Gas6-Axl receptor signaling is regulated by glucose in vascular smooth muscle cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 28, Issue 5, 2008, Pages 886-891

  Cavet, Megan E ^a   Smolock, Elaine M ^a   Ozturk, Oktay H ^a   World, Cameron ^a   Pang, Jinjiang ^a   Konishi, Atsushi ^a   Berk, Bradford C ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Axl; Glucose; Signaling; Vascular smooth muscle migration

Indexed keywords

GLUCOSE; GROWTH ARREST SPECIFIC PROTEIN 6; LIGAND; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AXL; PROTEIN KINASE B; PROTEIN P85; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 2; REACTIVE OXYGEN METABOLITE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DIABETIC ANGIOPATHY; DIABETIC NEPHROPATHY; ENZYME ACTIVATION; GLUCOSE BLOOD LEVEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE, SMOOTH, VASCULAR; ONCOGENE PROTEINS; PROTEIN KINASES; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 42149130373     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.108.162693     Document Type: Article

References (41)

1. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA. 2002;287:2570-2581.
2. Creager MA, Luscher TF, Cosentino F, Beckman JA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation. 2003;108:1527-1532.
3. King GL, Kunisaki M, Nishio Y, Inoguchi T, Shiba T, Xia P. Biochemical and molecular mechanisms in the development of diabetic vascular complications. Diabetes. 1996;45 Suppl 3:S105-108.
4. Melaragno MG, Fridell YW, Berk BC. The Gas6/Axl system: a novel regulator of vascular cell function. Trends Cardiovasc Med. 1999;9:250-253.
5. Berk BC. Angiotensin II signal transduction in vascular smooth muscle: pathways activated by specific tyrosine kinases. J Am Soc Nephrol. 1999;10 Suppl 11:S62-S68.
6. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C, Mattsson K, Fisher J, Gies DR, Jones PF, et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell. 1995;80:661- 670.
7. Varnum BC, Young C, Elliott G, Garcia A, Bartley TD, Fridell YW, Hunt RW, Trail G, Clogston C, Toso RJ, Yanagihara D, Bennett L, Sylber M, Merewether LA, Tseng A, Escobar E, Liu T, Yamane HK. Axl receptor tyrosine kinase stimulated by the vitamin K-dependent protein encoded by growth-arrest-specific gene 6. Nature. 1995;373:623- 626.
8. Fridell YW, Jin Y, Quilliam LA, Burchert A, McCloskey P, Spizz G, Varnum B, Der C, Liu ET. Differential activation of the Ras/extracellular-signal- regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Mol Cell Biol. 1996;16:135-145.
9. 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 3T3 fibroblasts. Mol Cell Biol. 1997;17:4442-4453.
10. 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;18:4224-4236.
11. Melaragno M, Cavet M, Yan C, Tai L, Jin Z, Haendeler J, Berk B. Gas6 inhibits apoptosis in vascular smooth muscle: role of Axl kinase and Akt. J Mol Cell Cardiol. In press.
12. Fridell YW, Villa J Jr, Attar EC, Liu ET. GAS6 induces Axl-mediated chemotaxis of vascular smooth muscle cells. J Biol Chem. 1998;273:7123-7126.
13. 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;278:18229-18234.
14. Melaragno MG, Wuthrich DA, Poppa V, Gill D, Lindner V, Berk BC, Corson MA. Increased expression of Axl tyrosine kinase after vascular injury and regulation by G protein-coupled receptor agonists in rats. Circ Res. 1998;83:697-704.
15. 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;279:28766-28770.
16. Konishi A, Berk BC. Epidermal growth factor receptor transactivation is regulated by glucose in vascular smooth muscle cells. J Biol Chem. 2003;278:35049-35056.
17. Ishida T, Ishida M, Suero J, Takahashi M, Berk BC. Agonist-stimulated cytoskeletal reorganization and signal transduction at focal adhesions in vascular smooth muscle cells require c-Src. J Clin Invest. 1999;103:789-797.
18. Hwang JB, Frost SC. Effect of alternative glycosylation on insulin receptor processing. J Biol Chem. 1999;274:22813-22820.
19. Kitzman HH Jr, McMahon RJ, Williams MG, Frost SC. Effect of glucose deprivation of GLUT 1 expression in 3T3-L1 adipocytes. J Biol Chem. 1993;268:1320-1325.
20. Zheng Z, Cummings RD, Pummill PE, Kincade PW. Growth as a solid tumor or reduced glucose concentrations in culture reversibly induce CD44-mediated hyaluronan recognition by Chinese hamster ovary cells. J Clin Invest. 1997;100:1217-1229.
21. Parodi AJ. Role of N-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J. 2000;348 Pt 1:1-13.
22. 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;12:471-480.
23. 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;105:1970-1976.
24. Deb TB, Wong L, Salomon DS, Zhou G, Dixon JE, Gutkind JS, Thompson SA, Johnson GR. A common requirement for the catalytic activity and both SH2 domains of SHP-2 in mitogen-activated protein (MAP) kinase activation by the ErbB family of receptors. A specific role for SHP-2 in map, but not c-Jun amino-terminal kinase activation. J Biol Chem. 1998;273:16643-16646.
25. Maroun CR, Naujokas MA, Holgado-Madruga M, Wong AJ, Park M. The tyrosine phosphatase SHP-2 is required for sustained activation of extracellular signal-regulated kinase and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol Cell Biol. 2000;20:8513-8525.
26. Shi ZQ, Yu DH, Park M, Marshall M, Feng GS. Molecular mechanism for the Shp-2 tyrosine phosphatase function in promoting growth factor stimulation of Erk activity. Mol Cell Biol. 2000;20:1526-1536.
27. Oudit GY, Sun H, Kerfant BG, Crackower MA, Penninger JM, Backx PH. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J Mol Cell Cardiol. 2004;37:449-471.
28. Li H, Telemaque S, Miller RE, Marsh JD. High glucose inhibits apoptosis induced by serum deprivation in vascular smooth muscle cells via upregulation of Bcl-2 and Bcl-xl. Diabetes. 2005;54:540 -545.
29. Sakuma H, Yamamoto M, Okumura M, Kojima T, Maruyama T, Yasuda K. High glucose inhibits apoptosis in human coronary artery smooth muscle cells by increasing bcl-xL and bfl-1/A1. Am J Physiol Cell Physiol. 2002;283:C422-C428.
30. Hall JL, Matter CM, Wang X, Gibbons GH. Hyperglycemia inhibits vascular smooth muscle cell apoptosis through a protein kinase C-dependent pathway. Circ Res. 2000;87:574 -580.
31. Yamaguchi H, Igarashi M, Hirata A, Sugae N, Tsuchiya H, Jimbu Y, Tominaga M, Kato T. Altered PDGF-BB-induced p38 MAP kinase activation in diabetic vascular smooth muscle cells: roles of protein kinase C-delta. Arterioscler Thromb Vasc Biol. 2004;24:2095-2101.
32. Natarajan R, Scott S, Bai W, Yerneni KK, Nadler J. Angiotensin II signaling in vascular smooth muscle cells under high glucose conditions. Hypertension. 1999;33:378-384.
33. Dormond O, Madsen JC, Briscoe DM. The effects of mTOR-Akt interactions on anti-apoptotic signaling in vascular endothelial cells. J Biol Chem. 2007;282:23679-23686.
34. Braunger J, Schleithoff L, Schulz AS, Kessler H, Lammers R, Ullrich A, Bartram CR, Janssen JW. Intracellular signaling of the Ufo/Axl receptor tyrosine kinase is mediated mainly by a multi-substrate docking-site. Oncogene. 1997;14:2619-2631.
35. Hafizi S, Alindri F, Karlsson R, Dahlback B. Interaction of Axl receptor tyrosine kinase with C1-TEN, a novel C1 domain-containing protein with homology to tensin. Biochem Biophys Res Commun. 2002;299:793-800.
36. Fernandes H, Cohen S, Bishayee S. Glycosylation-induced conformational modification positively regulates receptor-receptor association: a study with an aberrant epidermal growth factor receptor (EGFRvIII/DeltaEGFR) expressed in cancer cells. J Biol Chem. 2001;276:5375-5383.
37. Whitson KB, Whitson SR, Red-Brewer ML, McCoy AJ, Vitali AA, Walker F, Johns TG, Beth AH, Staros JV. Functional effects of glycosylation at Asn-579 of the epidermal growth factor receptor. Biochemistry. 2005;44:14920-14931.
38. Yu X, Sharma KD, Takahashi T, Iwamoto R, Mekada E. Ligand-independent dimer formation of epidermal growth factor receptor (EGFR) is a step separable from ligand-induced EGFR signaling. Mol Biol Cell. 2002;13:2547-2557.
39. Nagai K, Matsubara T, Mima A, Sumi E, Kanamori H, Iehara N, Fukatsu A, Yanagita M, Nakano T, Ishimoto Y, Kita T, Doi T, Arai H. Gas6 induces Akt/mTOR-mediated mesangial hypertrophy in diabetic nephropathy. Kidney Int. 2005;68:552-561.
40. Faries PL, Rohan DI, Takahara H, Wyers MC, Contreras MA, Quist WC, King GL, Logerfo FW. Human vascular smooth muscle cells of diabetic origin exhibit increased proliferation, adhesion, and migration. J Vasc Surg. 2001;33:601-607.
41. Suzuki LA, Poot M, Gerrity RG, Bornfeldt KE. Diabetes accelerates smooth muscle accumulation in lesions of atherosclerosis: lack of direct growth-promoting effects of high glucose levels. Diabetes. 2001;50:851-860.