Clr4
Schizosaccharomyces pombe Proteins
/ metabolism
Schizosaccharomyces
/ metabolism
Heterochromatin
/ metabolism
Ubiquitination
Cell Cycle Proteins
/ metabolism
RNA, Untranslated
/ metabolism
Histone-Lysine N-Methyltransferase
/ metabolism
Gene Silencing
Gene Expression Regulation, Fungal
Methyltransferases
/ metabolism
Ubiquitin-Conjugating Enzymes
/ metabolism
Centromere
/ metabolism
Transcription, Genetic
Histones
/ metabolism
Chromosomal Proteins, Non-Histone
/ metabolism
Phase Separation
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
21
03
2023
accepted:
02
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
Transcriptional silencing by RNAi paradoxically relies on transcription, but how the transition from transcription to silencing is achieved has remained unclear. The Cryptic Loci Regulator complex (CLRC) in Schizosaccharomyces pombe is a cullin-ring E3 ligase required for silencing that is recruited by RNAi. We found that the E2 ubiquitin conjugating enzyme Ubc4 interacts with CLRC and mono-ubiquitinates the histone H3K9 methyltransferase Clr4
Identifiants
pubmed: 39477922
doi: 10.1038/s41467-024-53417-9
pii: 10.1038/s41467-024-53417-9
doi:
Substances chimiques
Schizosaccharomyces pombe Proteins
0
clr4 protein, S pombe
EC 2.1.1.43
Heterochromatin
0
Cell Cycle Proteins
0
Swi6 protein, S pombe
0
RNA, Untranslated
0
Histone-Lysine N-Methyltransferase
EC 2.1.1.43
Methyltransferases
EC 2.1.1.-
Ubiquitin-Conjugating Enzymes
EC 2.3.2.23
Histones
0
Chromosomal Proteins, Non-Histone
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9384Subventions
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R35GM144206
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM117406
Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)
ID : 5PP30CA045508
Organisme : National Science Foundation (NSF)
ID : 2217560
Informations de copyright
© 2024. The Author(s).
Références
Castel, S. E. & Martienssen, R. A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet 14, 100–112 (2013).
pubmed: 23329111
doi: 10.1038/nrg3355
Janssen, A., Colmenares, S. U. & Karpen, G. H. Heterochromatin: Guardian of the Genome. Annu Rev. Cell Dev. Biol. 34, 265–288 (2018).
pubmed: 30044650
doi: 10.1146/annurev-cellbio-100617-062653
Allshire, R. C. & Madhani, H. D. Ten principles of heterochromatin formation and function. Nat. Rev. Mol. Cell Biol. 19, 229–244 (2018).
pubmed: 29235574
doi: 10.1038/nrm.2017.119
Martienssen, R. & Moazed, D. RNAi and heterochromatin assembly. Cold Spring Harb. Perspect. Biol. 7, a019323 (2015).
pubmed: 26238358
doi: 10.1101/cshperspect.a019323
Gutbrod, M. J. et al. Dicer promotes genome stability via the bromodomain transcriptional co-activator BRD4. Nat. Commun. 13, 1001 (2022).
pubmed: 35194019
doi: 10.1038/s41467-022-28554-8
Hall, I. M., Noma, K. & Grewal, S. I. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc. Natl Acad. Sci. USA 100, 193–198 (2003).
pubmed: 12509501
doi: 10.1073/pnas.232688099
Provost, P. et al. Dicer is required for chromosome segregation and gene silencing in fission yeast cells. Proc. Natl Acad. Sci. USA 99, 16648–16653 (2002).
pubmed: 12482946
doi: 10.1073/pnas.212633199
Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124 (2001).
pubmed: 11242054
doi: 10.1038/35065138
Nakayama, J., Rice, J. C., Strahl, B. D., Allis, C. D. & Grewal, S. I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110–113 (2001).
pubmed: 11283354
doi: 10.1126/science.1060118
Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593–599 (2000).
pubmed: 10949293
doi: 10.1038/35020506
Colmenares, S. U., Buker, S. M., Buhler, M., Dlakić, M. & Moazed, D. Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol. Cell 27, 449–461 (2007).
pubmed: 17658285
doi: 10.1016/j.molcel.2007.07.007
Djupedal, I. et al. Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. Embo J. 28, 3832–3844 (2009).
pubmed: 19942857
doi: 10.1038/emboj.2009.351
Motamedi, M. R. et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789–802 (2004).
pubmed: 15607976
doi: 10.1016/j.cell.2004.11.034
Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833–1837 (2002).
pubmed: 12193640
doi: 10.1126/science.1074973
Verdel, A. et al. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303, 672–676 (2004).
pubmed: 14704433
doi: 10.1126/science.1093686
Gutbrod, M. J. & Martienssen, R. A. Conserved chromosomal functions of RNA interference. Nat. Rev. Genet 21, 311–331 (2020).
pubmed: 32051563
doi: 10.1038/s41576-019-0203-6
Chen, E. S. et al. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451, 734–737 (2008).
pubmed: 18216783
doi: 10.1038/nature06561
Jih, G. et al. Unique roles for histone H3K9me states in RNAi and heritable silencing of transcription. Nature 547, 463–467 (2017).
pubmed: 28682306
doi: 10.1038/nature23267
Kloc, A., Zaratiegui, M., Nora, E. & Martienssen, R. RNA interference guides histone modification during the S phase of chromosomal replication. Curr. Biol. 18, 490–495 (2008).
pubmed: 18394897
doi: 10.1016/j.cub.2008.03.016
Cappadocia, L. & Lima, C. D. Ubiquitin-like Protein Conjugation: Structures, Chemistry, and Mechanism. Chem. Rev. 118, 889–918 (2018).
pubmed: 28234446
doi: 10.1021/acs.chemrev.6b00737
Hochstrasser, M. Origin and function of ubiquitin-like proteins. Nature 458, 422–429 (2009).
pubmed: 19325621
doi: 10.1038/nature07958
Rape, M. Ubiquitylation at the crossroads of development and disease. Nat. Rev. Mol. Cell Biol. 19, 59–70 (2018).
pubmed: 28928488
doi: 10.1038/nrm.2017.83
Swatek, K. N. & Komander, D. Ubiquitin modifications. Cell Res. 26, 399–422 (2016).
pubmed: 27012465
doi: 10.1038/cr.2016.39
Ye, Y. & Rape, M. Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755–764 (2009).
pubmed: 19851334
doi: 10.1038/nrm2780
Hong, E. J., Villén, J., Gerace, E. L., Gygi, S. P. & Moazed, D. A cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol. 2, 106–111 (2005).
pubmed: 17114925
doi: 10.4161/rna.2.3.2131
Horn, P. J., Bastie, J. N. & Peterson, C. L. A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev. 19, 1705–1714 (2005).
pubmed: 16024659
doi: 10.1101/gad.1328005
Jia, S., Kobayashi, R. & Grewal, S. I. Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat. Cell Biol. 7, 1007–1013 (2005).
pubmed: 16127433
doi: 10.1038/ncb1300
Kuscu, C. et al. CRL4-like Clr4 complex in Schizosaccharomyces pombe depends on an exposed surface of Dos1 for heterochromatin silencing. Proc. Natl Acad. Sci. USA 111, 1795–1800 (2014).
pubmed: 24449894
doi: 10.1073/pnas.1313096111
Thon, G. et al. The Clr7 and Clr8 directionality factors and the Pcu4 cullin mediate heterochromatin formation in the fission yeast Schizosaccharomyces pombe. Genetics 171, 1583–1595 (2005).
pubmed: 16157682
doi: 10.1534/genetics.105.048298
Li, F. et al. Two novel proteins, dos1 and dos2, interact with rik1 to regulate heterochromatic RNA interference and histone modification. Curr. Biol. 15, 1448–1457 (2005).
pubmed: 16040243
doi: 10.1016/j.cub.2005.07.021
Banani, S. F., Lee, H. O., Hyman, A. A. & Rosen, M. K. Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 18, 285–298 (2017).
pubmed: 28225081
doi: 10.1038/nrm.2017.7
Brangwynne, C. P. et al. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324, 1729–1732 (2009).
pubmed: 19460965
doi: 10.1126/science.1172046
Kato, M. et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753–767 (2012).
pubmed: 22579281
doi: 10.1016/j.cell.2012.04.017
Rhine, K., Vidaurre, V. & Myong, S. RNA Droplets. Annu Rev. Biophys. 49, 247–265 (2020).
pubmed: 32040349
doi: 10.1146/annurev-biophys-052118-115508
Rippe, K. Liquid-Liquid Phase Separation in Chromatin. Cold Spring Harb Perspect Biol 14, https://doi.org/10.1101/cshperspect.a040683 (2022).
Weber, S. C. & Brangwynne, C. P. Getting RNA and protein in phase. Cell 149, 1188–1191 (2012).
pubmed: 22682242
doi: 10.1016/j.cell.2012.05.022
Molliex, A. et al. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163, 123–133 (2015).
pubmed: 26406374
doi: 10.1016/j.cell.2015.09.015
Mittag, T. & Parker, R. Multiple Modes of Protein-Protein Interactions Promote RNP Granule Assembly. J. Mol. Biol. 430, 4636–4649 (2018).
pubmed: 30099026
doi: 10.1016/j.jmb.2018.08.005
Gibson, B. A. et al. Organization of Chromatin by Intrinsic and Regulated Phase Separation. Cell 179, 470–484.e421 (2019).
pubmed: 31543265
doi: 10.1016/j.cell.2019.08.037
Larson, A. G. et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240 (2017).
pubmed: 28636604
doi: 10.1038/nature22822
Sabari, B. R. et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science 361, https://doi.org/10.1126/science.aar3958 (2018).
Strom, A. R. et al. Phase separation drives heterochromatin domain formation. Nature 547, 241–245 (2017).
pubmed: 28636597
doi: 10.1038/nature22989
Wang, L. et al. Histone Modifications Regulate Chromatin Compartmentalization by Contributing to a Phase Separation Mechanism. Mol. Cell 76, 646–659.e646 (2019).
pubmed: 31543422
doi: 10.1016/j.molcel.2019.08.019
Irvine, D. V. et al. Mapping epigenetic mutations in fission yeast using whole-genome next-generation sequencing. Genome Res. 19, 1077–1083 (2009).
pubmed: 19423874
doi: 10.1101/gr.089318.108
Javerzat, J. P., Cranston, G. & Allshire, R. C. Fission yeast genes which disrupt mitotic chromosome segregation when overexpressed. Nucleic Acids Res. 24, 4676–4683 (1996).
pubmed: 8972853
doi: 10.1093/nar/24.23.4676
Schalch, T. et al. High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol. Cell 34, 36–46 (2009).
pubmed: 19362535
doi: 10.1016/j.molcel.2009.02.024
Ishimoto, K. et al. Ubiquitination of Lysine 867 of the Human SETDB1 Protein Upregulates Its Histone H3 Lysine 9 (H3K9) Methyltransferase Activity. PLoS One 11, e0165766 (2016).
pubmed: 27798683
doi: 10.1371/journal.pone.0165766
Sun, L. & Fang, J. E3-Independent Constitutive Monoubiquitination Complements Histone Methyltransferase Activity of SETDB1. Mol. Cell 62, 958–966 (2016).
pubmed: 27237050
doi: 10.1016/j.molcel.2016.04.022
Iglesias, N. et al. Native Chromatin Proteomics Reveals a Role for Specific Nucleoporins in Heterochromatin Organization and Maintenance. Mol. Cell 77, 51–66.e58 (2020).
pubmed: 31784357
doi: 10.1016/j.molcel.2019.10.018
Hoeller, D. et al. E3-independent monoubiquitination of ubiquitin-binding proteins. Mol. Cell 26, 891–898 (2007).
pubmed: 17588522
doi: 10.1016/j.molcel.2007.05.014
Akoury, E. et al. Disordered region of H3K9 methyltransferase Clr4 binds the nucleosome and contributes to its activity. Nucleic Acids Res. 47, 6726–6736 (2019).
pubmed: 31165882
doi: 10.1093/nar/gkz480
Iglesias, N. et al. Automethylation-induced conformational switch in Clr4 (Suv39h) maintains epigenetic stability. Nature 560, 504–508 (2018).
pubmed: 30051891
doi: 10.1038/s41586-018-0398-2
Zhang, K., Mosch, K., Fischle, W. & Grewal, S. I. Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15, 381–388 (2008).
pubmed: 18345014
doi: 10.1038/nsmb.1406
Ishida, M. et al. Intrinsic nucleic acid-binding activity of Chp1 chromodomain is required for heterochromatic gene silencing. Mol. Cell 47, 228–241 (2012).
pubmed: 22727667
doi: 10.1016/j.molcel.2012.05.017
Kagansky, A. et al. Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324, 1716–1719 (2009).
pubmed: 19556509
doi: 10.1126/science.1172026
Holla, S. et al. Positioning Heterochromatin at the Nuclear Periphery Suppresses Histone Turnover to Promote Epigenetic Inheritance. Cell 180, 150–164.e115 (2020).
pubmed: 31883795
doi: 10.1016/j.cell.2019.12.004
Ragunathan, K., Jih, G. & Moazed, D. Epigenetics. Epigenetic inheritance uncoupled from sequence-specific recruitment. Science 348, 1258699 (2015).
pubmed: 25831549
doi: 10.1126/science.1258699
Shan, C. M. et al. A histone H3K9M mutation traps histone methyltransferase Clr4 to prevent heterochromatin spreading. Elife 5, https://doi.org/10.7554/eLife.17903 (2016).
Bayne, E. H. et al. Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140, 666–677 (2010).
pubmed: 20211136
doi: 10.1016/j.cell.2010.01.038
Ban, H., Sun, W., Chen, Y. H., Chen, Y. & Li, F. Dri1 mediates heterochromatin assembly via RNAi and histone deacetylation. Genetics 218, https://doi.org/10.1093/genetics/iyab032 (2021).
Shin, Y. & Brangwynne, C. P. Liquid phase condensation in cell physiology and disease. Science 357, https://doi.org/10.1126/science.aaf4382 (2017).
Alberti, S., Gladfelter, A. & Mittag, T. Considerations and Challenges in Studying Liquid-Liquid Phase Separation and Biomolecular Condensates. Cell 176, 419–434 (2019).
pubmed: 30682370
doi: 10.1016/j.cell.2018.12.035
Kroschwald, S. et al. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules. Elife 4, e06807 (2015).
pubmed: 26238190
pmcid: 4522596
doi: 10.7554/eLife.06807
Canzio, D. et al. Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol. Cell 41, 67–81 (2011).
pubmed: 21211724
doi: 10.1016/j.molcel.2010.12.016
Hinde, E., Cardarelli, F. & Gratton, E. Spatiotemporal regulation of Heterochromatin Protein 1-alpha oligomerization and dynamics in live cells. Sci. Rep. 5, 12001 (2015).
pubmed: 26238434
doi: 10.1038/srep12001
Müller-Ott, K. et al. Specificity, propagation, and memory of pericentric heterochromatin. Mol. Syst. Biol. 10, 746 (2014).
pubmed: 25134515
doi: 10.15252/msb.20145377
Elbaum-Garfinkle, S. et al. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc. Natl Acad. Sci. USA 112, 7189–7194 (2015).
pubmed: 26015579
doi: 10.1073/pnas.1504822112
Maharana, S. et al. RNA buffers the phase separation behavior of prion-like RNA binding proteins. Science 360, 918–921 (2018).
pubmed: 29650702
doi: 10.1126/science.aar7366
Van Lindt, J. et al. F/YGG-motif is an intrinsically disordered nucleic-acid binding motif. RNA Biol. 19, 622–635 (2022).
pubmed: 35491929
doi: 10.1080/15476286.2022.2066336
Oya, E. et al. H3K14 ubiquitylation promotes H3K9 methylation for heterochromatin assembly. EMBO Rep. 20, e48111 (2019).
pubmed: 31468675
doi: 10.15252/embr.201948111
Aagaard, L. et al. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromere-associated proteins which complex with the heterochromatin component M31. Embo J. 18, 1923–1938 (1999).
pubmed: 10202156
doi: 10.1093/emboj/18.7.1923
Yamamoto, K. & Sonoda, M. Self-interaction of heterochromatin protein 1 is required for direct binding to histone methyltransferase, SUV39H1. Biochem Biophys. Res. Commun. 301, 287–292 (2003).
pubmed: 12565857
doi: 10.1016/S0006-291X(02)03021-8
Sanulli, S. et al. HP1 reshapes nucleosome core to promote phase separation of heterochromatin. Nature 575, 390–394 (2019).
pubmed: 31618757
doi: 10.1038/s41586-019-1669-2
Pidoux, A. L., Uzawa, S., Perry, P. E., Cande, W. Z. & Allshire, R. C. Live analysis of lagging chromosomes during anaphase and their effect on spindle elongation rate in fission yeast. J. Cell Sci. 113, 4177–4191 (2000).
pubmed: 11069763
doi: 10.1242/jcs.113.23.4177
Braun, S. et al. The Cul4-Ddb1(Cdt)² ubiquitin ligase inhibits invasion of a boundary-associated antisilencing factor into heterochromatin. Cell 144, 41–54 (2011).
pubmed: 21215368
doi: 10.1016/j.cell.2010.11.051
Trewick, S. C., Minc, E., Antonelli, R., Urano, T. & Allshire, R. C. The JmjC domain protein Epe1 prevents unregulated assembly and disassembly of heterochromatin. Embo j. 26, 4670–4682 (2007).
pubmed: 17948055
doi: 10.1038/sj.emboj.7601892
Zofall, M. & Grewal, S. I. Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol. Cell 22, 681–692 (2006).
pubmed: 16762840
doi: 10.1016/j.molcel.2006.05.010
Keller, C., Kulasegaran-Shylini, R., Shimada, Y., Hotz, H. R. & Bühler, M. Noncoding RNAs prevent spreading of a repressive histone mark. Nat. Struct. Mol. Biol. 20, 994–1000 (2013).
pubmed: 23872991
doi: 10.1038/nsmb.2619
Kim, H. S. et al. Identification of a BET family bromodomain/casein kinase II/TAF-containing complex as a regulator of mitotic condensin function. Cell Rep. 6, 892–905 (2014).
pubmed: 24565511
doi: 10.1016/j.celrep.2014.01.029
Wang, J. et al. Epe1 recruits BET family bromodomain protein Bdf2 to establish heterochromatin boundaries. Genes Dev. 27, 1886–1902 (2013).
pubmed: 24013502
doi: 10.1101/gad.221010.113
Komander, D., Clague, M. J. & Urbé, S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550–563 (2009).
pubmed: 19626045
doi: 10.1038/nrm2731
Leznicki, P. & Kulathu, Y. Mechanisms of regulation and diversification of deubiquitylating enzyme function. J. Cell Sci. 130, 1997–2006 (2017).
pubmed: 28476940
doi: 10.1242/jcs.201855
Reyes-Turcu, F. E., Zhang, K., Zofall, M., Chen, E. & Grewal, S. I. Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat. Struct. Mol. Biol. 18, 1132–1138 (2011).
pubmed: 21892171
doi: 10.1038/nsmb.2122
Ryan, C. J. et al. Hierarchical modularity and the evolution of genetic interactomes across species. Mol. Cell 46, 691–704 (2012).
pubmed: 22681890
doi: 10.1016/j.molcel.2012.05.028
Liu, Y. et al. Functional characterization of the Arabidopsis ubiquitin-specific protease gene family reveals specific role and redundancy of individual members in development. Plant J. 55, 844–856 (2008).
pubmed: 18485060
doi: 10.1111/j.1365-313X.2008.03557.x
Bühler, M., Spies, N., Bartel, D. P. & Moazed, D. TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat. Struct. Mol. Biol. 15, 1015–1023 (2008).
pubmed: 18776903
doi: 10.1038/nsmb.1481
Kuzdere, T. et al. Differential phosphorylation of Clr4(SUV39H) by Cdk1 accompanies a histone H3 methylation switch that is essential for gametogenesis. EMBO Rep. e55928, https://doi.org/10.15252/embr.202255928 (2022).
Babu, M. M. The contribution of intrinsically disordered regions to protein function, cellular complexity, and human disease. Biochem Soc. Trans. 44, 1185–1200 (2016).
pubmed: 27911701
doi: 10.1042/BST20160172
Bah, A. & Forman-Kay, J. D. Modulation of Intrinsically Disordered Protein Function by Post-translational Modifications. J. Biol. Chem. 291, 6696–6705 (2016).
pubmed: 26851279
doi: 10.1074/jbc.R115.695056
Bah, A. et al. Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch. Nature 519, 106–109 (2015).
pubmed: 25533957
doi: 10.1038/nature13999
Oldfield, C. J. & Dunker, A. K. Intrinsically disordered proteins and intrinsically disordered protein regions. Annu Rev. Biochem 83, 553–584 (2014).
pubmed: 24606139
doi: 10.1146/annurev-biochem-072711-164947
Qamar, S. et al. FUS Phase Separation Is Modulated by a Molecular Chaperone and Methylation of Arginine Cation-π Interactions. Cell 173, 720–734.e715 (2018).
pubmed: 29677515
doi: 10.1016/j.cell.2018.03.056
Stowell, J. A. W. et al. A low-complexity region in the YTH domain protein Mmi1 enhances RNA binding. J. Biol. Chem. 293, 9210–9222 (2018).
pubmed: 29695507
doi: 10.1074/jbc.RA118.002291
Yang, P. et al. G3BP1 Is a Tunable Switch that Triggers Phase Separation to Assemble Stress Granules. Cell 181, 325–345.e328 (2020).
pubmed: 32302571
doi: 10.1016/j.cell.2020.03.046
Keller, C. et al. HP1(Swi6) mediates the recognition and destruction of heterochromatic RNA transcripts. Mol. Cell 47, 215–227 (2012).
pubmed: 22683269
doi: 10.1016/j.molcel.2012.05.009
Johnson, W. L. et al. RNA-dependent stabilization of SUV39H1 at constitutive heterochromatin. Elife 6, https://doi.org/10.7554/eLife.25299 (2017).
Shirai, A. et al. Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly. Elife 6, https://doi.org/10.7554/eLife.25317 (2017).
Velazquez Camacho, O. et al. Major satellite repeat RNA stabilize heterochromatin retention of Suv39h enzymes by RNA-nucleosome association and RNA:DNA hybrid formation. Elife 6, https://doi.org/10.7554/eLife.25293 (2017).
Gerace, E. L., Halic, M. & Moazed, D. The methyltransferase activity of Clr4Suv39h triggers RNAi independently of histone H3K9 methylation. Mol. Cell 39, 360–372 (2010).
pubmed: 20705239
doi: 10.1016/j.molcel.2010.07.017
Bühler, M., Verdel, A. & Moazed, D. Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 125, 873–886 (2006).
pubmed: 16751098
doi: 10.1016/j.cell.2006.04.025
Al-Sady, B., Madhani, H. D. & Narlikar, G. J. Division of labor between the chromodomains of HP1 and Suv39 methylase enables coordination of heterochromatin spread. Mol. Cell 51, 80–91 (2013).
pubmed: 23849629
doi: 10.1016/j.molcel.2013.06.013
Chang, A. Y., Castel, S. E., Ernst, E., Kim, H. S. & Martienssen, R. A. The Conserved RNA Binding Cyclophilin, Rct1, Regulates Small RNA Biogenesis and Splicing Independent of Heterochromatin Assembly. Cell Rep. 19, 2477–2489 (2017).
pubmed: 28636937
doi: 10.1016/j.celrep.2017.05.086
Bähler, J. et al. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943–951 (1998).
pubmed: 9717240
doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y
Murray, J. M., Watson, A. T. & Carr, A. M. Transformation of Schizosaccharomyces pombe: Lithium Acetate/ Dimethyl Sulfoxide Procedure. Cold Spring Harb. Protoc. 2016, https://doi.org/10.1101/pdb.prot090969 (2016).
pubmed: 27037075
doi: 10.1101/pdb.prot090969
Winston, F. EMS and UV mutagenesis in yeast. Curr. Protoc. Mol. Biol. Chapter 13, Unit 13.13B (2008).
Roche, B., Arcangioli, B. & Martienssen, R. A. RNA interference is essential for cellular quiescence. Science 354, https://doi.org/10.1126/science.aah5651 (2016).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286
doi: 10.1038/nmeth.1923
Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. arXiv e-prints, arXiv:1207.3907 (2012). < https://ui.adsabs.harvard.edu/abs/2012arXiv1207.3907G >.
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
pubmed: 19261174
pmcid: 2690996
doi: 10.1186/gb-2009-10-3-r25
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
doi: 10.1093/bioinformatics/btq033
Keller, A., Nesvizhskii, A. I., Kolker, E. & Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383–5392 (2002).
pubmed: 12403597
doi: 10.1021/ac025747h
Nesvizhskii, A. I., Keller, A., Kolker, E. & Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646–4658 (2003).
pubmed: 14632076
doi: 10.1021/ac0341261
Wang, H. et al. Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature 566, 131–135 (2019).
pubmed: 30675061
doi: 10.1038/s41586-019-0880-5