Topoisomerase II deficiency leads to a postreplicative structural shift in all Saccharomyces cerevisiae chromosomes

The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a ch...

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Published inScientific reports Vol. 11; no. 1; p. 14940
Main Authors Ayra-Plasencia, Jessel, Ramos-Pérez, Cristina, Santana-Sosa, Silvia, Quevedo, Oliver, Medina-Suárez, Sara, Matos-Perdomo, Emiliano, Zamora-Dorta, Marcos, Brown, Grant W., Lisby, Michael, Machín, Félix
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 22.07.2021
Nature Publishing Group
Nature Portfolio
Subjects
631/80/103
631/80/641
Anaphase
Cell Cycle
Chromatids
Chromosome Segregation
Chromosomes
Chromosomes, Fungal - genetics
Cytokinesis
Deoxyribonucleic acid
DNA
DNA damage
DNA topoisomerase (ATP-hydrolysing)
DNA Topoisomerases, Type II - deficiency
DNA Topoisomerases, Type II - genetics
Electrophoresis
Electrophoresis, Gel, Pulsed-Field
Gel electrophoresis
Gene Knockout Techniques
Genetic analysis
Humanities and Social Sciences
Inactivation
Intermediates
Mitosis
multidisciplinary
Pulsed-field gel electrophoresis
Recombination
Replication
Retention
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - physiology
Saccharomyces cerevisiae Proteins - genetics
Science
Science (multidisciplinary)
Sister chromatids
Yeasts
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Abstract The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G 2 /M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
AbstractList Abstract The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G2/M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G /M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G 2 /M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G2/M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
Abstract The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about distinct cell cycle responses. In the case of the conditional top2-5 allele, interphase and mitosis progress on schedule but cells suffer from a chromosome segregation catastrophe. We here show that top2-5 chromosomes fail to enter a Pulsed-Field Gel Electrophoresis (PFGE) in the first cell cycle, a behavior traditionally linked to the presence of replication and recombination intermediates. We distinguished two classes of affected chromosomes: the rDNA-bearing chromosome XII, which fails to enter a PFGE at the beginning of S-phase, and all the other chromosomes, which fail at a postreplicative stage. In synchronously cycling cells, this late PFGE retention is observed in anaphase; however, we demonstrate that this behavior is independent of cytokinesis, stabilization of anaphase bridges, spindle pulling forces and, probably, anaphase onset. Strikingly, once the PFGE retention has occurred it becomes refractory to Top2 re-activation. DNA combing, two-dimensional electrophoresis, genetic analyses, and GFP-tagged DNA damage markers suggest that neither recombination intermediates nor unfinished replication account for the postreplicative PFGE shift, which is further supported by the fact that the shift does not trigger the G 2 /M checkpoint. We propose that the absence of Top2 activity leads to a general chromosome structural/topological change in mitosis.
ArticleNumber 14940
Author Santana-Sosa, Silvia
Ayra-Plasencia, Jessel
Machín, Félix
Matos-Perdomo, Emiliano
Quevedo, Oliver
Zamora-Dorta, Marcos
Lisby, Michael
Brown, Grant W.
Ramos-Pérez, Cristina
Medina-Suárez, Sara
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  surname: Santana-Sosa
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  givenname: Félix
  surname: Machín
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  email: fmachin@fciisc.es
  organization: Unidad de Investigación, Hospital Universitario Nuestra Señora de la Candelaria, Instituto de Tecnologías Biomédicas, Universidad de la Laguna, Facultad de Ciencias de la Salud, Universidad Fernando Pessoa Canarias
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SSID ssj0000529419
Score 2.3862789
Snippet The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings about...
Abstract The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings...
Abstract The key role of Topoisomerase II (Top2) is the removal of topological intertwines between sister chromatids. In yeast, inactivation of Top2 brings...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
springer
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 14940
SubjectTerms 631/80/103
631/80/641
Anaphase
Cell Cycle
Chromatids
Chromosome Segregation
Chromosomes
Chromosomes, Fungal - genetics
Cytokinesis
Deoxyribonucleic acid
DNA
DNA damage
DNA topoisomerase (ATP-hydrolysing)
DNA Topoisomerases, Type II - deficiency
DNA Topoisomerases, Type II - genetics
Electrophoresis
Electrophoresis, Gel, Pulsed-Field
Gel electrophoresis
Gene Knockout Techniques
Genetic analysis
Humanities and Social Sciences
Inactivation
Intermediates
Mitosis
multidisciplinary
Pulsed-field gel electrophoresis
Recombination
Replication
Retention
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - physiology
Saccharomyces cerevisiae Proteins - genetics
Science
Science (multidisciplinary)
Sister chromatids
Yeasts
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Title Topoisomerase II deficiency leads to a postreplicative structural shift in all Saccharomyces cerevisiae chromosomes
URI https://link.springer.com/article/10.1038/s41598-021-93875-5
https://www.ncbi.nlm.nih.gov/pubmed/34294749
https://www.proquest.com/docview/2554122745
https://search.proquest.com/docview/2555110119
https://pubmed.ncbi.nlm.nih.gov/PMC8298500
https://doaj.org/article/7c08ad1d2a4f43afa57021c0e2001c32
Volume 11
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