The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells

Molecular Biology of the Cell

Volumn 23, Issue 7, 2012, Pages 1231-1242

  Liu, I Chun ^a,b,c   Chiu, Sheng Wen ^a,d   Lee, Hsin Yi ^a   Leu, Jun Yi ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GLUCOSE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 26; HEAT SHOCK PROTEIN 42; HISTONE DEACETYLASE; MUTANT PROTEIN; PROTEIN HOS 2; PROTEIN YCA1; SILENT INFORMATION REGULATOR PROTEIN 2; UNCLASSIFIED DRUG;

ARTICLE; CELL GRANULE; CELL VIABILITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CYTOPLASM; CYTOSOL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ACTIN CYTOSKELETON; CYTOPLASMIC GRANULES; EPIGENESIS, GENETIC; G0 PHASE; GENES, FUNGAL; GLUCOSE; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HISTONE DEACETYLASES; MUTATION; PROTEIN MULTIMERIZATION; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84859375205     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-09-0752     Document Type: Article

References (72)

1. An S, Kumar R, Sheets ED, Benkovic SJ (2008). Reversible compartmentalization of de novo purine biosynthetic complexes in living cells. Science 320, 103-106. (Pubitemid 351490764)
2. Anderson P, Kedersha N (2008). Stress granules: the Tao of RNA triage. Trends Biochem Sci 33, 141-150.
3. Anderson P, Kedersha N (2009). RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 10, 430-436.
4. Bitterman KJ, Medvedik O, Sinclair DA (2003). Longevity regulation in Saccharomyces cerevisiae: linking metabolism, genome stability, and heterochromatin. Microbiol Mol Biol Rev 67, 376-399. (Pubitemid 37122526)
5. Bolte S, Cordelieres FP (2006). A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224, 213-232. (Pubitemid 46010930)
6. Brengues M, Parker R (2007). Accumulation of polyadenylated mRNA, Pab1p, eIF4E, and eIF4G with P-bodies in Saccharomyces cerevisiae. Mol Biol Cell 18, 2592-2602. (Pubitemid 47025724)
7. Buchan JR, Muhlrad D, Parker R (2008). P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183, 441-455.
8. Buchan JR, Parker R (2009). Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36, 932-941.
9. Burtner CR, Murakami CJ, Kennedy BK, Kaeberlein M (2009). A molecular mechanism of chronological aging in yeast. Cell Cycle 8, 1256-1270.
10. Camblong J, Iglesias N, Fickentscher C, Dieppois G, Stutz F (2007). Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell 131, 706-717. (Pubitemid 350087198)
11. Cebollero E, Reggiori F (2009). Regulation of autophagy in yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1793, 1413-1421.
12. Chen Q, Ding Q, Keller JN (2005). The stationary phase model of aging in yeast for the study of oxidative stress and age-related neurodegeneration. Biogerontology 6, 1-13. (Pubitemid 41583288)
13. Choder M (1991). A general topoisomerase I-dependent transcriptional repression in the stationary phase in yeast. Genes Dev 5, 2315-2326.
14. Cohen TJ, Mallory MJ, Strich R, Yao TP (2008). Hos2p/Set3p deacetylase complex signals secretory stress through the Mpk1p cell integrity pathway. Eukaryot Cell 7, 1191-1199. (Pubitemid 351969333)
15. Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, Holstege FC, Weissman JS, Krogan NJ (2007). Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics 6, 439-450. (Pubitemid 46554539)
16. Costanzo M et al. (2010). The genetic landscape of a cell. Science 327, 425-431.
17. Cuesta R, Laroia G, Schneider RJ (2000). Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 14, 1460-1470. (Pubitemid 30421839)
18. Davie JK, Edmondson DG, Coco CB, Dent SY (2003). Tup1-Ssn6 interacts with multiple class I histone deacetylases in vivo. J Biol Chem 278, 50158-50162. (Pubitemid 37548854)
19. DeRisi JL, Iyer VR, Brown PO (1997). Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278, 680-686. (Pubitemid 27464965)
20. Dezwaan DC, Freeman BC (2008). HSP90: the Rosetta stone for cellular protein dynamics? Cell Cycle 7, 1006-1012.
21. Ellis RJ (2006). Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31, 395-401.
22. Ellis RJ, Minton AP (2006). Protein aggregation in crowded environments. Biol Chem 387, 485-497. (Pubitemid 44071450)
23. Erickson SL, Lykke-Andersen J (2011). Cytoplasmic mRNP granules at a glance. J Cell Sci 124, 293-297.
24. Eyles SJ, Gierasch LM (2010). Nature's molecular sponges: small heat shock proteins grow into their chaperone roles. Proc Natl Acad Sci USA 107, 2727-2728.
25. Fabrizio P, Hoon S, Shamalnasab M, Galbani A, Wei M, Giaever G, Nislow C, Longo VD (2010). Genome-wide screen in Saccharomyces cerevisiae identifies vacuolar protein sorting, autophagy, biosynthetic, and tRNA methylation genes involved in life span regulation. PLoS Genet 6, e1001024.
26. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11, 4241-4257.
27. Gavin AC et al. (2006). Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636.
28. Ge H, Wei M, Fabrizio P, Hu J, Cheng C, Longo VD, Li LM (2010). Comparative analyses of time-course gene expression profiles of the long-lived sch9¥ Ä mutant. Nucleic Acids Res 38, 143-158.
29. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, Anderson P (2004). Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15, 5383-5398. (Pubitemid 39564732)
30. Gong Y, Kakihara Y, Krogan N, Greenblatt J, Emili A, Zhang Z, Houry WA (2009). An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Mol Syst Biol 5, 275.
31. Gray JV, Petsko GA, Johnston GC, Ringe D, Singer RA, Werner-Washburne M (2004). "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 68, 187-206. (Pubitemid 38756862)
32. Grousl T et al. (2009). Robust heat shock induces eIF2α- phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J Cell Sci 122, 2078-2088.
33. Guan KL, Xiong Y (2011). Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci 36, 108-116.
34. Guarente L (2000). Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14, 1021-1026.
35. Haigis MC, Guarente LP (2006). Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev 20, 2913-2921. (Pubitemid 44771725)
36. Haslbeck M, Braun N, Stromer T, Richter B, Model N, Weinkauf S, Buchner J (2004). Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23, 638-649. (Pubitemid 38282395)
37. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005). Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12, 842-846. (Pubitemid 41486706)
38. Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich KU, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004). Chronological aging leads to apoptosis in yeast. J Cell Biol 164, 501-507. (Pubitemid 38233311)
39. Howson R, Huh WK, Ghaemmaghami S, Falvo JV, Bower K, Belle A, Dephoure N, Wykoff DD, Weissman JS, O'Shea EK (2005). Construction, verification and experimental use of two epitope-tagged collections of budding yeast strains. Comp Funct Genomics 6, 2-16. (Pubitemid 40450605)
40. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK (2003). Global analysis of protein localization in budding yeast. Nature 425, 686-691. (Pubitemid 37314307)
41. Imai S, Guarente L (2010). Ten years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases. Trends Pharmacol Sci 31, 212-220.
42. Kaeberlein M (2010). Lessons on longevity from budding yeast. Nature 464, 513-519.
43. Kim S, Benguria A, Lai CY, Jazwinski SM (1999). Modulation of life-span by histone deacetylase genes in Saccharomyces cerevisiae. Mol Biol Cell 10, 3125-3136. (Pubitemid 29489550)
44. Kraft C, Deplazes A, Sohrmann M, Peter M (2008). Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 10, 602-610. (Pubitemid 351627380)
45. Kushnirov VV (2000). Rapid and reliable protein extraction from yeast. Yeast 16, 857-860.
46. Kwon S, Zhang Y, Matthias P (2007). The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev 21, 3381-3394.
47. Laemmli UK (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
48. Lamming DW, Latorre-Esteves M, Medvedik O, Wong SN, Tsang FA, Wang C, Lin SJ, Sinclair DA (2005). HST2 mediates SIR2-independent life-span extension by calorie restriction. Science 309, 1861-1864. (Pubitemid 41325097)
49. Laporte D, Lebaudy A, Sahin A, Pinson B, Ceschin J, Daignan-Fornier B, Sagot I (2011). Metabolic status rather than cell cycle signals control quiescence entry and exit. J Cell Biol 192, 949-957.
50. Laporte D, Salin B, Daignan-Fornier B, Sagot I (2008). Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol 181, 737-745. (Pubitemid 351786980)
51. Lee RE, Brunette S, Puente LG, Megeney LA (2010). Metacaspase Yca1 is required for clearance of insoluble protein aggregates. Proc Natl Acad Sci USA 107, 13348-13353.
52. MacLean M, Harris N, Piper PW (2001). Chronological lifespan of stationary phase yeast cells; a model for investigating the factors that might influence the ageing of postmitotic tissues in higher organisms. Yeast 18, 499-509. (Pubitemid 32318332)
53. Martinez MJ et al. (2004). Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol Biol Cell 15, 5295-5305. (Pubitemid 39564725)
54. Mellert HS, McMahon SB (2009). Biochemical pathways that regulate acetyl-transferase and deacetylase activity in mammalian cells. Trends Biochem Sci 34, 571-578.
55. Minton AP (2001). The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276, 10577-10580.
56. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y (2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10, 458-467.
57. Narayanaswamy R, Levy M, Tsechansky M, Stovall GM, O'Connell JD, Mirrielees J, Ellington AD, Marcotte EM (2009). Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc Natl Acad Sci USA 106, 10147-10152.
58. Patel HV, Vyas KA, Li X, Savtchenko R, Roseman S (2004). Subcellular distribution of enzyme I of the Escherichia coli phosphoenolpyruvate:glycose phosphotransferase system depends on growth conditions. Proc Natl Acad Sci USA 101, 17486-17491. (Pubitemid 39662756)
59. Pijnappel WW, Schaft D, Roguev A, Shevchenko A, Tekotte H, Wilm M, Rigaut G, Seraphin B, Aasland R, Stewart AF (2001). The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev 15, 2991-3004. (Pubitemid 33078949)
60. Powers RW, III, Kaeberlein M, Caldwell SD, Kennedy BK, Fields S (2006). Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 20, 174-184.
61. Sagot I, Pinson B, Salin B, Daignan-Fornier B (2006). Actin bodies in yeast quiescent cells: an immediately available actin reserve? Mol Biol Cell 17, 4645-4655. (Pubitemid 44665735)
62. Sakahira H, Breuer P, Hayer-Hartl MK, Hartl FU (2002). Molecular chaperones as modulators of polyglutamine protein aggregation and toxicity. Proc Natl Acad Sci USA 99 (suppl 4), 16412-16418. (Pubitemid 35470987)
63. Sandmeier JJ, French S, Osheim Y, Cheung WL, Gallo CM, Beyer AL, Smith JS (2002). RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase. EMBO J 21, 4959-4968.
64. Stengel F, Baldwin AJ, Painter AJ, Jaya N, Basha E, Kay LE, Vierling E, Robinson CV, Benesch JL (2010). Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc Natl Acad Sci USA 107, 2007-2012.
65. Sun Y, MacRae TH (2005). Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62, 2460-2476. (Pubitemid 41801099)
66. Suzuki Y, Minami M, Suzuki M, Abe K, Zenno S, Tsujimoto M, Matsumoto K, Minami Y (2009). The Hsp90 inhibitor geldanamycin abrogates colocalization of eIF4E and eIF4E-transporter into stress granules and association of eIF4E with eIF4G. J Biol Chem 284, 35597-35604.
67. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371-382. (Pubitemid 40397171)
68. Thomas MG, Loschi M, Desbats MA, Boccaccio GL (2011). RNA granules: the good, the bad and the ugly. Cell Signal 23, 324-334.
69. Tudisca V, Recouvreux V, Moreno S, Boy-Marcotte E, Jacquet M, Portela P (2010). Differential localization to cytoplasm, nucleus or P-bodies of yeast PKA subunits under different growth conditions. Eur J Cell Biol 89, 339-348.
70. Wang A, Kurdistani SK, Grunstein M (2002). Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 298, 1412-1414. (Pubitemid 35346139)
71. Werner-Washburne M, Braun E, Johnston GC, Singer RA (1993). Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev 57, 383-401. (Pubitemid 23170098)
72. Wilkinson CR, Wallace M, Morphew M, Perry P, Allshire R, Javerzat JP, McIntosh JR, Gordon C (1998). Localization of the 26S proteasome during mitosis and meiosis in fission yeast. EMBO J 17, 6465-6476. (Pubitemid 28521782)