Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule
The karyosphere (karyosome) is a structure that forms in the oocyte nucleus—germinal vesicle (GV)—at the diplotene stage of meiotic prophase due to the assembly of all chromosomes in a limited portion of the GV. In some organisms, the karyosphere has an extrachromosomal external capsule, the marker...
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MDPI AG
2023-12-01
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| Series: | Journal of Developmental Biology |
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| author | Dmitry S. Bogolyubov Sergey V. Shabelnikov Alexandra O. Travina Maksim I. Sulatsky Irina O. Bogolyubova |
| author_facet | Dmitry S. Bogolyubov Sergey V. Shabelnikov Alexandra O. Travina Maksim I. Sulatsky Irina O. Bogolyubova |
| author_sort | Dmitry S. Bogolyubov |
| collection | DOAJ |
| description | The karyosphere (karyosome) is a structure that forms in the oocyte nucleus—germinal vesicle (GV)—at the diplotene stage of meiotic prophase due to the assembly of all chromosomes in a limited portion of the GV. In some organisms, the karyosphere has an extrachromosomal external capsule, the marker protein of which is nuclear F-actin. Despite many years of theories about the formation of the karyosphere capsule (KC) in the GV of the common frog <i>Rana temporaria</i>, we present data that cast doubt on its existence, at least in this species. Specific extrachromosomal strands, which had been considered the main elements of the frog’s KC, do not form a continuous layer around the karyosphere and, according to immunogold labeling, do not contain structural proteins, such as actin and lamin B. At the same time, F-actin is indeed noticeably concentrated around the karyosphere, creating the illusion of a capsule at the light microscopy/fluorescence level. The barrier-to-autointegration factor (BAF) and one of its functional partners—LEMD2, an inner nuclear membrane protein—are not localized in the strands, suggesting that the strands are not functional counterparts of the nuclear envelope. The presence of characteristic strands in the GV of <i>R. temporaria</i> late oocytes may reflect an excess of SMC1 involved in the structural maintenance of diplotene oocyte chromosomes at the karyosphere stage, since SMC1 has been shown to be the most abundant protein in the strands. Other characteristic microstructures—the so-called <i>annuli</i>, very similar in ultrastructure to the nuclear pore complexes—do not contain nucleoporins Nup35 and Nup93, and, therefore, they cannot be considered autonomous pore complexes, as previously thought. Taken together, our data indicate that traditional ideas about the existence of the <i>R. temporaria</i> KC as a special structural compartment of the GV are to be revisited. |
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| language | English |
| last_indexed | 2024-03-08T20:38:56Z |
| publishDate | 2023-12-01 |
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| spelling | doaj.art-770bc6a96b664f9e8aa75322fbc1f59f2023-12-22T14:17:57ZengMDPI AGJournal of Developmental Biology2221-37592023-12-011144410.3390/jdb11040044Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere CapsuleDmitry S. Bogolyubov0Sergey V. Shabelnikov1Alexandra O. Travina2Maksim I. Sulatsky3Irina O. Bogolyubova4Institute of Cytology of the Russian Academy of Sciences, St. Petersburg 194064, RussiaInstitute of Cytology of the Russian Academy of Sciences, St. Petersburg 194064, RussiaInstitute of Cytology of the Russian Academy of Sciences, St. Petersburg 194064, RussiaInstitute of Cytology of the Russian Academy of Sciences, St. Petersburg 194064, RussiaInstitute of Cytology of the Russian Academy of Sciences, St. Petersburg 194064, RussiaThe karyosphere (karyosome) is a structure that forms in the oocyte nucleus—germinal vesicle (GV)—at the diplotene stage of meiotic prophase due to the assembly of all chromosomes in a limited portion of the GV. In some organisms, the karyosphere has an extrachromosomal external capsule, the marker protein of which is nuclear F-actin. Despite many years of theories about the formation of the karyosphere capsule (KC) in the GV of the common frog <i>Rana temporaria</i>, we present data that cast doubt on its existence, at least in this species. Specific extrachromosomal strands, which had been considered the main elements of the frog’s KC, do not form a continuous layer around the karyosphere and, according to immunogold labeling, do not contain structural proteins, such as actin and lamin B. At the same time, F-actin is indeed noticeably concentrated around the karyosphere, creating the illusion of a capsule at the light microscopy/fluorescence level. The barrier-to-autointegration factor (BAF) and one of its functional partners—LEMD2, an inner nuclear membrane protein—are not localized in the strands, suggesting that the strands are not functional counterparts of the nuclear envelope. The presence of characteristic strands in the GV of <i>R. temporaria</i> late oocytes may reflect an excess of SMC1 involved in the structural maintenance of diplotene oocyte chromosomes at the karyosphere stage, since SMC1 has been shown to be the most abundant protein in the strands. Other characteristic microstructures—the so-called <i>annuli</i>, very similar in ultrastructure to the nuclear pore complexes—do not contain nucleoporins Nup35 and Nup93, and, therefore, they cannot be considered autonomous pore complexes, as previously thought. Taken together, our data indicate that traditional ideas about the existence of the <i>R. temporaria</i> KC as a special structural compartment of the GV are to be revisited.https://www.mdpi.com/2221-3759/11/4/44germinal vesiclenuclear compartmentskaryosomekaryospherekaryosphere capsuleelectron microscopy |
| spellingShingle | Dmitry S. Bogolyubov Sergey V. Shabelnikov Alexandra O. Travina Maksim I. Sulatsky Irina O. Bogolyubova Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule Journal of Developmental Biology germinal vesicle nuclear compartments karyosome karyosphere karyosphere capsule electron microscopy |
| title | Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule |
| title_full | Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule |
| title_fullStr | Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule |
| title_full_unstemmed | Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule |
| title_short | Special Nuclear Structures in the Germinal Vesicle of the Common Frog with Emphasis on the So-Called Karyosphere Capsule |
| title_sort | special nuclear structures in the germinal vesicle of the common frog with emphasis on the so called karyosphere capsule |
| topic | germinal vesicle nuclear compartments karyosome karyosphere karyosphere capsule electron microscopy |
| url | https://www.mdpi.com/2221-3759/11/4/44 |
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