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      Changes in chromosome territory position within the nucleus reflect alternations in gene expression related to embryonic lineage specification

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          Abstract

          Loss of totipotentcy in an early embryo is directed by molecular processes responsible for cell fate decisions. Three dimensional genome organisation is an important factor linking chromatin architecture with stage specific gene expression patterns. Little is known about the role of chromosome organisation in gene expression regulation of lineage specific factors in mammalian embryos. Using bovine embryos as a model we have described these interactions at key developmental stages. Three bovine chromosomes (BTA) that differ in size, number of carried genes, and contain loci for key lineage regulators OCT4, NANOG and CDX2, were investigated. The results suggest that large chromosomes regardless of their gene density (BTA12 gene-poor, BTA5 gene-rich) do not significantly change their radial position within the nucleus. Gene loci however, may change its position within the chromosome territory (CT) and relocate its periphery, when stage specific process of gene activation is required. Trophectoderm specific CDX2 and epiblast precursor NANOG loci tend to locate on the surface or outside of the CTs, at stages related with their high expression. We postulate that the observed changes in CT shape reflect global alternations in gene expression related to differentiation.

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          Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells.

          Embryonic stem (ES) cells undergo extended proliferation while remaining poised for multilineage differentiation. A unique network of transcription factors may characterize self-renewal and simultaneously suppress differentiation. We applied expression cloning in mouse ES cells to isolate a self-renewal determinant. Nanog is a divergent homeodomain protein that directs propagation of undifferentiated ES cells. Nanog mRNA is present in pluripotent mouse and human cell lines, and absent from differentiated cells. In preimplantation embryos, Nanog is restricted to founder cells from which ES cells can be derived. Endogenous Nanog acts in parallel with cytokine stimulation of Stat3 to drive ES cell self-renewal. Elevated Nanog expression from transgene constructs is sufficient for clonal expansion of ES cells, bypassing Stat3 and maintaining Oct4 levels. Cytokine dependence, multilineage differentiation, and embryo colonization capacity are fully restored upon transgene excision. These findings establish a central role for Nanog in the transcription factor hierarchy that defines ES cell identity.
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            Global transcription in pluripotent embryonic stem cells.

            The molecular mechanisms underlying pluripotency and lineage specification from embryonic stem cells (ESCs) are largely unclear. Differentiation pathways may be determined by the targeted activation of lineage-specific genes or by selective silencing of genome regions. Here we show that the ESC genome is transcriptionally globally hyperactive and undergoes large-scale silencing as cells differentiate. Normally silent repeat regions are active in ESCs, and tissue-specific genes are sporadically expressed at low levels. Whole-genome tiling arrays demonstrate widespread transcription in coding and noncoding regions in ESCs, whereas the transcriptional landscape becomes more discrete as differentiation proceeds. The transcriptional hyperactivity in ESCs is accompanied by disproportionate expression of chromatin-remodeling genes and the general transcription machinery. We propose that global transcription is a hallmark of pluripotent ESCs, contributing to their plasticity, and that lineage specification is driven by reduction of the transcribed portion of the genome.
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              Chromatin in pluripotent embryonic stem cells and differentiation.

              Embryonic stem (ES) cells are unique in that they are pluripotent and have the ability to self-renew. The molecular mechanisms that underlie these two fundamental properties are largely unknown. We discuss how unique properties of chromatin in ES cells contribute to the maintenance of pluripotency and the determination of differentiation properties.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Resources
                Role: Resources
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ResourcesRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2 August 2017
                2017
                : 12
                : 8
                : e0182398
                Affiliations
                [1 ] Department of Genetics and Animal Breeding, Poznan University of Life Sciences, Poznan, Poland
                [2 ] Veterinary Research Institute, Brno, Czech Republic
                Michigan State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9649-2422
                Article
                PONE-D-17-17861
                10.1371/journal.pone.0182398
                5540545
                28767705
                f0459733-89de-44fa-ac9b-d2b8597c5a0c
                © 2017 Orsztynowicz et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 10 May 2017
                : 17 July 2017
                Page count
                Figures: 8, Tables: 2, Pages: 22
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: PRO.2011/01N/N/NZ9/00792
                Award Recipient :
                This study was funded by The National Science Centre (NCN, Poland) grant number: PRO.2011/01N/N/NZ9/00792; https://www.ncn.gov.pl. MO and PP are a grant holders of the European Social Fund (Human Capital Program). DL is a member of the Management Committee of the Cost Action “Epiconcept” (FA1201).
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Embryos
                Biology and Life Sciences
                Genetics
                Genetic Loci
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Blastocysts
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromosomes
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromatin
                Biology and Life Sciences
                Genetics
                Epigenetics
                Chromatin
                Biology and Life Sciences
                Genetics
                Gene Expression
                Chromatin
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Germ Cells
                OVA
                Zygotes
                Biology and life sciences
                Genetics
                Gene expression
                DNA transcription
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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                Uncategorized

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