In vitro budding of intralumenal vesicles into late endosomes is regulated by alix and tsg101

Molecular Biology of the Cell

Volumn 19, Issue 11, 2008, Pages 4942-4955

  Falguières, Thomas ^a   Luyet, Pierre Philippe ^a   Bissig, Christin ^a   Scott, Cameron C ^a   Velluz, Marie Claire ^a   Gruenberg, Jean ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; ALG 2 INTERACTING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; TRYPSIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; ARYLSULFONIC ACID DERIVATIVE; CALCIUM BINDING PROTEIN; DNA BINDING PROTEIN; PROTEIN SUBUNIT; PYRANINE; TRANSCRIPTION FACTOR; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; CELL BUDDING; CELL MEMBRANE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL LINE; HAMSTER; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; PH; PROTEIN TRANSPORT; ULTRASTRUCTURE;

ANIMALS; ARYLSULFONATES; CALCIUM-BINDING PROTEINS; CELL LINE; CRICETINAE; DNA-BINDING PROTEINS; ENDOSOMES; HUMANS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSCRIPTION FACTORS; VESICULAR TRANSPORT PROTEINS;

EID: 58149280810     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-03-0239     Document Type: Article

References (80)

1. Abrami, L., Lindsay, M., Parton, R. G., Leppla, S. H., and van der Goot, F. G. (2004). Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J. Cell Biol. 166, 645-651.
2. Aniento, F., Emans, N., Griffiths, G., and Gruenberg, J. (1993a). Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123, 1373-1387.
3. Aniento, F., Roche, E., Cuervo, A. M., and Knecht, E. (1993b). Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lyso-somes. J. Biol. Chem. 268, 10463-10470.
4. Babst, M. (2005). A protein's final ESCRT. Traffic 6, 2-9.
5. Bache, K. G., Brech, A., Mehlum, A., and Stenmark, H. (2003a). Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442.
6. Bache, K. G., Raiborg, C., Mehlum, A., and Stenmark, H. (2003b). STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521.
7. 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.
8. Burnette, W. N. (1981). "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112, 195-203.
9. Cabezas, A., Bache, K. G., Brech, A., and Stenmark, H. (2005). Alix regulates cortical actin and the spatial distribution of endosomes. J. Cell Sci. 118, 2625-2635.
10. Carlton, J. G., and Martin-Serrano, J. (2007). Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912.
11. Cavalli, V., Vilbois, F., Corti, M., Marcote, M. J., Tamura, K., Karin, M., Arkinstall, S., and Gruenberg, J. (2001). The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol. Cell 7, 421-432.
12. Chatellard-Causse, C., Blot, B., Cristina, N., Torch, S., Missotten, M., and Sadoul, R. (2002). Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J. Biol. Chem. 277, 29108-29115.
13. Chevallier, J., Chamoun, Z., Jiang, G., Prestwich, G., Sakai, N., Matile, S., Parton, R. G., and Gruenberg, J. (2008). Lysobisphosphatidic acid controls endosomal cholesterol levels. J. Biol. Chem. (in press).
14. Doyotte, A., Russell, M. R., Hopkins, C. R., and Woodman, P. G. (2005). Depletion of TSG101 forms a mammalian "Class E" compartment: a multi-cisternal early endosome with multiple sorting defects. J. Cell Sci. 118, 3003-3017.
15. Fernandez-Borja, M., Wubbolts, R., Calafat, J., Janssen, H., Divecha, N., Dus-seljee, S., and Neefjes, J. (1999). Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr. Biol. 9, 55-58.
16. Fisher, R. D., Chung, H. Y., Zhai, Q., Robinson, H., Sundquist, W. I., and Hill, C. P. (2007). Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell. 128, 841-852.
17. Forgac, M. (2007). Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929.
18. Frelin, C., Vigne, P., Ladoux, A., and Lazdunski, M. (1988). The regulation of the intracellular pH in cells from vertebrates. Eur. J. Biochem. 174, 3-14.
19. Futter,C. E.,Collinson,L. M.,Backer,J. M.,and Hopkins,C. R. (2001). Human VPS34 is required for internal vesicle formation within multivesicular endo-somes. J. Cell Biol. 155, 1251-1264.
20. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G., and Stenmark, H. (2000). Localization of phosphatidyl-inositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
21. Gorvel, J. P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991). rab5 controls early endosome fusion in vitro. Cell 64, 915-925.
22. Gottlinger, H. G. (2007). How HIV-1 hijacks ALIX. Nat. Struct. Mol. Biol. 14, 254-256.
23. 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.
24. Gruenberg, J. (2001). The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2, 721-730.
25. Gruenberg, J., Griffiths, G., and Howell, K. E. (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316.
26. Gruenberg, J., and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
27. Gu, F., Aniento, F., Parton, R. G., and Gruenberg, J. (1997). Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. J. Cell Biol. 139, 1183-1195.
28. Hanson, P. I., Roth, R., Lin, Y., and Heuser, J. E. (2008). Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389-402.
29. Harder, T., Kellner, R., Parton, R., and Gruenberg, J. (1997). Specific release of membrane bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8, 533-545.
30. Hurley, J. H., and Emr, S. D. (2006). The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277-298.
31. Kobayashi, T., Beuchat, M. H., Chevallier, J., Makino, A., Mayran, N., Escola, J. M., Lebrand, C., Cosson, P., and Gruenberg, J. (2002). Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277, 32157-32164.
32. Kobayashi, T., Beuchat, M. H., Lindsay, M., Frias, S., Palmiter, R. D., Sakuraba, H., Parton, R. G., and Gruenberg, J. (1999). Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol 1, 113-118.
33. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G., and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
34. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
35. Le Blanc, I. et al. (2005). Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7, 653-664.
36. Lebrand, C., Corti, M., Goodson, H., Cosson, P., Cavalli, V., Mayran, N., Faure, J., and Gruenberg, J. (2002). Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J. 21, 1289-1300.
37. Liscum, L., and Faust, J. R. (1989). The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3- beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J. Biol. Chem. 264, 11796-11806.
38. Lloyd, T. E., Atkinson, R., Wu, M. N., Zhou, Y., Pennetta, G., and Bellen, H. J. (2002). Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269.
39. Mari, M., Bujny, M. V., Zeuschner, D., Geerts, W. J., Griffith, J., Petersen, C. M., Cullen, P. J., Klumperman, J., and Geuze, H. J. (2008). SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 9, 380-393.
40. Matsuo, H. et al. (2004). Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303, 531-534.
41. Maxfield, F. R., and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
42. Maxfield, F. R., and Tabas, I. (2005). Role of cholesterol and lipid organization in disease. Nature 438, 612-621.
43. Mayor, S., and Pagano, R. E. (2007). Pathways of clathrin-independent endo-cytosis. Nat. Rev. Mol. Cell Biol. 8, 603-612.
44. Mayran, N., Parton, R. G., and Gruenberg, J. (2003). Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 22, 3242-3253.
45. Mellman, I., Fuchs, R., and Helenius, A. (1986). Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55, 663-700.
46. Morel, E., and Gruenberg, J. (2007). The p11/S100A10 light chain of annexin A2 is dispensable for annexin A2 association to endosomes and functions in endosomal transport. PLoS ONE 2, e1118.
47. Morita, E., Sandrin, V., Alam, S. L., Eckert, D. M., Gygi, S. P., and Sundquist, W. I. (2007a). Identification of human MVB12 proteins as ESCRT-I subunits that function in HIV budding. Cell Host Microb. 2, 41-53.
48. Morita, E., Sandrin, V., Chung, H. Y., Morham, S. G., Gygi, S. P., Rodesch, C. K.,and Sundquist,W. I. (2007b). Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215-4227.
49. Munshi, U. M., Kim, J., Nagashima, K., Hurley, J. H., and Freed, E. O. (2006). An Alix fragment potently inhibits HIV-1 budding: characterization of binding to retroviral YPXL late domains. J. Biol. Chem. 282, 3847-3855.
50. Murk, J. L., Humbel, B. M., Ziese, U., Griffith, J. M., Posthuma, G., Slot, J. W., Koster, A. J., Verkleij, A. J., Geuze, H. J., and Kleijmeer, M. J. (2003). Endo-somal compartmentalization in three dimensions: implications for membrane fusion. Proc. Natl. Acad. Sci. USA 100, 13332-13337.
51. Nickerson, D. P., Russell, M. R., and Odorizzi, G. (2007). A concentric circle model of multivesicular body cargo sorting. EMBO Rep. 8, 644-650.
52. Odorizzi, G. (2006). The multiple personalities of Alix. J. Cell Sci. 119, 3025-3032.
53. Parton,R. G., Schrotz, P., Bucci, C.,and Gruenberg, J. (1992). Plasticityofearly endosomes. J. Cell Sci. 103, 335-348.
54. Petiot, A., Faure, J., Stenmark, H., and Gruenberg, J. (2003). PI3P signaling regulates receptor sorting but not transport in the endosomal pathway. J. Cell Biol. 162, 971-979.
55. Piper, R. C., and Katzmann, D. J. (2007). Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519-547.
56. Pons, V., Luyet, P.-P., Morel, E., Abrami, L., van der Goot, F. G., Parton, R. G., and Gruenberg, J. (2008). Hrs and SNX3 functions in sorting and membrane invagination within multivesicular bodies. PLoS Biol. 6, e214.
57. Pornillos, O., Alam, S. L., Rich, R. L., Myszka, D. G., Davis, D. R., and Sundquist, W. I. (2002). Structure and functional interactions of the Tsg101 UEV domain. EMBO J. 21, 2397-2406.
58. Raiborg, C., Bremnes, B., Mehlum, A., Gillooly, D. J., D'Arrigo, A., Stang, E., and Stenmark, H. (2001). FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J. Cell Sci. 114, 2255-2263.
59. Raiborg, C., Wesche, J., Malerod, L., and Stenmark, H. (2006). Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J. Cell Sci. 119, 2414-2424.
60. Raymond, C. K., Howald-Stevenson, I., Vater, C. A., and Stevens, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
61. Razi, M., and Futter, C. E. (2006). Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483.
62. Reaves, B. J., Bright, N. A., Mullock, B. M., and Luzio, J. P. (1996). The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J. Cell Sci. 109, 749-762.
63. Rojo, M., Peppercok, R., Emery, G., Kellner, R., Stang, E., Parton, R. G., and Gruenberg, J. (1997). Involvement of the transmembrane protein p23 in bio-synthetic protein transport. J. Cell Biol. 139, 1119-1135.
64. Schmidt, M. H., Hoeller, D., Yu, J., Furnari, F. B., Cavenee, W. K., Dikic, I., and Bogler, O. (2004). Alix/AIP1 antagonizes epidermal growth factor receptor downregulation by the Cbl-SETA/CIN85 complex. Mol. Cell. Biol. 24, 8981-8993.
65. Simons, K., and Gruenberg, J. (2000). Jamming the endosomal system: lipid rafts and lysosomal storage diseases. Trends Cell Biol. 10, 459-462.
66. Slagsvold, T., Pattni, K., Malerod, L., and Stenmark, H. (2006). Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol. 16, 317-326.
67. Sobo, K., Chevallier, J., Parton, R. G., Gruenberg, J., and van der Goot, F. G. (2007a). Diversity of raft-like domains in late endosomes. PLoS ONE 2, e391.
68. Sobo, K., Le Blanc, I., Luyet, P. P., Fivaz, M., Ferguson, C., Parton, R. G., Gruenberg, J., and van der Goot, F. G. (2007b). Late endosomal cholesterol accumulation leads to impaired intra-endosomal trafficking. PLoS ONE 2, e851.
69. Strack, B., Calistri, A., Craig, S., Popova, E., and Gottlinger, H. G. (2003). AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689-699.
70. Sturley, S. L., Patterson, M. C., Balch, W., and Liscum, L. (2004). The pathophysiology and mechanisms of NP-C disease. Biochim. Biophys. Acta 1685, 83-87.
71. Taub, N., Teis, D., Ebner, H. L., Hess, M. W., and Huber, L. A. (2007). Late endosomal traffic of the epidermal growth factor receptor ensures spatial and temporal fidelity of mitogen-activated protein kinase signaling. Mol. Biol. Cell 18, 4698-4710.
72. Tedesco, M. M., and Matile, S. (1999). Spectroscopic detection of endovesicu-lation by large unilamellar phosphatidylcholine vesicles: effects of chlorprom-azine, dibucaine, and safingol. Bioorg. Med. Chem. 7, 1373-1379.
73. Teis, D., Wunderlich, W., and Huber, L. A. (2002). Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803-814.
74. Urbe, S., Sachse, M., Row, P. E., Preisinger, C., Barr, F. A., Strous, G., Klumperman, J., and Clague, M. J. (2003). The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116, 4169-4179.
75. van der Goot, F. G., and Gruenberg, J. (2006). Intra-endosomal membrane traffic. Trends Cell Biol. 16, 514-521.
76. von Schwedler, U. K. et al. (2003). The protein network of HIV budding. Cell 114, 701-713.
77. White, I. J., Bailey, L. M., Aghakhani, M. R., Moss, S. E., and Futter, C. E. (2006). EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25, 1-12.
78. Williams, R. L., and Urbe, S. (2007). The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368.
79. Willoughby, D., Thomas, R. C., and Schwiening, C. J. (1998). Comparison of simultaneous pH measurements made with 8-hydroxypyrene-1,3,6-trisul-phonic acid (HPTS) and pH-sensitive microelectrodes in snail neurones. Pfluegers Arch. 436, 615-622.
80. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2, 107-117.