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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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 |
work_keys_str_mv |
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