The role of ESCRT proteins in attenuation of cell signalling

Biochemical Society Transactions

Volumn 37, Issue 1, 2009, Pages 137-142

  Rodahl, Lina M ^a,b   Stuffers, Susanne ^a,b   Lobert, Viola H ^a,b   Stenmark, Harald ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Apoptosis; Endosomal sorting complex required for transport (ESCRT); Growth factor receptor; Notch; Tumour suppressor; Ubiquitin

Indexed keywords

ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT PROTEIN; GROWTH FACTOR RECEPTOR; MEMBRANE PROTEIN; NOTCH RECEPTOR; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; TUMOR SUPPRESSOR PROTEIN;

APOPTOSIS; CAENORHABDITIS ELEGANS; CANCER INHIBITION; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETON; DOWN REGULATION; DOWNSTREAM PROCESSING; DROSOPHILA MELANOGASTER; ENDOSOME; GENE ACTIVATION; LETHALITY; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION; ANIMAL; HUMAN; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS; ENDOSOMES; HUMANS; MULTIPROTEIN COMPLEXES; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 59749099629     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0370137     Document Type: Review

References (52)

1. Slagsvold, T., Pattni, K., Malerød, L. and Stenmark, H. (2006) Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol. 16, 317-326
2. Katzmann, D.J., Odorizzi, G. and Emr, S.D. (2002) Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 893-905
3. Katzmann, D.J., Stefan, C.J., Babst, M. and Emr, S.D. (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423
4. Bache, K.G., Brech, A., Mehlum, A. and Stenmark, H. (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442
5. Lu, Q., Hope, L.W., Brasch, M., Reinhard, C. and Cohen, S.N. (2003) TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc. Natl. Acad. Sci. U.S.A. 100, 7626-7631
6. Williams, R.L. and Urbé, S. (2007) The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368
7. von Zastrow, M. and Sorkin, A. (2007) Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 19, 436-445
8. Bache, K.G., Slagsvold, T. and Stenmark, H. (2004) Defective downregulation of receptor tyrosine kinases in cancer. EMBO J. 23, 2707-2712
9. Hurley, J.H. and Emr, S.D. (2006) Structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277-298
10. Raiborg, C., Bremnes, B., Mehlum, A., Gillooly, D.J., 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
11. Slagsvold, T., Aasland, R., Hirano, S., Bache, K.G., Raiborg, C., Trambaiolo, D., Wakatsuki, S. and Stenmark, H. (2005) Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600-19606
12. Teo, H., Gill, D.J., Sun, J., Perisic, O., Veprintsev, D.B., Vallis, Y., Emr, S.D. and Williams, R.L. (2006) 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
13. 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
14. Teo, H., Perisic, O., Gonzalez, B. and Williams, R.L. (2004) ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7, 559-569
15. Clague, M.J. and Urbé, S. (2006) Endocytosis: the DUB version. Trends Cell Biol. 16, 551-559
16. 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 ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-739
17. 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
18. Hariharan, I.K. and Bilder, D. (2006) Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Annu. Rev. Genet. 40, 335-361
19. Bache, K.G., Raiborg, C., Mehlum, A. and Stenmark, H. (2003) STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521
20. Bishop, N., Horman, A. and Woodman, P. (2002) Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J. Cell Biol. 157, 91-101
21. Babst, M., Odorizzi, G., Estepa, E.J. and Emr, S.D. (2000) Mammalian tumor suceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258
22. Bache, K.G., Stuffers, S., Maleröd, L., Slagsvold, T., Raiborg, C., Lechardeur, D., Wälchli, S., Lukacs, G., Brech, A. and Stenmark, H. (2006) The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523
23. Malerod, L., Stuffers, S., Brech, A. and Stenmark, H. (2007) Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629
24. Raiborg, C., Malerod, L., Pedersen, N.M. and Stenmark, H. (2008) Differential functions of Hrs and ESCRT proteins in endocytic membrane trafficking. Exp. Cell Res. 314, 801-813
25. Lloyd, T.E., Atkinson, R., Wu, M.N., Zhou, Y., Pennetta, G. and Bellen, H.J. (2002) Hrs regulates endosome invagination and receptor tyrosine kinase signaling in Drosophila. Cell 108, 261-269
26. Jekely, G. and Rorth, P. (2003) Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4, 1163-1168
27. Le, B.R. (2006) Regulation of Notch signalling by endocytosis and endosomal sorting. Curr. Opin. Cell Biol. 18, 213-222
28. Vaccari, T., Lu, H., Kanwar, R., Fortini, M.E. and Bilder, D. (2008) Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J. Cell Biol. 180, 755-762
29. Thompson, B.J., Mathieu, J., Sung, H.H., Loeser, E., Rorth, P. and Cohen, S.M. (2005) Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720
30. Moberg, K.H., Schelble, S., Burdick, S.K. and Hariharan, I.K. (2005) Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9, 699-710
31. Vaccari, T. and Bilder, D. (2005) The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698
32. Komada, M. and Soriano, P. (1999) 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
33. Ruland, J., Sirard, C., Elia, A., MacPherson, D., Wakeham, A., Li, L., de la Pompa, J.L., Cohen, S.N. and Mak, T.W. (2001) p53 accumulation, defective cell proliferation, and early embryonic lethality in mice lacking tsg101. Proc. Natl. Acad. Sci. U.S.A. 98, 1859-1864
34. Wagner, K.U., Krempler, A., Qi, Y., Park, K., Henry, M.D., Triplett, A.A., Riedlinger, G., Rucker, III, E.B. and Hennighausen, L. (2003) Tsg101 is essential for cell growth, proliferation, and cell survival of embryonic and adult tissues. Mol. Cell. Biol. 23, 150-162
35. Herz, H.M., Chen, Z., Scherr, H., Lackey, M., Bolduc, C. and Bergmann, A. (2006) vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 133, 1871-1880
36. Odorizzi, G. (2006) The multiple personalities of Alix. J. Cell Sci. 119, 3025-3032
37. Mahul-Mellier, A.L., Hemming, F.J., Blot, B., Fraboulet, S. and Sadoul, R. (2006) Alix, making a link between apoptosis-linked gene-2, the endosomal sorting complexes required for transport, and neuronal death in vivo. J. Neurosci. 26, 542-549
38. Sevrioukov, E.A., Moghrabi, N., Kuhn, M. and Kramer, H. (2005) 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
39. 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
40. Scoles, D.R., Huynh, D.P., Chen, M.S., Burke, S.P., Gutmann, D.H. and Pulst, S.-M. (2000) The neurofibromatosis 2 tumor suppressor protein interacts with hepatocyte growth factor-regulated tyrosine kinase substrate. Hum. Mol. Genet. 9, 1567-1574
41. Yan, Q., Sun, W., Kujala, P., Lotfi, Y., Vida, T.A. and Bean, A.J. (2005) CART: an Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol. Biol. Cell 16, 2470-2482
42. Li, L. and Cohen, S.N. (1996) Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85, 319-329
43. Oh, K.B., Stanton, M.J., West, W.W., Todd, G.L. and Wagner, K.U. (2007) Tsg101 is upregulated in a subset of invasive human breast cancers and its targeted overexpression in transgenic mice reveals weak oncogenic properties for mammary cancer initiation. Oncogene 26, 5950-5959
44. Tanaka, N., Kyuuma, M. and Sugamura, K. (2008) Endosomal sorting complex required for transport proteins in cancer pathogenesis, vesicular transport, and non-endosomal functions. Cancer Sci. 99, 1293-1303
45. Bache, K.G., Slagsvold, T., Cabezas, A., Rosendal, K.R., Raiborg, C. and Stenmark, H. (2004) The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol. Biol. Cell 15, 4337-4346
46. Xu, Z., Liang, L., Wang, H., Li, T. and Zhao, M. (2003) HCRP1, a novel gene that is downregulated in hepatocellular carcinoma, encodes a growth-inhibitory protein. Biochem. Biophys. Res. Commun. 311, 1057-1066
47. Rusten, T.E., Vaccari, T., Lindmo, K., Rodahl, L.M., Nezis, I.P., Sem-Jacobsen, C., Wendler, F., Vincent, J.P., Brech, A., Bilder, D. and Stenmark, H. (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 17, 1817-1825
48. Raiborg, C., Bache, K.G., Mehlum, A. and Stenmark, H. (2001) Function of Hrs in endocytic trafficking and signalling. Biochem. Soc. Trans. 29, 472-475
49. Hanyaloglu, A.C., McCullagh, E. and von Zastrow, M. (2005) Essential role of Hrs in a recycling mechanism mediating functional resensitization of cell signaling. EMBO J. 24, 2265-2283
50. Raiborg, C., Rusten, T.E. and Stenmark, H. (2003) Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455
51. Kirkin, V. and Dikic, I. (2007) Role of ubiquitin- and Ubl-binding proteins in cell signaling. Curr. Opin. Cell Biol. 19, 199-205
52. Hammond, D.E., Carter, S., McCullough, J., Urbé, S., Vande Woude, G. and Clague, M.J. (2003) Endosomal dynamics of met determine signaling output. Mol. Biol. Cell 14, 1346-1354