Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 286, Issue 5 55-5, 2004, Pages

  Cho, Chung Hyun ^a   Lee, Chang Sup ^a   Chang, Mikyung ^a   Jang, Il Ho ^a   Kim, Soo Jin ^a   Hwang, Inhwan ^a   Ryu, Sung Ho ^a   Lee, Chin O ^a   Koh, Gou Young ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Caveolin 1; Phospholipase D; Protein kinase C ; Signaling; Vascular endothelial growth factor

Indexed keywords

ANTIMITOTIC AGENT; BUTANOL; CHOLESTEROL; METHYL BETA CYCLODEXTRIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDIC ACID; PHOSPHOLIPASE D2; PHOSPHOLIPASE INHIBITOR; PROTEIN KINASE C DELTA; RAS PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CAVEOLA; CELL FRACTIONATION; CELL MEMBRANE; CELL PROLIFERATION; CHOLESTEROL METABOLISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; ENDOTHELIUM CELL; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MITOSIS INHIBITION; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

CAVEOLAE; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOLIPASE D; PHOSPHORYLATION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 1942469316     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00786.2003     Document Type: Article

References (42)

1. Anderson RG and Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296: 1821-1825, 2002.
2. Bruns RR and Palade GE. Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries. J Cell Biol 37: 277-299, 1968.
3. Chang WJ, Rothberg KG, Kamen BA, and Anderson RG. Purification and characterization of smooth muscle cell caveolae. J Cell Biol 118: 63-69, 1992.
4. Du G, Altshuller YM, Kim Y, Han JM, Ryu SH, Morris AJ, and Frohman MA. Dual requirement for rho and protein kinase C in direct activation of phospholipase D1 through G protein-coupled receptor signaling. Mol Biol Cell 11: 4359-4368, 2000.
5. Exton JH. Regulation of phospholipase D. Biochim Biophys Acta 1439: 121-133, 1999.
6. Feng Y, Venema VJ, Venema RC, Tsai N, and Caldwell RB. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256: 192-197, 1999.
7. Feng Y, Venema VJ, Venema RC, Tsai N, Behzadian MA, and Caldwell RB. VEGF-induced permeability increase is mediated by caveolae. Invest Ophthalmol Vis Sci 40: 157-167, 1999.
8. Ferrara N and Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 18: 4-25, 1997.
9. Galbiati F, Razani B, and Lisanti MP. Emerging themes in lipid rafts and caveolae. Cell 106: 403-411, 2001.
10. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, and Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343, 1998.
11. Gomez-Cambronero J and Keire P. Phospholipase D: a novel major player in signal transduction. Cell Signal 6: 387-397, 1998.
12. Han JM, Kim JH, Lee BD, Lee SD, Kim Y, Jung YW, Lee S, Cho W, Ohba M, Kuroki T, Suh PG, and Ryu SH. Phosphorylation-dependent regulation of phospholipase D2 by protein kinase C8 in rat pheochromocytoma PC12 cells. J Biol Chem 277: 8290-8297, 2002.
13. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, and Koh GY. Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Circ Res 86: 24-29, 2000.
14. Kim I, Ryu YS, Kwak HJ, Ahn SY, Oh JL, Yancopoulos GD, Gale NW, and Koh GY. EphB ligand, ephrinB2, suppresses the VEGF- and angiopoietin 1-induced Ras/mitogen-activated protein kinase pathway in venous endothelial cells. FASEB J 16: 1126-1128, 2002.
15. Kim JH, Kim Y, Lee SD, Lopez I, Arnold RS, Lambeth JD, Suh PG, and Ryu SH. Selective activation of phospholipase D2 by unsaturated fatty acid. FEBS Lett 454: 42-46, 1999.
16. Kim JH, Lee SD, Han JM, Lee TG, Kim Y, Park JB, Lambeth JD, Suh PG, and Ryu SH. Activation of phospholipase D1 by direct interaction with ADP-ribosylation factor 1 and RalA. FEBS Lett 430: 231-235, 1998.
17. Kim Y, Han JM, Park JB, Lee SD, Oh YS, Chung C, Lee TG, Kim JH, Park SK, Yoo JS, Suh PG, and Ryu SH. Phosphorylation and activation of phospholipase D1 by protein kinase C in vivo: determination of multiple phosphorylation sites. Biochemistry 38: 10344-10351, 1999.
18. Kroll J and Waltenberger J. The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J Biol Chem 272: 32521-32527, 1997.
19. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, and Beliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell 14: 334-347, 2003.
20. Liscovitch M, Czarny M, Fiucci G, and Tang X. Phospholipase D: molecular and cell biology of a novel gene family. Biochem J 345: 401-415, 1999.
21. Meadows KN, Bryant P, and Pumiglia K. Vascular endothelial growth factor induction of the angiogenic phenotype requires Ras activation. J Biol Chem 276: 49289-49298, 2001.
22. Morales-Ruiz M, Fulton D, Sowa G, Languino LR, Fujio Y, Walsh K, and Sessa WC. Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ Res 86: 892-896, 2000.
23. Neufeld G, Cohen T, Gengrinovitch S, and Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13: 9-22, 1999.
24. Palade G. The fine structure of blood capillaries. J Appl Phys 24: 1424, 1953.
25. Park SK, Provost JJ, Bae CD, Ho WT, and Exton JH. Cloning and characterization of phospholipase D from rat brain. J Biol Chem 272: 29263-29271, 1997.
26. Parton RG. Caveolae-from ultrastructure to molecular mechanisms. Nat Rev Mol Cell Biol 4: 162-167, 2003.
27. Parton RG. Caveolae and caveolins. Curr Opin Cell Biol 8: 542-548, 1996.
28. Pedram A, Razandi M, and Levin ER. Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 273: 26722-26728, 1998.
29. Rizzo MA, Shome K, Vasudevan C, Stolz DB, Sung TC, Frohman MA, Watkins SC, and Romero G. Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent raf-1 translocation to the plasma membrane and the activation of the mitogen-activated protein kinase pathway. J Biol Chem 274: 1131-1139, 1999.
30. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, and Sandvig K. Extraction of cholesterol with methy-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 10: 961-974, 1999.
31. Seymour LW, Shoaibi MA, Martin A, Ahmed A, Elvin P, Kerr DJ, and Wakelam MJ. Vascular endothelial growth factor stimulates protein kinase C-dependent phospholipase D activity in endothelial cells. Lab Invest 75: 427-437, 1996.
32. Shaul PW and Anderson RG. Role of plasmalemmal caveolae in signal transduction. Am J Physiol Lung Cell Mol Physiol 275: L843-L851, 1998.
33. Simionescu N, Simionescu M, and Palade GE. Permeability of muscle capillaries to small heme-peptides. Evidence for the existence of patent transendothelial channels. J Cell Biol 64: 586-607, 1975.
34. Simons K and Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39, 2000.
35. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, and Lisanti MP. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19: 7289-7304, 1999.
36. Smart EJ, Ying Y, Donzell WC, and Anderson RG. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271: 29427-29435, 1996.
37. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, and Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271: 15160-15165, 1996.
38. Takahashi T, Ueno H, and Shibuya M. VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18: 2221-2230, 1999.
39. Takahashi T, Yamaguchi S, Chida K, and Shibuya M. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-γ and DNA synthesis in vascular endothelial cells. EMBO J 20: 2768-2778, 2001.
40. Veikkola T and Alitalo K. VEGFs, receptors and angiogenesis. Semin Cancer Biol 9: 211-220, 1999.
41. Wu LW, Mayo LD, Dunbar JD, Kessler KM, Baerwald MR, Jaffe EA, Wang D, Warren RS, and Donner DB. Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation. J Biol Chem 275: 5096-5103, 2000.
42. Xia P, Aiello LP, Ishii H, Jiang ZY, Park DJ, Robinson GS, Takagi H, Newsome WP, Jirousek MR, and King GL. Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C, its isoforms, and endothelial cell growth. J Clin Invest 98: 2018-2026, 1996.