Ligand-stimulated VEGFR2 signaling is regulated by co-ordinated trafficking and proteolysis

Traffic

Volumn 11, Issue 1, 2010, Pages 161-174

  Bruns, Alexander F ^a   Herbert, Shane P ^a   Odell, Adam F ^a   Jopling, Helen M ^a   Hooper, Nigel M ^a   Zachary, Ian C ^b   Walker, John H ^a   Ponnambalam, Sreenivasan ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Endosome; Lysosome; Migration; Proteolysis; Signaling; VEGF A; VEGFR2

Indexed keywords

CLATHRIN HEAVY CHAIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; PROTEASOME; PROTEIN KINASE B; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENDOTHELIUM CELL; GENE ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION;

CELL LINE; CELL MOVEMENT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOSOMES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; LIGANDS; LYSOSOMES; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PATHOLOGIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 71849097154     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.01001.x     Document Type: Article

References (58)

1. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
2. Holmes K, Roberts OL, Thomas AM, Cross MJ. Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 2007, 19:2003-2012.
3. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005, 438:932-936.
4. Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005, 438:937-945.
5. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature 2005, 438:967-974.
6. Shibuya M, Yamaguchi S, Yamane A, Ikeda T, Tojo A, Matsushime H, Sato M. Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 1990, 5:519-524.
7. Terman BI, Carrion ME, Kovacs E, Rasmussen BA, Eddy RL, Shows TB. Identification of a new endothelial cell growth factor receptor tyrosine kinase. Oncogene 1991, 6:1677-1683.
8. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 1998, 95:9349-9354.
9. Fong GH, Zhang L, Bryce DM, Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 1999, 126:3015-3025.
10. Duval M, Bedard-Goulet S, Delisle C, Gratton JP. Vascular endothelial growth factor-dependent down-regulation of Flk-1/KDR involves Cbl-mediated ubiquitination. Consequences on nitric oxide production from endothelial cells. J Biol Chem 2003, 278:20091-20097.
11. 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 PLCγ1 activation and angiogenesis. Proc Natl Acad Sci USA 2007, 104:5413-5418.
12. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J Cell Biol 2006, 174:593-604.
13. Grazia Lampugnani M, Zanetti A, Corada M, Takahashi T, Balconi G, Breviario F, Orsenigo F, Cattelino A, Kemler R, Daniel TO, Dejana E. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J Cell Biol 2003, 161:793-804.
14. Singh AJ, Meyer RD, Band H, Rahimi N. The carboxyl terminus of VEGFR-2 is required for PKC-mediated down-regulation. Mol Biol Cell 2005, 16:2106-2118.
15. Wong C, Jin ZG. Protein kinase C-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J Biol Chem 2005, 280:33262-33269.
16. Qin L, Zeng H, Zhao D. Requirement of protein kinase D tyrosine phosphorylation for VEGF-A165-induced angiogenesis through its interaction and regulation of phospholipase Cgamma phosphorylation. J Biol Chem 2006, 281:32550-32558.
17. Haglund K, Di Fiore PP, Dikic I. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem Sci 2003, 28:598-603.
18. Marmor MD, Yarden Y. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene 2004, 23:2057-2070.
19. Ewan LC, Jopling HM, Jia H, Mittar S, Bagherzadeh A, Howell GJ, Walker JH, Zachary IC, Ponnambalam S. Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic 2006, 7:1270-1282.
20. Noble ME, Endicott JA, Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004, 303:1800-1805.
21. Lainakis G, Bamias A. Targeting angiogenesis in renal cell carcinoma. Curr Cancer Drug Targets 2008, 8:349-358.
22. Le Tourneau C, Raymond E, Faivre S. Sunitinib: a novel tyrosine kinase inhibitor. A brief review of its therapeutic potential in the treatment of renal carcinoma and gastrointestinal stromal tumors (GIST). Ther Clin Risk Manag 2007, 3:341-348.
23. Takahashi T, Shibuya M. The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLCγ pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene 1997, 14:2079-2089.
24. Hicke L. Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 1999, 9:107-112.
25. Pickart CM. Ubiquitin in chains. Trends Biochem Sci 2000, 25:544-548.
26. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2001, 2:169-178.
27. Hicke L. Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J 1997, 11:1215-1226.
28. Smith RM, Jarett L. Ultrastructural basis for chloroquine-induced increase in intracellular insulin in adipocytes: alteration of lysosomal function. Proc Natl Acad Sci USA 1982, 79:7302-7306.
29. van Weert AW, Dunn KW, Gueze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995, 130:821-834.
30. Murdaca J, Treins C, Monthouel-Kartmann MN, Pontier-Bres R, Kumar S, Van Obberghen E, Giorgetti-Peraldi S. Grb10 prevents Nedd4-mediated vascular endothelial growth factor receptor-2 degradation. J Biol Chem 2004, 279:26754-26761.
31. Longva KE, Blystad FD, Stang E, Larsen AM, Johannessen LE, Madshus IH. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J Cell Biol 2002, 156:843-854.
32. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315:201-205.
33. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 2003, 5:461-466.
34. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006, 21:737-748.
35. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nature Rev Mol Cell Biol 2006, 7:359-371.
36. Mittar S, Ulyatt C, Howell GJ, Bruns AF, Zachary IC, Walker JH, Ponnambalam S. VEGFR1 receptor tyrosine kinase localization to the Golgi apparatus is calcium-dependent. Exp Cell Res 2009, 315:877-889.
37. Maiti D, Xu Z, Duh EJ. Vascular endothelial growth factor induces MEF2C and MEF2-dependent activity in endothelial cells. Invest Ophthalmol Vis Sci 2008, 49:3640-3648.
38. Garrett TA, Van Buul JD, Burridge K. VEGF-induced Rac1 activation in endothelial cells is regulated by the guanine nucleotide exchange factor Vav2. Exp Cell Res 2007, 313:3285-3297.
39. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, Bussolino F. Role of αVβ3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 1999, 18:882-892.
40. Mahabeleshwar GH, Feng W, Reddy K, Plow EF, Byzova TV. Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res 2007, 101:570-580.
41. Mahabeleshwar GH, Chen J, Feng W, Somanath PR, Razorenova OV, Byzova TV. Integrin affinity modulation in angiogenesis. Cell Cycle 2008, 7:335-347.
42. Kermorgant S, Parker PJ. c-Met signalling: spatio-temporal decisions. Cell Cycle 2005, 4:352-355.
43. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ. The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 2003, 116:4169-4179.
44. van Kerkhof P, Govers R. Alves dos Santos CM, Strous GJ. Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J Biol Chem 2000, 275:1575-1580.
45. van Kerkhof P, Alves dos Santos CM, Sachse M, Klumperman J, Bu G, Strous GJ. Proteasome inhibitors block a late step in lysosomal transport of selected membrane but not soluble proteins. Mol Biol Cell 2001, 12:2556-2566.
46. Walrafen P, Verdier F, Kadri Z, Chretien S, Lacombe C, Mayeux P. Both proteasomes and lysosomes degrade the activated erythropoietin receptor. Blood 2005, 105:600-608.
47. Lu JC, Piazza TM, Schuler LA. Proteasomes mediate prolactin-induced receptor down-regulation and fragment generation in breast cancer cells. J Biol Chem 2005, 280:33909-33916.
48. Martinez-Moczygemba M, Huston DP. Proteasomal regulation of βc signaling reveals a novel mechanism for cytokine receptor heterotypic desensitization. J Clin Invest 2001, 108:1797-1806.
49. Offterdinger M, Schofer C, Weipoltshammer K, Grunt TW. c-erbB-3: a nuclear protein in mammary epithelial cells. J Cell Biol 2002, 157:929-939.
50. Williams CC, Allison JG, Vidal GA, Burow ME, Beckman BS, Marrero L, Jones FE. The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J Cell Biol 2004, 167:469-478.
51. Swendeman S, Mendelson K, Weskamp G, Horiuchi K, Deutsch U, Scherle P, Hooper A, Rafii S, Blobel CP. VEGF-A stimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circ Res 2008, 103:916-918.
52. Bernatchez PN, Acevedo L, Fernandez-Hernando C, Murata T, Chalouni C, Kim J, Erdjument-Bromage H, Shah V, Gratton JP, McNally EM, Tempst P, Sessa WC. Myoferlin regulates vascular endothelial growth factor receptor-2 stability and function. J Biol Chem 2007, 282:30745-30753.
53. Li Y, Kumar KG, Tang W, Spiegelman VS, Fuchs SY. Negative regulation of prolactin receptor stability and signaling mediated by SCF (β-TrCP) E3 ubiquitin ligase. Mol Cell Biol 2004, 24:4038-4048.
54. van Kerkhof P, Putters J, Strous GJ. The ubiquitin ligase SCF (βTrCP) regulates the degradation of the growth hormone receptor. J Biol Chem 2007, 282:20475-20483.
55. Vecchi M, Carpenter G. Constitutive proteolysis of the ErbB-4 receptor tyrosine kinase by a unique, sequential mechanism. J Cell Biol 1997, 139:995-1003.
56. Howell GJ, Herbert SP, Smith JM, Mittar S, Ewan LC, Mohammed M, Hunter AR, Simpson N, Turner AJ, Zachary I, Walker JH, Ponnambalam S. Endothelial cell confluence regulates Weibel-Palade body formation. Mol Membr Biol 2004, 21:413-421.
57. Ponnambalam S, Rabouille C, Luzio JP, Nilsson T, Warren G. The TGN38 glycoprotein contains two non-overlapping signals that mediate localization to the trans-Golgi network. J Cell Biol 1994, 125:253-268.
58. Herbert SP, Ponnambalam S, Walker JH. Cytosolic phospholipase A2α mediates endothelial cell proliferation and Is inactivated by association with the Golgi apparatus. Mol Biol Cell 2005, 16:3800-3809.