Cargando…

rDNA array length is a major determinant of replicative lifespan in budding yeast

The complex processes and interactions that regulate aging and determine lifespan are not fully defined for any organism. Here, taking advantage of recent technological advances in studying aging in budding yeast, we discovered a previously unappreciated relationship between the number of copies of...

Descripción completa

Detalles Bibliográficos
Autores principales: Hotz, Manuel, Thayer, Nathaniel H., Hendrickson, David G., Schinski, Elizabeth L., Xu, Jun, Gottschling, Daniel E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9169770/
https://www.ncbi.nlm.nih.gov/pubmed/35394872
http://dx.doi.org/10.1073/pnas.2119593119
_version_ 1784721270052487168
author Hotz, Manuel
Thayer, Nathaniel H.
Hendrickson, David G.
Schinski, Elizabeth L.
Xu, Jun
Gottschling, Daniel E.
author_facet Hotz, Manuel
Thayer, Nathaniel H.
Hendrickson, David G.
Schinski, Elizabeth L.
Xu, Jun
Gottschling, Daniel E.
author_sort Hotz, Manuel
collection PubMed
description The complex processes and interactions that regulate aging and determine lifespan are not fully defined for any organism. Here, taking advantage of recent technological advances in studying aging in budding yeast, we discovered a previously unappreciated relationship between the number of copies of the ribosomal RNA gene present in its chromosomal array and replicative lifespan (RLS). Specifically, the chromosomal ribosomal DNA (rDNA) copy number (rDNA CN) positively correlated with RLS and this interaction explained over 70% of variability in RLS among a series of wild-type strains. In strains with low rDNA CN, SIR2 expression was attenuated and extrachromosomal rDNA circle (ERC) accumulation was increased, leading to shorter lifespan. Suppressing ERC formation by deletion of FOB1 eliminated the relationship between rDNA CN and RLS. These data suggest that previously identified rDNA CN regulatory mechanisms limit lifespan. Importantly, the RLSs of reported lifespan-enhancing mutations were significantly impacted by rDNA CN, suggesting that changes in rDNA CN might explain the magnitude of some of those reported effects. We propose that because rDNA CN is modulated by environmental, genetic, and stochastic factors, considering rDNA CN is a prerequisite for accurate interpretation of lifespan data.
format Online
Article
Text
id pubmed-9169770
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-91697702022-06-07 rDNA array length is a major determinant of replicative lifespan in budding yeast Hotz, Manuel Thayer, Nathaniel H. Hendrickson, David G. Schinski, Elizabeth L. Xu, Jun Gottschling, Daniel E. Proc Natl Acad Sci U S A Biological Sciences The complex processes and interactions that regulate aging and determine lifespan are not fully defined for any organism. Here, taking advantage of recent technological advances in studying aging in budding yeast, we discovered a previously unappreciated relationship between the number of copies of the ribosomal RNA gene present in its chromosomal array and replicative lifespan (RLS). Specifically, the chromosomal ribosomal DNA (rDNA) copy number (rDNA CN) positively correlated with RLS and this interaction explained over 70% of variability in RLS among a series of wild-type strains. In strains with low rDNA CN, SIR2 expression was attenuated and extrachromosomal rDNA circle (ERC) accumulation was increased, leading to shorter lifespan. Suppressing ERC formation by deletion of FOB1 eliminated the relationship between rDNA CN and RLS. These data suggest that previously identified rDNA CN regulatory mechanisms limit lifespan. Importantly, the RLSs of reported lifespan-enhancing mutations were significantly impacted by rDNA CN, suggesting that changes in rDNA CN might explain the magnitude of some of those reported effects. We propose that because rDNA CN is modulated by environmental, genetic, and stochastic factors, considering rDNA CN is a prerequisite for accurate interpretation of lifespan data. National Academy of Sciences 2022-04-08 2022-04-12 /pmc/articles/PMC9169770/ /pubmed/35394872 http://dx.doi.org/10.1073/pnas.2119593119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Hotz, Manuel
Thayer, Nathaniel H.
Hendrickson, David G.
Schinski, Elizabeth L.
Xu, Jun
Gottschling, Daniel E.
rDNA array length is a major determinant of replicative lifespan in budding yeast
title rDNA array length is a major determinant of replicative lifespan in budding yeast
title_full rDNA array length is a major determinant of replicative lifespan in budding yeast
title_fullStr rDNA array length is a major determinant of replicative lifespan in budding yeast
title_full_unstemmed rDNA array length is a major determinant of replicative lifespan in budding yeast
title_short rDNA array length is a major determinant of replicative lifespan in budding yeast
title_sort rdna array length is a major determinant of replicative lifespan in budding yeast
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9169770/
https://www.ncbi.nlm.nih.gov/pubmed/35394872
http://dx.doi.org/10.1073/pnas.2119593119
work_keys_str_mv AT hotzmanuel rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast
AT thayernathanielh rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast
AT hendricksondavidg rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast
AT schinskielizabethl rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast
AT xujun rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast
AT gottschlingdaniele rdnaarraylengthisamajordeterminantofreplicativelifespaninbuddingyeast