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A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes

The inner nuclear membrane (INM) proteome regulates gene expression, chromatin organization, and nuclear transport; however, it is poorly understood how changes in INM protein composition contribute to developmentally regulated processes, such as gametogenesis. We conducted a screen to determine how...

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Autores principales: Shelton, Shary N, Smith, Sarah E, Unruh, Jay R, Jaspersen, Sue L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8664494/
https://www.ncbi.nlm.nih.gov/pubmed/34849801
http://dx.doi.org/10.1093/g3journal/jkab345
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author Shelton, Shary N
Smith, Sarah E
Unruh, Jay R
Jaspersen, Sue L
author_facet Shelton, Shary N
Smith, Sarah E
Unruh, Jay R
Jaspersen, Sue L
author_sort Shelton, Shary N
collection PubMed
description The inner nuclear membrane (INM) proteome regulates gene expression, chromatin organization, and nuclear transport; however, it is poorly understood how changes in INM protein composition contribute to developmentally regulated processes, such as gametogenesis. We conducted a screen to determine how the INM proteome differs between mitotic cells and gametes. In addition, we used a strategy that allowed us to determine if spores synthesize their INM proteins de novo, rather than inheriting their INM proteins from the parental cell. This screen used a split-GFP complementation system, where we were able to compare the distribution of all C-terminally tagged transmembrane proteins in Saccharomyces cerevisiae in gametes to that of mitotic cells. Gametes contain a distinct INM proteome needed to complete gamete formation, including expression of genes linked to cell wall biosynthesis, lipid biosynthetic and metabolic pathways, protein degradation, and unknown functions. Based on the inheritance pattern, INM components are made de novo in the gametes. Whereas mitotic cells show a strong preference for proteins with small extraluminal domains, gametes do not exhibit this size preference likely due to the changes in the nuclear permeability barrier during gametogenesis. Taken together, our data provide evidence for INM changes during gametogenesis and shed light on mechanisms used to shape the INM proteome of spores.
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spelling pubmed-86644942021-12-13 A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes Shelton, Shary N Smith, Sarah E Unruh, Jay R Jaspersen, Sue L G3 (Bethesda) Mutant Screen Report The inner nuclear membrane (INM) proteome regulates gene expression, chromatin organization, and nuclear transport; however, it is poorly understood how changes in INM protein composition contribute to developmentally regulated processes, such as gametogenesis. We conducted a screen to determine how the INM proteome differs between mitotic cells and gametes. In addition, we used a strategy that allowed us to determine if spores synthesize their INM proteins de novo, rather than inheriting their INM proteins from the parental cell. This screen used a split-GFP complementation system, where we were able to compare the distribution of all C-terminally tagged transmembrane proteins in Saccharomyces cerevisiae in gametes to that of mitotic cells. Gametes contain a distinct INM proteome needed to complete gamete formation, including expression of genes linked to cell wall biosynthesis, lipid biosynthetic and metabolic pathways, protein degradation, and unknown functions. Based on the inheritance pattern, INM components are made de novo in the gametes. Whereas mitotic cells show a strong preference for proteins with small extraluminal domains, gametes do not exhibit this size preference likely due to the changes in the nuclear permeability barrier during gametogenesis. Taken together, our data provide evidence for INM changes during gametogenesis and shed light on mechanisms used to shape the INM proteome of spores. Oxford University Press 2021-10-19 /pmc/articles/PMC8664494/ /pubmed/34849801 http://dx.doi.org/10.1093/g3journal/jkab345 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Mutant Screen Report
Shelton, Shary N
Smith, Sarah E
Unruh, Jay R
Jaspersen, Sue L
A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title_full A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title_fullStr A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title_full_unstemmed A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title_short A distinct inner nuclear membrane proteome in Saccharomyces cerevisiae gametes
title_sort distinct inner nuclear membrane proteome in saccharomyces cerevisiae gametes
topic Mutant Screen Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8664494/
https://www.ncbi.nlm.nih.gov/pubmed/34849801
http://dx.doi.org/10.1093/g3journal/jkab345
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