang, S.F. Chen, H.M. Jin, and R.M. Hu Differential analyses of angiogenesis and expression of growth factors in micro- and macrovascular endothelial cells of type 2 diabetic rats Life Sci. 84 7-8 2009 240 249
51. E. Chou, I. Suzuma, K.J. Way, D. Opland, A.C. Clermont, K. Naruse, K. Suzuma, N.L. Bowling, C.J. Vlahos, L.P. Aiello, and G.L. King Decreased cardiac expression of vascular endothelial growth factor and its receptors in insulin-resistant and diabetic States: a possible explanation for impaired collateral formation in cardiac tissue Circulation 105 3 2002 373 379
52. J.R. Dyck, and G.D. Lopaschuk AMPK alterations in cardiac physiology and pathology: enemy or ally? J. Physiol. 574 Pt (1) 2006 95 112
53. S.V. Penumathsa, M. Thirunavukkarasu, S.M. Samuel, L. Zhan, G. Maulik, M. Bagchi, D. Bagchi, and N. Maulik Niacin bound chromium treatment induces myocardial Glut-4 translocation and caveolar interaction via Akt, AMPK and eNOS phosphorylation in streptozotocin induced diabetic rats after ischemia-referfusion injury Biochim. Biophys. Acta 1792 1 2009 39 48
54. Z. Hu, J. Chen, Q. Wei, and Y. Xia Bidirectional actions of hydrogen peroxide on endothelial nitric-oxide synthase phosphorylation and function: co-commitment and interplay of Akt and AMPK J. Biol. Chem. 283 37 2008 25256 25263
55. Z.P. Chen, K.I. Mitchelhill, B.J. Michell, D. Stapleton, I. Rodriguez-Crespo, L.A. Witters, D.A. Power, P.R. Ortiz de Montellano, and B.E. Kemp AMP-activated protein kinase phosphprylation of endothelial NO synthase FEBS Lett. 443 3 1999 285 289
56. C. Luque, D. ontreras, R. Vargas, H. obles, E. Romo, A. Rios, and B. Escalante The role of nitric oxide in the post-ischemic revascularization process Pharmacol. Ther. 112 2 2006 553 563
57. X. Xu, B.S. Jhun, C.H. Ha, and Z.G. Jin Molecular mechanisms of ghrelin-mediated endothelial nitric oxide synthase activation Endocrinology 149 8 2008 4183 4192