Cooperative Action of Cdk1/cyclin B and SIRT1 Is Required for Mitotic Repression of rRNA Synthesis

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In metazoans, transcription is arrested during mitosis. Previous studies have established that mitotic repression of cellular transcription is mediated by Cdk1/cyclin B-dependent phosphorylation of basal transcription factors that nucleate transcription complex formation. Repression of rDNA transcription at the onset of mitosis is brought about by inactivation of the TBP-containing transcription factor SL1 by Cdk1/cyclin B-dependent phosphorylation of the TAFI110 subunit, which impairs the interaction with UBF and the assembly of pre-initiation complexes. Here we show that hCdc14B, the phosphatase that regulates Cdk1/cyclin B activity and progression through mitosis, promotes reactivation of rDNA transcription by dephosphorylating TAFI110. In addition, the NAD+-dependent deacetylase SIRT1 becomes transiently enriched in nucleoli at the onset of mitosis. SIRT1 deacetylates TAFI68, another subunit of SL1, hypoacetylation of TAFI68 destabilizing SL1 binding to the rDNA promoter and impairing transcription complex assembly. The results reveal that modulation of SL1 activity by reversible acetylation of TAFI68 and phosphorylation of TAFI110 are key modifications that mediate oscillation of rDNA transcription during cell cycle progression.

Vyšlo v časopise: Cooperative Action of Cdk1/cyclin B and SIRT1 Is Required for Mitotic Repression of rRNA Synthesis. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005246
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005246

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Zdroje

1. Taylor JH. Nucleic acid synthesis in relation to the cell division cycle. Ann N Y Acad Sci. 1960;90 : 409–421. 13775619

2. Prescott DM, Bender MA. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp Cell Res. 1962;26 : 260–268. 14488623

3. Hernandez-Verdun D. Assembly and disassembly of the nucleolus during the cell cycle. Nucleus. 2011;2 : 189–194. doi: 10.4161/nucl.2.3.16246 21818412

4. Kadauke S, Blobel GA. Mitotic bookmarking by transcription factors. Epigenetics Chromatin. 2013;6 : 6. doi: 10.1186/1756-8935-6-6 23547918

5. Segil N, Guermah M, Hoffmann A, Roeder RG, Heintz N. Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization. Genes Dev. 1996;10 : 2389–2400. 8843192

6. Long JJ, Leresche A, Kriwacki RW, Gottesfeld JM. Repression of TFIIH transcriptional activity and TFIIH-associated cdk7 kinase activity at mitosis. Mol Cell Biol. 1998;18 : 1467–1476. 9488463

7. Akoulitchev S, Reinberg D. The molecular mechanism of mitotic inhibition of TFIIH is mediated by phosphorylation of CDK7. Genes Dev. 1998;12 : 3541–3550. 9832506

8. Cisek LJ, Corden JL. Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2. Nature. 1989;339 : 679–684. 2662013

9. Hartl P, Gottesfeld J, Forbes DJ. Mitotic repression of transcription in vitro. J Cell Biol. 1993;120 : 13–24.

10. Gottesfeld JM, Wolf J, Dang T, Forbes DJ, Hartl P. Mitotic repression of RNA polymerase III transcription in vitro mediated by phosphorylation of a TFIIIB component. Science. 1994;263 : 81–84. 8272869

11. White RJ, Gottlieb TM, Downes CS, Jackson SP. Cell cycle regulation of RNA polymerase III transcription. Mol Cell Biol. 1995;15 : 6653–6662. 8524230

12. Sirri V, Roussel P, Hernandez-Verdun D. The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery. J Cell Sci. 1999;112 : 3259–3268. 10504331

13. Heix J, Vente A, Voit R, Budde A, Michaelidis TM, Grummt I. Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J. 1998;17 : 7373–7381. 9857193

14. Zomerdijk JC, Beckmann H, Comai L, Tjian R. Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits. Science. 1994;266 : 2015–2018. 7801130

15. Heix J, Zomerdijk JCBM, Ravanpay A, Tjian R, Grummt I. Cloning of murine RNA polymerase I-specific TAF factors: conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1. Proc Natl Acad Sci USA. 1997;94 : 1733–1738. 9050847

16. Denissov S, van Driel M, Voit R, Hekkelman M, Hulsen T, Hernandez N, et al. Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J. 2007;26 : 944–954. 17268553

17. Gorski JJ, Pathak S, Panov K, Kasciukovic T, Panova T, Russell J, et al. A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J. 2007;26 : 1560–1568. 17318177

18. Kuhn A, Vente A, Doree M, Grummt I. Mitotic phosphorylation of the TBP-containing factor SL1 represses ribosomal gene transcription. J Mol Biol. 1998;284 : 1–5. 9811537

19. Klein J, Grummt I. Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. Proc Natl Acad Sci USA. 1999;96 : 6096–6101. 10339547

20. Tumurbaatar I, Cizmecioglu O, Hoffmann I, Grummt I, Voit R. Human Cdc14B promotes progression through mitosis by dephosphorylating Cdc25 and regulating Cdk1/cyclin B activity. PLoS One. 2011;6: e14711. doi: 10.1371/journal.pone.0014711 21379580

21. Muth V, Nadaud S, Grummt I, Voit R. Acetylation of TAFI68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J. 2001;20 : 1353–1362. 11250901

22. Mais C, Wright JE, Prieto JL, Raggett SL, McStay B. UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev. 2005;19 : 50–94. 15598984

23. Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell. 2008;134 : 256–267. doi: 10.1016/j.cell.2008.05.043 18662541

24. Chen D, Dundr M, Wang C, Leung A, Lamond A, Misteli T, et al. Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J Cell Biol. 2005;168 : 41–54. 15623580

25. Naidu S, Friedrich JK, Russell J, Zomerdijk JCBM. TAF1B is a TFIIB-like component of the basal transcription machinery for RNA polymerase I. Science. 2011;333 : 1640–1642. doi: 10.1126/science.1207656 21921199

26. Choudhary C, Kumar C, Gnad F, Nielsen M, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009;325 : 834–840. doi: 10.1126/science.1175371 19608861

27. Ford E, Voit R, Liszt G, Magin C, Grummt I, Guarente L. Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev. 2006;20 : 1075–1080. 16618798

28. Chen S, Santiago-Reichelt M, Seiler J, Felbel K, Grummt, I, Voit R. Repression of RNA polymerase I transcription upon stress is caused by inhibition of RNA-dependent deacetylation of PAF53 by SIRT7. Mol Cell. 2013;52 : 303–313 doi: 10.1016/j.molcel.2013.10.010 24207024

29. Grob A, Colleran C, McStay B. Construction of synthetic nucleoli in human cells reveals how a major functional nuclear domain is formed and propagated through cell division. Genes Dev. 2014;28 : 220–230. doi: 10.1101/gad.234591.113 24449107

30. Zatsepina OV, Voit R, Grummt I, Spring H, Semenov MV, Trendelenburg MF. The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes. Chromosoma. 1993;102 : 599–611. 8306821

31. Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L, Reinberg D. SIRT1 regulates the histone methyl-transferase during heterochromatin formation. Nature 2007;450 : 440–444. 18004385

32. Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P, Reinberg D. Human SirT1 interacts with histone H1 and promotes formation of facultative heterochromatin. Mol Cell. 2004;16 : 93–105. 15469825

33. Fatoba ST, Okorokov AL. Human SIRT1 associates with mitotic chromatin and contributes to chromosomal condensation. Cell Cycle. 2011;10 : 2317–2322. 21636977

34. Chang HC, Guarente L. SIRT1 and other sirtuins in metabolism. Trends Endocrin Metab. 2014;3 : 138–145.

35. Gorski SA, Snyder SK, John S, Grummt I, Misteli T. Modulation of RNA polymerase assembly in transcriptional regulation. Mol Cell. 2008;30 : 486–497. doi: 10.1016/j.molcel.2008.04.021 18498750

36. Voit R, Hoffmann M, Grummt I. Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J. 1999;18 : 1891–1899. 10202152

37. Seither P, Zatsepina O, Hoffmann M, Grummt I. Constitutive and strong association of PAF53 with RNA polymerase I. Chromosoma 1997;106 : 216–225. 9254723

38. Percipalle P, Fomproix N, Cavellán E, Voit R, Reimer G, Krüger T, et al. The chromatin remodeling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep. 2006;7 : 525–530. 16514417

39. Hoppe S, Bierhoff H, Cado I, Weber A, Tiebe M, Grummt I, et al. AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc Natl Acad Sci USA. 2009;106 : 17781–17786. doi: 10.1073/pnas.0909873106 19815529

40. Gavet O, Pines J. Progressive activation of cyclin B1-Cdk1 coordinates entry to mitosis. Dev Cell. 2010;18 : 533–543. doi: 10.1016/j.devcel.2010.02.013 20412769

41. Schnapp A, Grummt I. Transcription complex formation at the mouse rDNA promoter involves the stepwise association of four transcription factors and RNA polymerase. J Biol Chem. 1991;266 : 24588–24595. 1761556

42. Boyle WJ, van der Geer P, Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991;210 : 110–149.