Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

Production of healthy gametes in meiosis relies on the quality control and proper distribution of both nuclear and cytoplasmic contents. Meiotic differentiation naturally eliminates age-induced cellular damage by an unknown mechanism. Using time-lapse fluorescence microscopy in budding yeast, we fou...

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Main Authors: Grant A King, Jay S Goodman, Jennifer G Schick, Keerthana Chetlapalli, Danielle M Jorgens, Kent L McDonald, Elçin Ünal
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/47156
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spelling doaj-d5f9f5f175d94deb8d3c7662d4345c852021-05-05T17:49:47ZengeLife Sciences Publications LtdeLife2050-084X2019-08-01810.7554/eLife.47156Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeastGrant A King0https://orcid.org/0000-0001-9854-3174Jay S Goodman1https://orcid.org/0000-0002-4788-3918Jennifer G Schick2Keerthana Chetlapalli3Danielle M Jorgens4Kent L McDonald5Elçin Ünal6https://orcid.org/0000-0002-6768-609XDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesElectron Microscope Lab, University of California, Berkeley, Berkeley, United StatesElectron Microscope Lab, University of California, Berkeley, Berkeley, United StatesDepartment of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United StatesProduction of healthy gametes in meiosis relies on the quality control and proper distribution of both nuclear and cytoplasmic contents. Meiotic differentiation naturally eliminates age-induced cellular damage by an unknown mechanism. Using time-lapse fluorescence microscopy in budding yeast, we found that nuclear senescence factors – including protein aggregates, extrachromosomal ribosomal DNA circles, and abnormal nucleolar material – are sequestered away from chromosomes during meiosis II and subsequently eliminated. A similar sequestration and elimination process occurs for the core subunits of the nuclear pore complex in both young and aged cells. Nuclear envelope remodeling drives the formation of a membranous compartment containing the sequestered material. Importantly, de novo generation of plasma membrane is required for the sequestration event, preventing the inheritance of long-lived nucleoporins and senescence factors into the newly formed gametes. Our study uncovers a new mechanism of nuclear quality control and provides insight into its function in meiotic cellular rejuvenation.https://elifesciences.org/articles/47156meiosisagingnuclear pore complexnucleolusprotein aggregationquality control
collection DOAJ
language English
format Article
sources DOAJ
author Grant A King
Jay S Goodman
Jennifer G Schick
Keerthana Chetlapalli
Danielle M Jorgens
Kent L McDonald
Elçin Ünal
spellingShingle Grant A King
Jay S Goodman
Jennifer G Schick
Keerthana Chetlapalli
Danielle M Jorgens
Kent L McDonald
Elçin Ünal
Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
eLife
meiosis
aging
nuclear pore complex
nucleolus
protein aggregation
quality control
author_facet Grant A King
Jay S Goodman
Jennifer G Schick
Keerthana Chetlapalli
Danielle M Jorgens
Kent L McDonald
Elçin Ünal
author_sort Grant A King
title Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
title_short Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
title_full Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
title_fullStr Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
title_full_unstemmed Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
title_sort meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-08-01
description Production of healthy gametes in meiosis relies on the quality control and proper distribution of both nuclear and cytoplasmic contents. Meiotic differentiation naturally eliminates age-induced cellular damage by an unknown mechanism. Using time-lapse fluorescence microscopy in budding yeast, we found that nuclear senescence factors – including protein aggregates, extrachromosomal ribosomal DNA circles, and abnormal nucleolar material – are sequestered away from chromosomes during meiosis II and subsequently eliminated. A similar sequestration and elimination process occurs for the core subunits of the nuclear pore complex in both young and aged cells. Nuclear envelope remodeling drives the formation of a membranous compartment containing the sequestered material. Importantly, de novo generation of plasma membrane is required for the sequestration event, preventing the inheritance of long-lived nucleoporins and senescence factors into the newly formed gametes. Our study uncovers a new mechanism of nuclear quality control and provides insight into its function in meiotic cellular rejuvenation.
topic meiosis
aging
nuclear pore complex
nucleolus
protein aggregation
quality control
url https://elifesciences.org/articles/47156
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