The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins (original) (raw)

• Gruenberg, J. & Stenmark, H. The biogenesis of multivesicular endosomes. Nature Rev. Mol. Cell Biol. 5, 317–323 (2004).
  Article CAS Google Scholar
• Katzmann, D. J., Odorizzi, G. & Emr, S. D. Receptor downregulation and multivesicular-body sorting. Nature Rev. Mol. Cell Biol. 3, 893–905 (2002).
  Article CAS Google Scholar
• d'Azzo, A., Bongiovanni, A. & Nastasi, T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 6, 429–441 (2005).
  Article CAS PubMed Google Scholar
• Hicke, L. & Dunn, R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141–172 (2003).
  Article CAS PubMed Google Scholar
• Hicke, L. & Riezman, H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84, 277–287 (1996).
  Article CAS PubMed Google Scholar
• Galan, J. M., Moreau, V., Andre, B., Volland, C. & Haguenauer-Tsapis, R. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271, 10946–10952 (1996).
  Article CAS PubMed Google Scholar
• Babst, M., Katzmann, D. J., Snyder, W. B., Wendland, B. & Emr, S. D. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3, 283–289 (2002). This paper describes the first biochemical and functional characterization of ESCRT-II.
  Article CAS PubMed Google Scholar
• Babst, M., Katzmann, D. J., Estepa-Sabal, E. J., Meerloo, T. & Emr, S. D. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell 3, 271–282 (2002). This is the first biochemical and functional characterization of ESCRT-III, and identification of Vps20–Vps32 and Vps24–Vps2 as subcomplexes of ESCRT-III.
  Article CAS PubMed Google Scholar
• Katzmann, D. J., Babst, M. & Emr, S. D. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145–155 (2001). This paper coins the ESCRT name and provides the concept of an endosomal machinery that sorts ubiquitylated cargo into MVEs. It describes the first biochemical and functional characterization of ESCRT-I.
  Article CAS PubMed Google Scholar
• Bache, K. G., Brech, A., Mehlum, A. & Stenmark, H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435–442 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Katzmann, D. J., Stefan, C. J., Babst, M. & Emr, S. D. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413–423 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Lu, Q., Hope, L. W., Brasch, M., Reinhard, C. & Cohen, S. N. TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc. Natl Acad. Sci. USA 100, 7626–7631 (2003).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Hurley, J. H. ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20, 4–11 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Williams, R. L. & Urbe, S. The emerging shape of the ESCRT machinery. Nature Rev. Mol. Cell Biol. 8, 355–368 (2007).
  Article CAS Google Scholar
• Prag, G. et al. The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev. Cell 12, 973–986 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hofmann, K. & Falquet, L. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26, 347–350 (2001).
  Article CAS PubMed Google Scholar
• Raiborg, C., Bache, K. G., Mehlum, A., Stang, E. & Stenmark, H. Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008–5021 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• McCullough, J. et al. Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Curr. Biol. 16, 160–165 (2006).
  Article CAS PubMed Google Scholar
• Gaullier, J.-M. et al. FYVE fingers bind PtdIns(3)P. Nature 394, 432–433 (1998).
  Article ADS CAS PubMed Google Scholar
• Burd, C. G. & Emr, S. D. Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domain. Mol. Cell 2, 157–162 (1998).
  Article CAS PubMed Google Scholar
• Raiborg, C. et al. FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J. Cell Sci. 114, 2255–2263 (2001).
  Article CAS PubMed Google Scholar
• Roxrud, I., Raiborg, C., Pedersen, N. M., Stang, E. & Stenmark, H. An endosomally localized isoform of Eps15 interacts with Hrs to mediate degradation of epidermal growth factor receptor. J. Cell Biol. 180, 1205–1218 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Leung, K. F., Dacks, J. B. & Field, M. C. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9, 1698–1716 (2008).
  Article CAS PubMed Google Scholar
• Puertollano, R. & Bonifacino, J. S. Interactions of GGA3 with the ubiquitin sorting machinery. Nature Cell Biol. 6, 244–251 (2004).
  Article CAS PubMed Google Scholar
• Puertollano, R. Interactions of TOM1L1 with the multivesicular body sorting machinery. J. Biol. Chem. 280, 9258–9264 (2005).
  Article CAS PubMed Google Scholar
• Seet, L. F., Liu, N., Hanson, B. J. & Hong, W. Endofin recruits TOM1 to endosomes. J. Biol. Chem. 279, 4670–4679 (2004).
  Article CAS PubMed Google Scholar
• Stuchell, M.D. et al. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J. Biol. Chem. 279, 36059–36071 (2004).
  Article CAS PubMed Google Scholar
• Kostelansky, M. S. et al. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129, 485–498 (2007). By combining data from several crystallographic studies, this paper describes a model of almost the whole ESCRT-I from yeast.
  Article CAS PubMed PubMed Central Google Scholar
• Morita, E. et al. Identification of human MVB12 proteins as ESCRT-I subunits that function in HIV budding. Cell Host Microbe 2, 41–53 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Chu, T., Sun, J., Saksena, S. & Emr, S. D. New component of ESCRT-I regulates endosomal sorting complex assembly. J. Cell Biol. 175, 815–823 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Im, Y. J. & Hurley, J. H. Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev. Cell 14, 902–913 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Hierro, A. et al. Structure of the ESCRT-II endosomal trafficking complex. Nature 431, 221–225 (2004). This is the first determination of the core of yeast ESCRT-II, showing that the core consists of eight winged-helix domains and that ESCRT-II consists of one Vps22, one Vps36 and two copies of Vps25.
  Article ADS CAS PubMed Google Scholar
• Teo, H., Perisic, O., Gonzalez, B. & Williams, R. L. ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7, 559–569 (2004).
  Article CAS PubMed Google Scholar
• Slagsvold, T. et al. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600–19606 (2005).
  Article CAS PubMed Google Scholar
• Hirano, S. et al. Structural basis of ubiquitin recognition by mammalian Eap45 GLUE domain. Nature Struct. Mol. Biol. 13, 1031–1032 (2006).
  Article CAS Google Scholar
• Alam, S. L. et al. Structural basis for ubiquitin recognition by the human ESCRT-II EAP45 GLUE domain. Nature Struct. Mol. Biol. 13, 1029–1030 (2006).
  Article CAS Google Scholar
• Teo, H. et al. ESCRT-I core and ESCRT-II GLUE domain structures reveal central role for GLUE domain in linking to ESCRT-I and membranes. Cell 125, 99–111 (2006). This paper shows that the GLUE domain of yeast Vps36 binds Vps28 in ESCRT-I and ubiquitin via yeast-specific NZF zinc fingers, and that another face of the GLUE domain binds the endosomal lipid PtdIns(3)P.
  Article CAS PubMed Google Scholar
• Lata, S. et al. Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378, 816–825 (2008).
  Article CAS Google Scholar
• Teis, D., Saksena, S. & Emr, S. D. Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev. Cell 15, 578–589 (2008). On the basis of biochemical studies of intact yeast cells, this paper provides a model for the ordered assembly of ESCRT-III on membranes.
  Article CAS PubMed Google Scholar
• Saksena, S., Wahlman, J., Teis, D., Johnson, A. E. & Emr, S. D. Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97–109 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rue, S. M., Mattei, S., Saksena, S. & Emr, S. D. Novel Ist1–Did2 complex functions at a late step in multivesicular body sorting. Mol. Biol. Cell 19, 475–484 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Raiborg, C. et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nature Cell Biol. 4, 394–398 (2002). This paper shows that Hrs functions in degradative endosomal sorting of ubiquitylated membrane proteins, and that ESCRT-0 is concentrated in restricted microdomains of the endosome membrane.
  Article CAS PubMed Google Scholar
• Hirano, S. et al. Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Nature Struct. Mol. Biol. 13, 272–277 (2006).
  Article CAS Google Scholar
• Fisher, R. D. et al. Structure and ubiquitin binding of the ubiquitin-interacting motif. J. Biol. Chem. 278, 28976–28984 (2003).
  Article CAS PubMed Google Scholar
• Haglund, K. et al. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nature Cell Biol. 5, 461–466 (2003).
  Article CAS PubMed Google Scholar
• Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S. & Sorkin, A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737–748 (2006).
  Article CAS PubMed Google Scholar
• Umebayashi, K., Stenmark, H. & Yoshimori, T. Ubc4/5 and c-Cbl continue to ubiquitinate EGF receptor after internalization to facilitate polyubiquitination and degradation. Mol. Biol. Cell 19, 3454–3462 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C. & Piper, R. C. The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nature Cell Biol. 4, 534–539 (2002).
  Article CAS PubMed Google Scholar
• Raiborg, C., Wesche, J., Malerød, L. & Stenmark, H. Flat clathrin coats on endosomes mediate degradative protein sorting by scaffolding Hrs in dynamic microdomains. J. Cell Sci. 119, 2414–2424 (2006).
  Article CAS PubMed Google Scholar
• Sachse, M., Urbe, S., Oorschot, V., Strous, G. J. & Klumperman, J. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol. Biol. Cell 13, 1313–1328 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Komada, M. & Kitamura, N. Growth factor-induced tyrosine phosphorylation of Hrs, a novel 115-kilodalton protein with a structurally conserved putative zinc finger domain. Mol. Cell. Biol. 15, 6213–6221 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Takeshita, T. et al. Cloning of a novel signal-transducing adaptor molecule containing an SH3 domain and ITAM. Biochem. Biophys. Res. Commun. 225, 1035–1039 (1996).
  Article CAS PubMed Google Scholar
• Polo, S. et al. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416, 451–455 (2002).
  Article ADS CAS PubMed Google Scholar
• Hoeller, D. et al. Regulation of ubiquitin-binding proteins by monoubiquitination. Nature Cell Biol. 8, 163–169 (2006).
  Article CAS PubMed Google Scholar
• Kim, B. Y., Olzmann, J. A., Barsh, G. S., Chin, L. S. & Li, L. Spongiform neurodegeneration-associated E3 ligase mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell 18, 1129–1142 (2007).
  Article PubMed PubMed Central Google Scholar
• Doyotte, A., Russell, M. R., Hopkins, C. R. & Woodman, P. G. Depletion of TSG101 forms a mammalian “Class E” compartment: a multicisternal early endosome with multiple sorting defects. J. Cell Sci. 118, 3003–3017 (2005).
  Article CAS PubMed Google Scholar
• Conner, S. D. & Schmid, S. L. Regulated portals of entry into the cell. Nature 422, 37–44 (2003).
  Article ADS CAS PubMed Google Scholar
• Hanson, P. I., Roth, R., Lin, Y. & Heuser, J. E. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389–402 (2008). By using deep-etch electron microscopy of the plasma membrane of cells overexpressing ESCRT subunits, this paper provides spectacular images suggesting that membrane deformation is driven by circular arrays of Vps32 multimers.
  Article CAS PubMed PubMed Central Google Scholar
• Lata, S. et al. Helical structures of ESCRT-III are disassembled by VPS4. Science 321, 1354–1357 (2008).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Ghazi-Tabatabai, S. et al. Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure 16, 1345–1356 (2008).
  Article CAS PubMed Google Scholar
• Pons, V. et al. Hrs and SNX3 functions in sorting and membrane invagination within multivesicular bodies. PLoS Biol. 6, e214 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Obita, T. et al. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735–739 (2007).
  Article ADS CAS PubMed Google Scholar
• Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L. & Bell, S. D. A role for the ESCRT system in cell division in Archaea. Science 322, 1710–1713, (2008). This paper shows that ESCRT-III and Vps4 function in cell division in the archaebacterium Sulfolobus acidocaldarius.
  Article ADS CAS PubMed PubMed Central Google Scholar
• Spitzer, C. et al. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679–4689 (2006). This is the first demonstration that ESCRT proteins are involved in cytokinesis.
  Article CAS PubMed Google Scholar
• Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908–1912 (2007). This paper provides the first demonstration that ESCRT proteins are involved in mammalian cytokinesis and identifies CEP55 as a key recruiter of ESCRTs to the midbody.
  Article ADS CAS PubMed Google Scholar
• Morita, E. et al. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215–4227 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Pineda-Molina, E. et al. The crystal structure of the C-terminal domain of Vps28 reveals a conserved surface required for Vps20 recruitment. Traffic 7, 1007–1016 (2006).
  Article CAS PubMed Google Scholar
• Martin-Serrano, J. The role of ubiquitin in retroviral egress. Traffic 8, 1297–1303 (2007).
  Article CAS PubMed Google Scholar
• Morita, E. & Sundquist, W. I. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20, 395–425 (2004).
  Article CAS PubMed Google Scholar
• Langelier, C. et al. Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J. Virol. 80, 9465–9480 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Bowers, K. et al. Degradation of endocytosed epidermal growth factor and virally-ubiquitinated MHC class I is independent of mammalian ESCRTII. J. Biol. Chem. 81, 5094–5105 (2005).
  Google Scholar
• von Schwedler, U. K. et al. The protein network of HIV budding. Cell 114, 701–713 (2003).
  Article CAS PubMed Google Scholar
• McCullough, J., Fisher, R. D., Whitby, F. G., Sundquist, W. I. & Hill, C. P. ALIX–CHMP4 interactions in the human ESCRT pathway. Proc. Natl Acad. Sci. USA 105, 7687–7691 (2008).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Amerik, A. Y., Nowak, J., Swaminathan, S. & Hochstrasser, M. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11, 3365–3380 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Swaminathan, S., Amerik, A. Y. & Hochstrasser, M. The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell 10, 2583–2594 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Nikko, E. & Andre, B. Evidence for a direct role of the Doa4 deubiquitinating enzyme in protein sorting into the MVB pathway. Traffic 8, 566–581 (2007).
  Article CAS PubMed Google Scholar
• Row, P. E., Prior, I. A., McCullough, J., Clague, M. J. & Urbe, S. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281, 12618–12624 (2006).
  Article CAS PubMed Google Scholar
• Mizuno, E., Kobayashi, K., Yamamoto, A., Kitamura, N. & Komada, M. A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic 7, 1017–1031 (2006).
  Article CAS PubMed Google Scholar
• Komatsu, M. et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880–884 (2006).
  Article ADS CAS PubMed Google Scholar
• Ravikumar, B. et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nature Genet. 36, 585–595 (2004).
  Article CAS PubMed Google Scholar
• Nixon, R. A. & Cataldo, A. M. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J. Alzheimers Dis. 9, 277–289 (2006).
  Article CAS PubMed Google Scholar
• Bjørkøy, G. et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603–614 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131–24145 (2007).
  Article CAS PubMed Google Scholar
• Filimonenko, M. et al. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179, 485–500 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Rusten, T. E., Filimonenko, M., Rodahl, L. M., Stenmark, H. & Simonsen, A. ESCRTing autophagic clearance of aggregating proteins. Autophagy 4, 233–236 (2008).
  Article CAS Google Scholar
• Lee, J. A., Beigneux, A., Ahmad, S. T., Young, S. G. & Gao, F. B. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17, 1561–1567 (2007).
  Article CAS PubMed Google Scholar
• Kim, B. Y. & Akazawa, C. Endosomal trafficking of EGFR regulated by hVps18 via interaction of MVB sorting machinery. Biochem. Biophys. Res. Commun. Advance online publication doi:10.1016/j.bbrc.2007.08.046 (2007).
• Parkinson, N. et al. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67, 1074–1077 (2006).
  Article CAS PubMed Google Scholar
• Skibinski, G. et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nature Genet. 37, 806–808 (2005).
  Article CAS PubMed Google Scholar
• Li, L. & Cohen, S. N. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85, 319–329 (1996).
  Article CAS PubMed Google Scholar
• Xu, Z., Liang, L., Wang, H., Li, T. & Zhao, M. HCRP1, a novel gene that is downregulated in hepatocellular carcinoma, encodes a growth-inhibitory protein. Biochem. Biophys. Res. Commun. 311, 1057–1066 (2003).
  Article CAS PubMed Google Scholar
• Li, J., Belogortseva, N., Porter, D. & Park, M. Chmp1A functions as a novel tumor suppressor gene in human embryonic kidney and ductal pancreatic tumor cells. Cell Cycle 7, 2886–2893 (2008).
  Article CAS PubMed Google Scholar
• Krempler, A., Henry, M. D., Triplett, A. A. & Wagner, K. U. Targeted deletion of the Tsg101 gene results in cell cycle arrest at G1/S and p53-independent cell death. J. Biol. Chem. 277, 43216–43223 (2002).
  Article CAS PubMed Google Scholar
• Vaccari, T. & Bilder, D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating Notch trafficking. Dev. Cell 9, 687–698 (2005).
  Article CAS PubMed Google Scholar
• Thompson, B. J. et al. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila . Dev. Cell 9, 711–720 (2005).
  Article CAS PubMed Google Scholar
• Moberg, K. H., Schelble, S., Burdick, S. K. & Hariharan, I. K. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699–710 (2005).
  Article CAS PubMed Google Scholar
• Philips, J. A., Porto, M. C., Wang, H., Rubin, E. J. & Perrimon, N. ESCRT factors restrict mycobacterial growth. Proc. Natl Acad. Sci. USA 105, 3070–3075 (2008).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Vieira, O. V. et al. Acquisition of Hrs, an essential component of phagosomal maturation, is impaired by mycobacteria. Mol. Cell. Biol. 24, 4593–4604 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Singh, S. B., Davis, A. S., Taylor, G. A. & Deretic, V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313, 1438–1441 (2006).
  Article ADS CAS PubMed Google Scholar
• Wollert, T., Wunder, C., Lippincott-Schwartz, J. & Hurley, J. H. Membrane scission by the ESCRT-III complex. Nature 458, 159–160 (2009)
  Article CAS Google Scholar