Cargando…

The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis

BACKGROUND: The oocyte chromosomes of the red flour beetle, Tribolium castaneum, are gathered into a knot, forming a karyosphere at the diplotene stage of meiotic prophase. Chromatin rearrangement, which is a characteristic feature of oocyte maturation, is well documented. The T. castaneum karyosphe...

Descripción completa

Detalles Bibliográficos
Autores principales: Kiselev, Artem M., Stepanova, Irina S., Adonin, Leonid S., Batalova, Florina M., Parfenov, Vladimir N., Bogolyubov, Dmitry S., Podgornaya, Olga I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5679382/
https://www.ncbi.nlm.nih.gov/pubmed/29151891
http://dx.doi.org/10.1186/s13039-017-0342-4
_version_ 1783277578230956032
author Kiselev, Artem M.
Stepanova, Irina S.
Adonin, Leonid S.
Batalova, Florina M.
Parfenov, Vladimir N.
Bogolyubov, Dmitry S.
Podgornaya, Olga I.
author_facet Kiselev, Artem M.
Stepanova, Irina S.
Adonin, Leonid S.
Batalova, Florina M.
Parfenov, Vladimir N.
Bogolyubov, Dmitry S.
Podgornaya, Olga I.
author_sort Kiselev, Artem M.
collection PubMed
description BACKGROUND: The oocyte chromosomes of the red flour beetle, Tribolium castaneum, are gathered into a knot, forming a karyosphere at the diplotene stage of meiotic prophase. Chromatin rearrangement, which is a characteristic feature of oocyte maturation, is well documented. The T. castaneum karyosphere is surrounded by a complex extrachromosomal structure termed the karyosphere capsule. The capsule contains the vast majority of oocyte RNA. We have previously shown using a BrUTP assay that oocyte chromosomes in T. castaneum maintain residual transcription up to the very end of oocyte maturation. Karyosphere transcription requires evidently not only transcription factors but also mRNA processing factors, including the components of the exon junction complex with its core component, the splicing factor Y14. We employed a gene engineering approach with injection of mRNA derived from the Myc-tagged Y14 plasmid-based construct in order to monitor the newly synthesized fusion protein in the oocyte nuclei. RESULTS: Our preliminary data have been presented as a brief correspondence elsewhere. Here, we provide a full-length article including immunoelectron-microscopy localization data on Y14–Myc distribution in the nucleus of previtellogenic and vitellogenic oocytes. The injections of the fusion protein Y14–Myc mRNA into the oocytes showed a dynamic pattern of the protein distribution. At the previtellogenic stage, there are two main locations for the protein: SC35 domains (the analogues of interchromatin granule clusters or nuclear speckles) and the karyosphere capsule. At the vitellogenic stage, SC35 domains were devoid of labels, and Y14–Myc was found in the perichromatin region of the karyosphere, presumably at the places of residual transcription. We show that karyosphere formation is accompanied by the movement of a nuclear protein while the residual transcription occurs during genome inactivation. CONCLUSIONS: Our data indicate that the karyosphere capsule, being a destination site for a protein involved in mRNA splicing and export, is not only a specializes part of nuclear matrix separating the karyosphere from the products of chromosome activity, as believed previously, but represents a special nuclear compartment involved in the processes of gene expression in the case the karyosphere retains residual transcription activity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13039-017-0342-4) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5679382
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-56793822017-11-17 The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis Kiselev, Artem M. Stepanova, Irina S. Adonin, Leonid S. Batalova, Florina M. Parfenov, Vladimir N. Bogolyubov, Dmitry S. Podgornaya, Olga I. Mol Cytogenet Research BACKGROUND: The oocyte chromosomes of the red flour beetle, Tribolium castaneum, are gathered into a knot, forming a karyosphere at the diplotene stage of meiotic prophase. Chromatin rearrangement, which is a characteristic feature of oocyte maturation, is well documented. The T. castaneum karyosphere is surrounded by a complex extrachromosomal structure termed the karyosphere capsule. The capsule contains the vast majority of oocyte RNA. We have previously shown using a BrUTP assay that oocyte chromosomes in T. castaneum maintain residual transcription up to the very end of oocyte maturation. Karyosphere transcription requires evidently not only transcription factors but also mRNA processing factors, including the components of the exon junction complex with its core component, the splicing factor Y14. We employed a gene engineering approach with injection of mRNA derived from the Myc-tagged Y14 plasmid-based construct in order to monitor the newly synthesized fusion protein in the oocyte nuclei. RESULTS: Our preliminary data have been presented as a brief correspondence elsewhere. Here, we provide a full-length article including immunoelectron-microscopy localization data on Y14–Myc distribution in the nucleus of previtellogenic and vitellogenic oocytes. The injections of the fusion protein Y14–Myc mRNA into the oocytes showed a dynamic pattern of the protein distribution. At the previtellogenic stage, there are two main locations for the protein: SC35 domains (the analogues of interchromatin granule clusters or nuclear speckles) and the karyosphere capsule. At the vitellogenic stage, SC35 domains were devoid of labels, and Y14–Myc was found in the perichromatin region of the karyosphere, presumably at the places of residual transcription. We show that karyosphere formation is accompanied by the movement of a nuclear protein while the residual transcription occurs during genome inactivation. CONCLUSIONS: Our data indicate that the karyosphere capsule, being a destination site for a protein involved in mRNA splicing and export, is not only a specializes part of nuclear matrix separating the karyosphere from the products of chromosome activity, as believed previously, but represents a special nuclear compartment involved in the processes of gene expression in the case the karyosphere retains residual transcription activity. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13039-017-0342-4) contains supplementary material, which is available to authorized users. BioMed Central 2017-11-09 /pmc/articles/PMC5679382/ /pubmed/29151891 http://dx.doi.org/10.1186/s13039-017-0342-4 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kiselev, Artem M.
Stepanova, Irina S.
Adonin, Leonid S.
Batalova, Florina M.
Parfenov, Vladimir N.
Bogolyubov, Dmitry S.
Podgornaya, Olga I.
The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title_full The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title_fullStr The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title_full_unstemmed The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title_short The exon junction complex factor Y14 is dynamic in the nucleus of the beetle Tribolium castaneum during late oogenesis
title_sort exon junction complex factor y14 is dynamic in the nucleus of the beetle tribolium castaneum during late oogenesis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5679382/
https://www.ncbi.nlm.nih.gov/pubmed/29151891
http://dx.doi.org/10.1186/s13039-017-0342-4
work_keys_str_mv AT kiselevartemm theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT stepanovairinas theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT adoninleonids theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT batalovaflorinam theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT parfenovvladimirn theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT bogolyubovdmitrys theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT podgornayaolgai theexonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT kiselevartemm exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT stepanovairinas exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT adoninleonids exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT batalovaflorinam exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT parfenovvladimirn exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT bogolyubovdmitrys exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis
AT podgornayaolgai exonjunctioncomplexfactory14isdynamicinthenucleusofthebeetletriboliumcastaneumduringlateoogenesis