A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination

Journal of Cell Biology

Volumn 192, Issue 2, 2011, Pages 229-242

  Stringer, Daniel K ^a   Piper, Robert C ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; UBIQUITINATION; YEAST;

ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; MEMBRANE PROTEINS; MULTIVESICULAR BODIES; PLASMIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITINATION;

EID: 78951480972     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201008121     Document Type: Article

References (72)

1. Amit, I., L. Yakir, M. Katz, Y. Zwang, M.D. Marmor, A. Citri, K. Shtiegman, I. Alroy, S. Tuvia, Y. Reiss, et al. 2004. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 18:1737-1752. doi:10.1101/gad.294904
2. Babst, M., T.K. Sato, L.M. Banta, and S.D. Emr. 1997. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16:1820-1831. doi:10.1093/emboj/16.8.1820 (Pubitemid 27170943)
3. Banta, L.M., J.S. Robinson, D.J. Klionsky, and S.D. Emr. 1988. Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol. 107:1369-1383. doi:10.1083/jcb.107.4.1369
4. Bilodeau, P.S., J.L. Urbanowski, S.C. Winistorfer, and R.C. Piper. 2002. The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4:534-539.
5. Bilodeau, P.S., S.C. Winistorfer, M.M. Allaman, K. Surendhran, W.R. Kearney, A.D. Robertson, and R.C. Piper. 2004. The GAT domains of clathrin-associated GGA proteins have two ubiquitin binding motifs. J. Biol. Chem. 279:54808-54816. doi:10.1074/jbc.M406654200
6. Blondel, M.O., J. Morvan, S. Dupré, D. Urban-Grimal, R. Haguenauer-Tsapis, and C. Volland. 2004. Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5pdependent ubiquitylation. Mol. Biol. Cell. 15:883-895. doi:10.1091/mbc.E03- 04-0202
7. Brachmann, C.B., A. Davies, G.J. Cost, E. Caputo, J. Li, P. Hieter, and J.D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 14:115-132. doi:10.1002/(SICI)1097- 0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2
8. Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science. 309:127-130. doi:10.1126/science.1110340 (Pubitemid 40934990)
9. Chellappa, R., P. Kandasamy, C.S. Oh, Y. Jiang, M. Vemula, and C.E. Martin. 2001. The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression. Fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator. J. Biol. Chem. 276:43548-43556. doi:10.1074/jbc.M107845200 (Pubitemid 37383913)
10. Curtiss, M., C. Jones, and M. Babst. 2007. Efficient cargo sorting by ESCRT-I and the subsequent release of ESCRT-I from multivesicular bodies requires the subunit Mvb12. Mol. Biol. Cell. 18:636-645. doi:10.1091/mbc.E06-07- 0588 (Pubitemid 46213231)
11. Deng, Y., Y. Guo, H. Watson, W.C. Au, M. Shakoury-Elizeh, M.A. Basrai, J.S. Bonifacino, and C.C. Philpott. 2009. Gga2 mediates sequential ubiquitin-independent and ubiquitin-dependent steps in the trafficking of ARN1 from the trans-Golgi network to the vacuole. J. Biol. Chem. 284:23830-23841. doi:10.1074/jbc.M109.030015
12. Dores, M.R., J.D. Schnell, L. Maldonado-Baez, B. Wendland, and L. Hicke. 2010. The function of yeast Epsin and Ede1 ubiquitin-binding domains during receptor internalization. Traffic. 11:151-160. doi:10.1111/j.1600-0854.2009. 01003.x
13. Dunn, R., and L. Hicke. 2001. Domains of the Rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis. Mol. Biol. Cell. 12:421-435. (Pubitemid 33051585)
14. Ejercito, P.M., E.D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J. Gen. Virol. 2:357-364. doi:10.1099/0022-1317-2-3-357
15. Erpapazoglou, Z., M. Froissard, I. Nondier, E. Lesuisse, R. Haguenauer-Tsapis, and N. Belgareh-Touzé. 2008. Substrate- and ubiquitin-dependent trafficking of the yeast siderophore transporter Sit1. Traffic. 9:1372-1391. doi:10.1111/j.1600-0854.2008.00766.x (Pubitemid 352016293)
16. Galan, J.M., A. Wiederkehr, J.H. Seol, R. Haguenauer-Tsapis, R.J. Deshaies, H. Riezman, and M. Peter. 2001. Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast. Mol. Cell. Biol. 21:3105-3117. doi:10.1128/MCB.21.9.3105-3117.2001
17. Giaever, G., A.M. Chu, L. Ni, C. Connelly, L. Riles, S. Véronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. André, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature. 418:387-391. doi:10.1038/nature00935
18. Gredmark, S., C. Schlieker, V. Quesada, E. Spooner, and H.L. Ploegh. 2007. A functional ubiquitin-specific protease embedded in the large tegument protein (ORF64) of murine gammaherpesvirus 68 is active during the course of infection. J. Virol. 81:10300-10309. doi:10.1128/JVI.01149-07 (Pubitemid 47463305)
19. Gueldener, U., J. Heinisch, G.J. Koehler, D. Voss, and J.H. Hegemann. 2002. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30:e23. doi:10.1093/nar/30.6.e23
20. Haglund, K., and H. Stenmark. 2006. Working out coupled monoubiquitination. Nat. Cell Biol. 8:1218-1219. doi:10.1038/ncb1106-1218
21. Hicke, L., H.L. Schubert, and C.P. Hill. 2005. Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6:610-621. doi:10.1038/nrm1701
22. Hoeller, D., C.M. Hecker, S. Wagner, V. Rogov, V. Dötsch, and I. Dikic. 2007. E3-independent monoubiquitination of ubiquitin-binding proteins. Mol. Cell. 26:891-898. doi:10.1016/j.molcel.2007.05.014
23. Hoppe, T., K. Matuschewski, M. Rape, S. Schlenker, H.D. Ulrich, and S. Jentsch. 2000. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell. 102:577-586. doi:10.1016/S0092-8674(00)00080-5
24. Huang, T.T., S.M. Nijman, K.D. Mirchandani, P.J. Galardy, M.A. Cohn, W. Haas, S.P. Gygi, H.L. Ploegh, R. Bernards, and A.D. D'Andrea. 2006. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat. Cell Biol. 8:339-347.
25. Janke, C., M.M. Magiera, N. Rathfelder, C. Taxis, S. Reber, H. Maekawa, A. Moreno-Borchart, G. Doenges, E. Schwob, E. Schiebel, and M. Knop. 2004. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 21:947-962. doi:10.1002/yea.1142
26. Kato, M., K. Miyazawa, and N. Kitamura. 2000. A deubiquitinating enzyme UBPY interacts with the Src homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP. J. Biol. Chem. 275:37481-37487. doi:10.1074/jbc.M007251200 (Pubitemid 32004855)
27. Kattenhorn, L.M., G.A. Korbel, B.M. Kessler, E. Spooner, and H.L. Ploegh. 2005. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell. 19:547-557. doi:10.1016/j.molcel.2005.07.003
28. Katz, M., K. Shtiegman, P. Tal-Or, L. Yakir, Y. Mosesson, D. Harari, Y. Machluf, H. Asao, T. Jovin, K. Sugamura, and Y. Yarden. 2002. Ligand-independent degradation of epidermal growth factor receptor involves receptor ubiquitylation and Hgs, an adaptor whose ubiquitin-interacting motif targets ubiquitylation by Nedd4. Traffic. 3:740-751. doi:10.1034/j.1600-0854.2002.31006. x
29. Kee, Y., N. Lyon, and J.M. Huibregtse. 2005. The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J. 24:2414-2424. doi:10.1038/sj.emboj.7600710 (Pubitemid 41032592)
30. Kee, Y., W. Muñoz, N. Lyon, and J.M. Huibregtse. 2006. The deubiquitinating enzyme Ubp2 modulates Rsp5-dependent Lys63-linked polyubiquitin conjugates in Saccharomyces cerevisiae. J. Biol. Chem. 281:36724-36731. doi:10.1074/jbc.M608756200 (Pubitemid 46042139)
31. Kim, H.C., and J.M. Huibregtse. 2009. Polyubiquitination by HECT E3s and the determinants of chain type specificity. Mol. Cell. Biol. 29:3307-3318. doi:10.1128/MCB.00240-09
32. Kim, B.Y., J.A. Olzmann, G.S. Barsh, L.S. Chin, and L. Li. 2007. Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell. 18:1129-1142. doi:10.1091/mbc.E06-09-0787
33. Kim, E.T., S.E. Oh, Y.O. Lee, W. Gibson, and J.H. Ahn. 2009. Cleavage specificity of the UL48 deubiquitinating protease activity of human cytomegalovirus and the growth of an active-site mutant virus in cultured cells. J. Virol. 83:12046-12056. doi:10.1128/JVI.00411-09
34. Kölling, R., and C.P. Hollenberg. 1994. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J. 13:3261-3271. (Pubitemid 24226940)
35. Komada, M., and N. Kitamura. 2005. The Hrs/STAM complex in the down-regulation of receptor tyrosine kinases. J. Biochem. 137:1-8. doi:10.1093/jb/mvi001 (Pubitemid 40502401)
36. Kulathu, Y., M. Akutsu, A. Bremm, K. Hofmann, and D. Komander. 2009. Two-sided ubiquitin binding explains specificity of the TAB2 NZF domain. Nat. Struct. Mol. Biol. 16:1328-1330. doi:10.1038/nsmb.1731
37. Lauwers, E., C. Jacob, and B. André. 2009. K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J. Cell Biol. 185:493-502. doi:10.1083/jcb.200810114
38. Lauwers, E., Z. Erpapazoglou, R. Haguenauer-Tsapis, and B. André. 2010. The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20:196-204. doi:10.1016/j.tcb.2010.01.004
39. Liu, K., Z. Hua, J.A. Nepute, and T.R. Graham. 2007. Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol. Biol. Cell. 18:487-500. doi:10.1091/mbc.E06-07-0592
40. 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. doi:10.1016/S1534-5807(03)00321-6
41. McCullough, J., M.J. Clague, and S. Urbé. 2004. AMSH is an endosome-associated ubiquitin isopeptidase. J. Cell Biol. 166:487-492. doi:10.1083/jcb.200401141
42. Miller, S.L., E. Malotky, and J.P. O'Bryan. 2004. Analysis of the role of ubiquitin-interacting motifs in ubiquitin binding and ubiquitylation. J. Biol. Chem. 279:33528-33537. doi:10.1074/jbc.M313097200
43. Munn, A.L., A. Heese-Peck, B.J. Stevenson, H. Pichler, and H. Riezman. 1999. Specific sterols required for the internalization step of endocytosis in yeast. Mol. Biol. Cell. 10:3943-3957.
44. Nikko, E., and H.R. Pelham. 2009. Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic. 10:1856-1867. doi:10.1111/j.1600-0854. 2009.00990.x
45. Paiva, S., N. Vieira, I. Nondier, R. Haguenauer-Tsapis, M. Casal, and D. Urban-Grimal. 2009. Glucose-induced ubiquitylation and endocytosis of the yeast Jen1 transporter: role of lysine 63-linked ubiquitin chains. J. Biol. Chem. 284:19228-19236. doi:10.1074/jbc.M109.008318
46. Piper, R.C., and D.J. Katzmann. 2007. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23:519-547. doi:10.1146/annurev .cellbio.23.090506.123319
47. Polo, S., S. Sigismund, M. Faretta, M. Guidi, M.R. Capua, G. Bossi, H. Chen, P. De Camilli, and P.P. Di Fiore. 2002. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature. 416:451-455. doi:10.1038/416451a
48. Puertollano, R., and J.S. Bonifacino. 2004. Interactions of GGA3 with the ubiquitin sorting machinery. Nat. Cell Biol. 6:244-251. doi:10.1038/ncb1106
49. Raymond, C.K., I. Howald-Stevenson, C.A. Vater, and T.H. Stevens. 1992. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell. 3:1389-1402.
50. Reggiori, F., and H.R. Pelham. 2001. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20:5176-5186. doi:10.1093/emboj/20.18.5176
51. Ren, X., and J.H. Hurley. 2010. VHS domains of ESCRT-0 cooperate in highavidity binding to polyubiquitinated cargo. EMBO J. 29:1045-1054. doi:10.1038/emboj.2010.6
52. Ren, J., Y. Kee, J.M. Huibregtse, and R.C. Piper. 2007. Hse1, a component of the yeast Hrs-STAM ubiquitin-sorting complex, associates with ubiquitin peptidases and a ligase to control sorting efficiency into multivesicular bodies. Mol. Biol. Cell. 18:324-335. doi:10.1091/mbc.E06-06-0557
53. Ren, J., N. Pashkova, S. Winistorfer, and R.C. Piper. 2008. DOA1/UFD3 plays a role in sorting ubiquitinated membrane proteins into multivesicular bodies. J. Biol. Chem. 283:21599-21611. doi:10.1074/jbc.M802982200
54. Reyes-Turcu, F.E., K.H. Ventii, and K.D. Wilkinson. 2009. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78:363-397. doi:10.1146/annurev.biochem.78.082307.091526
55. Rotin, D., and S. Kumar. 2009. Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10:398-409. doi:10.1038/nrm2690
56. Row, P.E., I.A. Prior, J. McCullough, M.J. Clague, and S. Urbé. 2006. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281:12618-12624. doi:10.1074/jbc.M512615200
57. Roxrud, I., H. Stenmark, and L. Malerød. 2010. ESCRT & Co. Biol. Cell. 102:293-318. doi:10.1042/BC20090161
58. Schlieker, C., W.A. Weihofen, E. Frijns, L.M. Kattenhorn, R. Gaudet, and H.L. Ploegh. 2007. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes. Mol. Cell. 25:677-687. doi:10.1016/j.molcel.2007.01.033
59. Scott, P.M., P.S. Bilodeau, O. Zhdankina, S.C. Winistorfer, M.J. Hauglund, M.M. Allaman, W.R. Kearney, A.D. Robertson, A.L. Boman, and R.C. Piper. 2004. GGA proteins bind ubiquitin to facilitate sorting at the trans-Golgi network. Nat. Cell Biol. 6:252-259. doi:10.1038/ncb1107
60. Shields, S.B., A.J. Oestreich, S. Winistorfer, D. Nguyen, J.A. Payne, D.J. Katzmann, and R. Piper. 2009. ESCRT ubiquitin-binding domains function cooperatively during MVB cargo sorting. J. Cell Biol. 185:213-224. doi:10.1083/jcb.200811130
61. Sikorski, R.S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
62. Spence, J., S. Sadis, A.L. Haas, and D. Finley. 1995. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol. Cell. Biol. 15:1265-1273.
63. Struhl, K., and R.W. Davis. 1977. Production of a functional eukaryotic enzyme in Escherichia coli: cloning and expression of the yeast structural gene for imidazole-glycerolphosphate dehydratase (his3). Proc. Natl. Acad. Sci. USA. 74:5255-5259. doi:10.1073/pnas.74.12.5255
64. Tsunematsu, T., E. Yamauchi, H. Shibata, M. Maki, T. Ohta, and H. Konishi. 2010. Distinct functions of human MVB12A and MVB12B in the ESCRT-I dependent on their posttranslational modifications. Biochem. Biophys. Res. Commun. 399:232-237. doi:10.1016/j.bbrc.2010.07.060
65. Uchiki, T., H.T. Kim, B. Zhai, S.P. Gygi, J.A. Johnston, J.P. O'Bryan, and A.L. Goldberg. 2009. The ubiquitin-interacting motif protein, S5a, is ubiquitinated by all types of ubiquitin ligases by a mechanism different from typical substrate recognition. J. Biol. Chem. 284:12622-12632. doi:10.1074/jbc.M900556200
66. Urbanowski, J.L., and R.C. Piper. 2001. Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/vacuole. Traffic. 2:622-630. doi:10.1034/j.1600-0854.2001.20905.x
67. Wang, G., J. Yang, and J.M. Huibregtse. 1999. Functional domains of the Rsp5 ubiquitin-protein ligase. Mol. Cell. Biol. 19:342-352.
68. Wang, X., R.A. Herr, W.J. Chua, L. Lybarger, E.J. Wiertz, and T.H. Hansen. 2007. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J. Cell Biol. 177:613-624. doi:10.1083/jcb.200611063
69. Wiederkehr, A., S. Avaro, C. Prescianotto-Baschong, R. Haguenauer-Tsapis, and H. Riezman. 2000. The F-box protein Rcy1p is involved in endocytic membrane traffic and recycling out of an early endosome in Saccharomyces cerevisiae. J. Cell Biol. 149:397-410. doi:10.1083/jcb.149.2.397
70. Williams, R.L., and S. Urbé. 2007. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8:355-368. doi:10.1038/nrm2162
71. Winzeler, E.A., D.D. Shoemaker, A. Astromoff, H. Liang, K. Anderson, B. Andre, R. Bangham, R. Benito, J.D. Boeke, H. Bussey, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science. 285:901-906. doi:10.1126/science.285.5429.901
72. Woelk, T., B. Oldrini, E. Maspero, S. Confalonieri, E. Cavallaro, P.P. Di Fiore, and S. Polo. 2006. Molecular mechanisms of coupled monoubiquitination. Nat. Cell Biol. 8:1246-1254. doi:10.1038/ncb1484