Phosphorylation of Caveolin-1 in Bovine Rod Outer Segments in vitro by an Endogenous Tyrosine Kinase

  • Michael H. Elliott
  • Abboud J. Ghalayini
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 613)

Caveolin-1 (Cav-1), the principal protein component of caveolar membrane domains (Glenney, Jr. and Soppet, 1992; Kurzchalia et al., 1992; Rothberg et al., 1992), was originally identified as a major tyrosine phosphoprotein in Rous sarcoma virus (v-Src) transformed cells (Glenney, Jr. and Zokas, 1989). Although Cav-1 can be phosphorylated on several tyrosine residues (Nomura and Fujimoto, 1999; Schlegel et al., 2001), the most well-characterized phosphorylation site on Cav-1 is tyrosine-14, a site specifically recognized by monoclonal antibodies developed to detect this phosphorylated residue (Lee et al., 2000; Nomura and Fujimoto, 1999).


Retinal Pigment Epithelium Tyrosine Phosphorylation Rous Sarcoma Virus Folate Receptor Alpha Stimulate Tyrosine Phosphorylation 
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  1. Bell, M. W., Alvarez, K., and Ghalayini, A. J., 1999, Association of the tyrosine phosphatase SHP-2 with transducin-alpha and a 97-kDa tyrosine-phosphorylated protein in photoreceptor rod outer segments, J. Neurochem. 73:2331.PubMedCrossRefGoogle Scholar
  2. Bell, M. W., Desai, N., Guo, X. X., and Ghalayini, A. J., 2000, Tyrosine phosphorylation of the alpha subunit of transducin and its association with Src in photoreceptor rod outer segments, J. Neurochem. 75:2006.PubMedCrossRefGoogle Scholar
  3. Boesze-Battaglia, K., Dispoto, J., and Kahoe, M. A., 2002, Association of a photoreceptor-specific tetraspanin protein, ROM-1, with triton X-100-resistant membrane rafts from rod outer segment disk membranes, J. Biol. Chem. 277:41843.PubMedCrossRefGoogle Scholar
  4. Bridges, C. C., El Sherbeny, A., Roon, P., Ola, M. S., Kekuda, R., Ganapathy, V., Camero, R. S., Cameron, P. L., and Smith, S. B., 2001, A comparison of caveolae and caveolin-1 to folate receptor alpha in retina and retinal pigment epithelium, Histochem. J. 33:149.PubMedCrossRefGoogle Scholar
  5. Cao, H., Sanguinetti, A. R., and Mastick, C. C., 2004, Oxidative stress activates both Src-kinases and their negative regulator Csk and induces phosphorylation of two targeting proteins for Csk: caveolin-1 and paxillin, Exp. Cell Res. 294:159.PubMedCrossRefGoogle Scholar
  6. Chen, D. B., Li, S. M., Qian, X. X., Moon, C., and Zheng, J., 2005, Tyrosine phosphorylation of caveolin 1 by oxidative stress is reversible and dependent on the c-src tyrosine kinase but not mitogen-activated protein kinase pathways in placental artery endothelial cells, Biol. Reprod. 73:761.PubMedCrossRefGoogle Scholar
  7. Elliott, M. H., Fliesler, S. J., and Ghalayini, A. J., 2003, Cholesterol-dependent association of caveolin-1 with the transducin alpha subunit in bovine photoreceptor rod outer segments: disruption by cyclodextrin and guanosine 5’-O-(3-thiotriphosphate), Biochemistry. 42:7892.PubMedCrossRefGoogle Scholar
  8. Feng, Y., Venema, V. J., Venema, R. C., Tsai, N., Behzadian, M. A., and Caldwell, R. B., 1999, VEGF-induced permeability increase is mediated by caveolae, Invest Ophthalmol. Vis. Sci. 40:157.PubMedGoogle Scholar
  9. Ghalayini, A. J., Desai, N., Smith, K. R., Holbrook, R. M., Elliott, M. H., and Kawakatsu, H., 2002, Light-dependent association of Src with photoreceptor rod outer segment membrane proteins in vivo, J. Biol. Chem. 277:1469.PubMedCrossRefGoogle Scholar
  10. Ghalayini, A. J., Guo, X. X., Koutz, C. A., and Anderson, R. E., 1998, Light stimulates tyrosine phosphorylation of rat rod outer segments In vivo, Exp. Eye Res. 66:817.PubMedCrossRefGoogle Scholar
  11. Glenney, J. R., Jr. and Soppet, D., 1992, Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts, Proc. Natl. Acad. Sci. U. S. A. 89:10517.PubMedCrossRefGoogle Scholar
  12. Glenney, J. R., Jr. and Zokas, L., 1989, Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton, J. Cell Biol. 108:2401.PubMedCrossRefGoogle Scholar
  13. Kachi, S., Yamazaki, A., and Usukura, J., 2001, Localization of caveolin-1 in photoreceptor synaptic ribbons, Invest Ophthalmol. Vis. Sci. 42:850.PubMedGoogle Scholar
  14. Kim, H., Lee, T., Lee, J., Ahn, M., Moon, C., Wie, M. B., and Shin, T., 2006, Immunohistochemical study of caveolin-1 and -2 in the rat retina, J. Vet. Sci. 7:101.PubMedGoogle Scholar
  15. Kim, Y. N., Wiepz, G. J., Guadarrama, A. G., and Bertics, P. J., 2000, Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1. Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status, J. Biol. Chem. 275:7481.PubMedCrossRefGoogle Scholar
  16. Kiss, A. L., Turi, A., Mullner, N., Kovacs, E., Botos, E., and Greger, A., 2005, Oestrogen-mediated tyrosine phosphorylation of caveolin-1 and its effect on the oestrogen receptor localisation: an in vivo study, Mol. Cell Endocrinol. 245:128.PubMedCrossRefGoogle Scholar
  17. Kurzchalia, T. V., Dupree, P., Parton, R. G., Kellner, R., Virta, H., Lehnert, M., and Simons, K., 1992, VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles, J. Cell Biol. 118: 1003.PubMedCrossRefGoogle Scholar
  18. Labrecque, L., Nyalendo, C., Langlois, S., Durocher, Y., Roghi, C., Murphy, G., Gingras, D., and Beliveau, R., 2004, Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase, J. Biol. Chem. 279:52132.PubMedCrossRefGoogle Scholar
  19. Lee, H., Volonte, D., Galbiati, F., Iyengar, P., Lublin, D. M., Bregman, D. B., Wilson, M. T., Campos-Gonzalez, R., Bouzahzah, B., Pestell, R. G., Scherer, P. E., and Lisanti, M. P., 2000, Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette, Mol. Endocrinol. 14:1750.PubMedCrossRefGoogle Scholar
  20. Li, S., Seitz, R., and Lisanti, M. P., 1996, Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo, J. Biol. Chem. 271:3863.PubMedCrossRefGoogle Scholar
  21. Maggi, D., Biedi, C., Segat, D., Barbero, D., Panetta, D., and Cordera, R., 2002, IGF-I induces caveolin 1 tyrosine phosphorylation and translocation in the lipid rafts, Biochem. Biophys. Res. Commun. 295:1085.PubMedCrossRefGoogle Scholar
  22. Martin, R. E., Elliott, M. H., Brush, R. S., and Anderson, R. E., 2005, Detailed characterization of the lipid composition of detergent-resistant membranes from photoreceptor rod outer segment membranes, Invest Ophthalmol. Vis. Sci. 46:1147.PubMedCrossRefGoogle Scholar
  23. Mastick, C. C., Brady, M. J., and Saltiel, A. R., 1995, Insulin stimulates the tyrosine phosphorylation of caveolin, J. Cell Biol. 129:1523.PubMedCrossRefGoogle Scholar
  24. Mora, R. C., Bonilha, V. L., Shin, B. C., Hu, J., Cohen-Gould, L., Bok, D., and Rodriguez-Boulan, E., 2006, Bipolar assembly of caveolae in retinal pigment epithelium, Am. J. Physiol Cell Physiol. 290:C832.PubMedCrossRefGoogle Scholar
  25. Nair, K. S., Balasubramanian, N., and Slepak, V. Z., 2002, Signal-dependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors, Curr. Biol. 12:421.PubMedCrossRefGoogle Scholar
  26. Nomura, R. and Fujimoto, T., 1999, Tyrosine-phosphorylated caveolin-1: immunolocalization and molecular characterization, Mol. Biol. Cell. 10:975.PubMedGoogle Scholar
  27. Orlichenko, L., Huang, B., Krueger, E., and McNiven, M. A., 2006, Epithelial growth factor-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells, J. Biol. Chem. 281:4570.PubMedCrossRefGoogle Scholar
  28. Pike, L. J., 2004, Lipid rafts: heterogeneity on the high seas, Biochem. J. 378:281.PubMedCrossRefGoogle Scholar
  29. Rajala, R. V., McClellan, M. E., Ash, J. D., and Anderson, R. E., 2002, In vivo regulation of phosphoinositide 3-kinase in retina through light-induced tyrosine phosphorylation of the insulin receptor beta-subunit, J. Biol. Chem. 277:43319.PubMedCrossRefGoogle Scholar
  30. Rothberg, K. G., Heuser, J. E., Donzell, W. C., Ying, Y. S., Glenney, J. R., and Anderson, R. G., 1992, Caveolin, a protein component of caveolae membrane coats, Cell. 68:673.PubMedCrossRefGoogle Scholar
  31. Sahasrabuddhe, A. A., Ahmed, N., and Krishnasastry, M. V., 2006, Stress-induced phosphorylation of caveolin-1 and p38, and down-regulation of EGFr and ERK by the dietary lectin jacalin in two human carcinoma cell lines, Cell Stress. Chaperones. 11:135.PubMedCrossRefGoogle Scholar
  32. Sanguinetti, A. R., Cao, H., and Corley, M. C., 2003, Fyn is required for oxidative- and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1, Biochem. J. 376:159.PubMedCrossRefGoogle Scholar
  33. Sanguinetti, A. R. and Mastick, C. C., 2003, c-Abl is required for oxidative stress-induced phosphorylation of caveolin-1 on tyrosine 14, Cell Signal. 15:289.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. Senin, I. I., Hoppner-Heitmann, D., Polkovnikova, O. O., Churumova, V. A., Tikhomirova, N. K., Philippov, P. P., and Koch, K. W., 2004, Recoverin and rhodopsin kinase activity in detergent-resistant membrane rafts from rod outer segments, J. Biol. Chem. 279:48647.PubMedCrossRefGoogle Scholar
  36. Seno, K., Kishimoto, M., Abe, M., Higuchi, Y., Mieda, M., Owada, Y., Yoshiyama, W., Liu, H., and Hayashi, F., 2001, Light- and guanosine 5’-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments, J. Biol. Chem. 276:20813.PubMedCrossRefGoogle Scholar
  37. Shajahan, A. N., Wang, A., Decker, M., Minshall, R. D., Liu, M. C., and Clarke, R., 2006, Caveolin-1 tyrosine phosphorylation enhances paclitaxel-mediated cytotoxicity, J. Biol. Chem. 282:5934.PubMedCrossRefGoogle Scholar
  38. Stitt, A. W., Burke, G. A., Chen, F., McMullen, C. B., and Vlassara, H., 2000, Advanced glycation end-product receptor interactions on microvascular cells occur within caveolin-rich membrane domains, FASEB J. 14:2390.PubMedGoogle Scholar
  39. Volonte, D., Galbiati, F., Pestell, R. G., and Lisanti, M. P., 2001, Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress, J. Biol. Chem. 276:8094.PubMedCrossRefGoogle Scholar
  40. Zimmerman, W. F. and Godchaux, W., III, 1982, Preparation and characterization of sealed bovine rod cell outer segments, Methods Enzymol. 81:52.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of OphthalmologyUniversity of Oklahoma Health Sciences Center; Dean A. McGee Eye InstituteOklahoma CityUSA
  2. 2.Medical University of the AmericasNevisWest Indies

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