Regulation of yeast ESCRT-III membrane scission activity by the Doa4 ubiquitin hydrolase

Molecular Biology of the Cell

Volumn 28, Issue 5, 2017, Pages 661-672

  Johnson, Natalie ^a   West, Matt ^a   Odorizzi, Greg ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRO1 DOMAIN PROTEIN; CARBAMOYL PHOSPHATE SYNTHASE; DEUBIQUITINASE; DOA4 ENZYME; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT III COMPLEX; ESCRT PROTEIN; FUNGAL PROTEIN; HYDROLASE; PROTEIN SERINE THREONINE KINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 20 PROTEIN; DOA4 PROTEIN, S CEREVISIAE; PROTEIN BINDING; PROTEINASE; SACCHAROMYCES CEREVISIAE PROTEIN; UBIQUITIN; UBIQUITIN THIOLESTERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL BUDDING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOPLASM VESICLE; DEUBIQUITINATION; ENDOSOME; ENZYME ACTIVITY; ENZYME BINDING; GENE OVEREXPRESSION; INTRALUMENAL VESICLE; MEMBRANE BIOLOGY; MEMBRANE SCISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; CELL DIVISION; CYTOLOGY; INTRACELLULAR MEMBRANE; METABOLISM; MULTIVESICULAR BODY; PHYSIOLOGY; PROTEIN TRANSPORT;

CELL DIVISION; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; INTRACELLULAR MEMBRANES; MULTIVESICULAR BODIES; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN; UBIQUITIN THIOLESTERASE;

EID: 85014571358     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-11-0761     Document Type: Article

References (75)

1. Adell MA, Vogel GF, Pakdel M, Müller M, Lindner H, Hess MW, Teis D (2014). Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol 205, 33-49.
2. Alam SL, Sun J, Payne M, Welch BD, Blake BK, Davis DR, Meyer HH, Emr SD, Sundquist WI (2004). Ubiquitin interactions of NZF zinc fingers. EMBO J 23, 1411-1421.
3. Amerik AY, Nowak J, Swaminathan S, Hochstrasser M (2000). The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar proteinsorting and endocytic pathways. Mol Biol Cell 11, 3365-3380.
4. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002b). ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev Cell 3, 271-282.
5. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD (2002a). Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3, 283-289.
6. Babst M, Sato TK, Banta LM, Emr SD (1997). Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J 16, 1820-1831.
7. Babst M, Wendland B, Estepa EJ, Emr SD (1998). The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17, 2982-2993.
8. Barajas D, Jiang Y, Nagy PD (2009). A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5, e1000705.
9. Bilodeau PS, Urbanowski JL, Winistorfer SC, Piper RC (2002). The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat Cell Biol 4, 534-539.
10. Bowers K, Lottridge J, Helliwell SB, Goldthwaite LM, Luzio JP, Stevens TH (2004). Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 5, 194-210.
11. Carlton JG, Caballe A, Agromayor M, Kloc M, Martin-Serrano J (2012). ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science 336, 220-225.
12. Carlton JG, Martin-Serrano J (2007). Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912.
13. Cashikar AG, Shim S, Roth R, Maldazys MR, Heuser JE, Hanson PI (2014). Structure of cellular ESCRT-III spirals and their relationship to HIV budding. Elife 3, e02184.
14. Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S, Roux A (2015). Relaxation of loaded ESCRT-III spiral springs drives membrane deformation. Cell 163, 866-879.
15. Christ L, Wenzel EM, Liestøl K, Raiborg C, Campsteijn C, Stenmark H (2016). ALIX and ESCRT-I/II function as parallel ESCRT-III recruiters in cytokinetic abscission. J Cell Biol 212, 499-513.
16. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P (1992). Multifunctional yeast high-copy-number shuttle vectors. Gene 110, 119-122.
17. Cowles CR, Snyder WB, Burd CG, Emr SD (1997). Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J 16, 2769-2782.
18. Curtiss M, Jones C, Babst M (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.
19. Diaz A, Zhang J, Ollwerther A, Wang X, Ahlquist P (2015). Host ESCRT proteins are required for bromovirus RNA replication compartment assembly and function. PLoS Pathog 11, e1004742.
20. Dupre S, Haguenauer-Tsapis R (2001). Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol Cell Biol 21, 4482-4494.
21. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Côté M, Rich RL, et al. (2001). Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65.
22. Giddings TH (2003). Freeze-substitution protocols for improved visualization of membranes in high-pressure frozen samples. J Microsc 212, 53-61.
23. Hanson PI, Cashikar A (2012). Multivesicular body morphogenesis. Annu Rev Cell Dev Biol 28, 337-362.
24. Hanson PI, Roth R, Lin Y, Heuser JE (2008). Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J Cell Biol 180, 389-402.
25. Henne WM, Buchkovich NJ, Zhao Y, Emr SD (2012). The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices. Cell 151, 356-371.
26. Higuchi R, Krummel B, Saiki RK (1988). A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res 16, 7351-7367.
27. Hurley JH (2015). ESCRTs are everywhere. EMBO J 34, 2398-2407.
28. 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.
29. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F (2014). ESCRT machinery is required for plasma membrane repair. Science 343, 1247136.
30. Katzmann DJ, Babst M, Emr SD (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
31. Katzmann DJ, Sarkar S, Chu T, Audhya A, Emr SD (2004). Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol Biol Cell 15, 468-480.
32. Kerppola TK (2006). Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat Protoc 1, 1278-1286.
33. Kieffer C, Skalicky J, Morita E, Domenico I, Ward D, Kaplan J, Sundquist W (2008). Two distinct modes of ESCRT-III recognition are required for VPS4 functions in lysosomal protein targeting and HIV-1 budding. Dev Cell 15, 62-73.
34. Kim J, Sitaraman S, Hierro A, Beach BM, Odorizzi G, Hurley JH (2005). Structural basis for endosomal targeting by the Bro1 domain. Dev Cell 8, 937-947.
35. Kojima R, Obita T, Onoue K, Mizuguchi M (2016). Structural fine-tuning of MIT-interacting motif 2 (MIM2) and allosteric regulation of ESCRT-III by Vps4 in yeast. J Mol Biol 428, 2392-2404.
36. Kremer JR, Mastronarde DN, McIntosh JR (1996). Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-76.
37. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P (2003). Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc Natl Acad Sci USA 100, 15764-15769.
38. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
39. Losko S, Kopp F, Kranz A, Kölling R (2001). Uptake of the ATP-binding cassette (ABC) transporter Ste6 into the yeast vacuole is blocked in the doa4 mutant. Mol Biol Cell 12, 1047-1059.
40. Luhtala N, Odorizzi G (2004). Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J Cell Biol 166, 717-729.
41. MacDonald C, Buchkovich NJ, Stringer DK, Emr SD, Piper RC (2012). Cargo ubiquitination is essential for multivesicular body intralumenal vesicle formation. EMBO Rep 13, 331-338.
42. Mastronarde DN (1997). Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120, 343-352.
43. Mastronarde DN (2005). Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152, 36-51.
44. McNatt M, McKittrick I, West M, Odorizzi G (2007). Direct binding to Rsp5 mediates ubiquitin-independent sorting of Sna3 via the multivesicular body pathway. Mol Biol Cell 18, 697-706.
45. 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.
46. 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.
47. Odorizzi G, Katzmann DJ, Babst M, Audhya A, Emr SD (2003). Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae. J Cell Sci 116, 1893-1903.
48. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015). ESCRT-III controls nuclear envelope reformation. Nature 522, 236-239.
49. O'Toole ET, Winey M, McIntosh JR, Mastronarde DN (2002). Electron tomography of yeast cells. Methods Enzymol 351, 81-95.
50. Panavas T, Serviene E, Brasher J, Nagy P (2005). Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc Natl Acad Sci USA 102, 7326-7331.
51. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (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.
52. Richter C, West M, Odorizzi G (2007). Dual mechanisms specify Doa4-mediated deubiquitination at multivesicular bodies. EMBO J 26, 2454-2464.
53. Richter C, West M, Odorizzi G (2013). Doa4 function in ILV budding is restricted through its interaction with the Vps20 subunit of ESCRT-III. J Cell Sci 126, 1881-1890.
54. Rieder SE, Banta LM, Köhrer K, McCaffery JM, Emr SD (1996). Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol Biol Cell 7, 985-999.
55. Robinson JS, Klionsky DJ, Banta LM, Emr SD (1988). Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8, 4936-4948.
56. Sachse M, Strous GJ, Klumperman J (2004). ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. J Cell Sci 117, 1699-1708.
57. Saksena S, Wahlman J, Teis D, Johnson A, Emr S (2009). Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97-109.
58. Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008). A role for the ESCRT system in cell division in Archaea. Science 322, 1710-1713.
59. Schöneberg J, Lee I-HH, Iwasa JH, Hurley JH (2017). Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18, 5-17.
60. Shen Q-TT, Schuh AL, Zheng Y, Quinney K, Wang L, Hanna M, Mitchell JC, Otegui MS, Ahlquist P, Cui Q, et al. (2014). Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly. J Cell Biol 206, 763-777.
61. Shim S, Kimpler LA, Hanson PI (2007). Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8, 1068-1079.
62. Spormann DO, Heim J, Wolf DH (1992). Biogenesis of the yeast vacuole (lysosome). The precursor forms of the soluble hydrolase carboxypeptidase yscS are associated with the vacuolar membrane. J Biol Chem 267, 8021-8029.
63. Stuchell-Brereton MD, Skalicky JJ, Kieffer C, Karren MA, Ghaffarian S, Sundquist WI (2007). ESCRT-III recognition by VPS4 ATPases. Nature 449, 740-744.
64. Swaminathan S, Amerik AY, Hochstrasser M (1999). The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol Biol Cell 10, 2583-2594.
65. Tan S (2001). A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr Purif 21, 224-234.
66. Tang S, Buchkovich NJ, Henne WM, Banjade S, Kim YJ, Emr SD (2016). ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis. Elife 5, e15507.
67. Teis D, Saksena S, Emr S (2008). Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev Cell 15, 578-589.
68. Teis D, Saksena S, Judson BL, Emr SD (2010). ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J 29, 871-883.
69. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW, Christ L, Thoresen SB, Brech A, Raiborg C, Stenmark H (2015). Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522, 231-235.
70. Wang X, Diaz A, Hao L, Gancarz B, den Boon JA, Ahlquist P (2011). Intersection of the multivesicular body pathway and lipid homeostasis in RNA replication by a positive-strand RNA virus. J Virol 85, 5494-5503.
71. Webster BM, Colombi P, Jäger J, Lusk CP (2014). Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159, 388-401.
72. Wemmer M, Azmi I, West M, Davies B, Katzmann D, Odorizzi G (2011). Bro1 binding to Snf7 regulates ESCRT-III membrane scission activity in yeast. J Cell Biol 192, 295-306.
73. Wollert T, Hurley JH (2010). Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869.
74. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009). Membrane scission by the ESCRT-III complex. Nature 458, 172-177.
75. Wolters N, Amerik A (2015). The N-terminal domains determine cellular localization and functions of the Doa4 and Ubp5 deubiquitinating enzymes. Biochem Biophys Res Commun 467, 570-576.