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      A conserved function for pericentromeric satellite DNA

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          Abstract

          A universal and unquestioned characteristic of eukaryotic cells is that the genome is divided into multiple chromosomes and encapsulated in a single nucleus. However, the underlying mechanism to ensure such a configuration is unknown. Here, we provide evidence that pericentromeric satellite DNA, which is often regarded as junk, is a critical constituent of the chromosome, allowing the packaging of all chromosomes into a single nucleus. We show that the multi-AT-hook satellite DNA-binding proteins, Drosophila melanogaster D1 and mouse HMGA1, play an evolutionarily conserved role in bundling pericentromeric satellite DNA from heterologous chromosomes into ‘chromocenters’, a cytological association of pericentromeric heterochromatin. Defective chromocenter formation leads to micronuclei formation due to budding from the interphase nucleus, DNA damage and cell death. We propose that chromocenter and satellite DNA serve a fundamental role in encapsulating the full complement of the genome within a single nucleus, the universal characteristic of eukaryotic cells.

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          On Earth, life is divided into three domains. The smallest of these domains includes all the creatures, from sunflowers to yeasts to humans, that have the genetic information within their cells encased in a structure known as the nucleus. The genomes of these organisms are formed of long pieces of DNA, called chromosomes, which are packaged tightly and then unpackaged every time the cell divides. When a cell is not dividing, the chromosomes in the nucleus are loosely bundled up together.

          It is well known that DNA is the blueprint for the building blocks of life, but actually most of the genetic information in a cell codes for nothing, and has unknown roles. An example of such ‘junk DNA’ is pericentrometric satellite DNA, small repetitive sequences found on all chromosomes.

          However, new experiments by Jagannathan et al. show that, in the nucleus of animal cells, certain DNA binding proteins make chromosomes huddle together by attaching to multiple pericentrometric satellite DNA sequences on different chromosomes. In fact, if these proteins are removed from mice and fruit flies cells grown in the laboratory, the chromosomes cannot be clustered together. Instead, they ‘float away’, and the membranes of the nucleus get damaged, possibly buckling under the pressure of the unorganized DNA.

          These events damage the genetic information, which can lead to the cell dying or forming tumors. ‘Junk DNA’ therefore appears to participate in fundamental cellular processes across species, a result that opens up several new lines of research.

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          Most cited references44

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          Selfish genes, the phenotype paradigm and genome evolution.

          Natural selection operating within genomes will inevitably result in the appearance of DNAs with no phenotypic expression whose only 'function' is survival within genomes. Prokaryotic transposable elements and eukaryotic middle-repetitive sequences can be seen as such DNA's and thus no phenotypic or evolutionary function need be assigned to them.
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            Regulation of zygotic gene expression in Drosophila primordial germ cells.

            Activation of the zygotic genome is a prerequisite for the transition from maternal to zygotic control of development. The onset of zygotic transcription has been well studied in somatic cells, but evidence suggests that it is controlled differently in the germline. In Drosophila, zygotic transcription in the soma has been detected as early as one hour after egg laying (AEL) [1]. In the germline, general RNA synthesis is not detected until 3.5 hours AEL (stage 8) [2] and poly(A)-containing transcripts are not observed in early germ cell nuclei [3]. However, rRNA gene expression has been demonstrated at this time [4]. Therefore, either there is a general, low level activation of the genome in early germ cells, or specific classes of genes, such as those transcribed by RNA polymerase (RNAP) II, are repressed. We addressed this issue by localizing the potent transcriptional activator Gal4-VP16 to the germline, and we find that Gal4-VP16-dependent gene expression is repressed in early germ cells. In addition, localization of germ plasm to the anterior reveals that it is sufficient to repress Bicoid-dependent gene expression. Thus, even in the presence of known transcriptional activators, RNAP II dependent gene expression is actively repressed in early germ cells. Furthermore, once the germ cell genome is activated, we find that vasa is expressed specifically in germ cells. This expression does not require proper patterning of the soma, indicating that it is likely to be controlled by the germ plasm.
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              GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion.

              Precise control of sister chromatid separation is essential for the accurate transmission of genetic information. Sister chromatids must remain linked to each other from the time of DNA replication until the onset of chromosome segregation, when the linkage must be promptly dissolved. Recent studies suggest that the machinery that is responsible for the destruction of mitotic cyclins also degrades proteins that play a role in maintaining sister chromatid linkage, and that this machinery is regulated by the spindle-assembly checkpoint. Studies on these problems in budding yeast are hampered by the inability to resolve its chromosomes by light or electron microscopy. We have developed a novel method for visualizing specific DNA sequences in fixed and living budding yeast cells. A tandem array of 256 copies of the Lac operator is integrated at the desired site in the genome and detected by the binding of a green fluorescent protein (GFP)-Lac repressor fusion expressed from the HIS3 promoter. Using this method, we show that sister chromatid segregation precedes the destruction of cyclin B. In mad or bub cells, which lack the spindle-assembly checkpoint, sister chromatid separation can occur in the absence of microtubules. The expression of a tetramerizing form of the GFP-Lac repressor, which can bind Lac operators on two different DNA molecules, can hold sister chromatids together under conditions in which they would normally separate. We conclude that sister chromatid separation in budding yeast can occur in the absence of microtubule-dependent forces, and that protein complexes that can bind two different DNA molecules are capable of holding sister chromatids together.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                26 March 2018
                2018
                : 7
                : e34122
                Affiliations
                [1 ]deptLife Sciences Institute University of Michigan Ann ArborUnited States
                [2 ]deptDepartment of Cell and Developmental Biology University of Michigan Ann ArborUnited States
                [3 ]deptHoward Hughes Medical Institute University of Michigan Ann ArborUnited States
                [4]National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                [5]National Centre for Biological Sciences, Tata Institute of Fundamental Research India
                Author information
                http://orcid.org/0000-0003-3428-6812
                http://orcid.org/0000-0003-0540-9174
                http://orcid.org/0000-0001-5541-0216
                Article
                34122
                10.7554/eLife.34122
                5957525
                29578410
                8399fd34-46ad-4f88-a5da-bb88f52597b6
                © 2018, Jagannathan et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 05 December 2017
                : 24 March 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000968, American Heart Association;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Cell Biology
                Chromosomes and Gene Expression
                Custom metadata
                Satellite DNA mediates clustering of multiple chromosomes via formation of chromocenter to encapsulate the full complement of the genome into a single nucleus.

                Life sciences
                satellite dna,chromocenter,micronuclei,pericentromeric heterochromatin,d. melanogaster

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