Dynamic Sumoylation of a Conserved Transcription Corepressor Prevents Persistent Inclusion Formation during Hyperosmotic Stress

PLoS Genetics

Volumn 12, Issue 1, 2016, Pages

  Oeser, Michelle L ^a   Amen, Triana ^b   Nadel, Cory M ^a   Bradley, Amanda I ^a   Reed, Benjamin J ^a   Jones, Ramon D ^a   Gopalan, Janani ^a   Kaganovich, Daniel ^b   Gardner, Richard G ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

COREPRESSOR PROTEIN; PROTEIN CYC8; PROTEIN TUP1; UNCLASSIFIED DRUG; REPRESSOR PROTEIN;

ARTICLE; CELL STRESS; CONTROLLED STUDY; GENE EXPRESSION; HYPEROSMOTIC STRESS; NONHUMAN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SUMOYLATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; OSMOTIC PRESSURE; PROMOTER REGION; SACCHAROMYCES CEREVISIAE;

GENE EXPRESSION REGULATION, FUNGAL; OSMOTIC PRESSURE; PROMOTER REGIONS, GENETIC; PROTEOMICS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SUMOYLATION; TRANSCRIPTION, GENETIC;

EID: 84958730297     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005809     Document Type: Article

References (79)

1. Fulda S, Gorman AM, Hori O, Samali A, (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010: 214074. doi: 10.1155/2010/214074 20182529
2. Watts FZ, (2013) Starting and stopping SUMOylation. What regulates the regulator? Chromosoma 122: 451–463. doi: 10.1007/s00412-013-0422-0 23812602
3. Johnson ES, (2004) Protein modification by SUMO. Annu Rev Biochem 73: 355–382. 15189146
4. Castoralova M, Brezinova D, Sveda M, Lipov J, Ruml T, et al. (2012) SUMO-2/3 conjugates accumulating under heat shock or MG132 treatment result largely from new protein synthesis. Biochim Biophys Acta 1823: 911–919. doi: 10.1016/j.bbamcr.2012.01.010 22306003
5. Conti L, Price G, O'Donnell E, Schwessinger B, Dominy P, et al. (2008) Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and -2 regulate salt stress responses in Arabidopsis. Plant Cell 20: 2894–2908. doi: 10.1105/tpc.108.058669 18849491
6. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, et al. (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278: 6862–6872. 12482876
7. Zhou W, Ryan JJ, Zhou H, (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 279: 32262–32268. 15166219
8. Miller MJ, Scalf M, Rytz TC, Hubler SL, Smith LM, et al. (2013) Quantitative proteomics reveals factors regulating RNA biology as dynamic targets of stress-induced SUMOylation in Arabidopsis. Mol Cell Proteomics 12: 449–463. doi: 10.1074/mcp.M112.025056 23197790
9. Miller MJ, Vierstra RD, (2011) Mass spectrometric identification of SUMO substrates provides insights into heat stress-induced SUMOylation in plants. Plant Signal Behav 6: 130–133. 21270536
10. Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD, (2010) Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci U S A 107: 16512–16517. doi: 10.1073/pnas.1004181107 20813957
11. Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, et al. (2009) System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2: ra24. doi: 10.1126/scisignal.2000282 19471022
12. Tatham MH, Matic I, Mann M, Hay RT, (2011) Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal 4: rs4. doi: 10.1126/scisignal.2001484 21693764
13. Lewicki MC, Srikumar T, Johnson E, Raught B, (2015) The S. cerevisiae SUMO stress response is a conjugation-deconjugation cycle that targets the transcription machinery. J Proteomics 118: 39–48. doi: 10.1016/j.jprot.2014.11.012 25434491
14. Geiss-Friedlander R, Melchior F, (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8: 947–956. 18000527
15. Ahner A, Gong X, Schmidt BZ, Peters KW, Rabeh WM, et al. (2013) Small heat shock proteins target mutant cystic fibrosis transmembrane conductance regulator for degradation via a small ubiquitin-like modifier-dependent pathway. Mol Biol Cell 24: 74–84. doi: 10.1091/mbc.E12-09-0678 23155000
16. Gomes RA, Franco C, Da Costa G, Planchon S, Renaut J, et al. (2012) The proteome response to amyloid protein expression in vivo. PLoS One 7: e50123. doi: 10.1371/journal.pone.0050123 23185553
17. Wang Z, Prelich G, (2009) Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol Cell Biol 29: 1694–1706. doi: 10.1128/MCB.01470-08 19139279
18. Denison C, Rudner AD, Gerber SA, Bakalarski CE, Moazed D, et al. (2005) A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics 4: 246–254. 15542864
19. Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, et al. (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280: 4102–4110. 15590687
20. Johnson ES, Blobel G, (1999) Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol 147: 981–994. 10579719
21. Abu Irqeba A, Li Y, Panahi M, Zhu M, Wang Y, (2014) Regulating global sumoylation by a MAP kinase Hog1 and its potential role in osmo-tolerance in yeast. PLoS One 9: e87306. doi: 10.1371/journal.pone.0087306 24498309
22. Johnson ES, Schwienhorst I, Dohmen RJ, Blobel G, (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J 16: 5509–5519. 9312010
23. Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B, (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal Bioanal Chem 389: 1017–1031. 17668192
24. Richardson LA, Reed BJ, Charette JM, Freed EF, Fredrickson EK, et al. (2012) A conserved deubiquitinating enzyme controls cell growth by regulating RNA polymerase I stability. Cell Rep 2: 372–385. doi: 10.1016/j.celrep.2012.07.009 22902402
25. Rosenbaum JC, Fredrickson EK, Oeser ML, Garrett-Engele CM, Locke MN, et al. (2011) Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol Cell 41: 93–106. doi: 10.1016/j.molcel.2010.12.004 21211726
26. Malave TM, Dent SY, (2006) Transcriptional repression by Tup1-Ssn6. Biochem Cell Biol 84: 437–443. 16936817
27. Tzamarias D, Struhl K, (1994) Functional dissection of the yeast Cyc8-Tup1 transcriptional co-repressor complex. Nature 369: 758–761. 8008070
28. Tzamarias D, Struhl K, (1995) Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 corepressor complex to differentially regulated promoters. Genes Dev 9: 821–831. 7705659
29. Wykoff DD, O'Shea EK, (2005) Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol Cell Proteomics 4: 73–83. 15596868
30. Texari L, Dieppois G, Vinciguerra P, Contreras MP, Groner A, et al. (2013) The nuclear pore regulates GAL1 gene transcription by controlling the localization of the SUMO protease Ulp1. Mol Cell 51: 807–818. doi: 10.1016/j.molcel.2013.08.047 24074957
31. Panse VG, Hardeland U, Werner T, Kuster B, Hurt E, (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279: 41346–41351. 15292183
32. Xue Y, Zhou F, Fu C, Xu Y, Yao X, (2006) SUMOsp: a web server for sumoylation site prediction. Nucleic Acids Res 34: W254–257. 16845005
33. Chen K, Wilson MA, Hirsch C, Watson A, Liang S, et al. (2013) Stabilization of the promoter nucleosomes in nucleosome-free regions by the yeast Cyc8-Tup1 corepressor. Genome Res 23: 312–322. doi: 10.1101/gr.141952.112 23124522
34. Kobayashi Y, Inai T, Mizunuma M, Okada I, Shitamukai A, et al. (2008) Identification of Tup1 and Cyc8 mutations defective in the responses to osmotic stress. Biochem Biophys Res Commun 368: 50–55. doi: 10.1016/j.bbrc.2008.01.033 18201562
35. Patel BK, Gavin-Smyth J, Liebman SW, (2009) The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat Cell Biol 11: 344–349. doi: 10.1038/ncb1843 19219034
36. Proft M, Pascual-Ahuir A, de Nadal E, Arino J, Serrano R, et al. (2001) Regulation of the Sko1 transcriptional repressor by the Hog1 MAP kinase in response to osmotic stress. EMBO J 20: 1123–1133. 11230135
37. Proft M, Struhl K, (2002) Hog1 kinase converts the Sko1-Cyc8-Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress. Mol Cell 9: 1307–1317. 12086627
38. Sole C, Nadal-Ribelles M, Kraft C, Peter M, Posas F, et al. (2011) Control of Ubp3 ubiquitin protease activity by the Hog1 SAPK modulates transcription upon osmostress. EMBO J 30: 3274–3284. doi: 10.1038/emboj.2011.227 21743437
39. Wong KH, Struhl K, (2011) The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein. Genes Dev 25: 2525–2539. doi: 10.1101/gad.179275.111 22156212
40. O'Rourke SM, Herskowitz I, (2002) A third osmosensing branch in Saccharomyces cerevisiae requires the Msb2 protein and functions in parallel with the Sho1 branch. Mol Cell Biol 22: 4739–4749. 12052881
41. O'Rourke SM, Herskowitz I, (2004) Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15: 532–542. 14595107
42. Szopinska A, Degand H, Hochstenbach JF, Nader J, Morsomme P, (2011) Rapid response of the yeast plasma membrane proteome to salt stress. Mol Cell Proteomics 10: M111 009589.
43. Janer A, Werner A, Takahashi-Fujigasaki J, Daret A, Fujigasaki H, et al. (2010) SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded ataxin-7. Hum Mol Genet 19: 181–195. doi: 10.1093/hmg/ddp478 19843541
44. Krumova P, Meulmeester E, Garrido M, Tirard M, Hsiao HH, et al. (2011) Sumoylation inhibits alpha-synuclein aggregation and toxicity. J Cell Biol 194: 49–60. doi: 10.1083/jcb.201010117 21746851
45. Mukherjee S, Thomas M, Dadgar N, Lieberman AP, Iniguez-Lluhi JA, (2009) Small ubiquitin-like modifier (SUMO) modification of the androgen receptor attenuates polyglutamine-mediated aggregation. J Biol Chem 284: 21296–21306. doi: 10.1074/jbc.M109.011494 19497852
46. Rytinki M, Kaikkonen S, Sutinen P, Paakinaho V, Rahkama V, et al. (2012) Dynamic SUMOylation is linked to the activity cycles of androgen receptor in the cell nucleus. Mol Cell Biol 32: 4195–4205. 22890844
47. Malakhov MP, Mattern MR, Malakhova OA, Drinker M, Weeks SD, et al. (2004) SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J Struct Funct Genomics 5: 75–86. 15263846
48. Marblestone JG, Edavettal SC, Lim Y, Lim P, Zuo X, et al. (2006) Comparison of SUMO fusion technology with traditional gene fusion systems: enhanced expression and solubility with SUMO. Protein Sci 15: 182–189. 16322573
49. Burkewitz K, Choe K, Strange K, (2011) Hypertonic stress induces rapid and widespread protein damage in C. elegans. Am J Physiol Cell Physiol 301: C566–576. doi: 10.1152/ajpcell.00030.2011 21613604
50. Burkewitz K, Choe KP, Lee EC, Deonarine A, Strange K, (2012) Characterization of the proteostasis roles of glycerol accumulation, protein degradation and protein synthesis during osmotic stress in C. elegans. PLoS One 7: e34153. doi: 10.1371/journal.pone.0034153 22470531
51. Moronetti Mazzeo LE, Dersh D, Boccitto M, Kalb RG, Lamitina T, (2012) Stress and aging induce distinct polyQ protein aggregation states. Proc Natl Acad Sci U S A 109: 10587–10592. doi: 10.1073/pnas.1108766109 22645345
52. Shao J, Diamond MI, (2007) Polyglutamine diseases: emerging concepts in pathogenesis and therapy. Hum Mol Genet 16 Spec No. 2: R115–123. 17911155
53. Alberti S, Halfmann R, King O, Kapila A, Lindquist S, (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137: 146–158. doi: 10.1016/j.cell.2009.02.044 19345193
54. Bengtson MH, Joazeiro CA, (2010) Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467: 470–473. doi: 10.1038/nature09371 20835226
55. Buchan JR, Muhlrad D, Parker R, (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J Cell Biol 183: 441–455. doi: 10.1083/jcb.200807043 18981231
56. Dunn KW, Kamocka MM, McDonald JH, (2011) A practical guide to evaluating colocalization in biological microscopy. Am J Physiol Cell Physiol 300: C723–742. doi: 10.1152/ajpcell.00462.2010 21209361
57. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA, (1992) Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 103 (Pt 3): 857–862. 1478975
58. Duch A, de Nadal E, Posas F, (2012) The p38 and Hog1 SAPKs control cell cycle progression in response to environmental stresses. FEBS Lett 586: 2925–2931. doi: 10.1016/j.febslet.2012.07.034 22820251
59. Saito H, Posas F, (2012) Response to hyperosmotic stress. Genetics 192: 289–318. doi: 10.1534/genetics.112.140863 23028184
60. Klipp E, Nordlander B, Kruger R, Gennemark P, Hohmann S, (2005) Integrative model of the response of yeast to osmotic shock. Nat Biotechnol 23: 975–982. 16025103
61. Halfmann R, Lindquist S, (2008) Screening for amyloid aggregation by Semi-Denaturing Detergent-Agarose Gel Electrophoresis. J Vis Exp.
62. Kryndushkin DS, Alexandrov IM, Ter-Avanesyan MD, Kushnirov VV, (2003) Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J Biol Chem 278: 49636–49643. 14507919
63. Kaplan B, Shtrasburg S, Pras M, (2003) Micropurification techniques in the analysis of amyloid proteins. J Clin Pathol 56: 86–90. 12560384
64. Jarosz DF, Brown JC, Walker GA, Datta MS, Ung WL, et al. (2014) Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158: 1083–1093. doi: 10.1016/j.cell.2014.07.025 25171409
65. Jarosz DF, Lancaster AK, Brown JC, Lindquist S, (2014) An evolutionarily conserved prion-like element converts wild fungi from metabolic specialists to generalists. Cell 158: 1072–1082. doi: 10.1016/j.cell.2014.07.024 25171408
66. Amen T, Kaganovich D, (2015) Dynamic droplets: the role of cytoplasmic inclusions in stress, function, and disease. Cell Mol Life Sci.
67. Brangwynne CP, (2013) Phase transitions and size scaling of membrane-less organelles. J Cell Biol 203: 875–881. doi: 10.1083/jcb.201308087 24368804
68. Malinovska L, Kroschwald S, Alberti S, (2013) Protein disorder, prion propensities, and self-organizing macromolecular collectives. Biochim Biophys Acta 1834: 918–931. doi: 10.1016/j.bbapap.2013.01.003 23328411
69. Chang CF, Wai KM, Patterton HG, (2004) Calculating the statistical significance of physical clusters of co-regulated genes in the genome: the role of chromatin in domain-wide gene regulation. Nucleic Acids Res 32: 1798–1807. 15034148
70. Rosonina E, Duncan SM, Manley JL, (2010) SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev 24: 1242–1252. doi: 10.1101/gad.1917910 20504900
71. Ng CH, Akhter A, Yurko N, Burgener JM, Rosonina E, et al. (2015) Sumoylation controls the timing of Tup1-mediated transcriptional deactivation. Nat Commun 6: 6610. doi: 10.1038/ncomms7610 25766875
72. Drisaldi B, Colnaghi L, Fioriti L, Rao N, Myers C, et al. (2015) SUMOylation Is an Inhibitory Constraint that Regulates the Prion-like Aggregation and Activity of CPEB3. Cell Rep 11: 1694–1702. doi: 10.1016/j.celrep.2015.04.061 26074071
73. Kikis EA, Gidalevitz T, Morimoto RI, (2010) Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol 694: 138–159. 20886762
74. Krumova P, Weishaupt JH, (2013) Sumoylation in neurodegenerative diseases. Cell Mol Life Sci 70: 2123–2138. doi: 10.1007/s00018-012-1158-3 23007842
75. Guthrie C, Fink GR, (1991) Guide to yeast genetics and molecular biology. Methods Enzymol 194: 1–863. 2005781
76. Craig R, Beavis RC, (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20: 1466–1467. 14976030
77. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383–5392. 12403597
78. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863–14868. 9843981
79. Dosztanyi Z, Csizmok V, Tompa P, Simon I, (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433–3434. 15955779