The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo

Journal of Cell Biology

Volumn 165, Issue 1, 2004, Pages 135-144

  Dunn, Rebecca ^a,b   Klos, Deborah A ^a   Adler, Adam S ^a   Hicke, Linda ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

E3; Endocytosis; Multivesicular endosome; Phospholipid; Protein sorting

Indexed keywords

LYSINE; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITIDE; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE NEDD4; UBIQUITIN PROTEIN LIGASE RSP5; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOSOME; ENZYME BINDING; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSPORT VESICLE; UBIQUITINATION;

CARRIER PROTEINS; ENDOSOMES; INTRACELLULAR MEMBRANES; LYSINE; MEMBRANE PROTEINS; MUTATION; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSPORT VESICLES; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 2442509573     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200309026     Document Type: Article

References (56)

1. 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.
2. Babst, M., G. Odorizzi, E.J. Estepa, and S.D. Emr. 2000. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic. 1:248-258.
3. Babst, M., D.J. Katzmann, E.J. Estepa-Sabal, T. Meerloo, and S.D. Emr. 2002a. ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev. Cell. 3:271-282.
4. Babst, M., D.J. Katzmann, W.B. Snyder, B. Wendland, and S.D. Emr. 2002b. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell. 3:283-289.
5. Beaudenon, S.L., M.R. Huacani, G. Wang, D.P. McDonnell, and J.M. Huibregtse. 1999. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase 11 in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6972-6979.
6. Bishop, N., and P. Woodman. 2001. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276:11735-11742.
7. Catz, S.D., J.L. Johnson, and B.M. Babior. 2002. The C2A domain of JFC1 binds to 3′-phosphorylated phosphoinositides and directs plasma membrane association in living cells. Proc. Natl. Acad. Sci. USA. 99:11652-11657.
8. Chang, A., S. Cheang, X. Espanel, and M. Sudol. 2000. Rsp5 WW domains interact directly with the carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 275:20562-20571.
9. Cho, W. 2001. Membrane targeting by C1 and C2 domains. J. Biol. Chem. 276: 32407-32410.
10. 2+-dependent manner. In vitro characteristics and possible significance. J. Biol. Chem. 273: 10240-10248.
11. Cockcroft, S., and M.A. De Matteis. 2001. Inositol lipids as spatial regulators of membrane traffic. J. Membr. Biol. 180:187-194.
12. Dove, S.K., R.K. McEwen, A. Mayes, D.C. Hughes, J.D. Beggs, and R.H. Michell. 2002. Vac14 controls Ptdlns(3,5)P(2) synthesis and Fab1-dependent protein trafficking to the multivesicular body. Curr. Biol. 12:885-893.
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.
14. Dupré, S., and R. Haguenauer-Tsapis. 2001. Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 21:4482-4494.
15. Fukuda, M., J. Aruga, M. Niinobe, S. Aimoto, and K. Mikoshiba. 1994. Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J. Biol. Chem. 269:29206-29211.
16. Futter, C.E., L.M. Collinson, J.M. Backer, and C.R. Hopkins. 2001. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155:1251-1264.
17. Galan, J.M., V. Moreau, B. André, C. Volland, and R. Haguenauer-Tsapis. 1996. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271: 10946-10952.
18. 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. Cote, R.L. Rich, et al. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell. 107:55-65.
19. Halliwell, S.B., S. Losko, and C.A. Kaiser. 2001. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153:649-662.
20. Hershko, A., A. Ciechanover, and A. Varshavsky. 2000. The ubiquitin system. Nat. Med. 6:1073-1081.
21. Hicke, L., and H. Riezman. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell. 84:277-287.
22. Hicke, L., and R. Dunn. 2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Ann. Rev. Cell Dev. Biol. 19:141-172.
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.
24. Horvath, A., and H. Riezman. 1994. Rapid protein extraction from Saccharomyces cerevisiae. Yeast. 10:1305-1310.
25. Hurley, J.H., and S. Misra. 2000. Signaling and subcellular targeting by membrane-binding domains. Annu. Rev. Biophys. Biomol. Struct. 29:49-79.
26. Itoh, T., S. Koshiba, T. Kigawa, A. Kikuchi, S. Yokoyama, and T. Takenawa. 2001. Role of the ENTH domain in phosphatidylinositol-4, 5-bisphosphate binding and endocytosis. Science. 291:1047-1051.
27. Katzmann, D.J., M. Babst, and S.D. Emr. 2001. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal sorting complex, ESCRT-I. Cell. 106:145-155.
28. Katzmann, D.J., G. Odorizzi, and S.D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905.
29. Kavran, J.M., D.E. Klein, A. Lee, M. Falasca, S.J. Isakoff, E.Y. Skolnik, and M.A. Lemmon. 1998. Specificity and promiscuity in phosphoinositide binding by pleckstrin homology domains. J. Biol. Chem. 273:30497-30508.
30. Keleman, K., S. Rajagopalan, D. Cleppien, D. Teis, K. Paiha, L.A. Huber, G.M. Technau, and B.J. Dickson. 2002. Comm sorts Robo to control axon guidance at the Drosophila midline. Cell. 110:415-427.
31. Kohout, S.C., S. Corbalan-Garcia, J.C. Gomez-Fernandez, and J.J. Falke. 2003. C2 domain of protein kinase Cα: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling. Biochemistry. 42: 1254-1265.
32. Lee, J.O., H. Yang, M.M. Georgescu, A. Di Cristofano, T. Maehama, Y. Shi, J.E. Dixon, P. Pandolfi, and N.P. Pavletich. 1999. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell. 99:323-334.
33. Mehrotra, B., D.G. Myszka, and G.D. Prestwich. 2000. Binding kinetics and ligand specificity for the interactions of the C2B domain of synaptogmin II with inositol polyphosphates and phosphoinositides. Biochemistry. 39:9679-9686.
34. Myat, A., P. Henry, V. McCabe, L. Flintoft, D. Rotin, and G. Tear. 2002. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron. 35:447-459.
35. Nalefski, E.A., and J.J. Falke. 1996. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 5:2375-2390.
36. Odorizzi, G., M. Babst, and S.D. Emr. 1998. Fablp Ptdlns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell. 95:847-858.
37. Odorizzi, G., M. Babst, and S.D. Emr. 2000. Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25:229-235.
38. Pickart, C.M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-533.
39. 2+-dependent plasma membrane localization. J. Biol. Chem. 272:32329-32336.
40. 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.
41. Pryer, N.K., N.R. Salama, R. Schekman, and C.A. Kaiser. 1993. Cytosolic Sec13p complex is required for vesicle formation from the endoplasmic reticulum in vitro. J. Cell Biol. 120:865-875.
42. Raiborg, C., T.E. Rusten, and H. Stenmark. 2003. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15:446-455.
43. Raymond, C.K., I. Howald-Stevenson, C.A. Vaters, 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.
44. Reggiori, F., and H.R. Pelham. 2001. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20:5176-5186.
45. Reggiori, F., and H.R. Pelham. 2002. A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4:117-123.
46. Reggiori, F., M.W. Black, and H.R. Pelham. 2000. Polar transmembrane domains target proteins to the interior of the yeast vacuole. Mol. Biol. Cell. 11:3737-3749.
47. Rotin, D., O. Staub, and R. Haguenauer-Tsapis. 2000. Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176:1-17.
48. Schiavo, G., Q.M. Gu, G.D. Prestwich, T.H. Sollner, and J.E. Rothman. 1996. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. USA. 93:13327-13332.
49. Sehgal, B.U. 2002. Interactions of EF-hand and C2 proteins with calcium and lead. Ph.D. thesis. Northwestern University, Evanston, IL. 129 pp.
50. Sehgal, B.U., R. Dunn, L. Hicke, and H.A. Godwin. 2000. High-yield expression and purification of recombinant proteins in bacteria: a versatile vector for glutathione S-transferase fusion proteins containing two protease cleavage sites. Anal. Biochem. 281:232-234.
51. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
52. Shih, S.C., K.J. Katzmann, J.D. Schnell, M. Sutanto, S.C. Emr, and L.H. Hicke. 2002. Epsins and Vps27/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4:389-393.
53. Soetens, O., J.O. De Craene, and B. Andre. 2001. Ubiquitin is required for sorting to the vacuole of the yeast general amino acid permease, Gap1. J. Biol. Chem. 276:43949-43957.
54. Urbanowski, J., and R.C. Piper. 2001. Ubiquitin sorts proteins into the intralumenal degradative compartment of the late endosome/vacuole. Traffic. 2:623-631.
55. Vida, T.A., and S.D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Biol. Chem. 128:779-792.
56. Wang, G., M. McCaffrey, B. Wendland, S. Dupré, R. Haguenauer-Tsapis, and J. Huibregtse. 2001. Localization of the Rsp5p ubiquitin-protein ligase at multiple sites within the endocytic pathway. Mol. Cell. Biol. 21:3564-3575.