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Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development
Utilizing 3D structured illumination microscopy, we investigated the quality and quantity of nuclear invaginations and the distribution of nuclear pores during rabbit early embryonic development and identified the exact time point of nucleoporin 153 (NUP153) association with chromatin during mitosis...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Society for Reproduction and Development
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4848569/ https://www.ncbi.nlm.nih.gov/pubmed/26640117 http://dx.doi.org/10.1262/jrd.2015-100 |
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author | POPKEN, Jens SCHMID, Volker J. STRAUSS, Axel GUENGOER, Tuna WOLF, Eckhard ZAKHARTCHENKO, Valeri |
author_facet | POPKEN, Jens SCHMID, Volker J. STRAUSS, Axel GUENGOER, Tuna WOLF, Eckhard ZAKHARTCHENKO, Valeri |
author_sort | POPKEN, Jens |
collection | PubMed |
description | Utilizing 3D structured illumination microscopy, we investigated the quality and quantity of nuclear invaginations and the distribution of nuclear pores during rabbit early embryonic development and identified the exact time point of nucleoporin 153 (NUP153) association with chromatin during mitosis. Contrary to bovine early embryonic nuclei, featuring almost exclusively nuclear invaginations containing a small volume of cytoplasm, nuclei in rabbit early embryonic stages show additionally numerous invaginations containing a large volume of cytoplasm. Small-volume invaginations frequently emanated from large-volume nuclear invaginations but not vice versa, indicating a different underlying mechanism. Large- and small-volume nuclear envelope invaginations required the presence of chromatin, as they were restricted to chromatin-positive areas. The chromatin-free contact areas between nucleolar precursor bodies (NPBs) and large-volume invaginations were free of nuclear pores. Small-volume invaginations were not in contact with NPBs. The number of invaginations and isolated intranuclear vesicles per nucleus peaked at the 4-cell stage. At this stage, the nuclear surface showed highly concentrated clusters of nuclear pores surrounded by areas free of nuclear pores. Isolated intranuclear lamina vesicles were usually NUP153 negative. Cytoplasmic, randomly distributed NUP153-positive clusters were highly abundant at the zygote stage and decreased in number until they were almost absent at the 8-cell stage and later. These large NUP153 clusters may represent a maternally provided NUP153 deposit, but they were not visible as clusters during mitosis. Major genome activation at the 8- to 16-cell stage may mark the switch from a necessity for a deposit to on-demand production. NUP153 association with chromatin is initiated during metaphase before the initiation of the regeneration of the lamina. To our knowledge, the present study demonstrates for the first time major remodeling of the nuclear envelope and its underlying lamina during rabbit preimplantation development. |
format | Online Article Text |
id | pubmed-4848569 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | The Society for Reproduction and Development |
record_format | MEDLINE/PubMed |
spelling | pubmed-48485692016-04-28 Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development POPKEN, Jens SCHMID, Volker J. STRAUSS, Axel GUENGOER, Tuna WOLF, Eckhard ZAKHARTCHENKO, Valeri J Reprod Dev Original Article Utilizing 3D structured illumination microscopy, we investigated the quality and quantity of nuclear invaginations and the distribution of nuclear pores during rabbit early embryonic development and identified the exact time point of nucleoporin 153 (NUP153) association with chromatin during mitosis. Contrary to bovine early embryonic nuclei, featuring almost exclusively nuclear invaginations containing a small volume of cytoplasm, nuclei in rabbit early embryonic stages show additionally numerous invaginations containing a large volume of cytoplasm. Small-volume invaginations frequently emanated from large-volume nuclear invaginations but not vice versa, indicating a different underlying mechanism. Large- and small-volume nuclear envelope invaginations required the presence of chromatin, as they were restricted to chromatin-positive areas. The chromatin-free contact areas between nucleolar precursor bodies (NPBs) and large-volume invaginations were free of nuclear pores. Small-volume invaginations were not in contact with NPBs. The number of invaginations and isolated intranuclear vesicles per nucleus peaked at the 4-cell stage. At this stage, the nuclear surface showed highly concentrated clusters of nuclear pores surrounded by areas free of nuclear pores. Isolated intranuclear lamina vesicles were usually NUP153 negative. Cytoplasmic, randomly distributed NUP153-positive clusters were highly abundant at the zygote stage and decreased in number until they were almost absent at the 8-cell stage and later. These large NUP153 clusters may represent a maternally provided NUP153 deposit, but they were not visible as clusters during mitosis. Major genome activation at the 8- to 16-cell stage may mark the switch from a necessity for a deposit to on-demand production. NUP153 association with chromatin is initiated during metaphase before the initiation of the regeneration of the lamina. To our knowledge, the present study demonstrates for the first time major remodeling of the nuclear envelope and its underlying lamina during rabbit preimplantation development. The Society for Reproduction and Development 2015-12-04 2016-04 /pmc/articles/PMC4848569/ /pubmed/26640117 http://dx.doi.org/10.1262/jrd.2015-100 Text en ©2016 Society for Reproduction and Development http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. |
spellingShingle | Original Article POPKEN, Jens SCHMID, Volker J. STRAUSS, Axel GUENGOER, Tuna WOLF, Eckhard ZAKHARTCHENKO, Valeri Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title | Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title_full | Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title_fullStr | Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title_full_unstemmed | Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title_short | Stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
title_sort | stage-dependent remodeling of the nuclear envelope and lamina during rabbit early embryonic development |
topic | Original Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4848569/ https://www.ncbi.nlm.nih.gov/pubmed/26640117 http://dx.doi.org/10.1262/jrd.2015-100 |
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