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      The Nuclear Lamina as an Organizer of Chromosome Architecture

      review-article
      Author(s): 1 , * , 2
      Publication date (Electronic):
      Journal: Cells
      Publisher: MDPI
      Keywords: nuclear lamina, nuclear periphery, nuclear envelope, lamin, LAD, TAD, heterochromatin, HP1, H3K9me2/3

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          Abstract

          The nuclear lamina (NL) is a meshwork of lamins and lamin-associated proteins adjoining the inner side of the nuclear envelope. In early embryonic cells, the NL mainly suppresses background transcription, whereas, in differentiated cell types, its disruption affects gene expression more severely. Normally, the NL serves as a backbone for multiple chromatin anchoring sites, thus shaping the spatial organization of chromosomes in the interphase nucleus. However, upon cell senescence, aging, or in some types of terminally differentiated cells and lamin-associated diseases, the loss of NL-chromatin tethering causes drastic alterations in chromosome architecture. Here, we provide an overview of the recent advances in the field of NL-chromatin interactions, focusing on their impact on chromatin positioning, compaction, repression, and spatial organization.

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          Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain.

          A Bannister, P Zegerman, J F Partridge … (2001)
          Heterochromatin protein 1 (HP1) is localized at heterochromatin sites where it mediates gene silencing. The chromo domain of HP1 is necessary for both targeting and transcriptional repression. In the fission yeast Schizosaccharomyces pombe, the correct localization of Swi6 (the HP1 equivalent) depends on Clr4, a homologue of the mammalian SUV39H1 histone methylase. Both Clr4 and SUV39H1 methylate specifically lysine 9 of histone H3 (ref. 6). Here we show that HP1 can bind with high affinity to histone H3 methylated at lysine 9 but not at lysine 4. The chromo domain of HP1 is identified as its methyl-lysine-binding domain. A point mutation in the chromo domain, which destroys the gene silencing activity of HP1 in Drosophila, abolishes methyl-lysine-binding activity. Genetic and biochemical analysis in S. pombe shows that the methylase activity of Clr4 is necessary for the correct localization of Swi6 at centromeric heterochromatin and for gene silencing. These results provide a stepwise model for the formation of a transcriptionally silent heterochromatin: SUV39H1 places a 'methyl marker' on histone H3, which is then recognized by HP1 through its chromo domain. This model may also explain the stable inheritance of the heterochromatic state.
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            Comprehensive analysis of the chromatin landscape in Drosophila

            Peter V. Kharchenko, Artyom Alekseyenko, Yuri Schwartz … (2010)
            Summary Chromatin is composed of DNA and a variety of modified histones and non-histone proteins, which impact cell differentiation, gene regulation and other key cellular processes. We present a genome-wide chromatin landscape for Drosophila melanogaster based on 18 histone modifications, summarized by 9 prevalent combinatorial patterns. Integrative analysis with other data (non-histone chromatin proteins, DNaseI hypersensitivity, GRO-seq reads produced by engaged polymerase, short/long RNA products) reveals discrete characteristics of chromosomes, genes, regulatory elements, and other functional domains. We find that active genes display distinct chromatin signatures that are correlated with disparate gene lengths, exon patterns, regulatory functions, and genomic contexts. We also demonstrate a diversity of signatures among Polycomb targets that include a subset with paused polymerase. This systematic profiling and integrative analysis of chromatin signatures provides insights into how genomic elements are regulated, and will serve as a resource for future experimental investigations of genome structure and function.
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              Transcriptional repression mediated by repositioning of genes to the nuclear lamina.

              K Reddy, J Zullo, E Bertolino … (2008)
              Nuclear compartmentalization seems to have an important role in regulating metazoan genes. Although studies on immunoglobulin and other loci have shown a correlation between positioning at the nuclear lamina and gene repression, the functional consequences of this compartmentalization remain untested. We devised an approach for inducible tethering of genes to the inner nuclear membrane (INM), and tested the consequences of such repositioning on gene activity in mouse fibroblasts. Here, using three-dimensional DNA-immunoFISH, we demonstrate repositioning of chromosomal regions to the nuclear lamina that is dependent on breakdown and reformation of the nuclear envelope during mitosis. Moreover, tethering leads to the accumulation of lamin and INM proteins, but not to association with pericentromeric heterochromatin or nuclear pore complexes. Recruitment of genes to the INM can result in their transcriptional repression. Finally, we use targeted adenine methylation (DamID) to show that, as is the case for our model system, inactive immunoglobulin loci at the nuclear periphery are contacted by INM and lamina proteins. We propose that these molecular interactions may be used to compartmentalize and to limit the accessibility of immunoglobulin loci to transcription and recombination factors.
              Article 0 comments Cited 224 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cells
                Journal ID (iso-abbrev): Cells
                Journal ID (publisher-id): cells
                Title: Cells
                Publisher: MDPI
                ISSN (Electronic): 2073-4409
                Publication date (Electronic): 08 February 2019
                Publication date Collection: February 2019
                Volume: 8
                Issue: 2
                Electronic Location Identifier: 136
                Affiliations
                [1 ]Department of Molecular Genetics of Cell, Institute of Molecular Genetics, Russian Academy of Sciences, Moscow 123182, Russia; shevelev@ 123456img.ras.ru
                [2 ]Division of the Regulation of Transcription and Chromatin Dynamics, Institute of Gene Biology, Russian Academy of Sciences, Moscow 119334, Russia; sergey.v.ulyanov@ 123456gmail.com
                Author notes
                [* ]Correspondence: shevelev@ 123456img.ras.ru ; Tel.: +7-499-196-0809
                Author information
                https://orcid.org/0000-0002-0568-9236
                Article
                Publisher ID: cells-08-00136
                DOI: 10.3390/cells8020136
                PMC ID: 6406483
                PubMed ID: 30744037
                SO-VID: eebaa765-18f6-47b7-89da-76c5050d9af3
                Copyright © © 2019 by the authors.
                License:

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 31 December 2018
                Date accepted : 06 February 2019
                Categories
                Subject: Review

                Keywords: nuclear lamina,nuclear periphery,nuclear envelope,lamin,lad,tad,heterochromatin,hp1,h3k9me2/3
                Data availability:
                Keywords: nuclear lamina, nuclear periphery, nuclear envelope, lamin, lad, tad, heterochromatin, hp1, h3k9me2/3

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