Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton

Journal of Cell Science

Volumn 115, Issue 22, 2002, Pages 4327-4339

  Mundy, Dorothy I ^a   Machleidt, Thomas ^a   Ying, Yun Shu ^a   Anderson, Richard G W ^a   Bloom, George S ^b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Caveolae; Caveolin; Caveosome; Recycling endosome

Indexed keywords

CAVEOLIN 1; CELL MARKER; LATRUNCULIN A; NOCODAZOLE; CAVEOLIN; DIAGNOSTIC AGENT; FUSED HETEROCYCLIC RINGS; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN; THIAZOLE DERIVATIVE; THIAZOLIDINE DERIVATIVE;

ACTIN FILAMENT; ANIMAL CELL; CAVEOLA; CELL COMPARTMENTALIZATION; CELL MEMBRANE TRANSPORT; CELL MOTILITY; CELL STRUCTURE; CELL SURFACE; CELL VACUOLE; CENTROSOME; CHO CELL; CONTROLLED STUDY; CYTOCHEMISTRY; CYTOSKELETON; DEPOLYMERIZATION; FLUORESCENCE MICROSCOPY; LINEAR SYSTEM; MICROTUBULE ASSEMBLY; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEADY STATE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE; DRUG EFFECT; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOSOME; EUKARYOTIC CELL; HAMSTER; INTRACELLULAR MEMBRANE; METABOLISM; MICROFILAMENT; MICROSCOPY; MICROTUBULE; PHYSIOLOGY; PROTEIN TRANSPORT; ULTRASTRUCTURE;

ANIMALIA;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CAVEOLAE; CAVEOLIN 1; CAVEOLINS; CELL MEMBRANE; CENTROSOME; CHO CELLS; CRICETINAE; ENDOCYTOSIS; ENDOSOMES; EUKARYOTIC CELLS; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; LUMINESCENT PROTEINS; MICROFILAMENTS; MICROSCOPY, ELECTRON; MICROSCOPY, VIDEO; MICROTUBULES; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; THIAZOLES; THIAZOLIDINES;

EID: 0037113074     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00117     Document Type: Review

References (46)

1. Al-Haddad, A., Shonn, M. A., Redlich, B., Blocker, A., Burkhardt, J. K., Yu, H., Hammer, J. A., 3rd, Weiss, D. G., Steffen, W., Griffiths, G. et al. (2001). Myosin Va bound to phagosomes binds to F-actin and delays microtubule-dependent motility. Mol. Biol. Cell 12, 2742-2755.
2. Anderson, R. G. (1998). The caveolae membrane system. Annu. Rev. Biochem. 67, 199-225.
3. Anderson, R. G., Kamen, B. A., Rothberg, K. G. and Lacey, S. W. (1992). Potocytosis: sequestration and transport of small molecules by caveolae. Science 255, 410-411.
4. Apodaca, G. (2001). Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2, 149-159.
5. Bloom, G. S. and Goldstein, L. S. (1998). Cruising along microtubule highways: how membranes move through the secretory pathway. J. Cell Biol. 140, 1277-1280.
6. Brewer, C. B. (1994). Cytomegalovirus plasmid vectors for permanent lines of polarized epithelial cells. Methods Cell Biol. 43, 233-245.
7. Bridgman, P, C. (1999). Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J. Cell Biol. 146, 1045-1060.
8. Buss, F., Arden, S. D., Lindsay, M., Luzio, J. P. and Kendrick-Jones, J. (2001). Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J, 20, 3676-3684.
9. Cordonnier, M. N., Dauzonne, D., Louvard, D. and Coudrier, E. (2001). Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 12, 4013-4029.
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. Fath, K. R. and Burgess, D. R. (1993). Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J Cell Biol. 120, 117-127.
12. 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.
13. Gilbert, A., Paccaud, J. P., Foti, M., Porcheron, G., Balz, J. and Carpentier, J. L. (1999). Direct demonstration of the endocytic function of caveolae by a cell- free assay. J. Cell Sci. 112, 1101-1110.
14. Goldstein, J. L., Basu, S. K. and Brown, M. S. (1983). Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98, 241-260.
15. Izumi, T., Shibata, Y. and Yamamoto, T. (1989). The cytoplasmic surface structures of uncoated vesicles in various tissues of rat as revealed by quick-freeze, deep-etching replicas. J Electron Microsc. 38, 47-53.
16. Kamal, A., Ying, Y. and Anderson, R. G. (1998). Annexin VI-mediated loss of spectrin during coated pit budding is coupled to delivery of LDL to lysosomes. J Cell Biol. 142, 937-947.
17. Kogo, H. and Fujimoto, T. (2000). Concentration of caveolin-1 in the cleavage furrow as revealed by time- lapse analysis. Biochem. Biophys. Res. Commun. 268, 82-87.
18. Kuznetsov, S. A., Langford, G. M. and Weiss, D. G. (1992). Actin-dependent organelle movement in squid axoplasm. Nature 356, 722-725.
19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
20. Lamaze, C., Fujimoto, L. M., Yin, H. L. and Schmid, S. L. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335.
21. Lin, H. C., Moore, M. S., Sanan, D. A. and Anderson, R. G. (1991). Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881-891.
22. Lippincott-Schwartz, J. (1998). Cytoskeletal proteins and Golgi dynamics. Curr. Opin. Cell Biol. 10, 52-59.
23. Liu, P. and Anderson, R. G. (1995). Compartmentalized production of ceramide at the cell surface. J. Biol. Chem. 270, 27179-27185.
24. Machleidt, T., Li, W. P., Liu, P. and Anderson, R. G. (2000). Multiple domains in caveolin-1 control its intracellular traffic. J. Cell Biol. 148, 17-28.
25. Maxfield, F. R. and Yamashiro, D. J. (1987). Endosome acidification and the pathways of receptor- mediated endocytosis. Adv. Exp. Med. Biol. 225, 189-198.
26. Mayor, S., Sabharanjak, S. and Maxfield, F. R. (1998). Cholesterol-dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17, 4626-4638.
27. 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.
28. Morris, R. L. and Hollenbeck, P. J. (1995). Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 131, 1315-1326.
29. Nichols, B. J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4, 374-378.
30. Noda, Y., Okada, Y., Saito, N., Setou, M., Xu, Y., Zhang, Z. and Hirokawa, N. (2001). KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes. J. Cell Biol. 155, 77-88.
31. Palade, G. E. (1953). Fine Structure of Blood Capillaries. J. Appl. Phys. 24, 1424.
32. Parton, R. G., Joggerst, B. and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
33. 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.
34. Rodionov, V. I., Hope, A. J., Svitkina, T. M. and Borisy, G. G. (1998). Functional coordination of microtubule-based and actin-based motility in melanophores. Curr. Biol. 8, 165-168.
35. Rogers, S. L. and Gelfand, V. I. (1998). Myosin cooperates with microtubule motors during organelle transport in melanophores. Curr. Biol. 8, 161-164.
36. Rogers, S. L. and Gelfand, V. I. (2000). Membrane trafficking, organelle transport and the cytoskeleton. Curr. Opin. Cell Biol. 12, 57-62.
37. 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.
38. Simionescu, N. (1983). Cellular aspects of transcapillary exchange. Physiol. Rev. 63, 1536-1579.
39. 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.
40. 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.
41. Tuxworth, R. I. and Titus, M. A. (2000). Unconventional myosins: anchors in the membrane traffic relay. Traffic 1, 11-8.
42. Valetti, C., Wetzel, D. M., Schrader, M., Hasbani, M. J., Gill, S. R., Kreis, T. E. and Schroer, T. A. (1999). Role of dynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol. Biol. Cell 10, 4107-4120.
43. Volonte, D., Galbiati, F. and Lisanti, M. P. (1999). Visualization of caveolin-1, a caveolar marker protein, in living cells using green fluorescent protein (GFP) chimeras. The subcellular distribution of caveolin-1 is modulated by cell-cell contact. FEBS Lett. 445, 431-439.
44. Wu, X., Bowers, B., Rao, K., Wei, Q. and Hammer, J. A. (1998). Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J. Cell Biol. 143, 1899-1918.
45. Yamada, E. (1955). The fine structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1, 445-458.
46. Ying Y. S., Anderson, R. G. and Rothberg, K. G. (1992). Each caveola contains multiple glycosyl-phosphatidylinositol-anchored membrane proteins. Cold Spring Harbor Symp. Quant. Biol. 57, 593-604.