Proteasome storage granules are transiently associated with the insoluble protein deposit in Saccharomyces cerevisiae

Journal of Cell Science

Volumn 129, Issue 6, 2016, Pages 1190-1197

  Peters, Lee Zeev ^a   Karmon, Ofri ^a   Miodownik, Shir ^a   Ben Aroya, Shay ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Insoluble protein deposit; IPOD; Proteasome; Proteasome storage granules; Protein quality control; PSGs; Saccharomyces cerevisiae

Indexed keywords

CARBON; INSOLUBLE PROTEIN DEPOSIT; PROTEASOME; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CELL GRANULE; CELL STRUCTURE; CONCEPTUAL FRAMEWORK; CYTOSOL; IN VITRO STUDY; INTRACELLULAR SPACE; NONHUMAN; PRIORITY JOURNAL; PROTEASOME STORAGE GRANULE; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN QUALITY; SACCHAROMYCES CEREVISIAE; STARVATION; YEAST CELL; GENETICS; METABOLISM;

CYTOSOL; HEAT-SHOCK PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84961226369     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.179648     Document Type: Article

References (35)

1. Amen, T. and Kaganovich, D. (2014). Dynamic droplets: the role of cytoplasmic inclusions in stress, function, and disease. Cell. Mol. Life Sci. 72, 401-415.
2. Bajorek, M., Finley, D. and Glickman, M. H. (2003). Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr. Biol. 13, 1140-1144.
3. Ben-Aroya, S., Agmon, N., Yuen, K., Kwok, T., McManus, K., Kupiec, M. and Hieter, P. (2010). Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet. 6, e1000852.
4. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P. and Boeke, J. D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
5. Breker, M., Gymrek, M. and Schuldiner, M. (2013). A novel single-cell screening platform reveals proteome plasticity during yeast stress responses. J. Cell Biol. 200, 839-850.
6. Ciechanover, A. (2005). Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ. 12, 1178-1190.
7. Enenkel, C., Lehmann, A. and Kloetzel, P.-M. (1999). GFP-labelling of 26S proteasomes in living yeast: insight into proteasomal functions at the nuclear envelope/rough ER. Mol. Biol. Rep. 26, 131-135.
8. Escusa-Toret, S., Vonk, W. I. m. and Frydman, J. (2013). Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat. Cell Biol. 15, 1231-1243.
9. Eyles, S. J. andGierasch, L. M. (2010). Nature'smolecular sponges:small heat shock proteins grow into their chaperone roles. Proc. Natl. Acad. Sci. USA 107, 2727-2728.
10. Fukunaga, K., Kudo, T., Toh-e, A., Tanaka, K. and Saeki, Y. (2010). Dissection of the assembly pathway of the proteasome lid in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 396, 1048-1053.
11. Goldstein, A. L. and McCusker, J. H. (1999). Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553.
12. Haslbeck, M., Miess, A., Stromer, T., Walter, S. and Buchner, J. (2005). Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J. Biol. Chem. 280, 23861-23868.
13. Hershko, A. and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425-479.
14. Hill, S. M., Hao, X., Liu, B. and Nystrom, T. (2014). Life-span extension by a metacaspase in the yeast Saccharomyces cerevisiae. Science 344, 1389-1392.
15. Kaganovich, D., Kopito, R. and Frydman, J. (2008). Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095.
16. Laporte, D., Salin, B., Daignan-Fornier, B. and Sagot, I. (2008). Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J. Cell Biol. 181, 737-745.
17. Laporte, D., Lebaudy, A., Sahin, A., Pinson, B., Ceschin, J., Daignan-Fornier, B. and Sagot, I. (2011). Metabolic status rather than cell cycle signals control quiescence entry and exit. J. Cell Biol. 192, 949-957.
18. Lev, I., Volpe, M., Goor, L., Levinton, N., Emuna, L. and Ben-Aroya, S. (2013). Reverse PCA, a systematic approach for identifying genes important for the physical interaction between protein pairs. PLoS Genet. 9, e1003838.
19. Liu, I.-C., Chiu, S.-W., Lee, H.-Y. and Leu, J.-Y. (2012). The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells. Mol. Biol. Cell 23, 1231-1242.
20. Longtine, M. S., McKenzie, A., III, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
21. Miller, S. B. M., Mogk, A. and Bukau, B. (2015). Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J. Mol. Biol. 427, 1564-1574.
22. Narayanaswamy, R., Levy, M., Tsechansky, M., Stovall, G. M., O'Connell, J. D., Mirrielees, J., Ellington, A. D. and Marcotte, E. M. (2009). Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc. Natl. Acad. Sci. USA 106, 10147-10152.
23. Peters, L. Z., Hazan, R., Breker, M., Schuldiner, M. and Ben-Aroya, S. (2013). Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J. Cell Biol. 201, 663-671.
24. Peters, L. Z., Karmon, O., David-Kadoch, G., Hazan, R., Yu, T., Glickman, M. H. and Ben-Aroya, S. (2015). The protein quality control machinery regulates its misassembled proteasome subunits. PLoS Genet. 11, e1005178.
25. Russell, S. J., Steger, K. A. and Johnston, S. A. (1999). Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J. Biol. Chem. 274, 21943-21952.
26. Saunier, R., Esposito, M., Dassa, E. P. and Delahodde, A. (2013). Integrity of the Saccharomyces cerevisiae Rpn11 protein is critical for formation of proteasome storage granules (PSG) and survival in stationary phase. PLoS ONE 8, e70357.
27. Specht, S., Miller, S. B. M., Mogk, A. and Bukau, B. (2011). Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J. Cell Biol. 195, 617-629.
28. Spokoini, R., Moldavski, O., Nahmias, Y., England, J. L., Schuldiner, M. and Kaganovich, D. (2012). Confinement to organelle-associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep. 2, 738-747.
29. Sun, Y. and MacRae, T. H. (2005). Small heat shock proteins: molecular structure and chaperone function. Cell. Mol. Life Sci. 62, 2460-2476.
30. Tanaka, K. (2009). The proteasome: overview of structure and functions. Proc. Jpn. Acad. B Phys. Biol. Sci. 85, 12-36.
31. Torres, E. M., Dephoure, N., Panneerselvam, A., Tucker, C. M., Whittaker, C. A., Gygi, S. P., Dunham, M. J. and Amon, A. (2010). Identification of aneuploidy-tolerating mutations. Cell 143, 71-83.
32. Tyedmers, J., Mogk, A. and Bukau, B. (2010). Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 11, 777-788.
33. Wang, Y., Meriin, A. B., Costello, C. E. and Sherman, M. Y. (2007). Characterization of proteins associated with polyglutamine aggregates: a novel approach towards isolation of aggregates from protein conformation disorders. Prion 1, 128-135.
34. Wilkinson, C. R. M., Wallace, M., Morphew, M., Perry, P., Allshire, R., Javerzat, J.-P., McIntosh, J. R. and Gordon, C. (1998). Localization of the 26S proteasome during mitosis and meiosis in fission yeast. EMBO J. 17, 6465-6476.
35. Yang, Z., Stone, D. E. and Liebman, S.W. (2014). Prion-promoted phosphorylation of heterologous amyloid is coupled with ubiquitin-proteasome system inhibition and toxicity. Mol. Microbiol. 93, 1043-1056.