Xbp1 Directs Global Repression of Budding Yeast Transcription during the Transition to Quiescence and Is Important for the Longevity and Reversibility of the Quiescent State

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Pure populations of quiescent yeast can be obtained from stationary phase cultures that have ceased proliferation after exhausting glucose and other carbon sources from their environment. They are uniformly arrested in the G1 phase of the cell cycle, and display very high thermo-tolerance and longevity. We find that G1 arrest is initiated before all the glucose has been scavenged from the media. Maintaining G1 arrest requires transcriptional repression of the G1 cyclin, CLN3, by Xbp1. Xbp1 is induced as glucose is depleted and it is among the most abundant transcripts in quiescent cells. Xbp1 binds and represses CLN3 transcription and in the absence of Xbp1, or with extra copies of CLN3, cells undergo ectopic divisions and produce very small cells. The Rad53-mediated replication stress checkpoint reinforces the arrest and becomes essential when Cln3 is overproduced. The XBP1 transcript also undergoes metabolic oscillations under glucose limitation and we identified many additional transcripts that oscillate out of phase with XBP1 and have Xbp1 binding sites in their promoters. Further global analysis revealed that Xbp1 represses 15% of all yeast genes as they enter the quiescent state and over 500 of these transcripts contain Xbp1 binding sites in their promoters. Xbp1-repressed transcripts are highly enriched for genes involved in the regulation of cell growth, cell division and metabolism. Failure to repress some or all of these targets leads xbp1 cells to enter a permanent arrest or senescence with a shortened lifespan.

Vyšlo v časopise: Xbp1 Directs Global Repression of Budding Yeast Transcription during the Transition to Quiescence and Is Important for the Longevity and Reversibility of the Quiescent State. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003854
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003854

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Zdroje

1. AllenC, ButtnerS, AragonAD, ThomasJA, MeirellesO, et al. (2006) Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J Cell Biol 174 (1) 89–100.

2. DavidsonGS, JoeRM, RoyS, MeirellesO, AllenCP, et al. (2011) The proteomics of quiescent and non-quiescent cell differentiation in yeast stationary-phase cultures. Mol Biol Cell 22 (7) 988–98.

3. LillieSH (1980) PringleJR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143 (3) 1384–1394.

4. ShiL, SutterBM, YeX (2010) TuBP (2010) Trehalose Is a Key Determinant of the Quiescent Metabolic State That Fuels Cell Cycle Progression upon Return to Growth. Mol Biol Cell 21: 1982–1990.

5. McInernyCJ, PartridgeJF, MikesellGE, CreemerDP (1997) BreedenLL (1997) A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription. Genes Dev 11 (10) 1277–1288.

6. TyersM, TokiwaG (1993) FutcherB (1993) Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J 12: 1955–1968.

7. CostanzoM, NishikawaJL, TangX, MillmanJS, SchubO, et al. (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117 (7) 899–913.

8. de BruinRA, McDonaldWH, KalashnikovaTI, YatesJ (2004) Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 117 (7) 887–898.

9. ZegermanP (2009) DiffleyJF (2009) DNA replication as a target of the DNA damage checkpoint. DNA Repair (Amst) 8 (9) 1077–1088.

10. NashR, TokiwaG, AnandS, EricksonK (1988) FutcherAB (1988) The WHI1 gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J 7: 4335–4346.

11. CrossFR (1988) DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae. Mol Cell Biol 8: 4675–4684.

12. BarbetNC, SchneiderU, HelliwellSB, StansfieldI, TuiteMF, et al. (1996) TOR controls translation initiation and early G1 progression in yeast. Mol Biol Cell 7: 25–42.

13. AndalisAA, StorchovaZ, StylesC, GalitskiT, PellmanD, et al. (2004) Defects arising from whole-genome duplications in Saccharomyces cerevisiae. Genetics 167 (3) 1109–1121.

14. MaiB (1997) BreedenL (1997) Xbp1, a stress-induced transcriptional repressor of the saccharomyces cerevisiae Swi4/Mbp1 family. Mol Cell Biol 17 (11) 6491–6501.

15. MaiB (2000) BreedenL (2000) CLN1 and its repression by Xbp1 are important for efficient sporulation in budding yeast. Mol Cell Biol 20: 478–487.

16. LiuL, LiY, LiS, HuN, HeY, et al. (2012) Comparison of next-generation sequencing systems. Journal of biomedicine & biotechnology 2012: 251364.

17. NewcombLL, HallDD (2002) HeidemanW (2002) AZF1 is a glucose-dependent positive regulator of CLN3 transcription in Saccharomyces cerevisiae. Mol Cell Biol 22 (5) 1607–1614.

18. ParvizF, HallDD, MarkwardtDD (1998) HeidemanW (1998) Transcriptional Regulation of CLN3 Expression by Glucose in Saccharomyces cerevisiae. J Bacteriol 180: 4508–4515.

19. TaoR, ChenH, GaoC, XueP, YangF, et al. (2011) Xbp1-mediated histone H4 deacetylation contributes to DNA double-strand break repair in yeast. Cell Res 1 (11) 1619–33.

20. SopkoR, HuangD, PrestonN, ChuaG, PappB, et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21 (3) 319–330.

21. TanakaS (2002) DiffleyJF (2002) Deregulated G1-cyclin expression induces genomic instability by preventing efficient pre-RC formation. Genes Dev 16 (20) 2639–2649.

22. SidorovaJ (2002) BreedenLL (2002) Precocious S-phase entry in budding yeast prolongs replicative state and increases dependence upon Rad53 for viability. Genetics 160: 123–136.

23. VallenEA (1999) CrossFR (1999) Interaction Between the MEC1-Dependent DNA synthesis Checkpoint and G1 Cyclin Function in Saccaromyces Cerevisiae. Genetics 151: 459–471.

24. AllenJB, ZhouZ, SiedeW, FriedbergEC (1994) ElledgeSJ (1994) The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes & Dev 8 (20) 2401–2415.

25. BurtnerCR, MurakamiCJ, KennedyBK (2009) KaeberleinM (2009) A molecular mechanism of chronological aging in yeast. Cell Cycle 8 (8) 1256–1270.

26. WeinbergerM, RamachandranL, FengL, SharmaK, SunX, et al. (2005) Apoptosis in budding yeast caused by defects in initiation of DNA replication. J Cell Sci 118 (Pt 15) 3543–3553.

27. BurhansWC, WeinbergerM, MarchettiMA, RamachandranL, D'UrsoG, et al. (2003) Apoptosis-like yeast cell death in response to DNA damage and replication defects. Mutat Res 532 (1–2) 227–243.

28. WeinertTA, HartwellLH (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241 (4863) 317–322.

29. SunZ, HsiaoJ, FayDS (1998) SternDF (1998) Rad53 FHA Domain Associated with Phosphorylated Rad9 in the DNA Damage Checkpoint. Science 281: 272–274.

30. VialardJE, GilbertCS, GreenCM (1998) LowndesNF (1998) The Budding Yeast Rad9 Checkpoint Protein is Subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J 17: 5679–5688.

31. TuBP, KudlickiA, RowickaM (2005) McKnightSL (2005) Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310 (5751) 1152–1158.

32. HibbsMA, HessDC, MyersCL, HuttenhowerC, LiK, et al. (2007) Exploring the functional landscape of gene expression: directed search of large microarray compendia. Bioinformatics 23 (20) 2692–2699.

33. GrundyWN, BaileyTL, ElkanCP (1997) BakerME (1997) Meta-MEME: motif-based hidden Markov models of protein families. Comput Appl Biosci 13 (4) 397–406.

34. van HeldenJ (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31 (13) 3593–3596.

35. KudlickiA, RowickaM (2007) OtwinowskiZ (2007) SCEPTRANS: an online tool for analyzing periodic transcription in yeast. Bioinformatics 23 (12) 1559–1561.

36. BiE (2012) ParkHO (2012) Cell polarization and cytokinesis in budding yeast. Genetics 191 (2) 347–387.

37. McMurrayMA (2009) ThornerJ (2009) Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div 4: 18.

38. MehtaGD, RizviSM (2012) GhoshSK (2012) Cohesin: a guardian of genome integrity. Biochim Biophys Acta 1823 (8) 1324–1342.

39. BreedenL (1987) NasmythK (1987) Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48: 389–397.

40. LoyCJ, LydallD (1999) SuranaU (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.

41. LorenzMC (1998) HeitmanJ (1998) Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics 150 (4) 1443–1457.

42. SmithHE, SuSS, NeigebornL, DriscollSE (1990) MitchellAP (1990) Role of IME1 expression in regulation of meiosis in Saccharomyces cerevisiae. Mol Cell Biol 10 (12) 6103–6113.

43. Colman-LernerA, ChinTE (2001) BrentR (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107 (6) 739–750.

44. OrleanP (2012) Architecture and Biosynthesis of the Saccharomyces cerevisiae Cell Wall. Genetics 192 (3) 775–818.

45. RichardsonH, LewDJ, HenzeM, SugimotK (1992) ReedSI (1992) Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes & Dev 6: 2021–2034.

46. TennysonCN, LeeJ (1998) AndrewsBJ (1998) A role for the Pcl9-Pho85 cyclin-cdk complex at the M/G1 boundary in Saccharomyces cerevisiae. Mol Microbiol 28 (1) 69–79.

47. WarnerJR (1999) The economics of ribosome biosynthesis in yeast. TIBS 24: 437–440.

48. LiL, LuY, QinLX, Bar-JosephZ, Werner-WashburneM, et al. (2009) Budding yeast SSD1-V regulates transcript levels of many longevity genes and extends chronological life span in purified quiescent cells. Mol Biol Cell 20 (17) 3851–3864.

49. JossenR (2013) BermejoR (2013) The DNA damage checkpoint response to replication stress: A Game of Forks. Frontiers in genetics 4: 26.

50. Di MiccoR, FumagalliM, CicaleseA, PiccininS, GaspariniP, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444 (7119) 638–642.

51. BartkovaJ, RezaeiN, LiontosM, KarakaidosP, KletsasD, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444 (7119) 633–637.

52. MadeoF, Carmona-GutierrezD, RingJ, ButtnerS, EisenbergT, et al. (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382 (2) 227–231.

53. HarbisonCT, GordonDB, LeeTI, RinaldiNJ, MacisaacKD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431 (7004) 99–104.

54. ReimandJ, VaquerizasJM, ToddAE, ViloJ (2010) LuscombeNM (2010) Comprehensive reanalysis of transcription factor knockout expression data in Saccharomyces cerevisiae reveals many new targets. Nucleic Acids Res 38 (14) 4768–4777.

55. ZhuC, ByersKJ, McCordRP, ShiZ, BergerMF, et al. (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19 (4) 556–566.

56. TuBP (2006) McKnightSL (2006) Metabolic cycles as an underlying basis of biological oscillations. Nat Rev Mol Cell Biol 7 (9) 696–701.

57. RowickaM, KudlickiA, TuBP (2007) OtwinowskiZ (2007) High-resolution timing of cell cycle-regulated gene expression. Proc Natl Acad Sci U S A 104 (43) 16892–16897.

58. ShiL (2013) TuBP (2013) Acetyl-CoA induces transcription of the key G1 cyclin CLN3 to promote entry into the cell division cycle in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 110 (18) 7318–23.

59. ChoRJ, CampbellMJ, WinzelerEA, SteinmetzL, ConwayA, et al. (1998) A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell 2: 65–73.

60. SpellmanPT, SherlockG, ZhangMQ, IyerVR, AndersK, et al. (1998) Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9 (12) 3273–3297.

61. PramilaT, MilesS, GuhaThakurtaD, JemiloD (2002) BreedenLL (2002) Conserved homeodomain proteins interact with MADS box protein Mcm1 to restrict ECB-dependent transcription to the M/G1 phase of the cell cycle. Genes & Dev 16: 3034–3045.

62. GranovskaiaMV, JensenLJ, RitchieME, ToedlingJ, NingY, et al. (2010) High-resolution transcription atlas of the mitotic cell cycle in budding yeast. Genome Biol 11 (3) R24.

63. CastelliLM, LuiJ, CampbellSG, RoweW, ZeefLA, et al. (2011) Glucose depletion inhibits translation initiation via eIF4A loss and subsequent 48S preinitiation complex accumulation, while the pentose phosphate pathway is coordinately up-regulated. Mol Biol Cell 22 (18) 3379–3393.

64. WittenbergC (2005) ReedSI (2005) Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes. Oncogene 24 (17) 2746–2755.

65. GimenoCJ (1994) FinkGR (1994) Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol Cell Biol 14: 2100–2112.

66. PanX (2000) HeitmanJ (2000) Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol Cell Biol 20 (22) 8364–8372.

67. WardMP, GimenoCJ, FinkGR (1995) GarrettS (1995) SOK2 may regulate cyclic AMP-dependent protein kinase-stimulated growth and pseudohyphal development by repressing transcription. Mol Cell Biol 15 (12) 6854–6863.

68. MiledC, MannC (2001) FayeG (2001) Xbp1-Mediated Repression of CLB Gene Expression Contributes to the Modifications of Yeast Cell Morphology and Cell Cycle See during Nitrogen-Limited Growth. Mol Cell Biol 21 (11) 3714–3724.

69. NobileCJ, FoxEP, NettJE, SorrellsTR, MitrovichQM, et al. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148 (1–2) 126–138.

70. LengelerKB, TielkerD (2008) ErnstJF (2008) Protein-O-mannosyltransferases in virulence and development. Cell Mol Life Sci 65 (4) 528–544.

71. RouabhiaM, SemlaliA, ChandraJ, MukherjeeP, ChmielewskiW, et al. (2012) Disruption of the ECM33 gene in Candida albicans prevents biofilm formation, engineered human oral mucosa tissue damage and gingival cell necrosis/apoptosis. Mediators of inflammation 2012: 398207.

72. NettJE, SanchezH, CainMT, RossKM (2011) AndesDR (2011) Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot Cell 10 (12) 1660–1669.

73. SikorskiRS (1989) HieterP (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27.

74. LongtineMS, McKenzieAIII, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cervisiae. Yeast 14: 953–961.

75. TrapnellC, PachterL (2009) SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (9) 1105–1111.

76. AndersS (2010) HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11 (10) R106.

77. RigautG, ShevchenkoA, RutzB, WilmM, MannM, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030–1032.

78. EzhkovaE (2006) TanseyWP (2006) Chromatin immunoprecipitation to study protein-DNA interactions in budding yeast. Methods Mol Biol 313: 225–244.