Shaping development with ESCRTs

Nature Cell Biology

Volumn 14, Issue 1, 2012, Pages 38-45

  Rusten, Tor Erik ^a   Vaccari, Thomas ^b   Stenmark, Harald ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ESCRT 0 PROTEIN; ESCRT I PROTEIN; ESCRT II PROTEIN; ESCRT III PROTEIN; ESCRT PROTEIN; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; MICRORNA; NOTCH RECEPTOR; PROTEIN KINASE C; SONIC HEDGEHOG PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; UVOMORULIN; VERY LATE ACTIVATION ANTIGEN 5; WNT PROTEIN;

APOPTOSIS; AUTOPHAGOSOME; AUTOPHAGY; BIOGENESIS; CELL DIFFERENTIATION; CELL DIVISION; CELL INTERACTION; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CELL SELECTION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CYTOKINESIS; DEVELOPMENT; GENE SILENCING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UBIQUITINATION;

ANIMALS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MULTIVESICULAR BODIES; PROTEIN TRANSPORT;

EID: 84255195107     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2381     Document Type: Review

References (91)

1. 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).
2. 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).
3. 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). (Pubitemid 32772626)
4. 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).
5. Hurley, J. H. & Emr, S. D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Bioph. Biom. 35, 277-298 (2006). (Pubitemid 43877379)
6. Hurley, J. H. & Hanson, P. I. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11, 556-566 (2010).
7. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
8. Saksena, S., Sun, J., Chu, T. & Emr, S. D. ESCRTing proteins in the endocytic pathway. Trends Biochem. Sci. 32, 561-573 (2007). (Pubitemid 350123053)
9. Williams, R. L. & Urbe, S. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368 (2007). (Pubitemid 46643239)
10. Wollert, T. & Hurley, J. H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869 (2010).
11. Komander, D., Clague, M. J. & Urbe, S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563 (2009).
12. Wollert, T., Wunder, C., Lippincott-Schwartz, J. & Hurley, J. H. Membrane scission by the ESCRT-III complex. Nature 458, 172-177 (2009).
13. Babst, M., Wendland, B., Estepa, E. J. & Emr, S. D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993 (1998). (Pubitemid 28254371)
14. Lloyd, T. E. et al. Hrs regulates endosome invagination and receptor tyrosine kinase signaling in Drosophila. Cell 108, 261-269 (2002). (Pubitemid 34161145)
15. Jekely, G. & Rorth, P. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168 (2003). (Pubitemid 38088411)
16. Piddini, E., Marshall, F., Dubois, L., Hirst, E. & Vincent, J. P. Arrow (LRP6) and Frizzled2 cooperate to degrade Wingless in Drosophila imaginal discs. Development 132, 5479-5489 (2005). (Pubitemid 43125875)
17. Huang, H. R., Chen, Z. J., Kunes, S., Chang, G. D. & Maniatis, T. Endocytic pathway is required for Drosophila Toll innate immune signaling. Proc. Natl. Acad. Sci. USA 107, 8322-8327 (2010).
18. Chanut-Delalande, H. et al. The Hrs/Stam complex acts as a positive and negative regulator of RTK signaling during Drosophila development. PLoS. ONE. 5, e10245 (2010).
19. Thompson, B. J. et al. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720 (2005). (Pubitemid 41555152)
20. 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). (Pubitemid 41555151)
21. Herz, H. M. et al. vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 133, 1871-1880 (2006).
22. Rodahl, L. M. et al. Disruption of Vps4 and JNK function in Drosophila causes tumour growth. PLoS ONE. 4, e4354 (2009).
23. Bache, K. G. et al. The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523 (2006). (Pubitemid 43825490)
24. Malerød, L., Stuffers, S., Brech, A. & Stenmark, H. Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629 (2007). (Pubitemid 47578365)
25. Lobert, V. H. et al. Ubiquitination of α5β1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. Dev. Cell 19, 148-159 (2010).
26. 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). (Pubitemid 36760020)
27. Michelet, X. et al. The ESCRT-III protein CeVPS-32 is enriched in domains distinct from CeVPS-27 and CeVPS-23 at the endosomal membrane of epithelial cells. Biol. Cell 101, 599-615 (2009).
28. Audhya, A., McLeod, I. X., Yates, J. R. & Oegema, K. MVB-12, a fourth subunit of metazoan ESCRT-I, functions in receptor downregulation. PLoS ONE. 2, e956 (2007).
29. Vardhana, S., Choudhuri, K., Varma, R. & Dustin, M. L. Essential role of ubiquitin and TSG101 protein in formation and function of the central supramolecular activation cluster. Immunity. 32, 531-540 (2010).
30. Vaccari, T. & Bilder, D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698 (2005). (Pubitemid 41555150)
31. Taelman, V. F. et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 143, 1136-1148 (2010).
32. Mukai, A. et al. Balanced ubiquitylation and deubiquitylation of Frizzled regulate cellular responsiveness to Wg/Wnt. EMBO J. 29, 2114-2125 (2010).
33. Tu, C. et al. Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions. Proc. Natl. Acad. Sci. USA 107, 16107-16112 (2010).
34. Perez-Sala, D., Boya, P., Ramos, I., Herrera, M. & Stamatakis, K. The C-terminal sequence of RhoB directs protein degradation through an endo-lysosomal pathway. PLoS. ONE. 4, e8117 (2009).
35. Sevrioukov, E. A., Moghrabi, N., Kuhn, M. & Kramer, H. A mutation in dVps28 reveals a link between a subunit of the endosomal sorting complex required for transport-I complex and the actin cytoskeleton in Drosophila. Mol. Biol. Cell 16, 2301-2312 (2005). (Pubitemid 40632213)
36. Vaccari, T. et al. Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J. Cell Sci. 122, 2413-2423 (2009).
37. Komada, M. & Soriano, P. Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev. 13, 1475-1485 (1999). (Pubitemid 29270251)
38. Shim, J. H. et al. CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J. Cell Biol. 172, 1045-1056 (2006).
39. Yamada, M. et al. Loss of hippocampal CA3 pyramidal neurons in mice lacking STAM1. Mol. Cell Biol. 21, 3807-3819 (2001). (Pubitemid 32466992)
40. Yamada, M. et al. Signal-transducing adaptor molecules STAM1 and STAM2 are required for T-cell development and survival. Mol. Cell Biol. 22, 8648-8658 (2002). (Pubitemid 35397179)
41. Ruland, J. et al. p53 accumulation, defective cell proliferation, and early embryonic lethality in mice lacking tsg101. Proc. Natl. Acad. Sci. USA 98, 1859-1864 (2001). (Pubitemid 32165588)
42. Urwin, H. et al. Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations. Hum. Mol. Genet. 19, 2228-2238 (2010).
43. 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). (Pubitemid 47380392)
44. Gilbert, M. M., Robinson, B. S. & Moberg, K. H. Functional interactions between the erupted/tsg101 growth suppressor gene and the DaPKC and rbf1 genes in Drosophila imaginal disc tumors. PLoS. ONE. 4, e7039 (2009).
45. Buchanan, S. M., Schalm, S. S. & Maniatis, T. Proteolytic processing of protocadherin proteins requires endocytosis. Proc. Natl. Acad. Sci. USA 107, 17774-17779 (2010).
46. Auth, T. et al. The TSG101 protein binds to connexins and is involved in connexin degradation. Exp. Cell Res. 315, 1053-1062 (2009).
47. Leithe, E. et al. Ubiquitylation of the gap junction protein connexin-43 signals its trafficking from early endosomes to lysosomes in a process mediated by Hrs and Tsg101. J. Cell Sci. 122, 3883-3893 (2009).
48. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. & Horwitz, A. R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790 (2009).
49. Lobert, V. H. & Stenmark, H. The ESCRT machinery mediates polarization of fibroblasts through regulation of myosin light chain. J. Cell Sci. http://dx.doi.org/10.1242/jcs.088310 (in the press).
50. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008). (Pubitemid 351317450)
51. Berg, T. O., Fengsrud, M., Stromhaug, P. E., Berg, T. & Seglen, P. O. Isolation and characterization of rat liver amphisomes-Evidence for fusion of autophagosomes with both early and late endosomes. J. Biol. Chem. 273, 21883-21892 (1998). (Pubitemid 28405366)
52. Sahu, R. et al. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20, 131-139 (2011).
53. Rusten, T. E. & Stenmark, H. How do ESCRT proteins control autophagy? J. Cell Sci. 122, 2179-2183 (2009).
54. Roudier, N., Lefebvre, C. & Legouis, R. CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 6, 695-705 (2005). (Pubitemid 40959696)
55. Rusten, T. E. et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 17, 1817-1825 (2007). (Pubitemid 47576670)
56. 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). (Pubitemid 350074792)
57. 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). (Pubitemid 41149905)
58. Lee, J. A. & Gao, F. B. Inhibition of autophagy induction delays neuronal cell loss caused by dysfunctional ESCRT-III in frontotemporal dementia. J. Neurosci. 29, 8506-8511 (2009).
59. Denton, D. et al. Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. Biol. 19, 1741-1746 (2009).
60. Nezis, I. P. et al. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J. Cell Biol. 190, 523-531 (2010).
61. Morita, E. et al. Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc. Natl. Acad. Sci. USA 107, 12889-12894 (2010).
62. Carlton, J. G. & Martin-Serrano, J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912 (2007). (Pubitemid 47025792)
63. Fabbro, M. et al. Cdk1/Erk2-and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Dev. Cell 9, 477-488 (2005). (Pubitemid 41430731)
64. Bastos, R. N. & Barr, F. A. Plk1 negatively regulates Cep55 recruitment to the midbody to ensure orderly abscission. J. Cell Biol. 191, 751-760 (2010).
65. 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). (Pubitemid 47525161)
66. Elia, N., Sougrat, R., Spurlin, T. A., Hurley, J. H. & Lippincott-Schwartz, J. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc. Natl Acad. Sci. USA 108, 4846-4851 (2011).
67. Guizetti, J. et al. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 331, 1616-1620 (2011).
68. 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). (Pubitemid 32633697)
69. Sagona, A. P. et al. PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat. Cell Biol. 12, 362-371 (2010).
70. Spitzer, C. et al. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679-4689 (2006). (Pubitemid 46063080)
71. Gibbings, D. J., Ciaudo, C., Erhardt, M. & Voinnet, O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 11, 1143-1149 (2009).
72. Lee, Y. S. et al. Silencing by small RNAs is linked to endosomal trafficking. Nat. Cell Biol. 11, 1150-1156 (2009).
73. Irion, U. & St.Johnston D. bicoid RNA localisation requires specific binding of an endosomal sorting complex. Nature 445, 554-558 (2007). (Pubitemid 46197637)
74. 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).
75. Slagsvold, T. et al. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600-19606 (2005). (Pubitemid 41379482)
76. 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).
77. Samson, R. Y. et al. Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol. Cell 41, 186-196 (2011).
78. Lindas, A. C., Karlsson, E. A., Lindgren, M. T., Ettema, T. J. & Bernander, R. A unique cell division machinery in the Archaea. Proc. Natl. Acad. Sci. USA 105, 18942-18946 (2008).
79. Kantamneni, S. et al. GISP binding to TSG101 increases GABA(B) receptor stability by down-regulating ESCRT-mediated lysosomal degradation. J. Neurochem. 107, 86-95 (2008).
80. Bishop, N. & Woodman, P. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276, 11735-11742 (2001).
81. Bishop, N. & Woodman, P. ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11, 227-239 (2000). (Pubitemid 30075519)
82. Bache, K. G., Raiborg, C., Mehlum, A. & Stenmark, H. STAM and Hrs are subunits of a multivalent Ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521 (2003). (Pubitemid 36800240)
83. Babst, M., Odorizzi, G., Estepa, E. J. & Emr, S. D. Mammalian tumor suceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258 (2000).
84. 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). (Pubitemid 36988552)
85. Bache, K. G. et al. The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol. Biol. Cell 15, 4337-4346 (2004). (Pubitemid 39122034)
86. Malerod, L., Stuffers, S., Brech, A. & Stenmark, H. Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629 (2007). (Pubitemid 47578365)
87. Langelier, C. et al. Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J. Virol. 80, 9465-9480 (2006). (Pubitemid 44435625)
88. Tsunematsu, T. et al. Distinct functions of human MVB12A and MVB12B in the ESCRT-I dependent on their posttranslational modifications. Biochem. Biophys. Res. Commun. 399, 232-237 (2010).
89. Yorikawa, C. et al. Human CHMP6, a myristoylated ESCRT-III protein, interacts directly with an ESCRT-II component EAP20 and regulates endosomal cargo sorting. Biochem. J. 387, 17-26 (2005). (Pubitemid 40524070)
90. Seto, E. S. & Bellen, H. J. Internalization is required for proper Wingless signaling in Drosophila melanogaster. J. Cell Biol. 173, 95-106 (2006).
91. Martin-Serrano, J. & Neil, S. J. Host factors involved in retroviral budding and release. Nat. Rev. Microbiol. 9, 519-531 (2011).