Suppression of c-Cbl tyrosine phosphorylation inhibits neointimal formation in balloon-injured rat arteries

Circulation

Volumn 118, Issue 7, 2008, Pages 764-772

  Tang, Zhihui ^a   Wang, Ying ^a   Fan, Yanbo ^a   Zhu, Yi ^a   Chien, Shu ^b,d   Wang, Nanping ^a,c  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Angioplasty; Gene therapy; Restenosis; Signal transduction; Vessels

Indexed keywords

CBL PROTEIN; FIBROBLAST GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN KINASE B; ANGIOGENIC FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PLATELET-DERIVED GROWTH FACTOR BB; PROTEIN KINASE; TYROSINE;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY INJURY; ARTICLE; BLOOD VESSEL INJURY; CAROTID ARTERY; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; HYPERPLASIA; INTIMA; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RESTENOSIS; SMOOTH MUSCLE FIBER; UBIQUITINATION; WESTERN BLOTTING; ANGIOGENESIS; ANIMAL; BALLOON DILATATION; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; VASCULAR SMOOTH MUSCLE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANGIOGENESIS INDUCING AGENTS; ANIMALS; BALLOON DILATATION; CAROTID ARTERIES; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLAST GROWTH FACTORS; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-CBL; RATS; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; TUNICA INTIMA; TYROSINE;

EID: 50349102094     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.107.761932     Document Type: Article

References (43)

1. Lovqvist A, Emanuelsson H, Nilsson J, Lundqvist H, Carlsson J. Patho-physiological mechanisms for restenosis following coronary angioplasty: possible preventive alternatives. J Intern Med. 1993;233:215-226.
2. Schwartz SM, deBlois D, O'Brien ER. The intima: soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
3. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science. 1991;253:1129-1132.
4. Jawien A, Bowen-Pope DF, Lindner V, Schwartz SM, Clowes AW. Platelet-derived growth factor promotes smooth muscle migration and intimai thickening in a rat model of balloon angioplasty. J Clin Invest. 1992;89:507-511.
5. Agrotis A, Kanellakis P, Kostolias G, Di Vitto G, Wei C, Hannan R, Jennings G, Bobik A. Proliferation of neointimal smooth muscle cells after arterial injury: dependence on interactions between fibroblast growth factor receptor-2 and fibroblast growth factor-9. J Biol Chem. 2004;279:42221-42229.
6. Blake TJ, Shapiro M, Morse HC III, Langdon WY. The sequences of the human and mouse c-cbl proto-oncogenes show v-cbl was generated by a large truncation encompassing a proline-rich domain and a leucine zipper-like motif. Oncogene. 1991;6:653-657.
7. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol. 2001;2:294-307.
8. Swaminathan G, Tsygankov AY. The Cbl family proteins: ring leaders in regulation of cell signaling. J Cell Physiol. 2006;209:21-43.
9. Hartley D, Meisner H, Corvera S. Specific association of the beta isoform of the p85 subunit of phosphatidylinositol-3 kinase with the proto-oncogene c-cbl. J Biol Chem. 1995;270:18260-18263.
10. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I. FRS2 alpha attenuates FGF receptor signaling by Grb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci USA. 2002;99:6684-6689.
11. Rao N, Dodge I, Band H. The Cbl family of ubiquitin ligases: critical negative regulators of tyrosine kinase signaling in the immune system. J Leukoc Biol. 2002;71:753-763.
12. Feng Q, Baird D, Peng X, Wang J, Ly T, Guan JL, Cerione RA. Cool-1 functions as an essential regulatory node for EGF receptor- and Src-mediated cell growth. Nat Cell Biol. 2006;8:945-956.
13. Chiusaroli R, Sanjay A, Henriksen K, Engsig MT, Home WC, Gu H, Baron R. Deletion of the gene encoding c-Cbl alters the ability of osteoclasts to migrate, delaying resorption and ossification of cartilage during the development of long bones. Dev Biol. 2003;261:537-547.
14. Molero JC, Turner N, Thien CB, Langdon WY, James DE, Cooney GJ. Genetic ablation of the c-Cbl ubiquitin ligase domain results in increased energy expenditure and improved insulin action. Diabetes. 2006;55:3411-3417.
15. Saci A, Pain S, Rendu F, Bachelot-Loza C. Fc receptor-mediated platelet activation is dependent on phosphatidylinositol 3-kinase activation and involves p120(Cbl). J Biol Chem. 1999;274:1898-1904.
16. Miao H, Yuan S, Wang Y, Tsygankov A, Chien S. Role of Cbl in shear-activation of PI 3-kinase and JNK in endothelial cells. Biochem Biophys Res Commun. 2002;292:892-899.
17. Wang Y, Chang J, Li YC, Li YS, Shyy JY, Chien S. Shear stress and VEGF activate IKK via the Flk-1/Cbl/Akt signaling pathway. Am J Physiol Heart Circ Physiol. 2004;286:H685-H692.
18. Singh AJ, Meyer RD, Navruzbekov G, Shelke R, Duan L, Band H, Leeman SE, Rahimi N. A critical role for the E3-ligase activity of c-Cbl in VEGFR-2-mediated PLCγl activation and angiogenesis. Proc Natl Acad Sci USA. 2007;104:5413-5418.
19. Feshchenko EA, Langdon WY, Tsygankov AY. Fyn, Yes, and Syk phosphorylation sites in c-Cbl map to the same tyrosine residues that become phosphorylated in activated T cells. J Biol Chem. 1998;273: 8323-8331.
20. Wang N, Verna L, Liao H, Ballard A, Zhu Y, Stemerman MB. Adenovirus-mediated overexpression of dominant-negative mutant of c-Jun prevents intercellular adhesion molecule-1 induction by LDL: a critical role for activator protein-1 in endothelial activation. Arterioscler Thromb Vase Biol. 2001;21:1414-1420.
21. Wang N, Verna L, Chen NG, Chen J, Li H, Forman BM, Stemerman MB. Constitutive activation of peroxisome proliferator-activated receptor-gamma suppresses pro-inflammatory adhesion molecules in human vascular endothelial cells. J Biol Chem. 2002;277:34176-34181.
22. Qin X, Tian J, Zhang P, Fan Y, Chen L, Guan Y, Fu Y, Zhu Y, Chien S, Wang N. Laminar shear stress up-regulates the expression of stearoyl-CoA desaturase-1 in vascular endothelial cells. Cardiovasc Res. 2007;74:506-514.
23. Hsu PP, Li S, Li YS, Usami S, Ratcliffe A, Wang X, Chien S. Effects of flow patterns on endothelial cell migration into a zone of mechanical denudation. Biochem Biophys Res Commun. 2001;285:751-759.
24. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothe-lium. Lab Invest. 1983;49:327-333.
25. Feshchenko EA, Shore SK, Tsygankov AY. Tyrosine phosphorylation of c-Cbl facilitates adhesion and spreading while suppressing anchorage-independent growth of V-Abl-transformed NIH3T3 fibroblasts. Oncogene. 1999;18:3703-3715.
26. Miyake S, Mullane-Robinson KP, Lill NL, Douillard P, Band H. Cbl-mediated negative regulation of platelet-derived growth factor receptor-dependent cell proliferation: a critical role for Cbl tyrosine kinase-binding domain. J Biol Chem. 1999;274:16619-16628.
27. Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res. 1994;75:539-545.
28. Liu MW, Roubin GS, King SB III. Restenosis after coronary angio-plasty. Potential biologic determinants and role of intimai hyperplasia. Circulation. 1989;79:1374-1387.
29. Kamei T, Machida K, Nimura Y, Senga T, Yamada I, Yoshii S, Matsuda S, Hamaguchi M. c-Cbl protein in human cancer tissues is frequently tyrosine phosphorylated in a tumor-specific manner. Int J Oncol. 2000; 17:335-339.
30. Fukazawa T, Reedquist KA, Trub T, Soltoff S, Panchamoorthy G, Druker B, Cantley L, Shoelson SE, Band H. The SH3 domain-binding T cell tyrosyl phosphoprotein pi20: demonstration of its identity with the c-cbl protooncogene product and in vivo complexes with Fyn, Grb2, and phosphatidylinositol 3-kinase. J Biol Chem. 1995;270:19141-19150.
31. Meisner H, Conway BR, Hartley D, Czech MP. Interactions of Cbl with Grb2 and phosphatidylinositol 3′-kinase in activated Jurkat cells. Mol Cell Biol. 1995;15:3571-3578.
32. Stabile E, Zhou YF, Saji M, Castagna M, Shou M, Kinnaird TD, Baffour R, Ringel MD, Epstein SE, Fuchs S. Akt controls vascular smooth muscle cell proliferation in vitro and in vivo by delaying G1/S exit. Circ Res. 2003;93:1059-1065.
33. Zhou RH, Lee TS, Tsou TC, Rannou F, Li YS, Chien S, Shyy JY. Stent implantation activates Akt in the vessel wall: role of mechanical stretch in vascular smooth muscle cells. Arterioscler Thromb Vase Biol. 2003;23: 2015-2020.
34. Inoki K, Guan KL. Complexity of the TOR signaling network. Trends Cell Biol. 2006;16:206-212.
35. Zohlnhofer D, Nuhrenberg TG, Neumann FJ, Richter T, May AE, Schmidt R, Denker K, Clauss MA, Schomig A, Baeuerle PA. Rapamycin effects transcriptional programs in smooth muscle cells controlling pro-liferative and inflammatory properties. Mol Pharmacol. 2004;65: 880-889.
36. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science. 1999;286:309-312.
37. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, Beguinot L, Geiger B, Yarden Y. c-Cb1/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 1998;12:3663-3674.
38. Miyake S, Lupher ML Jr, Druker B, Band H. The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor alpha. Proc Natl Acad Sci USA. 1998;95:7927-7932.
39. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, Lipkowitz S, Yarden Y. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell. 1999;4: 1029-1040.
40. Tvorogov D, Carpenter G. EGF-dependent association of phospholipase C-gammal with c-Cbl. Exp Cell Res. 2002;277:86-94.
41. Sanjay A, Houghton A, Neff L, DiDomenico E, Bardelay C, Antoine E, Levy J, Gailit J, Bowtell D, Home WC, Baron R. Cbl associates with Pyk2 and Src to regulate Src kinase activity, alpha(v) beta(3) integrin-mediated signaling, cell adhesion, and osteoclast motility. J Cell Biol. 2001;152:181-195.
42. Sawasdikosol S, Chang JH, Pratt JC, Wolf G, Shoelson SE, Burakoff SJ. Tyrosine-phosphorylated Cbl binds to Crk after T cell activation. J Immunol. 1996;157:110-116.
43. Soubeyran P, Kowanetz K, Szymkiewicz I, Langdon WY, Dikic I. Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature. 2002;416:183-187.