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Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation

Telomeres and centromeres have traditionally been considered to perform distinct roles. During meiotic prophase, in a conserved chromosomal configuration called the bouquet, telomeres gather to the nuclear membrane (NM), often near centrosomes. We found previously that upon disruption of the fission...

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Autores principales: Fennell, Alex, Fernández-Álvarez, Alfonso, Tomita, Kazunori, Cooper, Julia Promisel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4332249/
https://www.ncbi.nlm.nih.gov/pubmed/25688135
http://dx.doi.org/10.1083/jcb.201409058
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author Fennell, Alex
Fernández-Álvarez, Alfonso
Tomita, Kazunori
Cooper, Julia Promisel
author_facet Fennell, Alex
Fernández-Álvarez, Alfonso
Tomita, Kazunori
Cooper, Julia Promisel
author_sort Fennell, Alex
collection PubMed
description Telomeres and centromeres have traditionally been considered to perform distinct roles. During meiotic prophase, in a conserved chromosomal configuration called the bouquet, telomeres gather to the nuclear membrane (NM), often near centrosomes. We found previously that upon disruption of the fission yeast bouquet, centrosomes failed to insert into the NM at meiosis I and nucleate bipolar spindles. Hence, the trans-NM association of telomeres with centrosomes during prophase is crucial for efficient spindle formation. Nonetheless, in approximately half of bouquet-deficient meiocytes, spindles form properly. Here, we show that bouquet-deficient cells can successfully undergo meiosis using centromere–centrosome contact instead of telomere–centrosome contact to generate spindle formation. Accordingly, forced association between centromeres and centrosomes fully rescued the spindle defects incurred by bouquet disruption. Telomeres and centromeres both stimulate focal accumulation of the SUN domain protein Sad1 beneath the centrosome, suggesting a molecular underpinning for their shared spindle-generating ability. Our observations demonstrate an unanticipated level of interchangeability between the two most prominent chromosomal landmarks.
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spelling pubmed-43322492015-08-16 Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation Fennell, Alex Fernández-Álvarez, Alfonso Tomita, Kazunori Cooper, Julia Promisel J Cell Biol Research Articles Telomeres and centromeres have traditionally been considered to perform distinct roles. During meiotic prophase, in a conserved chromosomal configuration called the bouquet, telomeres gather to the nuclear membrane (NM), often near centrosomes. We found previously that upon disruption of the fission yeast bouquet, centrosomes failed to insert into the NM at meiosis I and nucleate bipolar spindles. Hence, the trans-NM association of telomeres with centrosomes during prophase is crucial for efficient spindle formation. Nonetheless, in approximately half of bouquet-deficient meiocytes, spindles form properly. Here, we show that bouquet-deficient cells can successfully undergo meiosis using centromere–centrosome contact instead of telomere–centrosome contact to generate spindle formation. Accordingly, forced association between centromeres and centrosomes fully rescued the spindle defects incurred by bouquet disruption. Telomeres and centromeres both stimulate focal accumulation of the SUN domain protein Sad1 beneath the centrosome, suggesting a molecular underpinning for their shared spindle-generating ability. Our observations demonstrate an unanticipated level of interchangeability between the two most prominent chromosomal landmarks. The Rockefeller University Press 2015-02-16 /pmc/articles/PMC4332249/ /pubmed/25688135 http://dx.doi.org/10.1083/jcb.201409058 Text en This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Fennell, Alex
Fernández-Álvarez, Alfonso
Tomita, Kazunori
Cooper, Julia Promisel
Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title_full Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title_fullStr Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title_full_unstemmed Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title_short Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
title_sort telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4332249/
https://www.ncbi.nlm.nih.gov/pubmed/25688135
http://dx.doi.org/10.1083/jcb.201409058
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