ALIX binds a YPX 3L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting

Journal of Cell Biology

Volumn 197, Issue 3, 2012, Pages 407-419

  Dores, Michael R ^a   Chen, Buxin ^a   Lin, Huilan ^a   Soh, Unice J K ^a   Paing, May M ^c   Montagne, William A ^a   Meerloo, Timo ^b   Trejo, JoAnn ^a  

^a San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; PROTEIN; PROTEIN ALIX; PROTEINASE ACTIVATED RECEPTOR 1; SCATTER FACTOR; UBIQUITIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CALCIUM BINDING PROTEIN; CELL CYCLE PROTEIN; CHMP4A PROTEIN, HUMAN; CHMP4B PROTEIN, HUMAN; MESSENGER RNA; PDCD6IP PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SMALL INTERFERING RNA; VPS4A PROTEIN, HUMAN; VPS4B PROTEIN, HUMAN;

ARTICLE; HUMAN; HUMAN CELL; LYSOSOME; MULTIVESICULAR BODY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; DRUG ANTAGONISM; ENDOSOME; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HELA CELL; IMMUNOPRECIPITATION; METABOLISM; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; LYSOSOMES; MULTIVESICULAR BODIES; PROTEIN BINDING; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, PAR-1; RNA, MESSENGER; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITINATION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84862591663     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201110031     Document Type: Article

References (51)

1. Arora, P., T.K. Ricks, and J. Trejo. 2007. Protease-activated receptor signalling, endocytic sorting and dysregulation in cancer. J. Cell Sci. 120:921-928. http://dx.doi.org/10.1242/jcs.03409
2. Babst, M., B. Wendland, E.J. Estepa, and S.D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17:2982-2993. http://dx.doi.org/10.1093/emboj/17.11.2982
3. Bishop, N., and P. Woodman. 2000. ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell. 11:227-239.
4. Booden, M.A., L.B. Eckert, C.J. Der, and J. Trejo. 2004. Persistent signaling by dysregulated thrombin receptor trafficking promotes breast carcinoma cell invasion. Mol. Cell. Biol. 24:1990-1999. http://dx.doi.org/10.1128/MCB.24.5.1990-1999.2004
5. Cabezas, A., K.G. Bache, A. Brech, and H. Stenmark. 2005. Alix regulates cortical actin and the spatial distribution of endosomes. J. Cell Sci. 118:2625-2635. http://dx.doi.org/10.1242/jcs.02382
6. Carlton, J.G., M. Agromayor, and J. Martin-Serrano. 2008. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc. Natl. Acad. Sci. USA. 105:10541-10546. http://dx.doi.org/10.1073/pnas.0802008105
7. Coughlin, S.R. 2000. Thrombin signalling and protease-activated receptors. Nature. 407:258-264. http://dx.doi.org/10.1038/35025229
8. Fisher, R.D., H.-Y. Chung, Q. Zhai, H. Robinson, W.I. Sundquist, and C.P. Hill. 2007. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell. 128:841-852. http://dx.doi.org/10.1016/j.cell.2007.01.035
9. Garrus, J.E., U.K. von Schwedler, O.W. Pornillos, S.G. Morham, K.H. Zavitz, H.E. Wang, D.A. Wettstein, K.M. Stray, M. Côté, R.L. Rich, et al. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell. 107:55-65. http://dx.doi.org/10.1016/S0092-8674(01)00506-2
10. Géminard, C., A. De Gassart, L. Blanc, and M. Vidal. 2004. Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TFR for sorting into exosomes. Traffic. 5:181-193. http://dx.doi.org/10.1111/j.1600-0854.2004.0167.x
11. Gullapalli, A., B.L. Wolfe, C.T. Griffin, T. Magnuson, and J. Trejo. 2006. An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: Evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol. Biol. Cell. 17:1228-1238. http://dx.doi.org/10.1091/mbc.E05-09-0899
12. Hanyaloglu, A.C., and M. von Zastrow. 2008. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu. Rev. Pharmacol. Toxicol. 48:537-568. http://dx.doi.org/10.1146/annurev.pharmtox.48.113006.094830
13. Hasdemir, B., N.W. Bunnett, and G.S. Cottrell. 2007. Hepatocyte growth factorregulated tyrosine kinase substrate (HRS) mediates post-endocytic trafficking of protease-activated receptor 2 and calcitonin receptor-like receptor. J. Biol. Chem. 282:29646-29657. http://dx.doi.org/10.1074/jbc.M702974200
14. Henry, A.G., I.J. White, M. Marsh, M. von Zastrow, and J.N. Hislop. 2011. The role of ubiquitination in lysosomal trafficking of ?-opioid receptors. Traffic. 12:170-184. http://dx.doi.org/10.1111/j.1600-0854.2010.01145.x
15. Hislop, J.N., A. Marley, and M. Von Zastrow. 2004. Role of mammalian vacuolar protein-sorting proteins in endocytic trafficking of a non-ubiquitinated G protein-coupled receptor to lysosomes. J. Biol. Chem. 279:22522-22531. http://dx.doi.org/10.1074/jbc.M311062200
16. Hurley, J.H., and P.I. Hanson. 2010. Membrane budding and scission by the ESCRT machinery: It's all in the neck. Nat. Rev. Mol. Cell Biol. 11:556-566. http://dx.doi.org/10.1038/nrm2937
17. Kim, J., S. Sitaraman, A. Hierro, B.M. Beach, G. Odorizzi, and J.H. Hurley. 2005. Structural basis for endosomal targeting by the Bro1 domain. Dev. Cell. 8:937-947. http://dx.doi.org/10.1016/j.devcel.2005.04.001
18. Kyuuma, M., K. Kikuchi, K. Kojima, Y. Sugawara, M. Sato, N. Mano, J. Goto, T. Takeshita, A. Yamamoto, K. Sugamura, and N. Tanaka. 2007. AMSH, an ESCRT-III associated enzyme, deubiquitinates cargo on MVB/late endosomes. Cell Struct. Funct. 31:159-172. http://dx.doi.org/10.1247/csf.06023
19. Larkin, M.A., G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics. 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404
20. Lavoie, C., T. Meerloo, P. Lin, and M.G. Farquhar. 2002. Calnuc, an EF-hand Ca(2+)-binding protein, is stored and processed in the Golgi and secreted by the constitutive-like pathway in AtT20 cells. Mol. Endocrinol. 16:2462-2474. http://dx.doi.org/10.1210/me.2002-0079
21. Lu, Q., L.W. Hope, M. Brasch, C. Reinhard, and S.N. Cohen. 2003. TSG101 interaction with HRS mediates endosomal trafficking and receptor downregulation. Proc. Natl. Acad. Sci. USA. 100:7626-7631. http://dx.doi.org/10.1073/pnas.0932599100
22. Malerød, L., S. Stuffers, A. Brech, and H. Stenmark. 2007. Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic. 8:1617-1629. http://dx.doi.org/10.1111/j.1600-0854.2007.00630.x
23. Marchese, A., C. Raiborg, F. Santini, J.H. Keen, H. Stenmark, and J.L. Benovic. 2003. The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev. Cell. 5:709-722. http://dx.doi.org/10.1016/S1534-5807(03)00321-6
24. Marchese, A., M.M. Paing, B.R.S. Temple, and J. Trejo. 2008. G proteincoupled receptor sorting to endosomes and lysosomes. Annu. Rev. Pharmacol. Toxicol. 48:601-629. http://dx.doi.org/10.1146/annurev.pharmtox.48.113006.094646
25. Martin-Serrano, J., T. Zang, and P.D. Bieniasz. 2001. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7:1313-1319. http://dx.doi.org/10.1038/nm1201-1313
26. Martin-Serrano, J., A. Yarovoy, D. Perez-Caballero, and P.D. Bieniasz. 2003. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. USA. 100:12414-12419. http://dx.doi.org/10.1073/pnas.2133846100
27. McNatt, M.W., I. McKittrick, M. West, and G. Odorizzi. 2007. Direct binding to Rsp5 mediates ubiquitin-independent sorting of Sna3 via the multivesicular body pathway. Mol. Biol. Cell. 18:697-706. http://dx.doi.org/10.1091/mbc.E06-08-0663
28. Morita, E., V. Sandrin, H.-Y. Chung, S.G. Morham, S.P. Gygi, C.K. Rodesch, and W.I. Sundquist. 2007. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26:4215-4227. http://dx.doi.org/10.1038/sj.emboj.7601850
29. Odorizzi, G., D.J. Katzmann, M. Babst, A. Audhya, and S.D. Emr. 2003. Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae. J. Cell Sci. 116:1893-1903. http://dx.doi.org/10.1242/jcs.00395
30. Oestreich, A.J., M. Aboian, J. Lee, I. Azmi, J. Payne, R. Issaka, B.A. Davies, and D.J. Katzmann. 2007. Characterization of multiple multivesicular body sorting determinants within Sna3: A role for the ubiquitin ligase Rsp5. Mol. Biol. Cell. 18:707-720. http://dx.doi.org/10.1091/mbc.E06-08-0680
31. Paing, M.M., C.A. Johnston, D.P. Siderovski, and J. Trejo. 2006. Clathrin adaptor AP2 regulates thrombin receptor constitutive internalization and endothelial cell resensitization. Mol. Cell. Biol. 26:3231-3242. http://dx.doi.org/10.1128/MCB.26.8.3231-3242.2006
32. Ricks, T.K., and J. Trejo. 2009. Phosphorylation of protease-activated receptor-2 differentially regulates desensitization and internalization. J. Biol. Chem. 284:34444-34457. http://dx.doi.org/10.1074/jbc.M109.048942
33. Russo, A., U.J.K. Soh, M.M. Paing, P. Arora, and J. Trejo. 2009. Caveolae are required for protease-selective signaling by protease-activated receptor-1. Proc. Natl. Acad. Sci. USA. 106:6393-6397. http://dx.doi.org/10.1073/pnas.0810687106
34. Soto, A.G., and J. Trejo. 2010. N-linked glycosylation of protease-activated receptor-1 second extracellular loop: A critical determinant for ligandinduced receptor activation and internalization. J. Biol. Chem. 285: 18781-18793. http://dx.doi.org/10.1074/jbc.M110.111088
35. Strack, B., A. Calistri, S. Craig, E. Popova, and H.G. Göttlinger. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell. 114:689-699. http://dx.doi.org/10.1016/S0092-8674(03)00653-6
36. Tanzi, G.O., A.J. Piefer, and P. Bates. 2003. Equine infectious anemia virus utilizes host vesicular protein sorting machinery during particle release. J. Virol. 77:8440-8447. http://dx.doi.org/10.1128/JVI.77.15.8440-8447.2003
37. Theos, A.C., S.T. Truschel, D. Tenza, I. Hurbain, D.C. Harper, J.F. Berson, P.C. Thomas, G. Raposo, and M.S. Marks. 2006. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev. Cell. 10:343-354. http://dx.doi.org/10.1016/j.devcel.2006.01.012
38. Trajkovic, K., C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brügger, and M. Simons. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 319:1244-1247. http://dx.doi.org/10.1126/science.1153124
39. Trejo, J., and S.R. Coughlin. 1999. The cytoplasmic tails of proteaseactivated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J. Biol. Chem. 274:2216-2224. http://dx.doi.org/10.1074/jbc.274.4.2216
40. Trejo, J., S.R. Hammes, and S.R. Coughlin. 1998. Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc. Natl. Acad. Sci. USA. 95:13698-13702. http://dx.doi.org/10.1073/pnas.95.23.13698
41. Trejo, J., Y. Altschuler, H.-W. Fu, K.E. Mostov, and S.R. Coughlin. 2000. Protease-activated receptor-1 down-regulation: A mutant HeLa cell line suggests novel requirements for PAR1 phosphorylation and recruitment to clathrin-coated pits. J. Biol. Chem. 275:31255-31265. http://dx.doi.org/10.1074/jbc.M003770200
42. Usami, Y., S. Popov, and H.G. Göttlinger. 2007. Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81:6614-6622. http://dx.doi.org/10.1128/JVI.00314-07
43. van Niel, G., S. Charrin, S. Simoes, M. Romao, L. Rochin, P. Saftig, M.S. Marks, E. Rubinstein, and G. Raposo. 2011. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev. Cell. 21:708-721. http://dx.doi.org/10.1016/j.devcel.2011.08.019
44. Vroling, B., M. Sanders, C. Baakman, A. Borrmann, S. Verhoeven, J. Klomp, L. Oliveira, J. de Vlieg, and G. Vriend. 2011. GPCRDB: Information system for G protein-coupled receptors. Nucleic Acids Res. 39(Database issue):D309-D319. http://dx.doi.org/10.1093/nar/gkq1009
45. Vu, T.-K.H., D.T. Hung, V.I. Wheaton, and S.R. Coughlin. 1991. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 64:1057-1068. http://dx.doi.org/10.1016/0092-8674(91)90261-V
46. Watson, H., and J.S. Bonifacino. 2007. Direct binding to Rsp5p regulates ubiquitination-independent vacuolar transport of Sna3p. Mol. Biol. Cell. 18:1781-1789. http://dx.doi.org/10.1091/mbc.E06-10-0887
47. Wolfe, B.L., A. Marchese, and J. Trejo. 2007. Ubiquitination differentially regulates clathrin-dependent internalization of protease-activated receptor-1. J. Cell Biol. 177:905-916. http://dx.doi.org/10.1083/jcb.200610154
48. Wollert, T., and J.H. Hurley. 2010. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature. 464:864-869. http://dx.doi.org/10.1038/nature08849
49. Yi, X., R. Bouley, H.Y. Lin, S. Bechoua, T.X. Sun, E. Del Re, T. Shioda, M.K. Raychowdhury, H.A.J. Lu, A.B. Abou-Samra, et al. 2007. Alix (AIP1) is a vasopressin receptor (V2R)-interacting protein that increases lysosomal degradation of the V2R. Am. J. Physiol. Renal Physiol. 292:F1303- F1313. http://dx.doi.org/10.1152/ajprenal.00441.2005
50. Zhai, Q., R.D. Fisher, H.-Y. Chung, D.G. Myszka, W.I. Sundquist, and C.P. Hill. 2008. Structural and functional studies of ALIX interactions with YPX(n)L late domains of HIV-1 and EIAV. Nat. Struct. Mol. Biol. 15:43-49. http://dx.doi.org/10.1038/nsmb1319
51. Zhan, L., B. Liu, M. Jose-Lafuente, M.V. Chibalina, A. Grierson, A. Maclean, and J. Nasir. 2008. ALG-2 interacting protein AIP1: A novel link between D1 and D3 signalling. Eur. J. Neurosci. 27:1626-1633. http://dx.doi.org/10.1111/j.1460-9568.2008.06135.x