Barriers and silencers: A theoretical toolkit for control and containment of nucleosome-based epigenetic states

Journal of Molecular Biology

Volumn 414, Issue 4, 2011, Pages 624-637

  Dodd, Ian B ^a,b   Sneppen, Kim ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

bistability; chromatin; nucleosome modification; positive feedback; stochastic modeling

Indexed keywords

DNA BINDING PROTEIN;

ARTICLE; CHROMATIN; DNA REPLICATION; EPIGENETICS; GENE SILENCING; MATING; NONHUMAN; NUCLEOSOME; POSITIVE FEEDBACK; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STOCHASTIC MODEL;

SACCHAROMYCES CEREVISIAE;

EID: 82555176534     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.10.027     Document Type: Article

References (51)

1. Braunstein M., Sobel R.E., Allis C.D., Turner B.M., and Broach J.R. Efficient transcriptional silencing in Saccharomyces cerevisiae requires a heterochromatin histone acetylation pattern Mol. Cell. Biol. 16 1996 4349 4356 (Pubitemid 26251236)
2. Grewal S.I., and Moazed D. Heterochromatin and epigenetic control of gene expression Science 301 2003 798 802 (Pubitemid 36962612)
3. Dodd I.B., Micheelsen M.A., Sneppen K., and Thon G. Theoretical analysis of epigenetic cell memory by nucleosome modification Cell 129 2007 813 822 (Pubitemid 46802381)
4. Kaufman P.D., and Rando O.J. Chromatin as a potential carrier of heritable information Curr. Opin. Cell Biol. 22 2010 284 290
5. Ptashne M. On the use of the word 'epigenetic' Curr. Biol. 17 2007 R233 R236
6. Johnson A., Li G., Sikorski T.W., Buratowski S., Woodcock C.L., and Moazed D. Reconstitution of heterochromatin-dependent transcriptional gene silencing Mol. Cell 35 2009 769 781
7. Hansen K.H., Bracken A.P., Pasini D., Dietrich N., Gehani S.S., and Monrad A. A model for transmission of the H3K27me3 epigenetic mark Nat. Cell Biol. 10 2008 1291 1300
8. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., and Drury III.W.J. Role of the polycomb protein EED in the propagation of repressive histone marks Nature 461 2009 762 767
9. Danzer J.R., and Wallrath L.L. Mechanisms of HP1-mediated gene silencing in Drosophila Development 131 2004 3571 3580 (Pubitemid 39199368)
10. Wysocka J., Swigut T., Milne T.A., Dou Y., Zhang X., and Burlingame A.L. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development Cell 121 2005 859 872 (Pubitemid 40806418)
11. Sedighi M., and Sengupta A.M. Epigenetic chromatin silencing: bistability and front propagation Phys. Biol. 4 2007 246 255
12. Sneppen K., Micheelsen M.A., and Dodd I.B. Ultrasensitive gene regulation by positive feedback loops in nucleosome modification Mol. Syst. Biol. 4 2008 182
13. David-Rus D., Mukhopadhyay S., Lebowitz J.L., and Sengupta A.M. Inheritance of epigenetic chromatin silencing J. Theor. Biol. 258 2009 112 120
14. Mukhopadhyay S., Nagaraj V.H., and Sengupta A.M. Locus dependence in epigenetic chromatin silencing Biosystems 102 2010 49 54
15. Micheelsen M.A., Mitarai N., Sneppen K., and Dodd I.B. Theory for the stability and regulation of epigenetic landscapes Phys. Biol. 7 2010 026010
16. Deal R.B., Henikoff J.G., and Henikoff S. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones Science 328 2010 1161 1164
17. Thomas R., and Kaufman M. Multistationarity, the basis of cell differentiation and memory: I. Structural conditions of multistationarity and other nontrivial behavior Chaos 11 2001 170 179
18. Ferrell J.E. Jr Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability Curr. Opin. Cell Biol. 14 2002 140 148 (Pubitemid 34219501)
19. Maeda R.K., and Karch F. The ABC of the BX-C: the bithorax complex explained Development 133 2006 1413 1422 (Pubitemid 43732955)
20. Chow J., and Heard E. X inactivation and the complexities of silencing a sex chromosome Curr. Opin. Cell Biol. 21 2009 359 366
21. Rusché L.N., Kirchmaier A.L., and Rine J. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae Annu. Rev. Biochem. 72 2003 481 516 (Pubitemid 36930453)
22. Lynch P.J., and Rusché L.N. A silencer promotes the assembly of silenced chromatin independently of recruitment Mol. Cell. Biol. 29 2009 43 56
23. Cheng T.H., and Gartenberg M.R. Yeast heterochromatin is a dynamic structure that requires silencers continuously Genes Dev. 14 2000 452 463 (Pubitemid 30131890)
24. Gaszner M., and Felsenfeld G. Insulators: exploiting transcriptional and epigenetic mechanisms Nat. Rev. Genet. 7 2006 703 713 (Pubitemid 44260006)
25. Donze D., and Kamakaka R.T. RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae EMBO J. 20 2001 520 531 (Pubitemid 32126987)
26. Ishii K., and Laemmli U.K. Structural and dynamic functions establish chromatin domains Mol. Cell 11 2003 237 248 (Pubitemid 36126604)
27. Bi X., Yu Q., Sandmeier J.J., and Zou Y. Formation of boundaries of transcriptionally silent chromatin by nucleosome-excluding structures Mol. Cell. Biol. 24 2004 2118 2131 (Pubitemid 38248950)
28. Ferrari S., Simmen K.C., Dusserre Y., Muller K., Fourel G., Gilson E., and Mermod N. Chromatin domain boundaries delimited by a histone-binding protein in yeast J. Biol. Chem. 279 2004 55520 55530 (Pubitemid 40066554)
29. Hoppe G.J., Tanny J.C., Rudner A.D., Gerber S.A., Danaie S., Gygi S.P., and Moazed D. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation Mol. Cell. Biol. 22 2002 4167 4180 (Pubitemid 34556587)
30. Pillus L., and Rine J. Epigenetic inheritance of transcriptional states in S. cerevisiae Cell 59 1989 637 647 (Pubitemid 19282870)
31. Mahoney D.J., Marquardt R., Shei G.J., Rose A.B., and Broach J.R. Mutations in the HML E silencer of Saccharomyces cerevisiae yield metastable inheritance of transcriptional repression Genes Dev. 5 1991 605 615 (Pubitemid 21905981)
32. Sussel L., Vannier D., and Shore D. Epigenetic switching of transcriptional states: cis- and trans-acting factors affecting establishment of silencing at the HMR locus in Saccharomyces cerevisiae Mol. Cell. Biol. 13 1993 3919 3928 (Pubitemid 23187620)
33. Xu E.Y., Zawadzki K.A., and Broach J.R. Single-cell observations reveal intermediate transcriptional silencing states Mol. Cell 23 2006 219 229 (Pubitemid 44062370)
34. Martino F., Kueng S., Robinson P., Tsai-Pflugfelder M., van Leeuwen F., and Ziegler M. Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro Mol. Cell 33 2009 323 334
35. Weiss K., and Simpson R.T. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HML alpha Mol. Cell. Biol. 18 1998 5392 5403 (Pubitemid 28388122)
36. Ravindra A., Weiss K., and Simpson R.T. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMRa Mol. Cell. Biol. 19 1999 7944 7950 (Pubitemid 30413989)
37. Donze D., Adams C.R., Rine J., and Kamakaka R.T. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae Genes Dev. 13 1999 698 708 (Pubitemid 29155976)
38. Rudner A.D., Hall B.E., Ellenberger T., and Moazed D. A nonhistone protein-protein interaction required for assembly of the SIR complex and silent chromatin Mol. Cell. Biol. 25 2005 4514 4528 (Pubitemid 40705757)
39. Onishi M., Liou G.G., Buchberger J.R., Walz T., and Moazed D. Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly Mol. Cell 28 2007 1015 1028 (Pubitemid 350297032)
40. Xu F., Zhang Q.Y., Zhang K.L., Xie W., and Grunstein M. Sir2 deacetylates histone h3 lysine 56 to regulate telomeric heterochromatin structure in yeast Mol. Cell 27 2007 890 900 (Pubitemid 47488183)
41. Ng H.H., Ciccone D.N., Morshead K.B., Oettinger M.A., and Struhl K. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation Proc. Natl Acad. Sci. USA 100 2003 1820 1825 (Pubitemid 36254532)
42. Annunziato A.T. Split decision: what happens to nucleosomes during DNA replication? J. Biol. Chem. 280 2005 12065 12068
43. Meijsing S.H., and Ehrenhofer-Murray A.E. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae Genes Dev. 15 2001 3169 3182 (Pubitemid 33115680)
44. Shia W.J., Osada S., Florens L., Swanson S.K., Washburn M.P., and Workman J.L. Characterization of the yeast trimeric-SAS acetyltransferase complex J. Biol. Chem. 280 2005 11987 11994 (Pubitemid 40418516)
45. Waterborg J.H. Dynamics of histone acetylation in Saccharomyces cerevisiae Biochemistry 40 2001 2599 2605 (Pubitemid 32171735)
46. Katan-Khaykovich Y., and Struhl K. Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors Genes Dev. 16 2002 743 752 (Pubitemid 34274043)
47. Rippe K. Making contacts on a nucleic acid polymer Trends Biochem. Sci. 26 2001 733 740 (Pubitemid 34014840)
48. Ringrose L., Chabanis S., Angrand P.O., Woodroofe C., and Stewart A.F. Quantitative comparison of DNA looping in vitro and in vivo: chromatin increases effective DNA flexibility at short distances EMBO J. 18 1999 6630 6641
49. Venkatasubrahmanyam S., Hwang W.W., Meneghini M.D., Tong A.H., and Madhani H.D. Genome-wide, as opposed to local, antisilencing is mediated redundantly by the euchromatic factors Set1 and H2A.Z Proc. Natl Acad. Sci. USA 104 2007 16609 16614 (Pubitemid 350211064)
50. Smith J.S., Brachmann C.B., Pillus L., and Boeke J.D. Distribution of a limited Sir2 protein pool regulates the strength of yeast rDNA silencing and is modulated by Sir4p Genetics 149 1998 1205 1219 (Pubitemid 28334518)
51. Miele A., Bystricky K., and Dekker J. Yeast silent mating type loci form heterochromatic clusters through silencer protein-dependent long-range interactions PLoS Genet. 5 2009 e1000478