Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly

Molecular Biology of the Cell

Volumn 19, Issue 6, 2008, Pages 2661-2672

  Shim, Soomin ^a   Merrill, Samuel A ^a   Hanson, Phyllis I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGED MULTIVESICULAR BODY PROTEIN 1B; CHARGED MULTIVESICULAR BODY PROTEIN 2A; CHARGED MULTIVESICULAR BODY PROTEIN 3; CHARGED MULTIVESICULAR BODY PROTEIN 4A; CHARGED MULTIVESICULAR BODY PROTEIN 5; CHARGED MULTIVESICULAR BODY PROTEIN 6; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT III; PROTEIN LIP5; SYNTHETASE; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 2; VACUOLAR PROTEIN SORTING 20; VACUOLAR PROTEIN SORTING 24; VACUOLAR PROTEIN SORTING 4;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CELL LINE; ENDOSOMES; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE DELETION; TRANSFECTION; VESICULAR TRANSPORT PROTEINS;

EID: 46049118283     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-12-1263     Document Type: Article

References (46)

1. Azmi, I., Davies, B., Dimaano, C., Payne, J., Eckert, D., Babst, M., and Katzmann, D. J. (2006). Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J. Cell Biol. 172, 705-717.
2. Azmi, I. F., Davies, B. A., Xiao, J., Babst, M., Xu, Z., and Katzmann, D. J. (2008). ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev. Cell 14, 50-61.
3. Babst, M. (2005). A protein's final ESCRT. Traffic 6, 2-9.
4. Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T., and Emr, S. D. (2002). Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell 3, 271-282.
5. Babst, M., Sato, T. K., Banta, L. M., and Emr, S. D. (1997). Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16, 1820-1831.
6. Babst, M., Wendland, B., Estepa, E. J., and Emr, S. D. (1998). The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993.
7. Bieniasz, P. D. (2006). Late budding domains and host proteins in enveloped virus release. Virology 344, 55-63.
8. Bishop, N., and Woodman, P. (2000). ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11, 227-239.
9. Carlton, J. G., and Martin-Serrano, J. (2007). Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912.
10. Demirov, D. G., and Freed, E. O. (2004). Retrovirus budding. Virus Res. 106, 87-102.
11. Dimaano, C., Jones, C. B., Hanono, A., Curtiss, M., and Babst, M. (2008). Ist1 regulates Vps4 localization and assembly. Mol. Biol. Cell 19, 465-474.
12. Fujita, H., Yamanaka, M., Imamura, K., Tanaka, Y., Nara, A., Yoshimori, T., Yokota, S., and Himeno, M. (2003). A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J. Cell Sci. 116, 401-414.
13. Fujita, H., Umezuki, Y., Imamura, K., Ishikawa, D., Uchimura, S., Nara, A., Yoshimori, T., Hayashizaki, Y., Kawai, J., Ishidoh, K., Tanaka, Y., and Himeno, M. (2004). Mammalian class E proteins, SBP1 and mVps2/CHMP2A, interact with and regulate the function of an AAA-ATPase SKD1/Vps4B. J. Cell Sci. 117, 2997-3009.
14. Gruenberg, J., and Stenmark, H. (2004). The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323.
15. 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.
16. Hartmann, C., Chami, M., Zachariae, U., de Groot, B. L., Engel, A., and Grutter, M. G. (2008). Vacuolar protein sorting: two different functional states of the AAA-ATPase Vps4p. J. Mol. Biol. 377, 352-363.
17. Howard, T. L., Stauffer, D. R., Degnin, C. R., and Hollenberg, S. M. (2001). CHMP1 functions as a member of a newly defined family of vesicle trafficking proteins. J. Cell Sci. 114, 2395-2404.
18. 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.
19. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002). Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905.
20. Kranz, A., Kinner, A., and Kolling, R. (2001). A family of small coiled-coil-forming proteins functioning at the late endosome in yeast. Mol. Biol. Cell 12, 711-723.
21. Lin, Y., Kimpler, L. A., Naismith, T. V., Lauer, J. M., and Hanson, P. I. (2005). Interaction of the mammalian endosomal sorting complex required for transport (ESCRT) III protein hSnf7-1 with itself, membranes, and the AAA+ ATPase SKD1. J. Biol. Chem. 280, 12799-12809.
22. Lottridge, J. M., Flannery, A. R., Vincelli, J. L., and Stevens, T. H. (2006). Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proc. Natl. Acad. Sci. USA 103, 6202-6207.
23. Ma, Y. M., Boucrot, E., Villen, J., el Affar, B., Gygi, S. P., Gottlinger, H. G., and Kirchhausen, T. (2007). Targeting of AMSH to endosomes is required for epidermal growth factor receptor degradation. J. Biol. Chem. 282, 9805-9812.
24. Morita, E., Sandrin, V., Chung, H. Y., Morham, S. G., Gygi, S. P., Rodesch, C. K., and Sundquist, W. I. (2007). Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215-4227.
25. Morita, E., and Sundquist, W. I. (2004). Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20, 395-425.
26. Muziol, T., Pineda-Molina, E., Ravelli, R. B., Zamborlini, A., Usami, Y., Gottlinger, H., and Weissenhorn, W. (2006). Structural basis for budding by the ESCRT-III factor CHMP3. Dev. Cell 10, 821-830.
27. Nickerson, D. P., West, M., and Odorizzi, G. (2006). Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J. Cell Biol. 175, 715-720.
28. Obita, T., Saksena, S., Ghazi-Tabatabai, S., Gill, D. J., Perisic, O., Emr, S. D., and Williams, R. L. (2007). Structural basis for selective recognition of ESCRTIII by the AAA ATPase Vps4. Nature 449, 735-739.
29. Piper, R. C., and Katzmann, D. J. (2007). Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519-547.
30. 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.
31. Rue, S. M., Mattei, S., Saksena, S., and Emr, S. D. (2007). Novel Ist1-Did2 Complex Functions at a Late Step in MVB Sorting. Mol. Biol. Cell 19, 475-484.
32. Saksena, S., Sun, J., Chu, T., and Emr, S. D. (2007). ESCRTing proteins in the endocytic pathway. Trends Biochem Sci. 32, 561-573.
33. Scott, A. et al. (2005a). Structural and mechanistic studies of VPS4 proteins. EMBO J. 24, 3658-3669.
34. Scott, A., Gaspar, J., Stuchell-Brereton, M. D., Alam, S. L., Skalicky, J. J., and Sundquist, W. I. (2005b). Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A. Proc. Natl. Acad. Sci. USA 102, 13813-13818.
35. Shiflett, S. L., Ward, D. M., Huynh, D., Vaughn, M. B., Simmons, J. C., and Kaplan, J. (2004). Characterization of Vta1p, a class E Vps protein in S. cerevisiae. J. Biol. Chem. 279, 10982-10990.
36. Shim, J. H. et al. (2006). CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J. Cell Biol. 172, 1045-1056.
37. Shim, S., Kimpler, L. A., and Hanson, P. I. (2007). Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8, 1068-1079.
38. Stuchell-Brereton, M. D., Skalicky, J. J., Kieffer, C., Karren, M. A., Ghaffarian, S., and Sundquist, W. I. (2007). ESCRT-III recognition by VPS4 ATPases. Nature 449, 740-744.
39. Vajjhala, P. R., Wong, J. S., To, H. Y., and Munn, A. L. (2006). The beta domain is required for Vps4p oligomerization into a functionally active ATPase. FEBS J. 273, 2357-2373.
40. von Schwedler, U. K. et al. (2003). The protein network of HIV budding. Cell 114, 701-713.
41. Ward, D. M., Vaughn, M. B., Shiflett, S. L., White, P. L., Pollock, A. L., Hill, J., Schnegelberger, R., Sundquist, W. I., and Kaplan, J. (2005). The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. J. Biol. Chem. 280, 10548-10555.
42. Williams, R. L., and Urbe, S. (2007). The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368.
43. Xiao, J., Xia, H., Yoshino-Koh, K., Zhou, J., and Xu, Z. (2007). Structural characterization of the ATPase reaction cycle of endosomal AAA protein Vps4. J. Mol. Biol. 374, 655-670.
44. Xiao, J., Xia, H., Zhou, J., Azmi, I. F., Davies, B. A., Katzmann, D. J., and Xu, Z. (2008). Structural basis of Vta1 function in the multivesicular body sorting pathway. Dev. Cell 14, 37-49.
45. Yeo, S. C. et al. (2003). Vps20p and Vta1p interact with Vps4p and function in multivesicular body sorting and endosomal transport in Saccharomyces cerevisiae. J. Cell Sci. 116, 3957-3970.
46. Yu, Z., Gonciarz, M. D., Sundquist, W. I., Hill, C. P., and Jensen, G. J. (2008). Cryo-EM structure of dodecameric Vps4p and Its21 complex with Vta1p. J. Mol. Biol. 377, 364-377.