Cholesterol and fatty acids regulate dynamic caveolin trafficking through the golgi complex and between the cell surface and lipid bodies

Molecular Biology of the Cell

Volumn 16, Issue 4, 2005, Pages 2091-2105

  Pol, Albert ^a,b   Martin, Sally ^a   Fernández, Manuel A ^b   Ingelmo Torres, Mercedes ^b   Ferguson, Charles ^a   Enrich, Carlos ^b   Parton, Robert G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVEOLIN 3; CHOLESTEROL; FATTY ACID; LIPID; VESICULAR TRANSPORT PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL LEVEL; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; EXOCYTOSIS; FATTY ACID ANALYSIS; GOLGI COMPLEX; MOLECULAR DYNAMICS; MUSCULAR DYSTROPHY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS;

ANIMALS; CAVEOLIN 1; CAVEOLIN 3; CAVEOLINS; CELL MEMBRANE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHOLESTEROL; CRICETINAE; FATTY ACIDS; GOLGI APPARATUS; METHANOL; MICROSCOPY, VIDEO; MOLECULAR WEIGHT; OCTOXYNOL; PROTEIN TRANSPORT; SOLUBILITY; TEMPERATURE; TIME FACTORS;

EID: 16344368798     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-08-0737     Document Type: Article

References (48)

1. Bist, A., Fielding, C. J., and Fielding, P. E. (2000). p53 regulates caveolin gene transcription, cell cholesterol, and growth by a novel mechanism. Biochemistry 39, 1966-1972.
2. Bist, A., Fielding, P. E., and Fielding, C. J. (1997). Two sterol regulatory element-like sequences mediate up-regulation of caveolin gene transcription in response to low density lipoprotein free cholesterol. Proc. Natl. Acad. Sci. USA 94, 10693-10698.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Dundr, M., Hoffmann-Rohrer, U., Hu, Q., Grummt, I., Rothblum, L. I., Phair, R. D., and Misteli, T. (2002). A kinetic framework for a mammalian RNA polymerase in vivo. Science 298, 1623-1626.
5. 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.
6. Fielding, C. J., Bist, A., and Fielding, P. E. (1997). Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers. Proc. Natl. Acad. Sci. USA 94, 3753-3758.
7. Fielding, C. J., Bist, A., and Fielding, P. E. (1999). Intracellular cholesterol transport in synchronized human skin fibroblasts. Biochemistry 38, 2506-2513.
8. Frost, S. C., and Lane, M. D. (1985). Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes. J. Biol. Chem. 260, 2646-2652.
9. Fujimoto, T., Kogo, H., Ishiguro, K., Tauchi, K., and Nomura, R. (2001). Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J. Cell Biol. 152, 1079-1085.
10. Gagescu, R., Demaurex, N., Parton, R. G., Hunziker, W., Huber, L. A., and Gruenberg, J. (2000). The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell 11, 2775-2791.
11. Galbiati, F., Volonte, D., Minetti, C., Bregman, D. B., and Lisanti, M. P. (2000). Limb-girdle muscular dystrophy (LGMD-1C) mutants of caveolin-3 undergo ubiquitination and proteasomal degradation. Treatment with proteasomal inhibitors blocks the dominant negative effect of LGMD-1C mutants and rescues wild-type caveolin-3. J. Biol. Chem. 275, 37702-37711.
12. Galbiati, F., Volonte, D., Minetti, C., Chu, J. B., and Lisanti, M. P. (1999). Phenotypic behavior of caveolin-3 mutations that cause autosomal dominant limb girdle muscular dystrophy (LGMD-1C). Retention of LGMD-1C caveolin-3 mutants within the Golgi complex. J. Biol. Chem. 274, 25632-25641.
13. Gkantiragas, I., Brugger, B., Stuven, E., Kaloyanova, D., Li, X. Y., Lohr, K., Lottspeich, F., Wieland, F. T., and Helms, J. B. (2001). Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell 12, 1819-1833.
14. Hailstones, D., Sleer, L. S., Parton, R. G., and Stanley, K. K. (1998). Regulation of caveolin and caveolae by cholesterol in MDCK cells. J. Lipid Res. 39, 369-379.
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. 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.
17. Kurzchalia, T. V., and Parton, R. G. (1999). Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11, 424-431.
18. 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.
19. Liu, P., Ying, Y., Zhao, Y., Mundy, D. I., Zhu, M., and Anderson, R. G. (2004). Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279, 3787-3792.
20. 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, 1443-1459.
21. 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.
22. Mundy, D. I., Machleidt, T., Ying, Y. S., Anderson, R. G., and Bloom, G. S. (2002). Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J. Cell Sci. 115, 4327-4339.
23. 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. USA 92, 10339-10343.
24. Nichols, B. (2003). Caveosomes and endocytosis of lipid rafts. J. Cell Sci. 116, 4707-4714.
25. Nichols, B. J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol 4, 374-378.
26. Nomura, R., and Fujimoto, T. (1999). Tyrosine-phosphorylated caveolin-1, immunolocalization and molecular characterization. Mol. Biol. Cell 10, 975-986.
27. 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.
28. Parton, R. G., Joggerst, B., and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 277, 1199-1215.
29. Parton, R. G., Molero, J. C., Floetenmeyer, M., Green, K. M., and James, D. E. (2002). Characterization of a distinct plasma membrane macrodomain in differentiated adipocytes. J. Biol. Chem. 277, 46769-46778.
30. Pelkmans, L., Kartenbeck, J., and Helenius, A. (2001). Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3, 473-483.
31. Pelkmans, L., Puntener, D., and Helenius, A. (2002). Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535-539.
32. Phair, R. D., and Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
33. Pol, A., Calvo, M., Lu, A., and Enrich, C. (1999). The "early-sorting" endocytic compartment of rat hepatocytes is involved in the intracellular pathway of caveolin-1 (VIP-21). Hepatology 29, 1848-1857.
34. Pol, A., Luetterforst, R., Lindsay, M., Heino, S., Ikonen, E., and Parton, R. G. (2001). A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152, 1057-1070.
35. Pol, A., Martin, S., Fernandez, M. A., Ferguson, C., Carozzi, A., Luetterforst, R., Enrich, C., and Parton, R. G. (2004). Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol. Biol. Cell 15, 99-110.
36. Ren, X., Ostermeyer, A. G., Ramcharan, L. T., Zeng, Y., Lublin, D. M., and Brown, D. A. (2004). Conformational defects slow Golgi exit, block oligomerization, and reduce raft affinity of caveolin-1 mutant proteins. Mol. Biol. Cell 15, 4556-4567.
37. Robinson, L. J., Pang, S., Harris, D. S., Heuser, J., and James, D. E. (1992). Translocation of the glucose transporter (GLUT4) to the cell surface in permeabilized 3TS-L1 adipocytes: effects of ATP insulin, and GTP gamma S and localization of GLUT4 to clathrin lattices. J. Cell Biol. 117, 1181-1196.
38. 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.
39. 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.
40. 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.
41. 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.
42. Song, K. S., Tang, Z., Li, S., and Lisanti, M. P. (1997). Mutational analysis of the properties of caveolin-1. A novel role for the C-terminal domain in mediating homo-typic caveolin-caveolin interactions. J. Biol. Chem. 272, 4398-4403.
43. 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.
44. Trigatti, B. L., Anderson, R. G., and Gerber, G. E. (1999). Identification of caveolin-1 as a fatty acid binding protein. Biochem. Biophys. Res. Commun. 255, 34-39.
45. 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.
46. Way, M., and Parton, R. G. (1995). M-caveolin, a muscle-specific caveolin-related protein. FEBS Lett. 376, 108-112.
47. Ying, M., Grimmer, S., Iversen, T. G., Van Deurs, B., and Sandvig, K. (2003). Cholesterol loading induces a block in the exit of VSV-G from the TGN. Traffic 4, 772-784.
48. Zurzolo, C., van't Hof, W., van Meer, G., and Rodriguez-Boulan, E. (1994). VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 13, 42-53.