Chromatin Dynamics and the RNA Exosome Function in Concert to Regulate Transcriptional Homeostasis

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2015 Nov 21

PMID 26586442

Citations 27

Authors

Mayuri Rege

Vidya Subramanian

Chenchen Zhu

Tsung-Han S Hsieh

Assaf Weiner

Nir Friedman

Sandra Clauder-Munster

Lars M Steinmetz

Oliver J Rando

Laurie A Boyer

Craig L Peterson

Affiliations

Soon will be listed here.

Abstract

The histone variant H2A.Z is a hallmark of nucleosomes flanking promoters of protein-coding genes and is often found in nucleosomes that carry lysine 56-acetylated histone H3 (H3-K56Ac), a mark that promotes replication-independent nucleosome turnover. Here, we find that H3-K56Ac promotes RNA polymerase II occupancy at many protein-coding and noncoding loci, yet neither H3-K56Ac nor H2A.Z has a significant impact on steady-state mRNA levels in yeast. Instead, broad effects of H3-K56Ac or H2A.Z on RNA levels are revealed only in the absence of the nuclear RNA exosome. H2A.Z is also necessary for the expression of divergent, promoter-proximal noncoding RNAs (ncRNAs) in mouse embryonic stem cells. Finally, we show that H2A.Z functions with H3-K56Ac to facilitate formation of chromosome interaction domains (CIDs). Our study suggests that H2A.Z and H3-K56Ac work in concert with the RNA exosome to control mRNA and ncRNA expression, perhaps in part by regulating higher-order chromatin structures.

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References

Alcid E, Tsukiyama T . ATP-dependent chromatin remodeling shapes the long noncoding RNA landscape. Genes Dev. 2014; 28(21):2348-60. PMC: 4215180. DOI: 10.1101/gad.250902.114. View

Fox M, Gao H, Smith-Kinnaman W, Liu Y, Mosley A . The exosome component Rrp6 is required for RNA polymerase II termination at specific targets of the Nrd1-Nab3 pathway. PLoS Genet. 2015; 11(2):e1004999. PMC: 4378619. DOI: 10.1371/journal.pgen.1004999. View

Xue Y, Van C, Pradhan S, Su T, Gehrke J, Kuryan B . The Ino80 complex prevents invasion of euchromatin into silent chromatin. Genes Dev. 2015; 29(4):350-5. PMC: 4335291. DOI: 10.1101/gad.256255.114. View

Hainer S, Gu W, Carone B, Landry B, Rando O, Mello C . Suppression of pervasive noncoding transcription in embryonic stem cells by esBAF. Genes Dev. 2015; 29(4):362-78. PMC: 4335293. DOI: 10.1101/gad.253534.114. View

Zofall M, Fischer T, Zhang K, Zhou M, Cui B, Veenstra T . Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature. 2009; 461(7262):419-22. PMC: 2746258. DOI: 10.1038/nature08321. View

Halley J, Kaplan T, Wang A, Kobor M, Rine J . Roles for H2A.Z and its acetylation in GAL1 transcription and gene induction, but not GAL1-transcriptional memory. PLoS Biol. 2010; 8(6):e1000401. PMC: 2889906. DOI: 10.1371/journal.pbio.1000401. View

Morillo-Huesca M, Clemente-Ruiz M, Andujar E, Prado F . The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z. PLoS One. 2010; 5(8):e12143. PMC: 2920830. DOI: 10.1371/journal.pone.0012143. View

Schaeffer D, van Hoof A . Different nuclease requirements for exosome-mediated degradation of normal and nonstop mRNAs. Proc Natl Acad Sci U S A. 2011; 108(6):2366-71. PMC: 3038778. DOI: 10.1073/pnas.1013180108. View

Pappas Jr D, Hampsey M . Functional interaction between Ssu72 and the Rpb2 subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol Cell Biol. 2000; 20(22):8343-51. PMC: 102141. DOI: 10.1128/MCB.20.22.8343-8351.2000. View

10.

Dekker J, Rippe K, Dekker M, Kleckner N . Capturing chromosome conformation. Science. 2002; 295(5558):1306-11. DOI: 10.1126/science.1067799. View

11.

Dichtl B, Blank D, Ohnacker M, Friedlein A, Roeder D, Langen H . A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol Cell. 2002; 10(5):1139-50. DOI: 10.1016/s1097-2765(02)00707-4. View

12.

Mizuguchi G, Shen X, Landry J, Wu W, Sen S, Wu C . ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 2003; 303(5656):343-8. DOI: 10.1126/science.1090701. View

13.

Krishnamurthy S, He X, Reyes-Reyes M, Moore C, Hampsey M . Ssu72 Is an RNA polymerase II CTD phosphatase. Mol Cell. 2004; 14(3):387-94. DOI: 10.1016/s1097-2765(04)00235-7. View

14.

Longtine M, McKenzie 3rd A, DeMarini D, Shah N, Wach A, Brachat A . Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998; 14(10):953-61. DOI: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U. View

15.

Xu F, Zhang K, Grunstein M . Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell. 2005; 121(3):375-85. DOI: 10.1016/j.cell.2005.03.011. View

16.

Wyers F, Rougemaille M, Badis G, Rousselle J, Dufour M, Boulay J . Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell. 2005; 121(5):725-37. DOI: 10.1016/j.cell.2005.04.030. View

17.

Zhang H, Roberts D, Cairns B . Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell. 2005; 123(2):219-31. PMC: 2788555. DOI: 10.1016/j.cell.2005.08.036. View

18.

Raisner R, Hartley P, Meneghini M, Bao M, Liu C, Schreiber S . Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin. Cell. 2005; 123(2):233-48. PMC: 2039754. DOI: 10.1016/j.cell.2005.10.002. View

19.

David L, Huber W, Granovskaia M, Toedling J, Palm C, Bofkin L . A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci U S A. 2006; 103(14):5320-5. PMC: 1414796. DOI: 10.1073/pnas.0601091103. View

20.

Iuchi S, Marsch-Moreno M, Velez-delValle C, Easley K, Kuri-Harcuch W, Green H . An immortalized drug-resistant cell line established from 12-13-day mouse embryos for the propagation of human embryonic stem cells. Differentiation. 2006; 74(4):160-6. DOI: 10.1111/j.1432-0436.2006.00067.x. View