Ndd1 Turnover by SCF Is Inhibited by the DNA Damage Checkpoint in

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All cells must regulate cell division in response to extracellular and intracellular cues, and one of the most critical steps to regulate is the process of cell division, or mitosis. In response to DNA damage in budding yeast, cells activate a checkpoint that promotes DNA repair and arrests the cell cycle before division to give the cell time to repair the lesion. One of the key regulators of mitosis is an essential transcription factor called Ndd1. Ndd1 is known to be regulated by transcription and phosphorylation, both in unperturbed cells and following exposure to DNA damage. Here, we show that Ndd1 protein turnover is also regulated in both situations. Ndd1 is degraded quickly during an unperturbed cell cycle, but is strongly stabilized following exposure to DNA damage. We identify the machinery that targets Ndd1 for turnover and the signaling pathways required to stabilize Ndd1 in response to DNA damage. Maintaining high levels of Ndd1 after exposure to DNA damage may allow the cell to reactivate Ndd1 after the damage has been repaired to promote mitosis.

Vyšlo v časopise: Ndd1 Turnover by SCF Is Inhibited by the DNA Damage Checkpoint in. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005162
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005162

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Zdroje

1. Loy CJ, Lydall D, Surana U (1999) NDD1, a high-dosage suppressor of cdc28-1N, is essential for expression of a subset of late-S-phase-specific genes in Saccharomyces cerevisiae. Mol Cell Biol 19 : 3312–3327. 10207056

2. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, et al. (1998) Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9 : 3273–3297. 9843569

3. Koranda M, Schleiffer A, Endler L, Ammerer G (2000) Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters. Nature 406 : 94–98. 10894549

4. Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN, et al. (2000) Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406 : 90–94. 10894548

5. Darieva Z, Bulmer R, Pic-Taylor A, Doris KS, Geymonat M, Sedgwick SG, et al. (2006) Polo kinase controls cell-cycle-dependent transcription by targeting a coactivator protein. Nature 444 : 494–498. 17122856

6. Darieva Z, Han N, Warwood S, Doris KS, Morgan BA, Sharrocks AD (2012) Protein kinase C regulates late cell cycle-dependent gene expression. Mol Cell Biol 32 : 4651–4661. doi: 10.1128/MCB.06000-11 22966207

7. Darieva Z, Pic-Taylor A, Boros J, Spanos A, Geymonat M, Reece RJ, et al. (2003) Cell cycle-regulated transcription through the FHA domain of Fkh2p and the coactivator Ndd1p. Current Biology 13 : 1740–1745. 14521842

8. Pic-Taylor A, Darieva Z, Morgan BA, Sharrocks AD (2004) Regulation of cell cycle-specific gene expression through cyclin-dependent kinase-mediated phosphorylation of the forkhead transcription factor Fkh2p. Mol Cell Biol 24 : 10036–10046. 15509804

9. Reynolds D, Shi BJ, McLean C, Katsis F, Kemp B, Dalton S (2003) Recruitment of Thr 319-phosphorylated Ndd1p to the FHA domain of Fkh2p requires Clb kinase activity: a mechanism for CLB cluster gene activation. Genes Dev 17 : 1789–1802. 12865300

10. Veis J, Klug H, Koranda M, Ammerer G (2007) Activation of the G2/M-specific gene CLB2 requires multiple cell cycle signals. Mol Cell Biol 27 : 8364–8373. 17908798

11. Edenberg ER, Vashisht A, Benanti JA, Wohlschlegel J, Toczyski DP (2014) Rad53 downregulates mitotic gene transcription by inhibiting the transcriptional activator Ndd1. Mol Cell Biol 34 : 725–738. doi: 10.1128/MCB.01056-13 24324011

12. Gasch AP, Huang M, Metzner S, Botstein D, Elledge SJ, Brown PO (2001) Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol Biol Cell 12 : 2987–3003. 11598186

13. Jaehnig EJ, Kuo D, Hombauer H, Ideker TG, Kolodner RD (2013) Checkpoint kinases regulate a global network of transcription factors in response to DNA damage. Cell Rep 4 : 174–188. doi: 10.1016/j.celrep.2013.05.041 23810556

14. Yelamanchi SK, Veis J, Anrather D, Klug H, Ammerer G (2014) Genotoxic Stress Prevents Ndd1-Dependent Transcriptional Activation of G2/M-Specific Genes in Saccharomyces cerevisiae. Mol Cell Biol 34 : 711–724. doi: 10.1128/MCB.01090-13 24324010

15. Pramila T, Wu W, Miles S, Noble WS, Breeden LL (2006) The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev 20 : 2266–2278. 16912276

16. MacIsaac KD, Wang T, Gordon DB, Gifford DK, Stormo GD, Fraenkel E (2006) An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7 : 113. 16522208

17. Okaz E, Arguello-Miranda O, Bogdanova A, Vinod PK, Lipp JJ, Markova Z, et al. (2012) Meiotic prophase requires proteolysis of M phase regulators mediated by the meiosis-specific APC/CAma1. Cell 151 : 603–618. doi: 10.1016/j.cell.2012.08.044 23101628

18. Cimprich KA, Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9 : 616–627. doi: 10.1038/nrm2450 18594563

19. Edenberg ER, Downey M, Toczyski D (2014) Polymerase stalling during replication, transcription and translation. Curr Biol 24: R445–452. doi: 10.1016/j.cub.2014.03.060 24845677

20. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, Blethrow J, et al. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407 : 395–401. 11014197

21. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6 : 9–20. 15688063

22. Mark KG, Simonetta M, Maiolica A, Seller CA, Toczyski DP (2014) Ubiquitin ligase trapping identifies an SCF(Saf1) pathway targeting unprocessed vacuolar/lysosomal proteins. Mol Cell 53 : 148–161. doi: 10.1016/j.molcel.2013.12.003 24389104

23. Benanti JA, Cheung SK, Brady MC, Toczyski DP (2007) A proteomic screen reveals SCFGrr1 targets that regulate the glycolytic-gluconeogenic switch. Nat Cell Biol 9 : 1184–1191. 17828247

24. Landry BD, Doyle JP, Toczyski DP, Benanti JA (2012) F-box protein specificity for g1 cyclins is dictated by subcellular localization. PLoS Genet 8: e1002851. doi: 10.1371/journal.pgen.1002851 22844257

25. Barral Y, Jentsch S, Mann C (1995) G1 cyclin turnover and nutrient uptake are controlled by a common pathway in yeast. Genes Dev 9 : 399–409. 7883165

26. Spielewoy N, Flick K, Kalashnikova TI, Walker JR, Wittenberg C (2004) Regulation and recognition of SCFGrr1 targets in the glucose and amino acid signaling pathways. Mol Cell Biol 24 : 8994–9005. 15456873

27. Flick KM, Spielewoy N, Kalashnikova TI, Guaderrama M, Zhu Q, Chang HC, et al. (2003) Grr1-dependent inactivation of Mth1 mediates glucose-induced dissociation of Rgt1 from HXT gene promoters. Mol Biol Cell 14 : 3230–3241. 12925759

28. Vallier LG, Coons D, Bisson LF, Carlson M (1994) Altered regulatory responses to glucose are associated with a glucose transport defect in grr1 mutants of Saccharomyces cerevisiae. Genetics 136 : 1279–1285. 8013905

29. Hsiung YG, Chang HC, Pellequer JL, La Valle R, Lanker S, Wittenberg C (2001) F-box protein Grr1 interacts with phosphorylated targets via the cationic surface of its leucine-rich repeat. Mol Cell Biol 21 : 2506–2520. 11259599

30. Bastos de Oliveira FM, Harris MR, Brazauskas P, de Bruin RA, Smolka MB (2012) Linking DNA replication checkpoint to MBF cell-cycle transcription reveals a distinct class of G1/S genes. EMBO J 31 : 1798–1810. doi: 10.1038/emboj.2012.27 22333912

31. Mazumder A, Pesudo LQ, McRee S, Bathe M, Samson LD (2013) Genome-wide single-cell-level screen for protein abundance and localization changes in response to DNA damage in S. cerevisiae. Nucleic Acids Res 41 : 9310–9324. doi: 10.1093/nar/gkt715 23935119

32. Booher RN, Deshaies RJ, Kirschner MW (1993) Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12 : 3417–3426. 8253069

33. Amon A, Surana U, Muroff I, Nasmyth K (1992) Regulation of p34CDC28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 355 : 368–371. 1731251

34. Sorger PK, Murray AW (1992) S-phase feedback control in budding yeast independent of tyrosine phosphorylation of p34cdc28. Nature 355 : 365–368. 1731250

35. Enserink JM, Smolka MB, Zhou H, Kolodner RD (2006) Checkpoint proteins control morphogenetic events during DNA replication stress in Saccharomyces cerevisiae. J Cell Biol 175 : 729–741. 17130284

36. Liu H, Wang Y (2006) The function and regulation of budding yeast Swe1 in response to interrupted DNA synthesis. Mol Biol Cell 17 : 2746–2756. 16571676

37. Keaton MA, Bardes ES, Marquitz AR, Freel CD, Zyla TR, Rudolph J, et al. (2007) Differential susceptibility of yeast S and M phase CDK complexes to inhibitory tyrosine phosphorylation. Curr Biol 17 : 1181–1189. 17614281

38. Koivomagi M, Valk E, Venta R, Iofik A, Lepiku M, Morgan DO, et al. (2011) Dynamics of Cdk1 substrate specificity during the cell cycle. Mol Cell 42 : 610–623. doi: 10.1016/j.molcel.2011.05.016 21658602

39. Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H (2008) A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 7 : 1389–1396. doi: 10.1074/mcp.M700468-MCP200 18407956

40. Landry BD, Mapa CE, Arsenault HE, Poti KE, Benanti JA (2014) Regulation of a transcription factor network by Cdk1 coordinates late cell cycle gene expression. EMBO J 33 : 1044–1060. doi: 10.1002/embj.201386877 24714560

41. Jin P, Gu Y, Morgan DO (1996) Role of inhibitory CDC2 phosphorylation in radiation-induced G2 arrest in human cells. J Cell Biol 134 : 963–970. 8769420

42. O'Connell MJ, Raleigh JM, Verkade HM, Nurse P (1997) Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J 16 : 545–554. 9034337

43. Rhind N, Furnari B, Russell P (1997) Cdc2 tyrosine phosphorylation is required for the DNA damage checkpoint in fission yeast. Genes Dev 11 : 504–511. 9042863

44. Rhind N, Russell P (1998) Tyrosine phosphorylation of cdc2 is required for the replication checkpoint in Schizosaccharomyces pombe. Mol Cell Biol 18 : 3782–3787. 9632761

45. Rowley R, Hudson J, Young PG (1992) The wee1 protein kinase is required for radiation-induced mitotic delay. Nature 356 : 353–355. 1549179

46. Lew DJ (2003) The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15 : 648–653. 14644188

47. Stueland CS, Lew DJ, Cismowski MJ, Reed SI (1993) Full activation of p34CDC28 histone H1 kinase activity is unable to promote entry into mitosis in checkpoint-arrested cells of the yeast Saccharomyces cerevisiae. Mol Cell Biol 13 : 3744–3755. 8388545