Selective Lysosomal Transporter Degradation by Organelle Membrane Fusion

Developmental Cell

Volumn 40, Issue 2, 2017, Pages 151-167

  McNally, Erin Kate ^a   Karim, Mahmoud Abdul ^a   Brett, Christopher Leonard ^a  

^a Civil and Environmental Engineering   (Canada)

Author keywords

intralumenal fragment; lysosomal transporter; lysosome biology; membrane fusion; multivesicular body; protein degradation; protein quality control; TOR; vacuole

Indexed keywords

CARRIER PROTEIN; CELL MEMBRANE PROTEIN; CELL PROTEIN; HYDROLASE; LYSOSOMAL TRANSPORTER; SACCHAROMYCES CEREVISIAE PROTEIN; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG; CYCLOHEXIMIDE; ESCRT PROTEIN; GREEN FLUORESCENT PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CELL FUNCTION; CELL METABOLISM; CELL ORGANELLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCYTOSIS; HOMEOSTASIS; INTERNALIZATION; LYSOSOME; LYSOSOME MEMBRANE; MEMBRANE FUSION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MISFOLDING; PROTEIN TARGETING; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; AUTOPHAGY; DRUG EFFECTS; METABOLISM; PH; PROTEIN TRANSPORT;

AUTOPHAGY; CYCLOHEXIMIDE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; LYSOSOMES; MEMBRANE FUSION; MEMBRANE TRANSPORT PROTEINS; PROTEIN TRANSPORT; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 85010046704     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.11.024     Document Type: Article

References (68)

1. Aris, J.P., Fishwick, L.K., Marraffini, M.L., Seo, A.Y., Leeuwenburgh, C., Dunn, W.A., Amino acid homeostasis and chronological longevity in Saccharomyces cerevisiae. Subcell. Biochem. 51 (2012), 161–186.
2. Babst, M., MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr. Opin. Cell Biol. 23 (2011), 452–457.
3. Babst, M., Quality control at the plasma membrane: one mechanism does not fit all. J. Cell Biol. 205 (2014), 11–20.
4. Balderhaar, H.J.K., Ungermann, C., CORVET and HOPS tethering complexes—coordinators of endosome and lysosome fusion. J. Cell Sci. 126 (2013), 1307–1316.
5. Berger, A.C., Hanson, P.K., Nichols, J.W., Corbett, A.H., A yeast model system for functional analysis of the Niemann-Pick type C protein 1 homolog, Ncr1p. Traffic 6 (2005), 907–917.
6. + exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol. Biol. Cell 16 (2005), 1396–1405.
7. Brett, C.L., Plemel, R.L., Lobingier, B.T., Vignali, M., Fields, S., Merz, A.J., Efficient termination of vacuolar Rab GTPase signaling requires coordinated action by a GAP and a protein kinase. J. Cell Biol. 182 (2008), 1141–1151.
8. Cabrera, M., Ungermann, C., Purification and in vitro analysis of yeast vacuoles. Methods Enzymol. 451 (2008), 177–196.
9. Carlsson, S.R., Simonsen, A., Membrane dynamics in autophagosome biogenesis. J. Cell Sci. 128 (2015), 193–205.
10. Cary, G.A., Yoon, S.H., Torres, C.G., Wang, H., Hays, M., Ludlow, C., Goodlett, D.R., Dudley, A.M., Identification and characterization of a drug-sensitive strain enables puromycin-based translational assays in Saccharomyces cerevisiae. Yeast 31 (2014), 167–178.
11. Chen, B., Retzlaff, M., Roos, T., Frydman, J., Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol., 3, 2011, a004374.
12. D'Agostino, M., Risselada, H.J., Mayer, A., Steric hindrance of SNARE transmembrane domain organization impairs the hemifusion-to-fusion transition. EMBO Rep. 17 (2016), 1590–1608.
13. Davis, N.G., Horecka, J.L., Sprague, G.F. Jr., Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122 (1993), 53–65.
14. de Duve, C., Wattiaux, R., Functions of lysosomes. Annu. Rev. Physiol. 28 (1966), 435–492.
15. Diakov, T.T., Kane, P.M., Regulation of vacuolar proton-translocating ATPase activity and assembly by extracellular pH. J. Biol. Chem. 285 (2010), 23771–23778.
16. Dhonukshe, P., Baluška, F., Schlicht, M., Hlavacka, A., Šamaj, J., Friml, J., Gadella, T.W.J., Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev. Cell 10 (2006), 137–150.
17. Efeyan, A., Zoncu, R., Sabatini, D.M., Amino acids and mTORC1: from lysosomes to disease. Trends Mol. Med. 18 (2012), 524–533.
18. Ehrnstorfer, I.A., Geertsma, E.R., Pardon, E., Steyaert, J., Dutzler, R., Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport. Nat. Strcut. Mol. Biol. 11 (2011), 990–996.
19. Eitzen, G., Will, E., Gallwitz, D., Haas, A., Wickner, W.T., Sequential action of two GTPases to promote vacuole docking and fusion. EMBO J. 19 (2000), 6713–6720.
20. Fang, N.N., Chan, G.T., Zhu, M., Comyn, S.A., Persaud, A., Deshaies, R.J., Rotin, D., Gsponer, J., Mayor, T., Rsp5/Nedd4 is the main ubiquitin ligase that targets cytosolic misfolded proteins following heat stress. Nat. Cell Biol. 16 (2014), 1227–1237.
21. Fratti, R.A., Jun, Y., Merz, A.J., Margolis, N., Wickner, W.T., Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J. Cell Biol. 167 (2004), 1087–1098.
22. Forgac, M., Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8 (2007), 917–929.
23. Ghaddar, K., Merhl, A., Saliba, E., Krammer, E., Prévost, M., Bruno, A., Substrate-induced ubiquitylation and endocytosis of yeast amino acid permeases. Mol. Cell Biol. 34 (2014), 4447–4463.
24. Haas, A., A quantitative assay to measure homotypic vacuole fusion in vitro. Methods Cell Sci. 17 (1995), 283–294.
25. Heitman, J., Movva, N.R., Hall, M.N., Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253 (1991), 905–909.
26. Hennigar, S.R., Kelleher, S.L., TNFα post-translationally targets ZnT2 to accumulate zinc in lysosomes. J. Cell Physiol. 10 (2015), 2345–2350.
27. Jiang, P., Nishimura, T., Sakamaki, Y., Itakura, E., Hatta, T., Natsume, T., Mizushima, N., The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol. Biol. Cell 25 (2014), 1327–1337.
28. Jun, Y., Wickner, W.T., Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc. Natl. Acad. Sci. USA 104 (2007), 13010–13015.
29. Jun, Y., Thorngren, N., Starai, V.J., Fratti, R.A., Collins, K., Wickner, W.T., Reversible, cooperative reactions of yeast vacuole docking. EMBO J. 25 (2006), 5260–5269.
30. Jung, J., Genau, H.M., Behrends, C., Amino acid-dependent mTORC1 regulation by the lysosomal membrane protein SLC38A9. Mol. Cell Biol. 14 (2015), 2479–2494.
31. Katzmann, D.J., Babst, M., Emr, S.D., Ubiquitin-dependent sorting into the MultiVesicular Body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106 (2001), 145–155.
32. Keener, J.M., Babst, M., Quality control and substrate-dependent downregulation of the nutrient transporter Fur4. Traffic 14 (2013), 412–427.
33. Kiss, K., Kucsma, N., Brozik, A., Tusnady, G.E., Bergam, P., van Niel, G., Szakacs, G., Role of the N-terminal transmembrane domain in the endo-lysosomal targeting and function of the human ABCB6 protein. J. Biochem. 1 (2015), 127–139.
34. Kolter, T., Sandhoff, K., Principles of lysosome membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anion lysosomal lipids. Annu. Rev. Cell Dev. Biol. 21 (2005), 81–103.
35. Li, M., Rong, Y., Chuang, Y., Peng, D., Emr, S.D., Ubiquitin-dependent lysosomal membrane protein sorting and degradation. Mol. Cell 57 (2015), 467–478.
36. Li, M., Koshi, T., Emr, S.D., Membrane-anchored ubiquitin ligase complex is required for the turnover of lysosomal membrane proteins. J. Cell Biol. 211 (2015), 639–652.
37. Loewith, R., Hall, M.N., Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189 (2011), 1177–1201.
38. Luzio, J.P., Parkinson, M.D.J., Gray, S.R., Bright, N.A., The delivery of endocytosed cargo to lysosomes. Biochem. Soc. Trans. 37 (2009), 1019–1021.
39. MacDonald, I.R., Ellis, R.J., Does cycloheximide inhibit protein synthesis specifically in plant tissues?. Nature 222 (1969), 791–792.
40. MacDonald, C., Stringer, D.K., Piper, R.C., Sna3 is an Rsp5 adaptor protein that relies on ubiquitination for its MVB sorting. Traffic 13 (2012), 586–598.
41. MacGurn, J.A., Hsu, P., Smolka, M.B., Emr, S.D., TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147 (2011), 1104–1117.
42. Mageswaran, S.K., Johnson, N.K., Odorizzi, G., Babst, M., Constitutively active ESCRT-II suppresses the MVB-sorting phenotype of ESCRT-0 and ESCRT-I mutants. Mol. Biol. Cell 3 (2015), 554–568.
43. Mattie, S., McNally, E.M., Karim, M.A., Vali, H., Brett, C.L., How and why intralumenal membrane fragments form during vacuolar lysosome fusion. Mol. Biol. Cell, 2016, 10.1091/mbc.E15-11-0759.
44. Mayer, A., Wickner, W.T., Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J. Cell Biol. 136 (1997), 307–317.
45. Merz, A.J., Wickner, W.T., Resolution of organelle docking and fusion kinetics in a cell-free assay. Proc. Natl. Acad. Sci. USA 101 (2004), 11548–11553.
46. Michaillat, L., Baars, T.L., Mayer, A., Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol. Biol. Cell 23 (2012), 881–895.
47. McMahon, D., Cycloheximide is not a specific inhibitor of protein synthesis in vivo. Plant Physiol. 55 (1975), 815–821.
48. Nickerson, D.P., Russell, M.R.G., Odorizzi, G., A concentric circle model of multivesicular body cargo sorting. EMBO Rep. 8 (2007), 644–650.
49. Nickerson, D.P., Brett, C.L., Merz, A.J., Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21 (2009), 543–551.
50. Peng, J., Schwartz, D., Elias, J.E., Thoreen, C.C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D., Gygi, S.P., A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21 (2003), 921–926.
51. Pokrzywa, W., Guerriat, B., Dodzian, J., Morsomme, P., Dual sorting of the Saccharomyces cerevisiae vacuolar protein Sna4p. Eukaryot. Cell 8 (2009), 278–286.
52. Prosser, D.C., Whitworth, K., Wendland, B., Quantitative analysis of endocytosis with cytoplasmic pHluorin chimeras. Traffic 11 (2010), 1141–1150.
53. Rak, A., Fedorov, R., Alexandrov, K., Albert, S., Goody, R.S., Gallwitz, D., Scheidig, A.J., Crystal structure of the GAP domain of Gyp1p: first insights into interaction with Ypt/Rab proteins. EMBO J. 19 (2000), 5105–5113.
54. Schneider-Poetsch, T., Ju, J., Eyler, D.E., Dang, Y., Bhat, S., Merrick, W.C., Green, R., Shen, B., Liu, J.O., Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6 (2010), 209–217.
55. Schweigel-Rontgen, M., The families of zinc (SLC30 and SLC39) and copper (SCL31) transporters. Curr. Top. Membr. 73 (2014), 321–355.
56. Settembre, C., Fraldi, A., Medina, D.L., Ballabio, A., Signals for the lysosome: a control center for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14 (2013), 283–296.
57. Shields, S.B., Piper, R.C., How ubiquitin functions with ESCRTS. Traffic 10 (2011), 1306–1317.
58. + stimulation of astrocytic ATP release investigated using siRNA against ENT3. ASN Neuro, 4, 2014 1759091414543439 eCollection 2014.
59. Tarsio, M., Zheng, H., Smardon, A.M., Martinez-Munoz, G.A., Kane, P.M., Consequences of loss of Vph1 protein-containing vacuolar ATPases (V-ATPases) for overall cellular pH homeostasis. J. Biol. Chem. 286 (2011), 28089–28096.
60. Thorngren, N., Collins, K.M., Fratti, R.A., Wickner, W., Merz, A.J., A soluble SNARE drives rapid docking, bypassing ATP and Sec17/18p for vacuole fusion. EMBO J. 23 (2004), 2765–2776.
61. Urbanowski, J.L., Piper, R.C., The iron transporter Fth1 forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J. Biol. Chem. 274 (1999), 38061–38070.
62. Van Belle, D., André, B., A genomic view of yeast membrane transporters. Curr. Opin. Cell Biol. 13 (2001), 389–398.
63. Vembar, S.S., Brodsky, J.L., One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9 (2008), 944–957.
64. Waller-Evans, H., Lloyd-Evans, E., Regulation of TRPML1 function. Biochem. Soc. Trans. 43 (2015), 442–446.
65. Wang, L., Seeley, E.S., Wickner, W., Merz, A.J., Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle. Cell 108 (2002), 357–369.
66. Watanabe-Asano, T., Kuma, A., Mizushima, N., Cycloheximide inhibits starvation-induced autophagy through mTORC1 activation. Biochem. Biophys. Res. Commun. 445 (2014), 334–339.
67. Wickner, W., Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu. Rev. Cell Dev. Biol. 26 (2010), 115–136.
68. Wickner, W., Haas, A., Yeast homotypic vacuole fusion: a window on organelle trafficking mechanisms. Ann. Rev. Biochem. 69 (2000), 247–275.