Stochastic expression and epigenetic memory at the yeast HO promoter

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 34, 2013, Pages 14012-14017

  Zhang, Qian ^a   Yoon, Youngdae ^a   Yu, Yaxin ^b   Parnell, Emily J ^b   Garay, Juan Antonio Raygoza ^a   Mwangi, Michael M ^a   Cross, Frederick R ^c   Stillman, David J ^b   Bai, Lu ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Gene expression noise; HO regulation; Single cell measurement; Stochastic gene expression

Indexed keywords

ARTICLE; EPIGENETICS; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; HISTONE ACETYLATION; HO GENE; MEMORY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; YEAST;

GENE EXPRESSION NOISE; HO REGULATION; SINGLE-CELL MEASUREMENT; STOCHASTIC GENE EXPRESSION;

ACETYLATION; CHROMATIN IMMUNOPRECIPITATION; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, FLUORESCENCE; MUTAGENESIS; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STOCHASTIC PROCESSES; TIME-LAPSE IMAGING;

EID: 84882792164     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306113110     Document Type: Article

References (37)

1. Rando OJ, Winston F (2012) Chromatin and transcription in yeast. Genetics 190(2): 351-387.
2. Yuan G, Zhu B (2012) Histone variants and epigenetic inheritance. Biochim Biophys Acta 1819(3-4):222-229.
3. Ptashne M (2007) On the use of the word 'epigenetic' Curr Biol 17(7):R233-R236.
4. Bai L, Charvin G, Siggia ED, Cross FR (2010) Nucleosome-depleted regions in cell-cycleregulated promoters ensure reliable gene expression in every cell cycle. Dev Cell 18(4): 544-555.
5. Nasmyth K (1993) Regulating the HO endonuclease in yeast. Curr Opin Genet Dev 3(2):286-294.
6. Cosma MP, Tanaka T, Nasmyth K (1999) Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell 97(3):299-311.
7. Takahata S, Yu Y, Stillman DJ (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol Cell 34(4):405-415.
8. Mitra D, Parnell EJ, Landon JW, Yu Y, Stillman DJ (2006) SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol Cell Biol 26(11):4095-4110.
9. Cosma MP, Panizza S, Nasmyth K (2001) Cdk1 triggers association of RNA polymerase to cell cycle promoters only after recruitment of the mediator by SBF. Mol Cell 7(6): 1213-1220.
10. Sil A, Herskowitz I (1996) Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell 84(5):711-722.
11. Mateus C, Avery SV (2000) Destabilized green fluorescent protein for monitoring dynamic changes in yeast gene expression with flow cytometry. Yeast 16(14):1313-1323.
12. Bean JM, Siggia ED, Cross FR (2006) Coherence and timing of cell cycle start examined at single-cell resolution. Mol Cell 21(1):3-14.
13. Charvin G, Cross FR, Siggia ED (2008) A microfluidic device for temporally controlled gene expression and long-term fluorescent imaging in unperturbed dividing yeast cells. PLoS ONE 3(1):e1468.
14. Di Talia S, SkotheimJM, Bean JM, Siggia ED, Cross FR (2007) The effects ofmolecular noise and size control on variability in the budding yeast cell cycle. Nature 448(7156):947-951.
15. Colman-Lerner A, Chin TE, Brent R (2001) Yeast Cbk1 and Mob2 activate daughterspecific genetic programs to induce asymmetric cell fates. Cell 107(6):739-750.
16. Dohrmann PR, Voth WP, Stillman DJ (1996) Role of negative regulation in promoter specificity of the homologous transcriptional activators Ace2p and Swi5p. Mol Cell Biol 16(4):1746-1758.
17. Dohrmann PR, et al. (1992) Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Genes Dev 6(1):93-104.
18. Krebs JE, Kuo MH, Allis CD, Peterson CL (1999) Cell cycle-regulated histone acetylation required for expression of the yeast HO gene. Genes Dev 13(11):1412-1421.
19. Carrozza MJ, et al. (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123(4): 581-592.
20. Takahata S, Yu Y, Stillman DJ (2011) Repressive chromatin affects factor binding at yeast HO (homothallic switching) promoter. J Biol Chem 286(40):34809-34819.
21. Biswas D, Takahata S, Stillman DJ (2008) Different genetic functions for the Rpd3(L) and Rpd3(S) complexes suggest competition between NuA4 and Rpd3(S). Mol Cell Biol 28(14):4445-4458.
22. Koch C, Schleiffer A, Ammerer G, Nasmyth K (1996) Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2. Genes Dev 10(2):129-141.
23. Nasmyth K (1985) A repetitive DNA sequence that confers cell-cycle START (CDC28)-dependent transcription of the HO gene in yeast. Cell 42(1):225-235.
24. Ferrell JE, Jr., et al. (2009) Simple, realistic models of complex biological processes: Positive feedback and bistability in a cell fate switch and a cell cycle oscillator. FEBS Lett 583(24):3999-4005.
25. Ingolia NT, Murray AW (2007) Positive-feedback loops as a flexible biological module. Curr Biol 17(8):668-677.
26. Breeden L, Mikesell GE (1991) Cell cycle-specific expression of the SWI4 transcription factor is required for the cell cycle regulation of HO transcription. Genes Dev 5(7): 1183-1190.
27. Swain PS, Elowitz MB, Siggia ED (2002) Intrinsic and extrinsic contributions to stochasticity in gene expression. Proc Natl Acad Sci USA 99(20):12795-12800.
28. Xu EY, Zawadzki KA, Broach JR (2006) Single-cell observations reveal intermediate transcriptional silencing states. Mol Cell 23(2):219-229.
29. Biggar SR, Crabtree GR (2001) Cell signaling can direct either binary or graded transcriptional responses. EMBO J 20(12):3167-3176.
30. Raser JM, O'Shea EK (2004) Control of stochasticity in eukaryotic gene expression. Science 304(5678):1811-1814.
31. Boeger H, Griesenbeck J, Strattan JS, Kornberg RD (2004) Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol Cell 14(5):667-673.
32. Xu M, et al. (2010) Partitioning of histone H3-H4 tetramers during DNA replicationdependent chromatin assembly. Science 328(5974):94-98.
33. Jackson V, Shires A, Tanphaichitr N, Chalkley R (1976) Modifications to histones immediately after synthesis. J Mol Biol 104(2):471-483.
34. Allis CD, Chicoine LG, Richman R, Schulman IG (1985) Deposition-related histone acetylation in micronuclei of conjugating Tetrahymena. Proc Natl Acad Sci USA 82(23):8048-8052.
35. Ma XJ, Wu J, Altheim BA, Schultz MC, Grunstein M (1998) Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci USA 95(12):6693-6698.
36. Bonasio R, Tu S, Reinberg D (2010) Molecular signals of epigenetic states. Science 330(6004):612-616.
37. Voth WP, et al. (2007) Forkhead proteins control the outcome of transcription factor binding by antiactivation. EMBO J 26(20):4324-4334.