Cargando…

The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis

The budding yeast centrosome, often called the spindle pole body (SPB), nucleates microtubules for chromosome segregation during cell division. An appendage, called the half bridge, attaches to one side of the SPB and regulates SPB duplication and separation. Like DNA, the SPB is duplicated only onc...

Descripción completa

Detalles Bibliográficos
Autores principales: Agarwal, Meenakshi, Jin, Hui, McClain, Melainia, Fan, Jinbo, Koch, Bailey A., Jaspersen, Sue L., Yu, Hong-Guo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6085829/
https://www.ncbi.nlm.nih.gov/pubmed/29847244
http://dx.doi.org/10.1091/mbc.E18-03-0163
_version_ 1783346406454460416
author Agarwal, Meenakshi
Jin, Hui
McClain, Melainia
Fan, Jinbo
Koch, Bailey A.
Jaspersen, Sue L.
Yu, Hong-Guo
author_facet Agarwal, Meenakshi
Jin, Hui
McClain, Melainia
Fan, Jinbo
Koch, Bailey A.
Jaspersen, Sue L.
Yu, Hong-Guo
author_sort Agarwal, Meenakshi
collection PubMed
description The budding yeast centrosome, often called the spindle pole body (SPB), nucleates microtubules for chromosome segregation during cell division. An appendage, called the half bridge, attaches to one side of the SPB and regulates SPB duplication and separation. Like DNA, the SPB is duplicated only once per cell cycle. During meiosis, however, after one round of DNA replication, two rounds of SPB duplication and separation are coupled with homologue segregation in meiosis I and sister-chromatid segregation in meiosis II. How SPB duplication and separation are regulated during meiosis remains to be elucidated, and whether regulation in meiosis differs from that in mitosis is unclear. Here we show that overproduction of the half-bridge component Kar1 leads to premature SPB separation during meiosis. Furthermore, excessive Kar1 induces SPB overduplication to form supernumerary SPBs, leading to chromosome missegregation and erroneous ascospore formation. Kar1-­mediated SPB duplication bypasses the requirement of dephosphorylation of Sfi1, another half-bridge component previously identified as a licensing factor. Our results therefore reveal an unexpected role of Kar1 in licensing meiotic SPB duplication and suggest a unique mechanism of SPB regulation during budding yeast meiosis.
format Online
Article
Text
id pubmed-6085829
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher The American Society for Cell Biology
record_format MEDLINE/PubMed
spelling pubmed-60858292018-10-16 The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis Agarwal, Meenakshi Jin, Hui McClain, Melainia Fan, Jinbo Koch, Bailey A. Jaspersen, Sue L. Yu, Hong-Guo Mol Biol Cell Articles The budding yeast centrosome, often called the spindle pole body (SPB), nucleates microtubules for chromosome segregation during cell division. An appendage, called the half bridge, attaches to one side of the SPB and regulates SPB duplication and separation. Like DNA, the SPB is duplicated only once per cell cycle. During meiosis, however, after one round of DNA replication, two rounds of SPB duplication and separation are coupled with homologue segregation in meiosis I and sister-chromatid segregation in meiosis II. How SPB duplication and separation are regulated during meiosis remains to be elucidated, and whether regulation in meiosis differs from that in mitosis is unclear. Here we show that overproduction of the half-bridge component Kar1 leads to premature SPB separation during meiosis. Furthermore, excessive Kar1 induces SPB overduplication to form supernumerary SPBs, leading to chromosome missegregation and erroneous ascospore formation. Kar1-­mediated SPB duplication bypasses the requirement of dephosphorylation of Sfi1, another half-bridge component previously identified as a licensing factor. Our results therefore reveal an unexpected role of Kar1 in licensing meiotic SPB duplication and suggest a unique mechanism of SPB regulation during budding yeast meiosis. The American Society for Cell Biology 2018-08-01 /pmc/articles/PMC6085829/ /pubmed/29847244 http://dx.doi.org/10.1091/mbc.E18-03-0163 Text en © 2018 Agarwal et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Agarwal, Meenakshi
Jin, Hui
McClain, Melainia
Fan, Jinbo
Koch, Bailey A.
Jaspersen, Sue L.
Yu, Hong-Guo
The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title_full The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title_fullStr The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title_full_unstemmed The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title_short The half-bridge component Kar1 promotes centrosome separation and duplication during budding yeast meiosis
title_sort half-bridge component kar1 promotes centrosome separation and duplication during budding yeast meiosis
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6085829/
https://www.ncbi.nlm.nih.gov/pubmed/29847244
http://dx.doi.org/10.1091/mbc.E18-03-0163
work_keys_str_mv AT agarwalmeenakshi thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT jinhui thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT mcclainmelainia thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT fanjinbo thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT kochbaileya thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT jaspersensuel thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT yuhongguo thehalfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT agarwalmeenakshi halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT jinhui halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT mcclainmelainia halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT fanjinbo halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT kochbaileya halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT jaspersensuel halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis
AT yuhongguo halfbridgecomponentkar1promotescentrosomeseparationandduplicationduringbuddingyeastmeiosis