Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface

Nature Cell Biology

Volumn 8, Issue 4, 2006, Pages 317-328

  Choudhury, Amit ^a   Marks, David L ^a   Proctor, Kirsty M ^b   Gould, Gwyn W ^b   Pagano, Richard E ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; GANGLIOSIDE GM1; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN; SNARE PROTEIN; SYNTAXIN 6; UNCLASSIFIED DRUG;

ARTICLE; CAVEOLA; CELL MEMBRANE; CELL SURFACE; CELL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIPID TRANSPORT; MEMBRANE FUSION; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSPORT KINETICS;

CAVEOLAE; CAVEOLIN 1; CELL MEMBRANE; CELLS, CULTURED; ENDOCYTOSIS; FIBROBLASTS; G(M1) GANGLIOSIDE; GLYCOSYLPHOSPHATIDYLINOSITOLS; GOLGI APPARATUS; HUMANS; MEMBRANE GLYCOPROTEINS; OLIGONUCLEOTIDES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; STEM CELLS; VIRAL ENVELOPE PROTEINS;

BACTERIA (MICROORGANISMS); VESICULAR STOMATITIS VIRUS;

EID: 33645713636     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1380     Document Type: Article

References (48)

1. Cohen, A. W., Hnasko, R., Schubert, W. & Lisanti, M. P. Role of caveolae and caveolins in health and disease. Physiol. Rev. 84, 1341-1379 (2004).
2. Mineo, C. & Anderson, G. W. Potocytosis. Histochem. Cell Biol. 116, 109-118 (2001).
3. Parton, R. G. & Richards, A. A. Lipid rafts and caveolae as portals for endocytosis: New insights and common mechanisms. Traffic 4, 724-738 (2003).
4. Duncan, M. J., Shin, J. S. & Abraham, S. N. Microbial entry through caveolae: Variations on a theme. Cell Microbiol. 4, 783-791 (2002).
5. Lencer, W. I., Hirst, T. R. & Holmes, R. K. Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta. 1450, 177-190 (1999).
6. Marjomäki, V. S., Huovila, A.-P. J., Surkka, M. A., Jokinen, I. & Salminen, A. Lysosomal trafficking in rat cardiac myocytes. J. Histochem. Cytochem. 38, 1155-1164 (1990).
7. Norkin, L. C. Caveolae in the uptake and targeting of infectious agents and secreted toxins. Adv. Drug Deliv. Rev. 49, 301-315 (2001).
8. Pelkmans, L., Kartenbeck, J. & Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature Cell Biol. 3, 473-483 (2001).
9. Richterova, Z. et al. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J. Virol. 75, 10880-10891 (2001).
10. Shin, J.-S., Gao, Z. & Abraham, N. Involvement of cellular caveolae in bacterial entry into mast cells. Science 289, 785-788 (2000).
11. Kim, Y. N. & Bertics, P. J. The endocytosis-linked protein dynamin associates with caveolin-1 and is tyrosine phosphorylated in response to the activation of a noninternalizing epidermal growth factor receptor mutant. Endocrinology 143, 1726-1731 (2002).
12. Mineo, C., Gill, G. N. & Anderson, R. G. Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem. 274, 30636-30643 (1999).
13. Shajahan, A. N. et al. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J. Biol. Chem. 279, 20392-20400 (2004).
14. Sharma, D. K. et al. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell 15, 3114-3122 (2004).
15. Volonte, D. et al. Flotillins-cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J. Biol. Chem. 274, 12702-12709 (1999).
16. Chen, Y. A. & Scheller, R. H. SNARE-mediated membrane fusion. Nature Rev. Mol. Cell Biol. 2, 98-106 (2001).
17. McNew, J. A. et al. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153-159 (2000).
18. Ungar, D. & Hughson, F. M. SNARE protein structure and function. Annu. Rev. Cell Dev. Biol. 19, 493-517 (2003).
19. McIntosh, D. P. & Schnitzer, J. E. Caveolae require intact VAMP for targeted transport in vascular endothelium. Am. J. Physiol. 277, H2222-H2232 (1999).
20. Predescu, D., Horvat, R., Predescu, S. & Palade, G. E. Transcytosis in the continuous endothelium of the myocardial microvasculature is inhibited by N-ethylmaleimide. Proc. Natl Acad. Sci. USA 91, 3014-3018 (1994).
21. Schnitzer, J. E., Liu, J. & Oh, P. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. J. Biol. Chem. 270, 14399-14404 (1995).
22. Kuliawat, R. et al. Syntaxin-6 SNARE involvement in secretory and endocytic pathways of cultured pancreatic β-cells. Mol. Biol. Cell 15, 1690-1701 (2004).
23. Perera, H. K. I. et al. Syntaxin 6 regulates Glut4 trafficking in 3T3-L1 Adipocytes. Mol. Biol Cell 14, 2946-2958 (2003).
24. Wendler, F., Page, L., Urbe, S. & Tooze, S. A. Homotypic fusion of immature secretory granules during maturation requires syntaxin 6. Mol. Biol. Cell 12, 1699-1709 (2001).
25. Ros-Baro, A. et al. Lipid rafts are required for GLUT4 internalization in adipose cells. Proc. Natl Acad. Sci. USA 98, 12050-12055 (2001).
26. Shigematsu, S., Watson, R. T., Khan, A. H. & Pessin, J. E. The adipocyte plasma membrane caveolin functional-structural organization is necessary for the efficient endocytosis of GLUT4. J. Biol. Chem. 278, 10683-10690 (2003).
27. Shewan, A. M. et al. GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: Involvement of an acidic targeting motif. Mol. Biol. Cell 14, 973-986 (2003).
28. Puri, V. et al. Clathrin-dependent and independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 154, 535-547 (2001).
29. Sharma, D. K. et al. Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem. 278, 7564-7572 (2003).
30. Singh, R. D. et al. Selective caveolin-1-dependent endocytosis of glycosphingolipids. Mol. Biol. Cell 14, 3254-3265 (2003).
31. Olson, A. L., Knight, J. B. & Pessin, J. E. Syntaxin 4, VAMP2, and/or VAMP3-cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell Biol. 17, 2425-2435 (1997).
32. Tellam, J. T. et al. Characterization of Munc-18c and syntaxin-4 in 3T3-L1 adipocytes. Putative role in insulin-dependent movement of GLUT-4. J. Biol. Chem. 272, 6179-6186 (1997).
33. Shubert, W. et al. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J. Biol. Chem. 276, 48619-48622 (2001).
34. Prekeris, R., Klumperman, J., Chen, Y. A. & Scheller, R. H. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143, 957-971 (1998).
35. del Pozo, M. A. et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nature Cell Biol. 7, 901-908 (2005).
36. Orlichenko, L., Huang, B., Krueger, E. & McNiven, M. A. EGF-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells. J. Biol. Chem. 281, 4570-4579 (2006).
37. Chamberlain, L. H., Burgoyne, R. D. & Gould, G. W. SNARE proteins are highly enriched in lipid rafts in PC12 cells: Implications for the spatial control of exocytosis. Proc. Natl Acad. Sci. USA 98, 5619-5624 (2001).
38. Puri, V. et al. Sphingolipid storage induces accumulation of intracellular cholesterol by stimulating SREBP-1 cleavage. J. Biol. Chem. 278, 20961-20970 (2003).
39. Martin, L. B., Shewan, A., Millar, C. A., Gould, G. W. & James, D. E. Vesicle-associated membrane protein 2 plays a specific role in the insulin-dependent trafficking of the facilitative glucose transporter GLUT4 in 3T3-L1 adipocytes. J. Biol. Chem. 273, 1444-1452 (1998).
40. Volchuk, A. et al. Syntaxin 4 in 3T3-L1 adipocytes: Regulation by insulin and participation in insulin-dependent glucose transport. Mol. Biol. Cell 7, 1075-1082 (1996).
41. Morcos, P. A. Achieving efficient delivery of morpholino oligos in cultured cells. Genesis 30, 94-102 (2001).
42. Wendler, F. & Tooze, S. Syntaxin 6: The promiscuous behaviour of a SNARE protein. Traffic 2, 606-611 (2001).
43. Martin-Martin, B., Nabokina, S. M., Blasi, J., Lazo, P. A. & Mollinedo, F. Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 96, 2574-2583 (2000).
44. Sharma, D. K. et al. The glycosphingolipid, lactosylceramide, regulates β1-integrin clustering and endocytosis. Cancer Res. 65, 8233-8241 (2005).
45. Choudhury, A. et al. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 109, 1541-1550 (2002).
46. Martin, O. C. & Pagano, R. E. Internalization and sorting of a fluorescent analog of glucosylceramide to the Golgi apparatus of human skin fibroblasts: Utilization of endocytic and nonendocytic transport mechanisms. J. Cell Biol. 125, 769-781 (1994).
47. Sabharanjak, S., Sharma, P., Parton, R. G. & Mayor, S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Develop. Cell 2, 411-423 (2002).
48. Henley, J. R., Krueger, E. W., Oswald, B. J. & McNiven, M. A. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141, 85-99 (1998).