Enlargeosome, an exocytic vesicle resistant to nonionic detergents, undergoes endocytosis via a nonacidic route

Molecular Biology of the Cell

Volumn 15, Issue 12, 2004, Pages 5356-5368

  Cocucci, Emanuele ^a,b,c   Racchetti, Gabriella ^a   Podini, Paola ^a   Rupnik, Marjan ^b   Meldolesi, Jacopo ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b EUROPEAN NEUROSCIENCE INSTITUTE   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 NITROPHENOL; CALCIUM ION; CAVEOLIN; CELL MARKER; CHOLESTEROL; DESMOYOKIN; DETERGENT; EGTAZIC ACID; FLOTILLIN 1; IONOMYCIN; PROTEIN; PROTEIN THY1; TETANUS TOXIN; UNCLASSIFIED DRUG;

ACIDITY; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL SURFACE; CELL TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; CYTOLOGY; CYTOPLASM; ELECTROPHYSIOLOGY; ENDOCYTOSIS; ENLARGEOSOME; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; KINETICS; NONHUMAN; PHOTOLYSIS; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CELL LINE; CHOLESTEROL; DETERGENTS; ELECTRIC CAPACITANCE; ENDOCYTOSIS; ENDOSOMES; EXOCYTOSIS; HUMANS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; IONOMYCIN; IONS; KINETICS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; NEOPLASM PROTEINS; PHOTOLYSIS; RATS;

ANIMALIA;

EID: 9444225970     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-07-0577     Document Type: Article

References (50)

1. Adie, E.J., Francis, M.J., Davies, J., Smith, L., Marenghi, A., Hather, C., Hadingham, K., Michael, N.P., Milligan, G., and Game, S. (2003). CypHer 5, a generic approach for measuring the activation and trafficking of G protein-coupled receptors in live cells. Assay Drug Dev. Technol. 1, 251-259.
2. Anderson, R.G., and Jacobson, K. (2002). A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821-1825.
3. Bickel, P.E., Scherer, P.E., Schnitzer, J.E., Oh, P., Lisanti, M.P., and Lodish, H.F. (1997). Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272, 13793-13802.
4. Borgonovo, B., Cocucci, E., Racchetti, G., Podini, P., Bacbi, A., and Meldolesi, J. (2002). Regulated exocytosis: a novel, widely expressed system. Nat. Cell Biol. 4, 955-962.
5. Brown, D. (2003). The ins and outs of aquaporin-2 trafficking. Am. J. Physiol. 284, F893-F901.
6. Bryant, N.J., Govers, R., and James, D.E. (2002). Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell. Biol. 3, 267-277.
7. Burgoyne, R.D., and Morgan, A. (2003). Secretory granule exocytosis. Physiol. Rev. 83, 581-632.
8. 2+-dependent lysosomal exocytosis but not cell resealing. EMBO Rep. 5, 883-888.
9. 2+ triggers massive exocytosis in Chinese hamster ovary cells. EMBO J. 15, 3787-3791.
10. Gagnoux-Palacios, L., Dans, M., van't Hof, W., Mariotti, A., Pepe, A., Meneguzzi, G., Resh, M.D., and Giancotti, F.G. (2003). Compartmentalization of integrin alpha6beta4 signaling in lipid rafts. J. Cell Biol. 162, 1189-1196.
11. Gerber, S.H., and Sudhof, T.C. (2002). Molecular determinants of regulated exocytosis. Diabetes 51 (Suppl 1), S3-S11.
12. 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.
13. Gleeson, P.A., Lock, J.G., Luke, M.R., and Stow, J.L. (2004). Domains of the TGN: coats, tethers and G proteins. Traffic 5, 315-326.
14. Grundschober, C., Malosio, M.L., Astolfi, L., Giordano, T., Nef, P., and Meldolesi, J. (2002). Neurosecretion competence. A comprehensive gene expression program identified in PC12 cells. J. Biol. Chem. 277, 36715-36724.
15. Hashimoto, T., Gamou, S., Shimizu, N., Kitajima, Y., and Nishikawa, T. (1995). Regulation of translocation of the desmoyokin/AHNAK protein to the plasma membrane in keratinocytes by protein kinase C. Exp. Cell Res. 217, 258-266.
16. Helms, J.B., and Zurzolo, C. (2004). Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5, 247-254.
17. 2+-dependent exocytosis in the somata of dorsal root ganglion neurons. Neuron 17, 135-145.
18. Kasai, H., Kishimoto, T., Liu, T.T., Miyashita, Y., Podini, P., Grohovaz, F., and Meldolesi, J. (1999). Multiple and diverse forms of regulated exocytosis in wild-type and defective PC12 cells. Proc. Natl. Acad. Sci. USA 96, 945-949.
19. Kenworthy, A.K., Nichols, B.J., Remmert, C.L., Hendrix, G.M., Kumar, M., Zimmerberg, J., and Lippincott-Schwartz, J. (2004). Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165, 735-746.
20. Kokubo, H., Helms, J.B., Ohno-Iwashita, Y., Shimada, Y., Horikoshi, Y., and Yamaguchi, H. (2003). Ultrastructural localization of flotillin-1 to cholesterolrich membrane microdomains, rafts, in rat brain tissue. Brain Res. 965, 83-90.
21. Kreft, M., Gasman, S., Chasserot-Golaz, S., Kuster, V., Rupnik, M., Sikdar, S.K., Bader, M., and Zorec, R. (1999). The heterotrimeric Gi(3) protein acts in slow but not in fast exocytosis of rat melanotrophs. J. Cell Sci. 112, 4143-4150.
22. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., and Jahn, R. (2001). SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20, 2202-2213.
23. Malosio, M.L., Benfante, R., Racchetti, G., Borgonovo, B., Rosa, P., and Meldolesi, J. (1999). Neurosecretory cells without neurosecretion: evidence of an independently regulated trait of the cell phenotype. J. Physiol. 520, 43-52.
24. Massol, R.H., Larsen, J.E., Fujinaga, Y., Lencer, W.I., and Kirchhausen, T. (2004). Cholera Toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol. Biol. Cell 15, 323-331.
25. Maxfield, F.R. (2002). Plasma membrane microdomains. Curr. Opin. Cell Biol. 14, 483-487.
26. Maxfield, F.R., and McGraw, T.E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell. Biol. 5, 121-132.
27. Mayor, S., and Rao, M. (2004). Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 5, 231-240.
28. Morrow, I.C., Rea, S., Martin, S., Prior, I.A., Prohaska, R., Hancock, J.F., James, D.E., and Parton, R.G. (2002). Flotillin-1/reggie-2 traffics to surface raft domains via a novel Golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. J. Biol. Chem. 277, 48834-48841.
29. Nabi, I.R., and Le, P.U. (2003). Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673-677.
30. Nichols, B. (2003). Caveosomes and endocvtosis of lipid rafts. J. Cell Sci. 116, 4707-4714.
31. Nichols, B.J., and Lippincott-Schwartz, J. (2001). Endocytosis without clathrin coats. Trends Cell Biol. 11, 406-412.
32. 2+ compound. J. Biol. Chem. 271, 17751-17754.
33. Ochs, R.L., and Press, R.I. (1992). Centromere autoantigens are associated with the nucleolus. Exp. Cell Res. 200, 339-350.
34. Ohara-Imaizumi, M., Nishiwaki, C., Kikuta, T., Kumakura, K., Nakamichi, Y., and Nagamatsu, S. (2004). Site of docking and fusion of insulin secretory granules in live MIN6 beta cells analyzed by TAT-conjugated anti-syntaxin 1 antibody and total internal reflection fluorescence microscopy. J. Biol. Chem. 279, 8403-8408.
35. Parton, R.G., and Hancock, J.F. (2004). Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14, 141-147.
36. Parton, R.G., and Richards, A.A. (2003). Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4, 724-738.
37. Pralle, A., Keller, P., Florin, E.L., Simons, K., and Horber, J.K. (2000). Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148, 997-1008.
38. Salaun, C., James, D.J., and Chamberlain, L.H. (2004). Lipid rafts and the regulation of exocytosis. Traffic 5, 255-264.
39. Sankaranarayanan, S., and Ryan, T.A. (2001). Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4, 129-136.
40. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B.R., and Montecucco, C. (1992). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
41. 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.
42. Sheng, M., and Lee, S.H. (2001). AMPA receptor trafficking and the control of synaptic transmission. Cell 105, 825-828.
43. Shtivelman, E., and Bishop, J.M. (1993). The human gene AHNAK encodes a large phosphoprotein located primarily in the nucleus. J. Cell Biol. 20, 625-630.
44. Shtivelman, E., Cohen, F.E., and Bishop, J.M. (1992). A human gene (AHNAK) encoding an unusually large protein with a 1.2-microns polyionic rod structure. Proc. Natl. Acad. Sci. USA 89, 5472-5476.
45. Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1, 31-39.
46. Sorkin, A., and Von Zastrow, M. (2002). Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell. Biol. 3, 600-614.
47. van Deurs, B., Roepstorff, K., Hommelgaard, A.M., and Sandvig, K. (2003). Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 13, 92-100.
48. Wolf, A.A., Fujinaga, Y., and Lencer, W.I. (2002). Uncoupling of the cholera toxin-G(M1) ganglioside receptor complex from endocytosis, retrograde Golgi trafficking, and downstream signal transduction by depletion of membrane cholesterol. J. Biol. Chem. 277, 16249-16256.
49. Xu, T., Binz, T., Niemann, H., and Neher, E. (1998). Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1, 192-200.
50. 2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 99, 17060-17065.