Modulations of SIR-nucleosome Interactions of Reconstructed Yeast Silent Pre-heterochromatin by O-acetyl-ADP-ribose and Magnesium

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2016 Dec 10

PMID 27932495

Citations 6

Authors

Shu-Yun Tung

Sue-Hong Wang

Sue-Ping Lee

Shu-Ping Tsai

Hsiao-Hsuian Shen

Feng-Jung Chen

Yu-Yi Wu

Sheng-Pin Hsiao

Gunn-Guang Liou

Affiliations

Soon will be listed here.

Abstract

Yeast silent heterochromatin provides an excellent model with which to study epigenetic inheritance. Previously we developed an in vitro assembly system to demonstrate the formation of filament structures with requirements that mirror yeast epigenetic gene silencing in vivo. However, the properties of these filaments were not investigated in detail. Here we show that the assembly system requires Sir2, Sir3, Sir4, nucleosomes, and O-acetyl-ADP-ribose. We also demonstrate that all Sir proteins and nucleosomes are components of these filaments to prove that they are SIR-nucleosome filaments. Furthermore, we show that the individual localization patterns of Sir proteins on the SIR-nucleosome filament reflect those patterns on telomeres in vivo. In addition, we reveal that magnesium exists in the SIR-nucleosome filament, with a role similar to that for chromatin condensation. These results suggest that a small number of proteins and molecules are sufficient to mediate the formation of a minimal yeast silent pre-heterochromatin in vitro.

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References

Tanner K, Landry J, Sternglanz R, Denu J . Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc Natl Acad Sci U S A. 2000; 97(26):14178-82. PMC: 18891. DOI: 10.1073/pnas.250422697. View

Shintomi K, Takahashi T, Hirano T . Reconstitution of mitotic chromatids with a minimum set of purified factors. Nat Cell Biol. 2015; 17(8):1014-23. DOI: 10.1038/ncb3187. View

Rudner A, Hall B, Ellenberger T, Moazed D . A nonhistone protein-protein interaction required for assembly of the SIR complex and silent chromatin. Mol Cell Biol. 2005; 25(11):4514-28. PMC: 1140625. DOI: 10.1128/MCB.25.11.4514-4528.2005. View

Sperling A, Grunstein M . Histone H3 N-terminus regulates higher order structure of yeast heterochromatin. Proc Natl Acad Sci U S A. 2009; 106(32):13153-9. PMC: 2726386. DOI: 10.1073/pnas.0906866106. View

Yang B, Kirchmaier A . Bypassing the catalytic activity of SIR2 for SIR protein spreading in Saccharomyces cerevisiae. Mol Biol Cell. 2006; 17(12):5287-97. PMC: 1679691. DOI: 10.1091/mbc.e06-08-0669. View

Tung S, Lee K, Hong J, Lee S, Shen H, Liou G . Changes in the genome-wide localization pattern of Sir3 in Saccharomyces cerevisiae during different growth stages. Comput Struct Biotechnol J. 2014; 7:e201304001. PMC: 3962127. DOI: 10.5936/csbj.201304001. View

Aparicio O, Billington B, Gottschling D . Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell. 1991; 66(6):1279-87. DOI: 10.1016/0092-8674(91)90049-5. View

Liou G, Tanny J, Kruger R, Walz T, Moazed D . Assembly of the SIR complex and its regulation by O-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation. Cell. 2005; 121(4):515-527. DOI: 10.1016/j.cell.2005.03.035. View

Sauve A, Celic I, Avalos J, Deng H, Boeke J, Schramm V . Chemistry of gene silencing: the mechanism of NAD+-dependent deacetylation reactions. Biochemistry. 2001; 40(51):15456-63. DOI: 10.1021/bi011858j. View

10.

Derme M, Yang G, Sheagly E, Palitti F, Bustamante C . Effect of poly(ADP-ribosyl)ation and Mg2+ ions on chromatin structure revealed by scanning force microscopy. Biochemistry. 2001; 40(37):10947-55. DOI: 10.1021/bi002742a. View

11.

Strick R, Strissel P, GAVRILOV K . Cation-chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes. J Cell Biol. 2001; 155(6):899-910. PMC: 2150894. DOI: 10.1083/jcb.200105026. View

12.

Richards E, Elgin S . Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell. 2002; 108(4):489-500. DOI: 10.1016/s0092-8674(02)00644-x. View

13.

Imai S, ARMSTRONG C, Kaeberlein M, Guarente L . Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000; 403(6771):795-800. DOI: 10.1038/35001622. View

14.

Onishi M, Liou G, Buchberger J, Walz T, Moazed D . Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol Cell. 2007; 28(6):1015-28. DOI: 10.1016/j.molcel.2007.12.004. View

15.

Tanny J, Moazed D . Coupling of histone deacetylation to NAD breakdown by the yeast silencing protein Sir2: Evidence for acetyl transfer from substrate to an NAD breakdown product. Proc Natl Acad Sci U S A. 2001; 98(2):415-20. PMC: 14600. DOI: 10.1073/pnas.98.2.415. View

16.

Tanny J, Dowd G, Huang J, Hilz H, Moazed D . An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell. 2000; 99(7):735-45. DOI: 10.1016/s0092-8674(00)81671-2. View

17.

Rine J, Herskowitz I . Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987; 116(1):9-22. PMC: 1203125. DOI: 10.1093/genetics/116.1.9. View

18.

Sen D, Crothers D . Condensation of chromatin: role of multivalent cations. Biochemistry. 1986; 25(7):1495-503. DOI: 10.1021/bi00355a004. View

19.

Liou G, Jane W, Cohen S, Lin N, Lin-Chao S . RNA degradosomes exist in vivo in Escherichia coli as multicomponent complexes associated with the cytoplasmic membrane via the N-terminal region of ribonuclease E. Proc Natl Acad Sci U S A. 2001; 98(1):63-8. PMC: 14545. DOI: 10.1073/pnas.98.1.63. View

20.

Lee S, Tong L, Denu J . Quantification of endogenous sirtuin metabolite O-acetyl-ADP-ribose. Anal Biochem. 2008; 383(2):174-9. PMC: 2586145. DOI: 10.1016/j.ab.2008.08.033. View