Proline-rich regions and motifs in trafficking: From ESCRT interaction to viral exploitation

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Volumn 12, Issue 10, 2011, Pages 1282-1290

  Ren, Xuefeng ^a   Hurley, James H ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

ALG 2; ALIX; CEP55; Cytokinesis; Endosome; Protein structure; TSG101; UEV domain; Virus budding; WW domain

Indexed keywords

ESCRT PROTEIN; PROLINE RICH PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AUTOREGULATION; CRYSTAL STRUCTURE; CYTOKINESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; REVIEW;

AMINO ACID SEQUENCE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROLINE-RICH PROTEIN DOMAINS; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; VIRAL PROTEINS; VIRUS RELEASE;

EID: 80052626414     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01208.x     Document Type: Review

References (74)

1. Morita E, Sundquist WI. Retrovirus budding. Annu Rev Cell Dev Biol 2004;20:395-425.
2. Fujii K, Hurley JH, Freed EO. Beyond Tsg101: the role of Alix in 'ESCRTing' HIV-1. Nat Rev Microbiol 2007;5:912-916.
3. Chen BJ, Lamb RA. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 2008;372:221-232.
4. Usami Y, Popov S, Popova E, Inoue M, Weissenhorn W, Gottlinger HG. The ESCRT pathway and HIV-1 budding. Biochem Soc Trans 2009;37:181-184.
5. Bieniasz PD. The cell biology of HIV-1 virion genesis. Cell Host Microbe 2009;5:550-558.
6. Carlton JG, Martin-Serrano J. The ESCRT machinery: new functions in viral and cellular biology. Biochem Soc Trans 2009;37:195-199.
7. Hurley JH, Hanson PI. Membrane budding and scission by the ESCRT complexes: it's all in the neck. Nat Rev Mol Cell Biol 2010;11:556-566.
8. Freed EO. Viral late domains. J Virol 2002;76:4679-4687.
9. Williamson MP. The structure and function of proline-rich regions in proteins. Biochem J 1994;297:249-260.
10. Odorizzi G. The multiple personalities of Alix. J Cell Sci 2006;119:3025-3032.
11. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 2003;114:689-699.
12. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He GP, Cimbora DM, Scott A, Krausslich HG, Kaplan J, Morham SG, Sundquist WI. The protein network of HIV budding. Cell 2003;114:701-713.
13. Martin-Serrano J, Yaravoy A, Perez-Caballero D, Bieniasz PD. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci U S A 2003;100:12414-12419.
14. Chen B, Borinstein SC, Gillis J, Sykes VW, Bogler O. The glioma-associated protein SETA interacts with AIP1/Alix and AZIG-2 and modulates apoptosis in astrocytes. J Biol Chem 2000;275:19275-19281.
15. Usami Y, Popov S, Gottlinger HG. Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J Virol 2007;81:6614-6622.
16. Jozic D, Cardenes N, Deribe YL, Moncalian G, Hoeller D, Groemping Y, Dikic I, Rittinger K, Bravo J. Cbl promotes clustering of endocytic adaptor proteins. Nat Struct Mol Biol 2005;12:972-979.
17. Schmidt MHH, Dikic I, Bogler O. Src phosphorylation of Alix/AIP1 modulates its interaction with binding partners and antagonizes its activities. J Biol Chem 2005;280:3414-3425.
18. Dejournett RE, Kobayashi R, Pan S, Wu C, Etkin LD, Clark RB, Bogler O, Kuang J. Phosphorylation of the proline-rich domain of Xp95 modulates Xp95 interaction with partner proteins. Biochem J 2007;401:521-531.
19. Shi XL, Opi S, Lugari A, Restouin A, Coursindel T, Parrot I, Perez J, Madore E, Zimmermann P, Corbeil J, Huang MD, Arold ST, Collette Y, Morelli X. Identification and biophysical assessment of the molecular recognition mechanisms between the human haemopoietic cell kinase Src homology domain 3 and ALG-2-interacting protein X. Biochem J 2010;431:93-102.
20. Chatellard-Causse C, Blot B, Cristina N, Torch S, Missotten M, Sadoul R. Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J Biol Chem 2002;277:29108-29115.
21. Tsuda M, Seong KH, Aigaki T. POSH, a scaffold protein for JNK signaling, binds to ALG-2 and ALIX in Drosophila. FEBS Lett 2006;580:3296-3300.
22. Carlton JG, Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 2007;316:1908-1912.
23. Morita E, Sandrin V, Chung HY, Morham SG, Gygi S, Rodesch CK, Sundquist WI. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 2007;26:4215-4227.
24. Guizetti J, Schermelleh L, Mäntler J, Maar S, Poser I, Leonhardt H, Müller-Reichert T, Gerlich DW. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 2011;331:1616-1620.
25. Elia N, Sougrat R, Spurlin T, Hurley JH, Lippincott-Schwartz J. Dynamics of ESCRT machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A 2011;108:4846-4851.
26. Suzuki H, Kawasaki M, Inuzuka T, Okumura M, Kakiuchi T, Shibata H, Wakatsuki S, Maki M. Structural basis for Ca2+-dependent formation of ALG-2/Alix peptide complex: Ca2+/EF3-driven arginine switch mechanism. Structure 2008;16:1562-1573.
27. Nikko E, Andre B. Split-ubiquitin two-hybrid assay to analyze protein-protein interactions at the endosome: application to Saccharomyces cerevisiae Bro1 interacting with ESCRT complexes, the Doa4 ubiquitin hydrolase, and the Rsp5 ubiquitin ligase. Eukaryot Cell 2007;6:1266-1277.
28. Sette P, Jadwin JA, Dussupt V, Bello NF, Bouamr F. The ESCRT-associated protein Alix recruits the ubiquitin ligase Nedd4-1 to facilitate HIV-1 release through the LYPXnL L domain motif. J Virol 2010;84:8181-8192.
29. Munshi UM, Kim J, Nagashima K, Hurley JH, Freed EO. An Alix fragment potently inhibits HIV-1 budding - characterization of binding to retroviral YPXL late domains. J Biol Chem 2007;282:3847-3855.
30. Pires R, Hartlieb B, Signor L, Schoehn G, Lata S, Roessle M, Moriscot C, Popov S, Hinz A, Jamin M, Boyer V, Sadoul R, Forest E, Svergun DI, Gottlinger HG et al. A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments. Structure 2009;17:843-856.
31. Carlton JG, Agromayor M, Martin-Serrano J. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci U S A 2008;105:10541-10546.
32. Zhou X, Si J, Corvera J, Gallick GE, Kuang J. Decoding the intrinsic mechanism that prohibits ALIX interaction with ESCRT and viral proteins. Biochem J 2010;432:525-534.
33. Zhou X, Pan S, Sun L, Corvera J, Lin SH, Kuang J. The HIV-1 p6/EIAV p9 docking site in ALIX is autoinhibited as revealed by a conformation-sensitive anti-ALIX monoclonal antibody. Biochem J 2008;414:215-220.
34. Pan S, Wang R, Zhou X, He G, Koomen J, Kobayashi R, Sun L, Corvera J, Gallick GE, Kuang J. Involvement of the adaptor protein alix in actin cytoskeleton assembly. J Biol Chem 2006;281:34640-34650.
35. Kim J, Sitaraman S, Hierro A, Beach BM, Odorizzi G, Hurley JH. Structural basis for endosomal targeting by the Bro1 domain. Dev Cell 2005;8:937-947.
36. Fisher RD, Chung HY, Zhai Q, Robinson H, Sundquist WI, Hill CP. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 2007;128:841-852.
37. Katzmann DJ, Babst M, Emr SD. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 2001;106:145-155.
38. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, Myszka DG, Sundquist WI. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 2001;107:55-65.
39. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci U S A 2001;98:7724-7729.
40. Demirov DG, Ono A, Orenstein JM, Freed EO. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc Natl Acad Sci U S A 2002;99:955-960.
41. Martin-Serrano J, Zang T, Bieniasz PD. HIV-I and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat Med 2001;7:1313-1319.
42. Kostelansky MS, Schluter C, Tam YYC, Lee S, Ghirlando R, Beach B, Conibear E, Hurley JH. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 2007;129:485-498.
43. Lee HH, Elia N, Ghirlando R, Lippincott-Schwartz J, Hurley JH. Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 2008;322:576-580.
44. Bache KG, Brech A, Mehlum A, Stenmark H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 2003;162:435-442.
45. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He GP, Wang HE, Morham SG, Sundquist WI. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 2003;162:425-434.
46. Lu Q, Hope LWQ, Brasch M, Reinhard C, Cohen SN. TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc Natl Acad Sci U S A 2003;100:7626-7631.
47. Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, McKinnon R, Krausslich HG, Morham SG, Sundquist WI. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J Biol Chem 2004;279:36059-36071.
48. Schlundt A, Sticht J, Piotukh K, Kosslick D, Jahnke N, Keller S, Schuemann M, Krause E, Freund C. Proline-rich sequence recognition - II. Proteomics analysis of Tsg101 ubiquitin-E2-like variant (UEV) interactions. Mol Cell Proteomics 2009;8:2474-2486.
49. Puertollano R. Interactions of Tom1L1 with the multivesicular body sorting machinery. J Biol Chem 2005;280:9258-9264.
50. Puertollano R, Bonifacino JS. Interactions of GGA3 with the ubiquitin sorting machinery. Nat Cell Biol 2004;6:244-251.
51. Amit I, Yakir L, Katz M, Zwang Y, Marmor MD, Citri A, Shtiegman K, Alroy I, Tuvia S, Reiss Y, Roubini E, Cohen M, Wides R, Bacharach E, Schubert U et al. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev 2004;18:1737-1752.
52. Liu F, Stephen AG, Waheed AA, Aman MJ, Freed EO, Fisher RJ, Burke TR. SAR by oxime-containing peptide libraries: application to Tsg101 ligand optimization. ChemBioChem 2008;9:2000-2004.
53. Im YJ, Kuo L, Ren X, Burgos PV, Zhao XZ, Lui F, Burke TR, Bonifacino JS, Freed EO, Hurley JH. Crystallographic and functional analysis of the ESCRT-1/HIV-1 Gag PTAP interaction. Structure 2010;18:1536-1547.
54. Pornillos O, Alam SL, Rich RL, Myszka DG, Davis DR, Sundquist WI. Structure and functional interactions of the Tsg101 UEV domain. EMBO J 2002;21:2397-2406.
55. Pornillos O, Alam SL, Davis DR, Sundquist WI. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat Struct Biol 2002;9:812-817.
56. Kim SE, Liu F, Im YJ, Stephen AG, Waheed AA, Freed EO, Fisher RJ, Hurley JH, Burke TR. Elucidation of new binding interactions with the tumor suppressor gene 101 (tsg101) protein using modified HIV-1 Gag-p6 derived peptide ligands. ACS Med Chem Lett 2011; doi: 10.1021/ml1002579.
57. Bilodeau PS, Winistorfer SC, Kearney WR, Robertson AD, Piper RC. Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J Cell Biol 2003;163:237-243.
58. Wollert T, Hurley JH. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 2010;464:864-873.
59. Ren X, Hurley JH. Structural basis for endosomal recruitment of ESCRT-I by ESCRT-0 in yeast. EMBO J 2011; doi:10.1038/emboj. 2011.122.
60. Herrador A, Herranz S, Lara D, Vincent O. Recruitment of the ESCRT machinery to a putative seven-transmembrane-domain receptor is mediated by an arrestin-related protein. Mol Cell Biol 2010;30:897-907.
61. Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD. HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 2005;168:89-101.
62. Lin CH, MacGum JA, Chu T, Stefan CJ, Emr SD. Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 2008;135:714-725.
63. Rauch S, Martin-Serrano J. Multiple interactions between the ESCRT machinery and arrestin-related proteins: implications in PPXY-dependent budding. J Virol 2011;85:3546-3556.
64. Kasanov J, Pirozzi G, Uvegas AJ, Kay BK. Characterizing class I WW domains defines key specificity determinants and generates mutant domains with novel specificities. Chem Biol 2001;8:231-241.
65. Kanelis V, Rotin D, Forman-Kay JD. Solution structure of a Nedd4 WW domain-ENaC peptide complex. Nat Struct Biol 2001;8:407-412.
66. Lee S, Joshi A, Nagashima K, Freed EO, Hurley JH. Structural basis for viral late-domain binding to Alix. Nat Struct Mol Biol 2007;14:194-199.
67. Zhai Q, Fisher RD, Chung HY, Myszka DG, Sundquist WI, Hill CP. Structural and functional studies of ALIX interactions with YPXnL late domains of HIV-1 and EIAV. Nat Struct Mol Biol 2008;15:43-49.
68. Fujii K, Munshi UM, Ablan SD, Demirov DG, Soheilian F, Nagashima K, Stephen AG, Fisher RJ, Freed EO. Functional role of Alix in HIV-1 replication. Virology 2009;391:284-292.
69. Zhai Q, Landesman MB, Robinson H, Sundquist WI, Hill CP. Identification and structural characterization of the ALIX-binding late domains of simian immunodeficiency virus SIVmac239 and SIVagmTan-1. J Virol 2011;85:632-637.
70. Vincent O, Rainbow L, Tilburn J, Arst HN, Penalva MA. YPXL/I is a protein interaction motif recognized by Aspergillus PalA and its human homologue, AIP1/Alix. Mol Cell Biol 2003;23:1647-1655.
71. Iwamori T, Iwamori N, Ma L, Edson MA, Greenbaum MP, Matzuk MM. TEX14 interacts with CEP55 to block cell abscission. Mol Cell Biol 2010;30:2280-2292.
72. Katoh K, Suzuki H, Terasawa Y, Mizuno T, Yasuda J, Shibata H, Maki M. The penta-EF-hand protein ALG-2 interacts directly with the ESCRT-I component TSG101, and Ca2+-dependently co-localizes to aberrant endosomes with dominant-negative AAA ATPase SKD1/Vps4B. Biochem J 2005;391:677-685.
73. Okumura M, Ichioka F, Kobayashi R, Suzuki H, Yoshida H, Shibata H, Maki M. Penta-EF-hand protein ALG-2 functions as a Ca2+-dependent adaptor that bridges Alix and TSG101. Biochem Biophys Res Commun 2009;386:237-241.
74. Tavassoli A, Lu Q, Gam J, Pan H, Benkovic SJ, Cohen SN. Inhibition of HIV budding by a genetically selected cyclic peptide targeting the Gag-TSG101 interaction. ACS Chem Biol 2008;3:757-764.