Mechanism of Platelet-Derived Growth Factor-Dependent Caveolin-1 Phosphorylation: Relationship to Sterol Binding and the Role of Serine-80

Biochemistry

Volumn 43, Issue 9, 2004, Pages 2578-2586

  Fielding, Phoebe E ^a,b   Chau, Phuonglan ^a   Liu, Dong ^a   Spencer, Thomas A ^c   Fielding, Christopher J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Dartmouth College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; BIOCHEMISTRY; CHOLESTEROL; ENZYME INHIBITION; IMMUNOLOGY; MUSCLE;

IMMUNOPRECIPITATION; PHOSPHORYLATION;

CELLS;

CAVEOLIN 1; CHOLESTEROL DERIVATIVE; PHOSPHOTRANSFERASE; PHOSPHOTYROSINE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR INHIBITOR; PROTEIN KINASE C INHIBITOR; SERINE; STEROL; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL LABELING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOPRECIPITATION; LIPID TRANSPORT; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEOMICS; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANTICHOLESTEREMIC AGENTS; BIOLOGICAL TRANSPORT; CAVEOLAE; CAVEOLIN 1; CAVEOLINS; CELLS, CULTURED; CHOLESTEROL; HUMANS; MUSCLE, SMOOTH, VASCULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN BINDING; PROTEIN KINASE C; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SERINE; SIGNAL TRANSDUCTION; TYROSINE;

EID: 1542297710     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035442c     Document Type: Article

References (50)

1. Anderson, R. G. W. (1998) The caveolae membrane system, Annu. Rev. Biochem. 67, 199-225.
2. Smart, E. J., Graf, G. A., McNiven, M. A., Sessa, W. C., Engelman, J. A., Scherer, P. E., Okamoto, T., and Lisanti, M. P. (1999) Caveolins, liquid-ordered domains, and signal transduction, Mol. Cell. Biol. 19, 7289-7304.
3. Fielding, C. J., and Fielding, P. E. (2000) Cholesterol and caveolae: structural and functional relationships, Biochim. Biophys. Acta 1529, 210-222.
4. Heldin, C. H., Ostman, A., and Ronnstrand, L. (1998) Signal transduction via platelet-derived growth factor receptors, Biochim. Biophys. Acta 1378, F79-F113.
5. Heldin, C. H., and Westermark, B. (1999) Mechanisms of action and in vivo role of platelet-derived growth factor, Physiol. Rev. 79, 1283-1316.
6. Roy, S., Luetterforst, R., Harding, A., Apolloni, A., Etheridge, M., Stang, E., Rolls, B., Hancock, J. F., and Parton, R. G. (1999) Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains, Nat. Cell Biol. 1, 98-105.
7. Haidar, B., Mott, S., Boucher, B., Lee, C. Y., Marcil, M., and Genest, J. (2001) Cellular cholesterol efflux is modulated by phospholipid-derived signaling molecules in familial HDL deficiency/Tangier disease fibroblasts, J. Lipid Res. 42, 249-257.
8. Zundel, W., Swiersz, L. M., and Giaccia, A. (2000) Caveolin-1 mediated regulation of receptor tyrosine kinase-associated phosphatidylinositol-3-kinase activity by ceramide, Mol. Cell. Biol. 20, 1507-1514.
9. Newcomb, L. F., and Mastick, C. C. (2002) Src family kinase-dependent phosphorylation of a 29-kDa caveolin-associated protein, Biochem. Biophys. Res. Commun. 290, 1447-1453.
10. Chiarugi, P., Cirri, P., Taddei, M. L., Giannoni, E., Fiaschi, T., Buricchi, F., Camici, G., Raugei, R., and Ramponi, G. (2002) Insight into the role of low molecular weight phosphotyrosine phosphatase (LMW-PTP) on platelet-derived growth factor receptor (PDGF-r) signaling. LMW-PTP controls PDGF-r kinase activity through TYR-857 dephosphorylation, J. Biol. Chem. 277, 37331-37338.
11. Garver, W. S., Hossain, G. S., Winscott, M. M., and Heidenreich, R. A. (1999) The Npc1 mutation causes an altered expression of caveolin-1, annexin II and protein kinases and phosphorylation of caveolin-1 and annexin II in murine livers, Biochim. Biophys. Acta 1453, 193-206.
12. Schlegel, A., Arvan, P., and Lisanti, M. P. (2001) Caveolin-1 binding to endoplasmic reticulum membranes and entry into the regulated secretory pathway are regulated by serine phosphorylation. Protein sorting at the level of the endoplasmic reticulum, J. Biol. Chem. 276, 4398-4408.
13. Kimura, A., Mora, S., Shigematsu, S., Pessin, J. E., and Saltiel, A. R. (2002) The insulin receptor catalyzes the tyrosine phosphorylation of caveolin-1, J. Biol. Chem. 277, 30153-30158.
14. Maggi, D., Biedi, C., Segat, D., Barbero, D., Panetta, D., and Cordera, R. (2002) IGF-1 induces caveolin-1 tyrosine phosphorylation and translocation in the lipid rafts, Biochem. Biophys. Res. Commun. 295, 1085-1089.
15. Labrecque, L., Royal, I., Surprenant, D. S., Patternson, C., Gingrans, D., and Beliveau, R. (2003) Regulation of endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol, Mol. Biol. Cell 14, 334-347.
16. Caselli, A., Taddei, M. L., Manao, G., Camici, G., and Ramponi, G. (2001) Tyrosine phosphorylated caveolin is a physiological substrate of the low M(r) protein tyrosine phosphatase, J. Biol. Chem. 276, 18849-18854.
17. Murata, M., Peranen, J., Schreiner, R., Wieland, F., Kurzchalia, T. V., and Simons, K. (1995) VIP21/caveolin is a cholesterol binding protein, Proc. Natl. Acad. Sci. U.S.A. 92, 10339-10343.
18. Fielding, P. E., Russel, J. S., Spencer, T. A., Hakamata, H., Nagao, K., and Fielding, C. J. (2002) Sterol efflux to apolipoprotein A-1 originates from caveolin-rich microdomains and potentiates PDGF-dependent protein kinase activity, Biochemistry 41, 4929-4937.
19. Fielding, P. E., and Fielding, C. J. (1995) Plasma membrane caveolae mediate the efflux of cellular free cholesterol, Biochemistry 34, 14288-14292.
20. Uittenbogaard, A., Ying, Y., and Smart, E. J. (1998) Characterization of a cytosolic heat shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking, J. Biol. Chem. 273, 6525-6532.
21. Pike, L. J., and Miller, J. M. (1998) Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover, J. Biol. Chem. 273, 22298-22304.
22. Zheng, X. M., Resnick, R. J., and Shalloway, D. (2002) Mitotic activation of protein-tyrosine phosphatase alpha and regulation of its Src-mediated transforming activity by its sites of protein kinase C phosphorylation, J. Biol. Chem. 277, 21922-21929.
23. Li, Q., Tsujita, M., and Yokoyama, S. (1997) Selective down-regulation by protein kinase C inhibitors of apolipoprotein-mediated cellular cholesterol efflux in macrophages, Biochemistry 36, 12045-12052.
24. Sun, L., Tran, N., Liang, C., Tang, F., Rice, A., Schreck, R., Waltz, K., Shawver, L. K., McMahon, G., and Tang, C. (1999) Design, synthesis, and evaluation of substituted 3-[3- or 4-carboxyethylpyrrol-2-yl)methylidenyl]indolin-2-ones as inhibitors of VEGF, FGF and PDGF receptor tyrosine kinases, J. Med. Chem. 42, 5120-5130.
25. Mahboobi, S., Burgemeister, T., Dove, S., Kuhr, S., and Popp, A. (1999) Homoarcyriaflavin: synthesis of ring-expanded arcyriaflavin analogues, J. Org. Chem. 64, 8130-8137.
26. Gribble, B. G. W., Saulnier, M. G., Sibi, M. P., and Obaza-Nutaitis, J. A. (1984) Synthesis and Diels-Alder reactions of 1,3-dimethyl-4-(phenylsulfonyl)-4H-furo[3,4-b]indole. A new annulation strategy for the construction of ellipticine and isoellipticine, J. Org. Chem. 49, 4518-4523.
27. Fielding, C. J., Bist, A., and Fielding, P. E. (1997) Caveolin mRNA levels are upregulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers, Proc. Natl. Acad. Sci. U.S.A. 94, 3753-3758.
28. Furuchi, T., and Anderson, R. G. W. (1998) Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK), J. Biol. Chem. 273, 21099-21104.
29. Tang, Z. L., Scherer, P. E., and Lisanti, M. P. (1994) The primary sequence of murine caveolin reveals a conserved consensus site for phosphorylation by protein kinase C, Gene 147, 299-300.
30. Fielding, P. E., Nagao, K., Hakamata, H., Chimini, G., and Fielding, C. J. (2000) A two-step mechanism for free cholesterol and phospholipid efflux from human vascular cells to apolipoprotein A-1, Biochemistry 39, 14113-14120.
31. Parton, R. G. (2003) Caveolae - from ultrastructure to molecular mechanisms, Nat. Rev. Mol. Cell Biol. 4, 162-167.
32. Kovalenko, M., Ronnstrand, L., Heldin, C. H., Loubtchenkov, M., Gazit, A., Levitski, A., and Bohmer, F. D. (1997) Phosphorylation site-specific inhibition of platelet-derived growth factor beta-receptor autophosphorylation by the receptor-blocking tyrphostin AG1296, Biochemistry 36, 6260-6269.
33. Salazar, E. P., and Rozengurt, E. (1999) Bombesin and platelet-derived growth factor induce association of endogenous focal adhesion kinase with Src in intact Swiss 3T3 cells, J. Biol. Chem. 274, 28371-28378.
34. Goekjian, P. G., and Jirousek, M. R. (1999) Protein kinase C in the treatment of disease: signal transduction pathways, inhibitors, and agents in development, Curr. Med. Chem. 6, 877-903.
35. Marschall, M., Stein-Gerlach, M., Freitag, M., Kupfer, R., van den Bogaard, M., and Stamminger, T. (2001) Inhibitors of human cytomegalovirus replication drastically reduce the activity of the viral protein kinase pUL97, J. Gen. Virol. 82, 1439-1450.
36. Ward, N. E., and O'Brian, C. A. (1993) Inhibition of protein kinase C by N-myristoylated peptide substrate analogs, Biochemistry 32, 11903-11909.
37. Abram, C. L., and Courtneidge, S. A. (2000) Src family tyrosine kinases and growth factor signaling, Exp. Cell Res. 254, 1-13.
38. Chiarugi, P., Fiaschi, T., Taddei, M. L., Talini, D., Giannoni, E., Raugei, G., and Ramponi, G. (2001) Two vicinal cysteines confer a peculiar redox regulation to low molecular weight protein tyrosine phosphatase in response to platelet-derived growth factor receptor stimulation, J. Biol. Chem. 276, 33478-33487.
39. Sowa G., Pypaert, M., Fulton, D., and Sessa, W. C. (2003) The phosphorylation of caveolin-2 on serines 23 and 36 modulates caveolin-1-dependent caveolae formation, Proc. Natl. Acad. Sci. U.S.A. 100, 6511-6516.
40. Parat, M. O., Stachowicz, R. Z., and Fox, P. L. (2002) Oxidative stress inhibits caveolin-1 palmitoylation and trafficking in endothelial cells, Biochem. J. 361, 681-688.
41. Sargiacomo, M., Scherer, P. E., Tang, Z. L., Casanova, J. E., and Lisanti, M. P. (1994) In vitro phosphorylation of caveolin-rich membrane domains: identification of an associated serine kinase activity as a casein kinase II-like enzyme, Oncogene 9, 2589-2595.
42. Li, H., and Papadopoulos, V. (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern, Endocrinology 139, 4991-4997.
43. Mathieu, A. P., Lavigne, P., and LeHoux, J. G. (2002) Molecular modeling and structure-based thermodynamic analysis of the StAR protein, Endocr. Res. 28, 419-423.
44. Friedland, N., Liou, H. L., Lobel, P., and Stock, A. M. (2003) Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease, Proc. Natl. Acad. Sci. U.S.A. 100, 2512-2517.
45. Zheng, Y. H., Plemenitas, A., Fielding, C. J., and Peterlin, B. M. (2003) Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions, Proc. Natl. Acad. Sci. U.S.A. 100, 8460-8465.
46. Sanguinetti, A. R., and Mastick, C. C. (2003) c-Abl is required for oxidative stress-induced phosphorylation of caveolin-1 on tyrosine-14, Cell Signalling 15, 289-298.
47. Lee, H., Park, D. S., Wang, X. B., Scherer, P. E., Schwartz, P. E., and Lisanti, M. P. (2002) Src-induced phosphorylation of caveolin-2 on tyrosine-19. Phospho-caveolin-2(Tyr(P)19) is localized near focal adhesions, remains associated with lipid rafts/caveolae, but no longer forms a high molecular mass hetero-oligomer with caveolin-1, J. Biol. Chem. 277, 34556-34567.
48. Thyberg, J., Calara, F., Dimayuga, P., Nilsson, J., and Regnstrom, J. (1998) Role of caveolae in cholesterol transport in arterial smooth muscle cells exposed to lipoproteins in vivo and in vitro, Lab. Invest. 78, 825-837.
49. Lavie, Y., Fiucci, G., and Liscovitch, M. (1998) Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells, J. Biol. Chem. 273, 32380-32383.
50. Herrlich, A., Daub, H., Knebel, A., Herrlich, P., Ullrich, A., Schultz, G., and Gudermann, T. (1998) Ligand-independent activation of platelet-derived growth factor receptor is a necessary intermediate in lysophosphatidic acid-stimulated mitogenic activity in L cells, Proc. Natl. Acad. Sci. U.S.A. 95, 8985-8990.