Exendin-4 stimulates proliferation of human coronary artery endothelial cells through eNOS-, PKA- and PI3K/Akt-dependent pathways and requires GLP-1 receptor

Molecular and Cellular Endocrinology

Volumn 325, Issue 1-2, 2010, Pages 26-35

  Erdogdu, O ^a   Nathanson, D ^a   Sjoholm A ^a   Nystrom T ^a   Zhang, Q ^a  

^a STOCKHOLM SÖDER HOSPITAL   (Sweden)

Author keywords

Endothelial cell; Exendin 4; GLP 1 receptor; Glucagon like peptide 1 (GLP 1); Proliferation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 [7-36] AMIDE; GLUCAGON LIKE PEPTIDE 1 [9-36] AMIDE; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; HORMONE RECEPTOR BLOCKING AGENT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; UNCLASSIFIED DRUG;

ARTERY ENDOTHELIUM; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CORONARY ARTERY; DNA SYNTHESIS; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INCUBATION TIME; PRIORITY JOURNAL;

CELL PROLIFERATION; CELLS, CULTURED; CORONARY VESSELS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; NITRIC OXIDE SYNTHASE TYPE III; ONCOGENE PROTEIN V-AKT; PEPTIDES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; RECEPTORS, GLUCAGON; SIGNAL TRANSDUCTION; VENOMS;

EID: 77954384449     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.04.022     Document Type: Article

References (73)

1. Ahanchi S.S., Tsihlis N.D., Kibbe M.R. The role of nitric oxide in the pathophysiology of intimal hyperplasia. J. Vasc. Surg. 2007, 45(Suppl. A):A64-73.
2. Alessi D.R., Andjelkovic M., Caudwell B., Cron P., Morrice N., Cohen P., Hemmings B.A. Mechanism of activation of protein kinase B by insulin and IGF-1. Embo J. 1996, 15:6541-6551.
3. 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.
4. Ban K., Kim K.H., Cho C.K., Sauve M., Diamandis E.P., Backx P.H., Drucker D.J., Husain M. 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 2009, 151:1520-1531.
5. Bauer P.M., Fulton D., Boo Y.C., Sorescu G.P., Kemp B.E., Jo H., Sessa W.C. Compensatory phosphorylation and protein-protein interactions revealed by loss of function and gain of function mutants of multiple serine phosphorylation sites in endothelial nitric-oxide synthase. J. Biol. Chem. 2003, 278:14841-14849.
6. Bellis A., Castaldo D., Trimarco V., Monti M.G., 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. 2009, 29:1207-1212.
7. Berk B.C., Abe J.I., Min W., Surapisitchat J., Yan C. Endothelial atheroprotective and anti-inflammatory mechanisms. Ann. NY Acad. Sci. 2001, 947:93-109. discussion 109-111.
8. Biegelsen E.S., Loscalzo J. Endothelial function and atherosclerosis. Coron. Artery Dis. 1999, 10:241-256.
9. Brubaker P.L., Drucker D.J. Minireview: glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology 2004, 145:2653-2659.
10. Brunn G.J., Williams J., Sabers C., Wiederrecht G., Lawrence J.C., Abraham R.T. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. Embo J. 1996, 15:5256-5267.
11. Buteau J., Roduit R., Susini S., Prentki M. Glucagon-like peptide-1 promotes DNA synthesis, activates phosphatidylinositol 3-kinase and increases transcription factor pancreatic and duodenal homeobox gene 1 (PDX-1) DNA binding activity in beta (INS-1)-cells. Diabetologia 1999, 42:856-864.
12. Buteau J., Spatz M.L., Accili D. Transcription factor FoxO1 mediates glucagon-like peptide-1 effects on pancreatic beta-cell mass. Diabetes 2006, 55:1190-1196.
13. Butt E., Bernhardt M., Smolenski A., Kotsonis P., Frohlich L.G., Sickmann A., Meyer H.E., Lohmann S.M., Schmidt H.H. Endothelial nitric-oxide synthase (type III) is activated and becomes calcium independent upon phosphorylation by cyclic nucleotide-dependent protein kinases. J. Biol. Chem. 2000, 275:5179-5187.
14. Calles-Escandon J., Cipolla M. Diabetes and endothelial dysfunction: a clinical perspective. Endocr. Rev. 2001, 22:36-52.
15. Caplan B.A., Schwartz C.J. Increased endothelial cell turnover in areas of in vivo Evans Blue uptake in the pig aorta. Atherosclerosis 1973, 17:401-417.
16. Chen Z.P., Mitchelhill K.I., Michell B.J., Stapleton D., Rodriguez-Crespo I., Witters L.A., Power D.A., Ortiz de Montellano P.R., Kemp B.E. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999, 443:285-289.
17. Chen J., Somanath P.R., Razorenova O., Chen W.S., Hay N., Bornstein P., Byzova T.V. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 2005, 11:1188-1196.
18. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R., Zeiher A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999, 399:601-605.
19. Dixit M., Loot A.E., Mohamed A., Fisslthaler B., Boulanger C.M., Ceacareanu B., Hassid A., Busse R., Fleming I. Gab1, SHP2, and protein kinase A are crucial for the activation of the endothelial NO synthase by fluid shear stress. Circ. Res. 2005, 97:1236-1244.
20. 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.
21. Edwards S.J., Reader K.L., Lun S., Western A., Lawrence S., McNatty K.P., Juengel J.L. The cooperative effect of growth and differentiation factor-9 and bone morphogenetic protein (BMP)-15 on granulosa cell function is modulated primarily through BMP receptor II. Endocrinology 2008, 149:1026-1030.
22. Fleming I., Fisslthaler B., Dimmeler S., Kemp B.E., Busse R. Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity. Circ. Res. 2001, 88:E68-75.
23. Forstermann U., Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 2006, 113:1708-1714.
24. Fulton D., Gratton J.P., McCabe T.J., Fontana J., Fujio Y., Walsh K., Franke T.F., Papapetropoulos A., Sessa W.C. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999, 399:597-601.
25. Furfine E.S., Harmon M.F., Paith J.E., Garvey E.P. Selective inhibition of constitutive nitric oxide synthase by L-NG-nitroarginine. Biochemistry 1993, 32:8512-8517.
26. Heijnen H.F., Waaijenborg S., Crapo J.D., Bowler R.P., Akkerman J.W., Slot J.W. Colocalization of eNOS and the catalytic subunit of PKA in endothelial cell junctions: a clue for regulated NO production. J. Histochem. Cytochem. 2004, 52:1277-1285.
27. Hermann C., Assmus B., Urbich C., Zeiher A.M., Dimmeler S. Insulin-mediated stimulation of protein kinase Akt: a potent survival signaling cascade for endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2000, 20:402-409.
28. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 1995, 377:239-242.
29. Hui H., Nourparvar A., Zhao X., Perfetti R. Glucagon-like peptide-1 inhibits apoptosis of insulin-secreting cells via a cyclic 5'-adenosine monophosphate-dependent protein kinase A- and a phosphatidylinositol 3-kinase-dependent pathway. Endocrinology 2003, 144:1444-1455.
30. Idris I., Patiag D., Gray S., Donnelly R. Exendin-4 increases insulin sensitivity via a PI-3-kinase-dependent mechanism: contrasting effects of GLP-1. Biochem. Pharmacol. 2002, 63:993-996.
31. Isomaa B., Almgren P., Tuomi T., Forsen B., Lahti K., Nissen M., Taskinen M.R., Groop L. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 2001, 24:683-689.
32. Jiang B.H., Zheng J.Z., Aoki M., Vogt P.K. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:1749-1753.
33. Kawasaki K., Smith R.S., Hsieh C.M., Sun J., Chao J., Liao J.K. Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol. Cell Biol. 2003, 23:5726-5737.
34. Knudsen L.B., Pridal L. Glucagon-like peptide-1-(9-36) amide is a major metabolite of glucagon-like peptide-1-(7-36) amide after in vivo administration to dogs, and it acts as an antagonist on the pancreatic receptor. Eur. J. Pharmacol. 1996, 318:429-435.
35. Kojda G., Noack E. Effects of pentaerythrityl-tetranitrate and isosorbide-5-mononitrate in experimental atherosclerosis. Agents Actions Suppl. 1995, 45:201-206.
36. Kondapalli J., Flozak A.S., Albuquerque M.L. Laminar shear stress differentially modulates gene expression of p120 catenin. Kaiso transcription factor, and vascular endothelial cadherin in human coronary artery endothelial cells. J. Biol. Chem. 2004, 279:11417-11424.
37. Li D., Yang B., Mehta J.L. Ox-LDL induces apoptosis in human coronary artery endothelial cells: role of PKC, PTK, bcl-2, and Fas. Am. J. Physiol. 1998, 275:H568-H576.
38. List J.F., Habener J.F. Glucagon-like peptide 1 agonists and the development and growth of pancreatic beta-cells. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E875-E881.
39. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
40. Marshall S.M., Flyvbjerg A. Prevention and early detection of vascular complications of diabetes. BMJ 2006, 333:475-480.
41. Marzioni M., Alpini G., Saccomanno S., Candelaresi C., Venter J., Rychlicki C., Fava G., Francis H., Trozzi L., Glaser S., Benedetti A. Glucagon-like peptide-1 and its receptor agonist exendin-4 modulate cholangiocyte adaptive response to cholestasis. Gastroenterology 2007, 133:244-255.
42. Michell B.J., Chen Z., Tiganis T., Stapleton D., Katsis F., Power D.A., Sim A.T., Kemp B.E. Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 2001, 276:17625-17628.
43. Montagnani M., Golovchenko I., Kim I., Koh G.Y., Goalstone M.L., Mundhekar A.N., Johansen M., Kucik D.F., Quon M.J., Draznin B. Inhibition of phosphatidylinositol 3-kinase enhances mitogenic actions of insulin in endothelial cells. J. Biol. Chem. 2002, 277:1794-1799.
44. Morbidelli L., Chang C.H., Douglas J.G., Granger H.J., Ledda F., Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 1996, 270:H411-H415.
45. Mount P.F., Kemp B.E., Power D.A. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J. Mol. Cell Cardiol. 2007, 42:271-279.
46. Nakatsubo N., Kojima H., Kikuchi K., Nagoshi H., Hirata Y., Maeda D., Imai Y., Irimura T., Nagano T. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett. 1998, 427:263-266.
47. Nathanson D., Erdogdu O., Pernow J., Zhang Q., Nystrom T. Endothelial dysfunction induced by triglycerides is not restored by exenatide in rat conduit arteries ex vivo. Regul. Pept. 2009, 157:8-13.
48. 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. Physiol. Heart Circ. Physiol. 2005, 289:H2401-H2408.
49. Nishi J., Minamino T., Miyauchi H., Nojima A., Tateno K., Okada S., Orimo M., Moriya J., Fong G.H., Sunagawa K., Shibuya M., Komuro I. Vascular endothelial growth factor receptor-1 regulates postnatal angiogenesis through inhibition of the excessive activation of Akt. Circ. Res. 2008, 103:261-268.
50. Nystrom T. The potential beneficial role of glucagon-like peptide-1 in endothelial dysfunction and heart failure associated with insulin resistance. Horm. Metab. Res. 2008, 40:593-606.
51. Nystrom T., Gutniak M.K., Zhang Q., Zhang F., Holst J.J., Ahren B., Sjoholm A. Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am. J. Physiol. Endocrinol. Metab. 2004, 287:E1209-E1215.
52. Ossum A., van Deurs U., Engstrom T., Jensen J.S., 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. 2009, 60:411-417.
53. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 2001, 22:153-183.
54. Rask-Madsen C., King G.L. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat. Clin. Pract. Endocrinol. Metab. 2007, 3:46-56.
55. Redondo A., Trigo M.V., Acitores A., Valverde I., Villanueva-Penacarrillo M.L. Cell signalling of the GLP-1 action in rat liver. Mol. Cell Endocrinol. 2003, 204:43-50.
56. Rosiansky-Sultan M., Klipper E., Spanel-Borowski K., Meidan R. Inverse relationship between nitric oxide synthases and endothelin-1 synthesis in bovine corpus luteum: interactions at the level of luteal endothelial cell. Endocrinology 2006, 147:5228-5235.
57. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993, 362:801-809.
58. Rudic R.D., Shesely E.G., Maeda N., Smithies O., Segal S.S., Sessa W.C. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Invest. 1998, 101:731-736.
59. Schulz R., Rassaf T., Massion P.B., Kelm M., Balligand J.L. Recent advances in the understanding of the role of nitric oxide in cardiovascular homeostasis. Pharmacol. Ther. 2005, 108:225-256.
60. Seli E., Guzeloglu-Kayisli O., Cakmak H., Kayisli U.A., Selam B., Arici A. Estradiol increases apoptosis in human coronary artery endothelial cells by up-regulating Fas and Fas ligand expression. J. Clin. Endocrinol. Metab. 2006, 91:4995-5001.
61. Torella D., Gasparri C., Ellison G.M., Curcio A., Leone A., Vicinanza C., Galuppo V., Mendicino I., Sacco W., Aquila I., Surace F.C., Luposella M., Stillo G., Agosti V., Cosentino C., Avvedimento E.V., Indolfi C. Differential regulation of vascular smooth muscle and endothelial cell proliferation in vitro and in vivo by cAMP/PKA-activated p85alphaPI3K. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H2015-H2025.
62. Trumper K., Trumper A., Trusheim H., Arnold R., Goke B., Horsch D. Integrative mitogenic role of protein kinase B/Akt in beta-cells. Ann. NY Acad. Sci. 2000, 921:242-250.
63. Vahl T.P., Paty B.W., Fuller B.D., Prigeon R.L., D'Alessio D.A. Effects of GLP-1-(7-36)NH2, GLP-1-(7-37), and GLP-1- (9-36)NH2 on intravenous glucose tolerance and glucose-induced insulin secretion in healthy humans. J. Clin. Endocrinol. Metab. 2003, 88:1772-1779.
64. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., Woscholski R., Parker P.J., Waterfield M.D. Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 2001, 70:535-602.
65. Vlahos C.J., Matter W.F., Hui K.Y., Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 1994, 269:5241-5248.
66. von der Leyen H.E., Gibbons G.H., Morishita R., Lewis N.P., Zhang L., Nakajima M., Kaneda Y., Cooke J.P., Dzau V.J. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1137-1141.
67. Wajchenberg B.L. beta-cell failure in diabetes and preservation by clinical treatment. Endocr. Rev. 2007, 28:187-218.
68. Wang Q., Li L., Xu E., Wong V., Rhodes C., Brubaker P.L. Glucagon-like peptide-1 regulates proliferation and apoptosis via activation of protein kinase B in pancreatic INS-1 beta cells. Diabetologia 2004, 47:478-487.
69. Xu G., Stoffers D.A., Habener J.F., Bonner-Weir S. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 1999, 48:2270-2276.
70. Yang Z.Z., Tschopp O., Baudry A., Dummler B., Hynx D., Hemmings B.A. Physiological functions of protein kinase B/Akt. Biochem. Soc. Trans. 2004, 32:350-354.
71. Zhang X.P., Hintze T.H. cAMP signal transduction induces eNOS activation by promoting PKB phosphorylation. Am J. Physiol. Heart Circ. Physiol. 2006, 290:H2376-H2384.
72. 2+ and insulin secretion. Am. J. Physiol. Cell Physiol. 2006, 291:C466-C475.
73. Ziche M., Morbidelli L., Masini E., Amerini S., Granger H.J., Maggi C.A., Geppetti P., Ledda F. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 1994, 94:2036-2044.