High glucose induces human endothelial dysfunction through an Axl-dependent mechanism

Cardiovascular Diabetology

Volumn 13, Issue 1, 2014, Pages

  Lee, Chien Hsing ^a   Shieh, Yi Shing ^a,b   Hsiao, Fone Ching ^a   Kuo, Feng Chih ^a   Lin, Chih Yuan ^a   Hsieh, Chang Hsun ^a   Hung, Yi Jen ^a  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Diabetes; Endothelial cell; Gas6 Axl

Indexed keywords

CELL MARKER; GLUCOSE; GROWTH ARREST SPECIFIC PROTEIN 6; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE AXL; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; AXL RECEPTOR TYROSINE KINASE; GROWTH ARREST-SPECIFIC PROTEIN 6; ONCOPROTEIN; SIGNAL PEPTIDE;

ADULT; ARTERY; ARTICLE; CELL ADHESION; CELL VIABILITY; CONTROLLED STUDY; DIABETIC PATIENT; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENZYME PHOSPHORYLATION; FEMALE; GENE OVEREXPRESSION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; IMPAIRED GLUCOSE TOLERANCE; INTRACELLULAR SIGNALING; MAJOR CLINICAL STUDY; MALE; MICROVASCULAR ENDOTHELIAL CELL; MIDDLE AGED; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; PROTEIN BLOOD LEVEL; BIOSYNTHESIS; CELL CULTURE; CELL SURVIVAL; DRUG EFFECT; HEK293 CELL LINE; METABOLISM; MULTICENTER STUDY; PHYSIOLOGY; TRANSFORMED CELL LINE; VASCULAR ENDOTHELIUM;

CELL LINE, TRANSFORMED; CELL SURVIVAL; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FEMALE; GLUCOSE; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MIDDLE AGED; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84896709942     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-13-53     Document Type: Article

References (40)

1. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004, 27(5):1047-1053. 10.2337/diacare.27.5.1047, 15111519.
2. Stratton IM, Adler AI, Neil HA, Matthews DR, Manley SE, Cull CA, Hadden D, Turner RC, Holman RR. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000, 321(7258):405-412. 10.1136/bmj.321.7258.405, 27454, 10938048.
3. Ishibashi Y, Matsui T, Maeda S, Higashimoto Y, Yamagishi S. Advanced glycation end products evoke endothelial cell damage by stimulating soluble dipeptidyl peptidase-4 production and its interaction with mannose 6-phosphate/insulin-like growth factor II receptor. Cardiovasc Diabetol 2013, 12:125. 10.1186/1475-2840-12-125, 3765742, 23984879.
4. Xu Y, He Z, King GL. Introduction of hyperglycemia and dyslipidemia in the pathogenesis of diabetic vascular complications. Curr Diab Rep 2005, 5(2):91-97. 10.1007/s11892-005-0034-z, 15794910.
5. Hartge MM, Kintscher U, Unger T. Endothelial dysfunction and its role in diabetic vascular disease. Endocrinol Metab Clin North Am 2006, 35(3):551-560. viii-ix, 10.1016/j.ecl.2006.06.006, 16959585.
6. Moriya J, Ferrara N. Inhibiting the response to VEGF in diabetes. Sci Signal 2014, 7(307):e1.
7. Hafizi S, Dahlback B. Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 2006, 273(23):5231-5244. 10.1111/j.1742-4658.2006.05529.x, 17064312.
8. Linger RM, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008, 100:35-83. 3133732, 18620092.
9. Laurance S, Lemarie CA, Blostein MD. Growth arrest-specific gene 6 (gas6) and vascular hemostasis. Adv Nutr 2012, 3(2):196-203. 10.3945/an.111.001826, 3648720, 22516727.
10. Robins RS, Lemarie CA, Laurance S, Aghourian MN, Wu J, Blostein MD. Vascular Gas6 contributes to thrombogenesis and promotes tissue factor up-regulation after vessel injury in mice. Blood 2013, 121(4):692-699. 10.1182/blood-2012-05-433730, 23149844.
11. Tjwa M, Bellido-Martin L, Lin Y, Lutgens E, Plaisance S, Bono F, Delesque-Touchard N, Herve C, Moura R, Billiau AD, Aparicio C, Levi M, Daemen M, Dewerchin M, Lupu F, Arnout J, Herbert JM, Waer M, Garcia de Frutos P, Dahlback B, Carmeliet P, Hoylaerts MF, Moons L. Gas6 promotes inflammation by enhancing interactions between endothelial cells, platelets, and leukocytes. Blood 2008, 111(8):4096-4105. 10.1182/blood-2007-05-089565, 18156494.
12. Lutgens E, Tjwa M, Garcia De Frutos P, Wijnands E, Beckers L, Dahlback B, Daemen MJ, Carmeliet P, Moons L. Genetic loss of Gas6 induces plaque stability in experimental atherosclerosis. J Pathol 2008, 216(1):55-63. 10.1002/path.2381, 18570189.
13. Ekman C, Gottsater A, Lindblad B, Dahlback B. Plasma concentrations of Gas6 and soluble Axl correlate with disease and predict mortality in patients with critical limb ischemia. Clin Biochem 2010, 43(10-11):873-876.
14. Clauser S, Meilhac O, Bieche I, Raynal P, Bruneval P, Michel JB, Borgel D. Increased secretion of Gas6 by smooth muscle cells in human atherosclerotic carotid plaques. Thromb Haemost 2012, 107(1):140-149.
15. Nagai K, Arai H, Yanagita M, Matsubara T, Kanamori H, Nakano T, Iehara N, Fukatsu A, Kita T, Doi T. Growth arrest-specific gene 6 is involved in glomerular hypertrophy in the early stage of diabetic nephropathy. J Biol Chem 2003, 278(20):18229-18234. 10.1074/jbc.M213266200, 12644472.
16. Cavet ME, Smolock EM, Ozturk OH, World C, Pang J, Konishi A, Berk BC. Gas6-axl receptor signaling is regulated by glucose in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2008, 28(5):886-891. 10.1161/ATVBAHA.108.162693, 2731942, 18292389.
17. Hung YJ, Lee CH, Chu NF, Shieh YS. Plasma protein growth arrest-specific 6 levels are associated with altered glucose tolerance, inflammation, and endothelial dysfunction. Diabetes Care 2010, 33(8):1840-1844. 10.2337/dc09-1073, 2909074, 20504897.
18. Goruppi S, Ruaro E, Schneider C. Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 1996, 12(3):471-480.
19. Goruppi S, Ruaro E, Varnum B, Schneider C. Requirement of phosphatidylinositol 3-kinase-dependent pathway and Src for Gas6-Axl mitogenic and survival activities in NIH 3 T3 fibroblasts. Mol Cell Biol 1997, 17(8):4442-4453. 232298, 9234702.
20. Goruppi S, Ruaro E, Varnum B, Schneider C. Gas6-mediated survival in NIH3T3 cells activates stress signalling cascade and is independent of Ras. Oncogene 1999, 18(29):4224-4236. 10.1038/sj.onc.1202788, 10435635.
21. Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, Atchison RE, McLaughlin J, Swift SE, Pali ES, Yam G, Wong S, Lasaga J, Shen MR, Yu S, Xu W, Hitoshi Y, Bogenberger J, Nor JE, Payan DG, Lorens JB. Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 2005, 65(20):9294-9303. 10.1158/0008-5472.CAN-05-0993, 16230391.
22. Gallicchio M, Mitola S, Valdembri D, Fantozzi R, Varnum B, Avanzi GC, Bussolino F. Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Axl tyrosine kinase receptor. Blood 2005, 105(5):1970. 10.1182/blood-2004-04-1469, 15507525.
23. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, Kallop D, Ludlam MJ, Pei L. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009, 28(39):3442-3455. 10.1038/onc.2009.212, 19633687.
24. Korshunov VA, Mohan AM, Georger MA, Berk BC. Axl, a receptor tyrosine kinase, mediates flow-induced vascular remodeling. Circ Res 2006, 98(11):1446-1452. 10.1161/01.RES.0000223322.16149.9a, 16627783.
25. Korshunov VA, Daul M, Massett MP, Berk BC. Axl mediates vascular remodeling induced by deoxycorticosterone acetate-salt hypertension. Hypertension 2007, 50(6):1057-1062. 10.1161/HYPERTENSIONAHA.107.096289, 17923589.
26. D'Arcangelo D, Gaetano C, Capogrossi MC. Acidification prevents endothelial cell apoptosis by Axl activation. Circ Res 2002, 91(7):e4-12. 10.1161/01.RES.0000036753.50601.E9, 12364394.
27. Konishi A, Aizawa T, Mohan A, Korshunov VA, Berk BC. Hydrogen peroxide activates the Gas6-Axl pathway in vascular smooth muscle cells. J Biol Chem 2004, 279(27):28766-28770. 10.1074/jbc.M401977200, 15123721.
28. Son BK, Kozaki K, Iijima K, Eto M, Nakano T, Akishita M, Ouchi Y. Gas6/Axl-PI3K/Akt pathway plays a central role in the effect of statins on inorganic phosphate-induced calcification of vascular smooth muscle cells. Eur J Pharmacol 2007, 556(1-3):1-8.
29. Kim H, Kim HJ, Lee K, Kim JM, Kim HS, Kim JR, Ha CM, Choi YK, Lee SJ, Kim JY, Harris RA, Jeong D, Lee IK. alpha-Lipoic acid attenuates vascular calcification via reversal of mitochondrial function and restoration of Gas6/Axl/Akt survival pathway. J Cell Mol Med 2012, 16(2):273-286. 10.1111/j.1582-4934.2011.01294.x, 21362131.
30. Korshunov VA. Axl-dependent signalling: a clinical update. Clin Sci 2012, 122(8):361-368. 10.1042/CS20110411, 3609429, 22187964.
31. Sheetz MJ, King GL. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 2002, 288(20):2579-2588. 10.1001/jama.288.20.2579, 12444865.
32. Abaci A, Oguzhan A, Kahraman S, Eryol NK, Unal S, Arinc H, Ergin A. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 1999, 99(17):2239-2242. 10.1161/01.CIR.99.17.2239, 10226087.
33. Varma S, Lal BK, Zheng R, Breslin JW, Saito S, Pappas PJ, Hobson RW, Duran WN. Hyperglycemia alters PI3k and Akt signaling and leads to endothelial cell proliferative dysfunction. Am J Physiol Heart Circ Physiol 2005, 289(4):H1744-1751. 10.1152/ajpheart.01088.2004, 1618822, 15964918.
34. Hasanbasic I, Rajotte I, Blostein M. The role of gamma-carboxylation in the anti-apoptotic function of gas6. J Thromb Haemost 2005, 3(12):2790-2797. 10.1111/j.1538-7836.2005.01662.x, 16359517.
35. Altavilla D, Saitta A, Cucinotta D, Galeano M, Deodato B, Colonna M, Torre V, Russo G, Sardella A, Urna G, Campo GM, Cavallari V, Squadrito G, Squadrito F. Inhibition of lipid peroxidation restores impaired vascular endothelial growth factor expression and stimulates wound healing and angiogenesis in the genetically diabetic mouse. Diabetes 2001, 50(3):667-674. 10.2337/diabetes.50.3.667, 11246889.
36. Pinter E, Haigh J, Nagy A, Madri JA. Hyperglycemia-induced vasculopathy in the murine conceptus is mediated via reductions of VEGF-A expression and VEGF receptor activation. Am J Pathol 2001, 158(4):1199-1206. 10.1016/S0002-9440(10)64069-2, 1891927, 11290536.
37. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000, 6(4):389-395. 10.1038/74651, 10742145.
38. Goruppi S, Chiaruttini C, Ruaro ME, Varnum B, Schneider C. Gas6 induces growth, beta-catenin stabilization, and T-cell factor transcriptional activation in contact-inhibited C57 mammary cells. Mol Cell Biol 2001, 21(3):902-915. 10.1128/MCB.21.3.902-915.2001, 86681, 11154277.
39. Angelillo-Scherrer A, Burnier L, Flores N, Savi P, DeMol M, Schaeffer P, Herbert JM, Lemke G, Goff SP, Matsushima GK, Earp HS, Vesin C, Hoylaerts MF, Plaisance S, Collen D, Conway EM, Wehrle-Haller B, Carmeliet P. Role of Gas6 receptors in platelet signaling during thrombus stabilization and implications for antithrombotic therapy. J Clin Invest 2005, 115(2):237-246. 10.1172/JCI22079, 544035, 15650770.
40. McCloskey P, Fridell YW, Attar E, Villa J, Jin Y, Varnum B, Liu ET. GAS6 mediates adhesion of cells expressing the receptor tyrosine kinase Axl. J Biol Chem 1997, 272(37):23285-23291. 10.1074/jbc.272.37.23285, 9287338.