Pkh1/2-dependent phosphorylation of Vps27 regulates ESCRT-I recruitment to endosomes

Molecular Biology of the Cell

Volumn 23, Issue 20, 2012, Pages 4054-4064

  Morvan, Joëlle ^a,b   Rinaldi, Bruno ^a   Friant, Sylvie ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYPEPTIDASE; CARBOXYPEPTIDASE CPS1; ESCRT 1 PROTEIN; ESCRT 2 PROTEIN; ESCRT 3 PROTEIN; ESCRT PROTEIN; MEMBRANE PROTEIN; PKH1 PROTEIN; PKH2 PROTEIN; PROTEIN SERINE THREONINE KINASE; SERINE; UNCLASSIFIED DRUG; VPS27 PROTEIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION;

ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; GREEN FLUORESCENT PROTEINS; MULTIVESICULAR BODIES; MUTATION; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84867449334     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-01-0001     Document Type: Article

References (45)

1. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H (2008). A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7, 1389-1396. (Pubitemid 352038280)
2. Bilodeau PS, Winistorfer SC, Kearney WR, Robertson AD, Piper RC (2003). Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J Cell Biol 163, 237-243. (Pubitemid 37363125)
3. Boura E, Rozycki B, Herrick DZ, Chung HS, Vecer J, Eaton WA, Cafiso DS, Hummer G, Hurley JH (2011). Solution structure of the ESCRT-I complex by small-angle x-ray scattering, EPR, and FRET spectroscopy. Proc Natl Acad Sci USA 108, 9437-9442.
4. Bugnicourt A, Froissard M, Sereti K, Ulrich HD, Haguenauer-Tsapis R, Galan JM (2004). Antagonistic roles of ESCRT and Vps class C/HOPS complexes in the recycling of yeast membrane proteins. Mol Biol Cell 15, 4203-4214. (Pubitemid 39122023)
5. Casamayor A, Torrance PD, Kobayashi T, Thorner J, Alessi DR (1999). Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast. Curr Biol 9, 186-197. (Pubitemid 29120382)
6. Chen P, Lee KS, Levin DE (1993). A pair of putative protein kinase genes (YPK1 and YPK2) is required for cell growth in Saccharomyces cerevisiae. Mol Gen Genet 236, 443-447. (Pubitemid 23055589)
7. deHart AK, Schnell JD, Allen DA, Hicke L (2002). The conserved Pkh-Ypk kinase cascade is required for endocytosis in yeast. J Cell Biol 156, 241-248. (Pubitemid 34839906)
8. Feng Y, Davis NG (2000). Akr1p and the type I casein kinases act prior to the ubiquitination step of yeast endocytosis: Akr1p is required for kinase localization to the plasma membrane. Mol Cell Biol 20, 5350-5359. (Pubitemid 30431588)
9. Friant S, Lombardi R, Schmelzle T, Hall MN, Riezman H (2001). Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J 20, 6783-6792. (Pubitemid 33134208)
10. Friant S, Zanolari B, Riezman H (2000). Increased protein kinase or decreased PP2A activity bypasses sphingoid base requirement in endocytosis. EMBO J 19, 2834-2844. (Pubitemid 30386756)
11. Gietz D, St Jean A, Woods RA, Schiestl RH (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20, 1425.
12. Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, Emr SD, Williams RL (2007). Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J 26, 600-612. (Pubitemid 46160959)
13. Gruhler A, Olsen JV, Mohammed S, Mortensen P, Faergeman NJ, Mann M, Jensen ON (2005). Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol Cell Proteomics 4, 310-327. (Pubitemid 40439774)
14. Hanafusa H, Ishikawa K, Kedashiro S, Saigo T, Iemura S, Natsume T, Komada M, Shibuya H, Nara A, Matsumoto K (2011). Leucine-rich repeat kinase LRRK1 regulates endosomal trafficking of the EGF receptor. Nat Commun 2, 158.
15. Hicke L, Zanolari B, Riezman H (1998). Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J Cell Biol 141, 349-358. (Pubitemid 28237084)
16. Hierro A, Sun J, Rusnak AS, Kim J, Prag G, Emr SD, Hurley JH (2004). Structure of the ESCRT-II endosomal trafficking complex. Nature 431, 221-225. (Pubitemid 39243478)
17. Hoeller D et al. (2006). Regulation of ubiquitin-binding proteins by monoubiquitination. Nat Cell Biol 8, 163-169.
18. Hurley JH (2008). ESCRT complexes and the biogenesis of multivesicular bodies. Curr Opin Cell Biol 20, 4-11.
19. Im YJ, Wollert T, Boura E, Hurley JH (2009). Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev Cell 17, 234-243.
20. Inagaki M, Schmelzle T, Yamaguchi K, Irie K, Hall MN, Matsumoto K (1999). PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol Cell Biol 19, 8344-8352. (Pubitemid 30414028)
21. Katzmann DJ, Stefan CJ, Babst M, Emr SD (2003). Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol 162, 413-423. (Pubitemid 36988551)
22. Lata S, Schoehn G, Jain A, Pires R, Piehler J, Gottlinger HG, Weissenhorn W (2008). Helical structures of ESCRT-III are disassembled by VPS4. Science 321, 1354-1357.
23. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, Andre B (2010). The ubiquitin code of yeast permease trafficking. Trends Cell Biol 20, 196-204.
24. Marchal C, Dupre S, Urban-Grimal D (2001). Casein kinase I controls a late step in the endocytic trafficking of yeast uracil permease. J Cell Sci 115, 217-226.
25. Marchal C, Haguenauer-Tsapis R, Urban-Grimal D (1998). A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease. Mol Cell Biol 18, 314-321. (Pubitemid 28021042)
26. Marchal C, Haguenauer-Tsapis R, Urban-Grimal D (2000). Casein kinase I-dependent phosphorylation within a PEST sequence and ubiquitination at nearby lysines signal endocytosis of yeast uracil permease. J Biol Chem 275, 23608-23614. (Pubitemid 30624645)
27. Obita T, Saksena S, Ghazi-Tabatabai S, Gill DJ, Perisic O, Emr SD, Williams RL (2007). Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-739. (Pubitemid 47552090)
28. Odorizzi G, Babst M, Emr SD (1998). Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858. (Pubitemid 29014464)
29. Pornillos O, Alam SL, Davis DR, Sundquist WI (2002). Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat Struct Biol 9, 812-817. (Pubitemid 35257779)
30. Reggiori F, Pelham HR (2001). Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J 20, 5176-5186. (Pubitemid 32910912)
31. Ren X, Hurley JH (2011). Structural basis for endosomal recruitment of ESCRT-I by ESCRT-0 in yeast. EMBO J 30, 2130-2139.
32. Ren X, Kloer DP, Kim YC, Ghirlando R, Saidi LF, Hummer G, Hurley JH (2009). Hybrid structural model of the complete human ESCRT-0 complex. Structure 17, 406-416.
33. Robinson LC, Menold MM, Garrett S, Culbertson MR (1993). Casein kinase I-like protein kinases encoded by YCK1 and YCK2 are required for yeast morphogenesis. Mol Cell Biol 13, 2870-2881. (Pubitemid 23133958)
34. Roth AF, Papanayotou I, Davis NG (2011). The yeast kinase Yck2 has a tripartite palmitoylation signal. Mol Biol Cell 22, 2702-2715.
35. Saksena S, Sun J, Chu T, Emr SD (2007). ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 32, 561-573. (Pubitemid 350123053)
36. Smolka MB, Albuquerque CP, Chen SH, Zhou H (2007). Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci USA 104, 10364-10369. (Pubitemid 47185671)
37. Steen H, Kuster B, Fernandez M, Pandey A, Mann M (2002). Tyrosine phosphorylation mapping of the epidermal growth factor receptor signaling pathway. J Biol Chem 277, 1031-1039. (Pubitemid 34968848)
38. Stefan CJ, Blumer KJ (1999). A syntaxin homolog encoded by VAM3 mediates down-regulation of a yeast G protein-coupled receptor. J Biol Chem 274, 1835-1841.
39. Stern KA, Visser Smit GD, Place TL, Winistorfer S, Piper RC, Lill NL (2007). Epidermal growth factor receptor fate is controlled by Hrs tyrosine phosphorylation sites that regulate Hrs degradation. Mol Cell Biol 27, 888-898. (Pubitemid 46174554)
40. Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL (2006). ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125, 99-111.
41. Urbe S, Mills IG, Stenmark H, Kitamura N, Clague MJ (2000). Endosomal localization and receptor dynamics determine tyrosine phosphorylation of hepatocyte growth factor-regulated tyrosine kinase substrate. Mol Cell Biol 20, 7685-7692.
42. Volland C, Urban-Grimal D, Geraud G, Haguenauer-Tsapis R (1994). Endocytosis and degradation of the yeast uracil permease under adverse conditions. J Biol Chem 269, 9833-9841. (Pubitemid 24196592)
43. Williams RL, Urbe S (2007). The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol 8, 355-368. (Pubitemid 46643239)
44. Wollert T, Yang D, Ren X, Lee HH, Im YJ, Hurley JH (2009). The ESCRT machinery at a glance. J Cell Sci 122, 2163-2166.
45. Zanolari B, Friant S, Funato K, Sutterlin C, Stevenson BJ, Riezman H (2000). Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J 19, 2824-2833. (Pubitemid 30386755)