ESCRTS function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins

eLife

Volumn 6, Issue , 2017, Pages

  Zhu, Lu ^a,b   Jorgensen, Jeff R ^a,b   Li, Ming ^a,c   Chuang, Ya Shan ^a,b   Emr, Scott D ^a  

^a School of Integrative Plant Sciences   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; MEMBRANE PROTEIN; RAPAMYCIN; UBIQUITINATED PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN;

ARTICLE; CELL LYSATE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENETIC SCREENING; GENETIC SELECTION; IMMUNOPRECIPITATION; LYSOSOME MEMBRANE; MEMBRANE FUSION; MUTAGENESIS; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; UBIQUITINATION; WESTERN BLOTTING; GENETICS; LYSOSOME; METABOLISM; SACCHAROMYCES CEREVISIAE;

DOWN-REGULATION; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENETIC TESTING; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; SACCHAROMYCES CEREVISIAE; UBIQUITINATION;

EID: 85027172280     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.26403     Document Type: Article

References (55)

1. Amerik AY, Nowak J, Swaminathan S, Hochstrasser M. 2000. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Molecular Biology of the Cell 11:3365–3380. doi: 10.1091/mbc.11.10.3365, PMID: 11029042
2. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD. 2002. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Developmental Cell 3:283–289. doi: 10.1016/S1534-5807(02)00219-8, PMID: 12194858
3. Babst M, Odorizzi G, Estepa EJ, Emr SD. 2000. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1:248–258. doi: 10.1034/j.1600-0854.2000.010307.x, PMID: 11208108
4. Babst M, Sato TK, Banta LM, Emr SD. 1997. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. The EMBO Journal 16:1820–1831. doi: 10.1093/emboj/16.8.1820, PMID: 9155008
5. 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. The EMBO Journal 17:2982–2993. doi: 10.1093/emboj/17.11.2982, PMID: 9606181
6. Banaszynski LA, Liu CW, Wandless TJ. 2005. Characterization of the fkbp.rapamycin.frb ternary complex. Journal of the American Chemical Society 127:4715–4721. doi: 10.1021/ja043277y, PMID: 15796538
7. Buchkovich NJ, Henne WM, Tang S, Emr SD. 2013. Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Developmental Cell 27:201–214. doi: 10.1016/j.devcel.2013.09.009, PMID: 24139821
8. Carlton JG, Martin-Serrano J. 2007. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316:1908–1912. doi: 10.1126/science.1143422, PMID: 17556548
9. Cheever ML, Sato TK, de Beer T, Kutateladze TG, Emr SD, Overduin M. 2001. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nature Cell Biology 3:613–618. doi: 10.1038/35083000, PMID: 11433291
10. Clarke BL, Weigel PH. 1985. Recycling of the asialoglycoprotein receptor in isolated rat hepatocytes. ATP depletion blocks receptor recycling but not a single round of endocytosis. The Journal of Biological Chemistry 260:128–133. PMID: 3965443
11. Foster KG, Fingar DC. 2010. Mammalian target of rapamycin (mTOR): conducting the cellular signaling symphony. Journal of Biological Chemistry 285:14071–14077. doi: 10.1074/jbc.R109.094003, PMID: 20231296
12. Gahl WA, Thoene JG, Schneider JA. 2002. Cystinosis. New England Journal of Medicine 347:111–121. doi: 10. 1056/NEJMra020552, PMID: 12110740
13. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Côté M, Rich RL, Myszka DG, Sundquist WI. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55–65. doi: 10.1016/S0092-8674(01)00506-2, PMID: 11595185
14. Gerrard SR, Bryant NJ, Stevens TH. 2000. VPS21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. Molecular Biology of the Cell 11:613–626. doi: 10.1091/mbc.11.2.613, PMID: 10679018
15. Gietz RD, Schiestl RH. 2007. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols 2:31–34. doi: 10.1038/nprot.2007.13, PMID: 17401334
16. Henne WM, Buchkovich NJ, Emr SD. 2011. The ESCRT pathway. Developmental Cell 21:77–91. doi: 10.1016/j. devcel.2011.05.015, PMID: 21763610
17. 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. doi: 10.1016/j.cell.2012.08.039, PMID: 23063125
18. Herman PK, Stack JH, DeModena JA, Emr SD. 1991. A novel protein kinase homolog essential for protein sorting to the yeast lysosome-like vacuole. Cell 64:425–437. doi: 10.1016/0092-8674(91)90650-N, PMID: 1 988155
19. 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. doi: 10.1126/science.1247136, PMID: 24482116
20. Jun Y, Xu H, Thorngren N, Wickner W. 2007. Sec18p and Vam7p remodel trans-SNARE complexes to permit a lipid-anchored R-SNARE to support yeast vacuole fusion. The EMBO Journal 26:4935–4945. doi: 10.1038/sj. emboj.7601915, PMID: 18007597
21. Katzmann DJ, Stefan CJ, Babst M, Emr SD. 2003. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. The Journal of Cell Biology 162:413–423. doi: 10.1083/jcb.200302136, PMID: 12900393
22. Komander D, Reyes-Turcu F, Licchesi JD, Odenwaelder P, Wilkinson KD, Barford D. 2009. Molecular discrimination of structurally Equivalent Lys 63-linked and Linear polyubiquitin chains. EMBO Reports 10:466– 473. doi: 10.1038/embor.2009.55, PMID: 19373254
23. 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. doi: 10.1126/science.1161070, PMID: 18687924
24. Lee HH, Elia N, Ghirlando R, Lippincott-Schwartz J, Hurley JH. 2008. Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 322:576–580. doi: 10.1126/science.1162042, PMID: 18948538
25. Li M, Koshi T, Emr SD. 2015a. Membrane-anchored ubiquitin ligase complex is required for the turnover of lysosomal membrane proteins. The Journal of Cell Biology 211:639–652. doi: 10.1083/jcb.201505062, PMID: 26527740
26. Li M, Rong Y, Chuang YS, Peng D, Emr SD. 2015b. Ubiquitin-dependent lysosomal membrane protein sorting and degradation. Molecular Cell 57:467–478. doi: 10.1016/j.molcel.2014.12.012, PMID: 25620559
27. MacDonald C, Buchkovich NJ, Stringer DK, Emr SD, Piper RC. 2012. Cargo ubiquitination is essential for multivesicular body intralumenal vesicle formation. EMBO Reports 13:331–338. doi: 10.1038/embor.2012.18, PMID: 22370727
28. Martin-Serrano J, Zang T, Bieniasz PD. 2001. HIV-1 and ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nature Medicine 7:1313–1319. doi: 10.1038/nm1201-1313, PMID: 11726971
29. Mayer A, Wickner W, Haas A. 1996. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85:83–94. doi: 10.1016/S0092-8674(00)81084-3, PMID: 8620540
30. Mayers JR, Fyfe I, Schuh AL, Chapman ER, Edwardson JM, Audhya A. 2011. ESCRT-0 assembles as a heterotetrameric complex on membranes and binds multiple ubiquitinylated cargoes simultaneously. Journal of Biological Chemistry 286:9636–9645. doi: 10.1074/jbc.M110.185363, PMID: 21193406
31. McNally EK, Karim MA, Brett CL. 2017. Selective lysosomal transporter degradation by Organelle membrane fusion. Developmental Cell 40:151–167. doi: 10.1016/j.devcel.2016.11.024, PMID: 28017618
32. Miesenböck G, De Angelis DA, Rothman JE. 1998. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–195. doi: 10.1038/28190, PMID: 9671304
33. Nathan JA, Kim HT, Ting L, Gygi SP, Goldberg AL. 2013. Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? The EMBO Journal 32:552–565. doi: 10.1038/emboj.2012.354, PMID: 23314748
34. Novick P, Field C, Schekman R. 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:205–215. doi: 10.1016/0092-8674(80)90128-2, PMID: 6996832
35. 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. doi: 10.1016/S0092-8674(00)81707-9, PMID: 9865702
36. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG. 2015. ESCRT-III controls nuclear envelope reformation. Nature 522:236–239. doi: 10.1038/nature14503, PMID: 26040713
37. Parkinson-Lawrence EJ, Shandala T, Prodoehl M, Plew R, Borlace GN, Brooks DA. 2010. Lysosomal storage disease: revealing lysosomal function and physiology. Physiology 25:102–115. doi: 10.1152/physiol.00041.2009, PMID: 20430954
38. Piper RC, Cooper AA, Yang H, Stevens TH. 1995. VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. The Journal of Cell Biology 131:603–617. doi: 10.1083/jcb.131.3.603, PMID: 7593183
39. Prosser DC, Whitworth K, Wendland B. 2010. Quantitative analysis of endocytosis with cytoplasmic pHluorin chimeras. Traffic 11:1141–1150. doi: 10.1111/j.1600-0854.2010.01088.x, PMID: 20626707
40. Rieder SE, Emr SD. 1997. A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Molecular Biology of the Cell 8:2307–2327. doi: 10.1091/mbc.8.11.2307, PMID: 9362071
41. Robinson JS, Graham TR, Emr SD. 1991. A putative zinc finger protein, Saccharomyces cerevisiae Vps18p, affects late Golgi functions required for vacuolar protein sorting and efficient alpha-factor prohormone maturation. Molecular and Cellular Biology 11:5813–5824. doi: 10.1128/MCB.11.12.5813, PMID: 1840635
42. Sato TK, Darsow T, Emr SD. 1998. Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking. Molecular and Cellular Biology 18:5308–5319. doi: 10.1128/MCB. 18.9.5308, PMID: 9710615
43. Schmid SL, Carter LL. 1990. ATP is required for receptor-mediated endocytosis in intact cells. The Journal of Cell Biology 111:2307–2318. doi: 10.1083/jcb.111.6.2307, PMID: 2126013
44. Schulze H, Sandhoff K. 2011. Lysosomal lipid storage diseases. Cold Spring Harbor Perspectives in Biology 3: a004804. doi: 10.1101/cshperspect.a004804, PMID: 21502308
45. Shaner NC, Lambert GG, Chammas A, Ni Y, Cranfill PJ, Baird MA, Sell BR, Allen JR, Day RN, Israelsson M, Davidson MW, Wang J. 2013. A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nature Methods 10:407–409. doi: 10.1038/nmeth.2413, PMID: 23524392
46. Terpe K. 2003. Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Applied Microbiology and Biotechnology 60:523–533. doi: 10.1007/s00253-002-1158-6, PMID: 12536251
47. Tran JH, Chen CJ, Emr S, Schekman R. 2009. Cargo sorting into multivesicular bodies in vitro. PNAS 106:17395– 17400. doi: 10.1073/pnas.0909473106, PMID: 19805166
48. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA. 2001. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). PNAS 98:7724–7729. doi: 10.1073/pnas.131059198, PMID: 11427703
49. Vida TA, Emr SD. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. The Journal of Cell Biology 128:779–792. doi: 10.1083/jcb.128.5.779, PMID: 7533169
50. 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. doi: 10.1038/nature14408, PMID: 26040712
51. Vitner EB, Platt FM, Futerman AH. 2010. Common and uncommon pathogenic cascades in lysosomal storage diseases. Journal of Biological Chemistry 285:20423–20427. doi: 10.1074/jbc.R110.134452, PMID: 20430897
52. Webster BM, Colombi P, Jäger J, Lusk CP. 2014. Surveillance of nuclear pore complex assembly by ESCRT-III/ Vps4. Cell 159:388–401. doi: 10.1016/j.cell.2014.09.012, PMID: 25303532
53. Wickner W. 2010. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annual Review of Cell and Developmental Biology 26:115–136. doi: 10. 1146/annurev-cellbio-100109-104131, PMID: 20521906
54. Wollert T, Hurley JH. 2010. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464:864–869. doi: 10.1038/nature08849, PMID: 20305637
55. Xu H, Ren D. 2015. Lysosomal physiology. Annual Review of Physiology 77:57–80. doi: 10.1146/annurev-physiol-021014-071649, PMID: 25668017