Conformational defects slow golgi exit, block oligomerization, and reduce raft affinity of caveolin-1 mutant proteins

Molecular Biology of the Cell

Volumn 15, Issue 10, 2004, Pages 4556-4567

  Ren, Xiaoyan ^a   Ostermeyer, Anne G ^a   Ramcharan, Lynne T ^a   Zeng, Youchun ^b   Lublin, Douglas M ^b   Brown, Deborah A ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; MUTANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MELANOMA CELL; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROCESSING; RAT; THYROID CELL;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; CAVEOLIN 1; CAVEOLINS; CELL LINE; CYCLOHEXIMIDE; GOLGI APPARATUS; MEMBRANE MICRODOMAINS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; PROTEIN SORTING SIGNALS; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT;

ANIMALIA;

EID: 4644286390     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-06-0480     Document Type: Article

References (53)

1. Arbuzova, A., Wang, L., Wang, J., Hangyas-Mihalyne, G., Murray, D., Honig, B., and McLaughlin, S. (2000). Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS. Biochemistry 39, 10330-10339.
2. Arreaza, G., and Brown, D.A. (1995). Sorting and intracellular trafficking of a glycosylphosphatidylinositol-anchored protein and two hybrid proteins with the same ectodomain in MDCK kidney epithelial cells. J. Biol. Chem. 270, 23641-23647.
3. Bretscher, M.S., and Munro, S. (1993). Cholesterol and the Golgi apparatus. Science 261, 1280-1281.
4. Breuza, L., Corby, S., Arsanto, J.-P., Delgrossi, M.-H., Scheiffele, P., and Le Bivic, A. (2002). The scaffolding domain of caveolin 2 is responsible for its Golgi localization in Caco-2 cells. J. Cell Sci. 115, 4457-4467.
5. Brown, D.A., and London, E. (2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
6. Brown, D.A., and Rose, J.K. (1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544.
7. Choy, E., Chiu, V.K., Silletti, J., Feoktistov, M., Morimoto, T., Michaelson, D., Ivanov, I.E., and Philips, M.R. (1999). Endomembrane trafficking of Ras: the CAAX motif targets proteins to the ER and Golgi. Cell 98, 69-80.
8. Conrad, P.A., Smart, E.J., Ying, Y.-S., Anderson, R.G.W., and Bloom, G.S. (1995). Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131, 1421-1433.
9. Denker, S.P., McCaffrey, J.M., Palade, G.E., Insel, P.A., and Farquhar, M.G. (1996). Differential distribution of a subunits and βγ subunits of heterotrimeric G proteins on Golgi membranes of the exocrine pancreas. J. Cell Biol. 133, 1027-1040.
10. Dietzen, D.J., Hastings, W.R., and Lublin, D.M. (1995). Caveolin is palmitoylated on multiple cysteine residues: palmitoylation is not necessary for localization of caveolin to caveolae. J. Biol. Chem. 270, 6838-6842.
11. 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.
12. Eilers, M., Patel, A.B., Liu, W., and Smith, S.O. (2002). Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophys. J. 82, 2720-2736.
13. Fernandez, I., Ying, Y., Albanesi, J., and Anderson, R.G.W. (2002). Mechanism of caveolin filament assembly. Proc. Natl. Acad. Sci. USA 99, 11193-11198.
14. Fra, A.M., Williamson, E., Simons, K., and Parton, R.G. (1994). Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30745-30748.
15. Hayashi, K., Matsuda, S., Machida, K., Yamamoto, T., Fukuda, Y., Nimura, Y., Hayakawa, T., and Hamaguchi, M. (2001). Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res. 61, 2361-2364.
16. Kalinina, E.V., and Fricker, L.D. (2003). Palmitoylation of carboxypeptidase D. Implications for intracellular trafficking. J. Biol. Chem. 278, 9244-9249.
17. Kanaani, J., el-Husseini Ael, D., Aguilera-Moreno, A., Diacovo, J.M., Bredt, D.S., and Baekkeskov, S. (2002). A combination of three distinct trafficking signals mediates axonal targeting and presynaptic clustering of GAD65. J. Cell Biol. 158, 1229-1238.
18. 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, 1003-1014.
19. Lee, H., Park, D.S., Razani, B., Russell, R.G., Pestell, R.G., and Lisanti, M.P. (2002). Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am. J. Pathol. 161, 1357-1369.
20. Lipardi, C., Mora, R., Colomer, V., Paladino, S., Nitsch, L., Rodriguez-Boulan, E., and Zurzolo, C. (1998). Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J. Cell Biol. 140, 617-626.
21. London, E., and Brown, D.A. (2000). Insolubility of lipids in Triton X-100. Physical origin and relationship to sphingolipid/cholesterol domains (rafts). Biochim. Biophys. Acta 1508, 182-195.
22. Luetterforst, R., Stang, E., Zorzi, N., Carozzi, A., Way, M., and Parton, R.G. (1999). Molecular characterization of caveolin association with the Golgi complex: identification of a cis-Golgi targeting domain in the caveolin molecule. J. Cell Biol. 145, 1443-1460.
23. Machleidt, T., Li, W.-P., Liu, P., and Anderson, R.G.W. (2000). Multiple domains in caveolin-1 control its intracellular traffic. J. Cell Biol. 148, 17-28.
24. Martínez-Menárguez, J.A., Prekeris, R., Oorschot, V.M.J., Scheller, R., Slot, J.W., Geuze, H.J., and Klumperman, J. (2001). Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J. Cell Biol. 155, 1213-1224.
25. Mironov, A.A., et al. (2001). Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225-1238.
26. Monier, S., Dietzen, D.J., Hastings, W.R., Lublin, D.M., and Kurzchalia, T.V. (1996). Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388, 143-149.
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. Mora, R., Bonilha, V.L., Marmorstein, A., Scherer, P.E., Brown, D., Lisanti, M.P., and Rodriguez-Boulan, E. (1999). Caveolin-2 localizes to the Golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J. Biol. Chem. 274, 25708-25717.
29. Munro, S. (1995). An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695-4704.
30. Murata, M., Peränen, J., Schreiner, R., Wieland, F., Kurzchalia, T.V., and Simons, K. (1995). VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. USA 92, 10339-10343.
31. Navarro-Lérida, I., Alberto Álvarez-Barrientos, F.G., and Ignacio, and Rodriguez-Crespo, I. (2002). Distance-dependent cellular palmitoylation of de-novo-designed sequences and their translocation to plasma membrane sub-domains. J. Cell Sci. 115, 3119-3130.
32. Nichols, B.J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4, 374-378.
33. Ostermeyer, A.G., Beckrich, B.T., Ivarson, K.A., Grove, K.E., and Brown, D.A. (1999). Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. Methyl-beta-cyclodextrin does not affect cell-surface transport of a GPI-anchored protein. J. Biol. Chem. 274, 34459-34466.
34. Ostermeyer, A.G., Paci, J.M., Zeng, Y., Lublin, D.M., Munro, S., and Brown, D.A. (2001). Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J. Cell Biol. 152, 1071-1078.
35. Ostermeyer, A.G., Ramcharan, L.T., Zeng, Y., Lublin, D.M., and Brown, D.A. (2004). Role of the hydrophobic domain in targeting caveolin-1 to lipid droplets. J. Cell Biol. 164, 69-78.
36. Parolini, I., et al. (1999). Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the Golgi complex. J. Biol. Chem. 274, 25718-25725.
37. Pelham, H.R.B., and Rothman, J.E. (2000). The debate about transport in the Golgi-two sides of the same coin? Cell 102, 713-719.
38. Rothberg, K.G., Heuser, J.E., Donzell, W.C., Ying, Y.-S., Glenney, J.R., and Anderson, R.G.W. (1992). Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682.
39. Sargiacomo, M., Scherer, P.E., Tang, Z.L., Kübler, 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.
40. Schagger, H., Cramer, W.A., and von Jagow, G. (1994). Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal. Biochem. 217, 220-230.
41. 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.
42. Schlegel, A., and Lisanti, M.P. (2000). A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/ oligomer interactions in vivo. J. Biol. Chem. 275, 21605-21617.
43. Schlegel, A., Schwab, R.B., Scherer, P.E., and Lisanti, M.P. (1999). A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro. J. Biol. Chem. 274, 22660-22667.
44. Schroeder, R.J., Ahmed, S.N., Zhu, Y., London, E., and Brown, D.A. (1998). Cholesterol and sphingolipid enhance the Triton X-100-insolubility of GPI-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273, 1150-1157.
45. Schuck, S., Honsho, M., Ekroos, K., Shevchenko, A., and Simons, K. (2003). Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. USA 100, 5795-5800.
46. Shogomori, H., and Brown, D.A. (2003). Use of detergents to study membrane rafts: The good, the bad, and the ugly. Biol. Chem. 384, 1259-1263.
47. 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.
48. Takida, S., and Wedegaertner, P.B. (2003). Heterotrimer formation, together with isoprenylation, is required for plasma membrane targeting of Gβγ. J. Biol. Chem. 278, 17284-17290.
49. Takimoto, K., Yang, E.-K., and Conforti, L. (2002). Palmitoylation of KChIP splicing variants is required for efficient cell surface expression of Kv4.3 channels. J. Biol. Chem. 277, 26904-26911.
50. Thiele, C., Hannah, M.J., Fahrenholz, F., and Huttner, W.B. (2000). Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2, 42-49.
51. Thomsen, P., Roepstorff, K., Stahlhut, M., and van Deurs, B. (2002). Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13, 238-250.
52. van't Hof, W., and Crystal, R.G. (2002). Fatty acid modification of the cox-sackievirus and adenovirus receptor. J. Virol. 76, 6382-6386.
53. Xu, X., and London, E. (2000). The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39, 843-849.