Identification of filamin as a novel ligand for caveolin-1: Evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton

Molecular Biology of the Cell

Volumn 11, Issue 1, 2000, Pages 325-337

  Stahlhut, Martin ^a   Van Deurs, Bo ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; FILAMIN;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CYTOSKELETON; ESCHERICHIA COLI; IMMUNOGOLD STAINING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION;

ESCHERICHIA COLI;

EID: 0033973279     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.1.325     Document Type: Article

References (56)

1. Aktories, K. (1997). Rho proteins: targets for bacterial toxins. Trends Microbiol. 5, 282-288.
2. Anderson, R.G. (1998). The caveolae membrane system. Annu. Rev. Biochem. 67, 199-225.
3. Chang, W.J., Ying, Y.S., Rothberg, K.G., Hooper, N.M., Turner, A.J., Gambliel, H.A., De Gunzburg, J., Mumby, S.M., Gilman, A.G., and Anderson, R.G. (1994). Purification and characterization of smooth muscle cell caveolae. J. Cell Biol. 126, 127-138.
4. Couet, J., Li, S., Okamoto, T., Ikezu, T., and Lisanti, M.P. (1997). Identification of peptide and protein ligands for the caveolin-scaffolding domain: implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272, 6525-6533.
5. Cunningham, C.C., Gorlin, J.B., Kwiatkowski, D.J., Hartwig, J.H., Janmey, P.A., Byers, H.R., and Stossel, T.P. (1992). Actin-binding protein requirement for cortical stability and efficient locomotion. Science 255, 325-327.
6. Dupree, P., Parton, R.G., Raposo, G., Kurzchalia, T.V., and Simons, K. (1993). Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J. 12, 1597-1605.
7. Engelman, J.A., Wykoff, C.C., Yasuhara, S., Song, K.S., Okamoto, T., and Lisanti, M.P. (1997). Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J. Biol. Chem. 272, 16374-16381.
8. Fiorentini, C., Arancia, G., Caprioli, A., Falbo, V., Ruggeri, F.M., and Donelli, G. (1988). Cytoskeletal changes induced in HEp-2 cells by the cytotoxic necrotizing factor of Escherichia coli. Toxicon 26, 1047-1056.
9. Frangioni, J.V., and Neel, B.C. (1993). Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210, 179-187.
10. Fujimoto, T., Miyawaki, A., and Mikoshiba, K. (1995). Inositol 1,4,5-trisphosphate receptor-like protein in plasmalemmal caveolae is linked to actin filaments. J. Cell Sci. 108, 7-15.
11. Garcia-Cardena, G., Fan, R., Stern, D.F., Liu, J., and Sessa, W.C. (1996). Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J. Biol. Chem. 271, 27237-27240.
12. Gietz, R.D., and Schiestl, R.H. (1995). Transforming yeast with DNA. Methods Mol. Cell. Biol. 5, 255-269.
13. Glenney, J.R., Jr. (1989). Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J. Biol. Chem. 264, 20163-20166.
14. 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. USA 89, 10517-10521.
15. Glogauer, M., Arora, P., Chou, D., Janmey, P.A., Downey, G.P., and McCulloch, C.A. (1998). The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J. Biol. Chem. 273, 1689-1698.
16. Gorlin, J.B., Yamin, R., Egan, S., Stewart, M., Stossel, T.P., Kwiatkowski, D.J., and Hartwig, J.H. (1990). Human endothelial actinbinding protein (ABP-280, nonmuscle filamin): a molecular leaf spring. J. Cell Biol. 111, 1089-1105.
17. Horiguchi, Y., Senda, T., Sugimoto, N., Katahira, J., and Matsuda, M. (1995). Bordetella bronchiseptica dermonecrotizing toxin stimulates assembly of actin stress fibers and focal adhesions by modifying the small GTP-binding protein rho. J. Cell Sci. 208, 3243-3251.
18. Izumi, T., Shibata, Y., and Yamamoto, T. (1988). Striped structures on the cytoplasmic surface membranes of the endothelial vesicles of the rat aorta revealed by quick-freeze, deep-etching replicas. Anat. Rec. 220, 225-232.
19. Koleske, A.J., Baltimore, D., and Lisanti, M.P. (1995). Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Natl. Acad. Sci. USA 92, 1381-1385.
20. Kurzchalia, T.V., Dupree, P., Parton, R.G., Kellner, R., Virta, H., Lehnert, M., and Simons, K. (1992). VIP21, a 21-kDa membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J. Cell Biol. 118, 1003-1014.
21. Li, S., Couet, J., and Lisanti, M.P. (1996). Src tyrosine kinases, Gα subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin: caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271, 29182-29190.
22. Li, S., Okamoto, T., Chun, M., Sargiacomo, M., Casanova, J.E., Hansen, S.H., Nishimoto, I., and Lisanti, M.P. (1995). Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J. Biol. Chem. 270, 15693-15701.
23. Liu, G., Thomas, L., Warren, R.A., Enns, C.A., Cunningham, C.C., Hartwig, J.H., and Thomas, G. (1997). Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J. Cell Biol. 239, 1719-1733.
24. Liu, J., Razani, B., Tang, S., Terman, B.I., Ware, J.A., and Lisanti, M.P. (1999). Angiogenesis activators and inhibitors differentially regulate caveolin-1 expression and caveolae formation in vascular endothelial cells: angiogenesis inhibitors block vascular endothelial growth factor-induced down-regulation of caveolin-1. J. Biol. Chem. 274, 15781-15785.
25. Loo, D.T., Kanner, S.B., and Aruffo, A. (1998). Filamin binds to the cytoplasmic domain of the β1-integrin: identification of amino acids responsible for this interaction. J. Biol. Chem. 273, 23304-23312.
26. Meyer, S.C., Zuerbig, S., Cunningham, C.C., Hartwig, J.H., Bissell, T., Gardner, K., and Fox, J. (1997). Identification of the region in actin-binding protein that binds to the cytoplasmic domain of glycoprotein IBa. J. Biol. Chem. 272, 2914-2919.
27. Monier, S., Parton, R.G., Vogel, F., Behlke, J., Henske, A., and Kurzchalia, T.V. (1995). VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell 6, 911-927.
28. Mukherjee, S., Zha, X., Tabas, I., and Maxfield, F.R. (1998). Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75, 1915-1925.
29. Oh, P., and Schnitzer, J.E. (1999). Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage: toward understanding the basis of purification. J. Biol. Chem. 274, 23144-23154.
30. Oka, N., Yamamoto, M., Schwencke, C., Kawabe, J., Ebina, T., Ohno, S., Couet, J., Lisanti, M.P., and Ishikawa, Y. (1997). Caveolin interaction with protein kinase C: isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. J. Biol. Chem. 272, 33416-33421.
31. Okamoto, T., Schlegel, A., Scherer, P.E., and Lisanti, M.P. (1998). Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 273, 5419-5422.
32. Parton, R.G. (1996). Caveolae and caveolins. Curr. Opin. Cell Biol. 8, 542-548.
33. Parton, R.G., Joggerst, B., and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
34. Petersen, O.W., Hansen, S.H., Laursen, I., and van Deurs, B. (1989). Effect of insulin on growth and expression of smooth muscle isoactin in human breast gland myoepithelial cells in a chemically defined culture system. Eur. J. Cell Biol. 50, 500-509.
35. Pfaff, M., Liu, S., Erle, D.J., and Ginsberg, M.H. (1998). Integrin beta cytoplasmic domains differentially bind to cytoskeletal proteins. J. Biol. Chem. 273, 6104-6109.
36. Provance, D.W., Jr., McDowall, A., Marko, M., and Luby-Phelps, K. (1993). Cytoarchitecture of size-excluding compartments in living cells. J. Cell Sci. 106, 565-577.
37. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
38. Rohlich, P., and Allison, A.C. (1976). Oriented pattern of membrane-associated vesicles in fibroblasts. J. Ultrastruct Res. 57, 94-103.
39. 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, 673-682.
40. Sargiacomo, M., Scherer, P.E., Tang, Z., Kubler, E., Song, K.S., Sanders, M.C., and Lisanti, M.P. (1995). Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc. Natl. Acad. Sci. USA 92, 9407-9411.
41. Sargiacomo, M., Sudol, M., Tang, Z., and Lisanti, M.P. (1993). Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122, 789-807.
42. Scheiffele, P., Verkade, P., Fra, A.M., Virta, H., Simons, K., and Ikonen, E. (1998). Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140, 795-806.
43. Scherer, P.E., Lewis, R.Y., Volonte, D., Engelman, J.A., Galbiati, F., Couet, J., Kohtz, D.S., van Donselaar, E., Peters, P., and Lisanti, M.P. (1997). Cell-type and tissue-specific expression of caveolin-2: caveolins 1 and 2 colocalize and form a stable hetero-oligomeric complex in vivo. J. Biol. Chem. 272, 29337-29346.
44. Scherer, P.E., Okamoto, T., Chun, M., Nishimoto, I., Lodish, H.F., and Lisanti, M.P. (1996). Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc. Natl. Acad. Sci. USA 93, 131-135.
45. Scherer, P.E., Tang, Z., Chun, M., Sargiacomo, M., Lodish, H.F., and Lisanti, M.P. (1995). Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution: identification and epitope mapping of an isoform-specific monoclonal antibody probe. J. Biol. Chem. 270, 16395-16401.
46. Schnitzer, J.E., Oh, P., Jacobson, B.S., and Dvorak, A.M. (1995). Caveolae from luminal plasmalemma of rat lung endothelium: microdomains enriched in caveolin, Ca(2+)-ATPase, and inositol trisphosphate receptor. Proc. Natl. Acad. Sci. USA 92, 1759-1763.
47. Schroeder, F., Jefferson, J.R., Kier, A.B., Knittel, J., Scallen, T.J., Wood, W.G., and Hapala, I. (1991). Membrane cholesterol dynamics: cholesterol domains and kinetic pools. Proc. Soc. Exp. Biol. Med. 196, 235-252.
48. Senda, T., Horiguchi, Y., Umemoto, M., Sugimoto, N., and Matsuda, M. (1997). Bordetella bronchiseptica dermonecrotizing toxin, which activates a small GTP-binding protein rho, induces membrane organelle proliferation and caveolae formation. Exp. Cell Res. 230, 163-168.
49. Slot, J.W., Geuze, H.J., Gigengack, S., Lienhard, G.E., and James, D.E. (1991). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113, 123-135.
50. Smart, E.J., Ying, Y.S., Conrad, P.A., and Anderson, R.G. (1994). Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127, 1185-1197.
51. Smart, E.J., Ying, Y.S., Mineo, C., and Anderson, R.G. (1995). A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Natl. Acad. Sci. USA 92, 10104-10108.
52. Stan, R.V., Roberts, W.G., Predescu, D., Ihida, K., Saucan, L., Ghitescu, L., and Palade, G.E. (1997). Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol. Biol. Cell 8, 595-605.
53. Takafuta, T., Wu, G., Murphy, G.F., and Shapiro, S.S. (1998). Human β-filamin is a new protein that interacts with the cytoplasmic tail of glycoprotein Ibα. J. Biol. Chem. 273, 17531-17538.
54. van Deurs, B., Holm, P.K., Sandvig, K., and Hansen, S.H. (1993). Are caveolae involved in clathrin-independent endocytosis? Trends Cell Biol. 3, 249-251.
55. van Deurs, B., Nilausen, K., Faergeman, O., and Meinertz, H. (1982). Coated pits and pinocytosis of cationized ferritin in human skin fibroblasts. Eur. J. Cell Biol. 27, 270-278.
56. Vogel, U., Sandvig, K., and van Deurs, B. (1998). Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. J. Cell Sci. 111, 825-832.