Something Silent This Way Forms: the Functional Organization of the Repressive Nuclear Compartment

Overview

Journal Annu Rev Cell Dev Biol

Publisher Annual Reviews

Specialty Cell Biology

Date 2013 Jul 10

PMID 23834025

Citations 65

Authors

Joan C Ritland Politz

David Scalzo

Mark Groudine

Affiliations

Soon will be listed here.

Abstract

The repressive compartment of the nucleus is comprised primarily of telomeric and centromeric regions, the silent portion of ribosomal RNA genes, the majority of transposable element repeats, and facultatively repressed genes specific to different cell types. This compartment localizes into three main regions: the peripheral heterochromatin, perinucleolar heterochromatin, and pericentromeric heterochromatin. Both chromatin remodeling proteins and transcription of noncoding RNAs are involved in maintenance of repression in these compartments. Global reorganization of the repressive compartment occurs at each cell division, during early development, and during terminal differentiation. Differential action of chromatin remodeling complexes and boundary element looping activities are involved in mediating these organizational changes. We discuss the evidence that heterochromatin formation and compartmentalization may drive nuclear organization.

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References

Weintraub H, Groudine M . Chromosomal subunits in active genes have an altered conformation. Science. 1976; 193(4256):848-56. DOI: 10.1126/science.948749. View

Alexander R, Fang G, Rozowsky J, Snyder M, Gerstein M . Annotating non-coding regions of the genome. Nat Rev Genet. 2010; 11(8):559-71. DOI: 10.1038/nrg2814. View

KELLUM R, Schedl P . A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol. 1992; 12(5):2424-31. PMC: 364415. DOI: 10.1128/mcb.12.5.2424-2431.1992. View

Pluta A, Earnshaw W . Specific interaction between human kinetochore protein CENP-C and a nucleolar transcriptional regulator. J Biol Chem. 1996; 271(31):18767-74. DOI: 10.1074/jbc.271.31.18767. View

Pidoux A, Allshire R . The role of heterochromatin in centromere function. Philos Trans R Soc Lond B Biol Sci. 2005; 360(1455):569-79. PMC: 1569473. DOI: 10.1098/rstb.2004.1611. View

Follmer N, Wani A, Francis N . A polycomb group protein is retained at specific sites on chromatin in mitosis. PLoS Genet. 2013; 8(12):e1003135. PMC: 3527277. DOI: 10.1371/journal.pgen.1003135. View

Yusufzai T, Tagami H, Nakatani Y, Felsenfeld G . CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell. 2004; 13(2):291-8. DOI: 10.1016/s1097-2765(04)00029-2. View

Pollex T, Heard E . Recent advances in X-chromosome inactivation research. Curr Opin Cell Biol. 2012; 24(6):825-32. DOI: 10.1016/j.ceb.2012.10.007. View

Cabianca D, Casa V, Bodega B, Xynos A, Ginelli E, Tanaka Y . A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell. 2012; 149(4):819-31. PMC: 3350859. DOI: 10.1016/j.cell.2012.03.035. View

10.

Rajapakse I, Groudine M . On emerging nuclear order. J Cell Biol. 2011; 192(5):711-21. PMC: 3051810. DOI: 10.1083/jcb.201010129. View

11.

Lieberman-Aiden E, van Berkum N, Williams L, Imakaev M, Ragoczy T, Telling A . Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009; 326(5950):289-93. PMC: 2858594. DOI: 10.1126/science.1181369. View

12.

van Steensel B, Dekker J . Genomics tools for unraveling chromosome architecture. Nat Biotechnol. 2010; 28(10):1089-95. PMC: 3023824. DOI: 10.1038/nbt.1680. View

13.

McStay B, Grummt I . The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol. 2008; 24:131-57. DOI: 10.1146/annurev.cellbio.24.110707.175259. View

14.

He B, Caudy A, Parsons L, Rosebrock A, Pane A, Raj S . Mapping the pericentric heterochromatin by comparative genomic hybridization analysis and chromosome deletions in Drosophila melanogaster. Genome Res. 2012; 22(12):2507-19. PMC: 3514680. DOI: 10.1101/gr.137406.112. View

15.

Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M . G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 2002; 16(14):1779-91. PMC: 186403. DOI: 10.1101/gad.989402. View

16.

Mayer C, Neubert M, Grummt I . The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep. 2008; 9(8):774-80. PMC: 2515205. DOI: 10.1038/embor.2008.109. View

17.

Phillips J, Corces V . CTCF: master weaver of the genome. Cell. 2009; 137(7):1194-211. PMC: 3040116. DOI: 10.1016/j.cell.2009.06.001. View

18.

Ottaviani A, Schluth-Bolard C, Rival-Gervier S, Boussouar A, Rondier D, Foerster A . Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF. EMBO J. 2009; 28(16):2428-36. PMC: 2735173. DOI: 10.1038/emboj.2009.201. View

19.

Halic M, Moazed D . Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell. 2010; 140(4):504-16. PMC: 3020400. DOI: 10.1016/j.cell.2010.01.019. View

20.

Doucet A, Hulme A, Sahinovic E, Kulpa D, Moldovan J, Kopera H . Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet. 2010; 6(10). PMC: 2951350. DOI: 10.1371/journal.pgen.1001150. View