Direct demonstration of the endocytic function of caveolae by a cell-free assay

Journal of Cell Science

Volumn 112, Issue 7, 1999, Pages 1101-1110

  Gilbert, Anne ^a   Paccaud, Jean Pierre ^a   Foti, Michelangelo ^a   Porcheron, Geneviève ^a   Balz, Jacqueline ^a   Carpentier, Jean Louis ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Caveolae; Clathrin; Endocytosis

Indexed keywords

CHOLERA TOXIN; CLATHRIN; IODINE 125; MEMBRANE RECEPTOR; NUCLEOTIDE;

ANIMAL CELL; ARTICLE; BIOCHEMISTRY; CELL FREE SYSTEM; CELL MEMBRANE; COATED VESICLE; CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; ENDOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSPORT KINETICS;

3T3 CELLS; ADENOSINE TRIPHOSPHATE; ANIMALS; CELL MEMBRANE; CELL-FREE SYSTEM; CENTRIFUGATION, DENSITY GRADIENT; COATED PITS, CELL-MEMBRANE; CYTOSOL; EDETIC ACID; ENDOCYTOSIS; FILIPIN; GUANOSINE TRIPHOSPHATE; MICE; MICROSCOPY, ELECTRON; RADIOLIGAND ASSAY; TIME FACTORS;

ANIMALIA;

EID: 0032937877     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Anderson, R. G. (1993). Caveolae: where incoming and outgoing messengers meet. Proc. Natl. Acad. Sci. USA 90, 10909-10913.
2. Bar-Sagi, D. and Feramisco, J. R. (1986). Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science 233, 1061-1068.
3. Barlow, C., Orci, L., Young, T., Hosotuchi, M., Hamamoto, S., Salama, N., Renach, M. F., Ravazzola, M., Amherdt, M. and Schekman, R. (1994). COP II: A membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
4. Birn, H., Selhub, J. and Christensen, E. I. (1993). Internalization and intracellular transport of folate-binding protein in rat kidney proximal tubule. Am. J. Physiol. 264, 302-310.
5. Bruns, R. R. and Palade, G. E. (1968). Studies on blood capillaries: II. Transport of ferritin molecules across the wall of muscle capillaries. J. Cell Biol. 31, 277-299.
6. Bundgaard, M., Hagman, P. and Crone, C. (1983). The three dimensional organisation of plasmalemmal vesicular profiles in the endothelium of rat heart capillaries. Microvasc. Res. 25, 358-368.
7. Carpentier, J.-L., Brown, D., Iacopetta, B. and Orci, L. (1985). Detection of surface-bound ligands by freeze-fracture autoradiography. J. Cell Biol. 101, 887-890.
8. Carpentier, J.-L., Sawano, F., Geiger, D., Gorden. P., Perrelet, A. and Orci, L. (1989). Potassium depletion and hypertonic medium reduce 'non-coated' and clathrin-coated pit formation, as well as endocytosis through these two gates. J. Cell. Physiol. 138, 519-526.
9. Carpentier, J. L., Lew, D. P., Paccaud, J. P., Gil, R., Iacopetta, B., Kazatchkine, M., Stendhal, O. and Pozzan, T. (1991). Internalization pathways of C3b receptors in human neutrophils and its transmodulation by chemottractant receptors stimulation. Cell. Regul. 2, 41.
10. Carpentier, J.-L., Paccaud, J.-P., Backer, J., Gilbert, A., Orci, L. and Kahn, C. R. (1993). Two steps of insulin receptor internalization depend on different domaines of the β-subunit. J. Cell Biol. 122, 1243-1252.
11. Chang, W.-.J., Rothberg, K. G., KLamen, A. and Anderson R. G. W. (1992). Lowering of the cholesterol content of MA104 cells inhibits receptors mediated transport of folate. J. Cell Biol. 118, 63-69.
12. Chang, W.-J., Ying, Y.-S., Rothberg, K. G., Hooper, N. M., Turner, A. J., Gamblieel, H. A., De Gunzburg, J., Mumby, S. M., Gilman, A. G. and Anderson, R. G. W. (1994). Purification and characterization of smooth muscle cell caveolae. J. Cell Biol. 126, 127-138.
13. Cupers, P., Veithen, A., Kiss, A., Baudhin, P. and Courtoy, P. J. (1994) Clathrin polymerization is not required for bulk-phase endocytosis in rat fetal fibroblasts. J. Cell Biol. 127, 725-735.
14. Damke, H., Baba, T., van der Bliek, A. M. and Schmid, S. L. (1995) Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 131, 69-80.
15. Daukas, G. and Zigmond, S. H. (1985). Inhibition of receptor-mediated but not fluid-phase endocytosis in polymorphonuclear leukocytes. J Cell Biol. 101, 1673-1679
16. 2-Macroglobulin adsorbed to colloidal gold: a new probe in the study of receptor-mediated endocytosis. J. Cell Biol. 89, 29-34.
17. Fan, J. Y., Carpentier, J. L., van Obberghen, E., Grunfeld, C., Gorden, P. and Orci, L. (1983). Morphological changes of the 3T3-L1 fibroblast plasma membrane upon differentiation to the adipocyte form. J. Cell Sci. 61, 219-230.
18. Frokjaer-Jensen, J., Wagner, R. C., Andrews, S. B., Hagman, P. and Reese, T. S. (1988). Three-dimensional organisation of the plasmalemmal vesicular system in direcly frozen capillaries of the rete mirabile in the swim bladder of the eel. Cell Tissue Res. 254, 17-24.
19. Frokjaer-Jensen, J. (1991). The endothelial vesicle system in cryofixed frog mesenteric capillaries analysed by ultrathin serial sectioning. J Electron Microsc. Tech. 19, 291-304.
20. Fujimoto, T. (1993). Calcium pump of the plasma membrane is localized in caveolae. J. Cell Biol. 120, 1147-1157.
21. Fujimoto, T., Nakade, A., Miyawaki, A., Mikoshiba, K. and Ogawa, K. (1993). Localization of inositol 1,4.5-triphosphate receptor-like protein in plasmalemmal caveolae. J. Cell Biol. 119, 1507-1513.
22. Gafencu, A., Stanescu, M., Toderici, A. M., Heltianu, C. and Simionescu, M. (1998). Protein and fatty acid composition of caveolae from apical plasmalemma of aortic endothelial cells. Cell Tissue Res. 293, 101-110.
23. Gilbert, A., Paccaud, J.-P. and Carpentier J.-L. (1997). Direct measurement of clathrin-coated vesicle formation using a cell-free assay. J. Cell Sci. 110, 3105-3115.
24. 2-Macroglobulin-trypsin complexes in hepatocytes and adipocytes. Biochim. Biophys. Acta 756, 230-237.
25. 2-Macroglobulin-trypsin complexes in rat hepatocytes. Biochim. Biophys. Acta 885, 49-57.
26. Goldstein, J. L., Brown, M. S., Andersen, R. G. W., Russel, D. N. and Schneider, W. J. (1985). Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1, 1-39.
27. Griffiths, G., Back, R. and Marsh, M. (1989). A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J. Cell Biol. 109, 2703-2720.
28. Haigler, H., McKanna, J. A. and Cohen, S. (1979). Rapid stimulation of pinocytosis in human carcinoma cells A-431 by epidermal growth factor. J. Cell Biol. 83, 82-90.
29. Hansen, S. H., Sandvig, K. and Van Deurs, B. (1991). The preendosomal compartment comprises distinct coated and noncoated endocytic vesicle populations. J. Cell Biol. 113, 731-741.
30. Heuser, J. (1980). Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol. 84, 560-583.
31. Hjelle, J. T., Christensen, E. I., Carone, F. A. and Selhub, J. (1991) Cell fractionation and electron microscope studies of kidneys folate-binding protein. Am. J. Physiol. 260, 338-346.
32. Huet, C., Ash, J. F. and Singer, S. J. (1980). The antibody-induced clustering and endocytosis of HLA antigens on cultured human fibroblasts. Cell 21, 429-438.
33. Keller, G. A., Siegel, M. W. and Caras, I. W. (1992). Endocytosis of glycophospholipid-anchored and transmembrane forms of CD4 by different endocylic pathways. EMBO J. 11, 863-874.
34. Keller, H. U. (1990). Diacylglycerols and PMA are particularly effective stimulators of fluid pinocytosis in human neutrophils. J. Cell. Physiol. 145, 465-471.
35. Kiss, A. L. and Geuze, H. J. (1997). Caveolae can be alternative endocytotic structures in elicited macrophages. Eur. J. Cell Biol. 73, 19-27.
36. Lewis, W. H. (1931). Pinocytosis. Bull. John Hopkins Hospital XLIX, 17-27.
37. Lin, H. C., Moore, M. S., Sanan, D. A. and Anderson, R. G. W. (1991). Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881-891.
38. Lisanti, M. P., Scherer, P. E., Vidugirieene, J., Tang, Z., Hermanowskivosatka, A., Tu, Y.-H., Cook, F. C. and Sargiacomo, M. (1994). Characterization of caveolae-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J. Cell Biol. 126, 111-126.
39. Madshus, I. H., Tonnessen, T. I., Olsnes, S. and Sandvig, K. (1987). Effect of potassium depletion of Hep-2 cells on intracellular pH and on chloride uptake by anion antiport. J. Cell Physiol. 131, 6-13.
40. Malhotra, V., Serafini, T., Orci, L., Shepherd, J. C. and Rothman, J. E. (1989). Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58, 329-336.
41. Marsh, M. and Helenius, A. (1980). Adsorptive endocytosis of Semliki forest virus. J. Mol. Biol. 142, 439-454.
42. Milici, A. J., Watrous, N. E., Stukenbrok, H. and Palade, G. E. (1987). Transcytosis of albumin in capillary endothelium. J. Cell Biol. 105, 2603-2612.
43. Montesano, R., Roth, J., Robert, A. and Orci, L. (1982). Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296, 651-653.
44. Moore, M. S., Mahaffey, D. T., Brodsky, F. M. and Anderson, R. G. W. (1987). Assembly of clathrin-coated pits onto purified plasma membranes. Science 236, 558-563.
45. Oka, J. A., Christensen, M. D. and Weigel, P. H. (1989). Hypertonicity inhibits galactosyl receptor-mediated but not fluid-phase endocytosis in isolated rat hepatocyles. J. Biol. Chem. 264, 12016-12024.
46. Palade, G. E. (1953). Fine structure of blood capillaries. J. Appl. Physics 24, 368-384.
47. Parton, R. G. (1994). Ultrastructural localization of gangliosides. GM1 is concentrated in caveolae. J. Histochem. Cytochem. 42, 155-166.
48. Parton, R. G., Joggerst, B. and Simons, K. (1994) Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
49. Peters, K., Carley, W. W. and Palade, G. E. (1985). Endothelial plasmalemmal vesicles have characteristic striped bipolar structure. J. Cell Biol. 101, 2233-2238.
50. Predescu, S., Predescu, D. and Palade, G. (1997). Plasmalemmal vesicles function as transcytotic carriers for small proteins in the continuous endothelium. Am. J. Physiol. 272, H937-H939.
51. Raposo, G., Dunia, I., Delavier-Klutchko, C., Kaveri, S., Strosberg, A. D. and Benedetti, E. L. (1989). Internalization of β-adrenergic receptor in A431 cells involves non-coated vesicles. Eur. J. Cell Biol. 50, 340-352.
52. Rothberg, K. G., Ying, Y.-S., Kolhouse, J. K., Kamen, B. A. and Anderson, R. G. W. (1990). The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytosis pathway. J. Cell Biol. 110, 637-649.
53. 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.
54. Sandvig, K., Olsnes, S., Petersen, O. W. and Van Deurs, B. (1987). Acidification of the cytosol inhibits endocytosis from coated pits. J. Cell Biol. 105, 679-689.
55. Sandvig, K. and Van Deurs, B. (1994). Endocytosis without clathrin. Trends Cell Biol. 4, 275-277.
56. Scherer, P. E., Lisanti, M. P., Baldini, G., Sargiacomo, M., Mastick, C. C. and Lodish, H. F. (1994). Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J. Cell Biol 127, 1233-1243.
57. Schnitzer, J. E., Oh, P., Pinney, E. and Allard, J. (1994). Filipin-sensitive caveolae-medialed transport in endothelium: Reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127, 1217-1232.
58. Schnitzer, J. E., Oh, P. and McIntosh, D. P. (1996). Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science 274, 239-242.
59. Severs, N. J. (1988). Caveolae: static inpocketings of the plasma membrane. dynamic vesicles or plain artifact. J. Cell Sci. 90, 341-348.
60. Swanson, J. A. (1989). Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J. Cell Sci. 94, 135-142.
61. Swanson, J. A. and Watts, C. (1995). Macropinocytosis. Trends Cell Biol. 5, 424-428.
62. Tran, D., Carpentier, J.-L, Sawano, F., Gorden, P. and Orci, L. (1987). Ligands internalized through coated or non coated invaginations follow a common intracellular pathway. Proc. Nat. Acad. Sci. USA 84, 7957-7961.
63. Turek, J. J., Leamon, C. P. and Low, P. S. (1993). Endocytosis of folate-protein conjugates: ultrastructural localization in KB cells. J. Cell Sci. 106, 423-430.
64. van der Goot, F. G. (1997). Separation of early steps in endocytic membrane transport. Electrophoresis 18, 2689-2693.
65. van Deurs, B., Petersen, O. W., Olsner, S. and Sandvig, K. (1989). The ways of endocytosis. Int. Rev. Cytol. 117, 131-177.
66. van Deurs, B., Holm, P. K., Sandvig, K. and Hansen, S. H. (1993). Are caveolae involved in clathrin-independent endocytosis? Trends Cell Biol. 3, 249-265.