A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.

Increases in cellular Reactive Oxygen Species (ROS) concentration with age have been observed repeatedly in mammalian tissues. Concomitant increases in the proportion of replicatively senescent cells in ageing mammalian tissues have also been observed. Populations of mitotic human fibroblasts cultur...

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Main Authors: Conor Lawless, Diana Jurk, Colin S Gillespie, Daryl Shanley, Gabriele Saretzki, Thomas von Zglinicki, João F Passos
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032117&type=printable
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author Conor Lawless
Diana Jurk
Colin S Gillespie
Daryl Shanley
Gabriele Saretzki
Thomas von Zglinicki
João F Passos
author_facet Conor Lawless
Diana Jurk
Colin S Gillespie
Daryl Shanley
Gabriele Saretzki
Thomas von Zglinicki
João F Passos
author_sort Conor Lawless
collection DOAJ
description Increases in cellular Reactive Oxygen Species (ROS) concentration with age have been observed repeatedly in mammalian tissues. Concomitant increases in the proportion of replicatively senescent cells in ageing mammalian tissues have also been observed. Populations of mitotic human fibroblasts cultured in vitro, undergoing transition from proliferation competence to replicative senescence are useful models of ageing human tissues. Similar exponential increases in ROS with age have been observed in this model system. Tracking individual cells in dividing populations is difficult, and so the vast majority of observations have been cross-sectional, at the population level, rather than longitudinal observations of individual cells.One possible explanation for these observations is an exponential increase in ROS in individual fibroblasts with time (e.g. resulting from a vicious cycle between cellular ROS and damage). However, we demonstrate an alternative, simple hypothesis, equally consistent with these observations which does not depend on any gradual increase in ROS concentration: the Stochastic Step Model of Replicative Senescence (SSMRS). We also demonstrate that, consistent with the SSMRS, neither proliferation-competent human fibroblasts of any age, nor populations of hTERT overexpressing human fibroblasts passaged beyond the Hayflick limit, display high ROS concentrations. We conclude that longitudinal studies of single cells and their lineages are now required for testing hypotheses about roles and mechanisms of ROS increase during replicative senescence.
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spelling doaj-art-1da9c1db86c8410ebf20ad1c829a70db2025-08-20T03:25:10ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0172e3211710.1371/journal.pone.0032117A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.Conor LawlessDiana JurkColin S GillespieDaryl ShanleyGabriele SaretzkiThomas von ZglinickiJoão F PassosIncreases in cellular Reactive Oxygen Species (ROS) concentration with age have been observed repeatedly in mammalian tissues. Concomitant increases in the proportion of replicatively senescent cells in ageing mammalian tissues have also been observed. Populations of mitotic human fibroblasts cultured in vitro, undergoing transition from proliferation competence to replicative senescence are useful models of ageing human tissues. Similar exponential increases in ROS with age have been observed in this model system. Tracking individual cells in dividing populations is difficult, and so the vast majority of observations have been cross-sectional, at the population level, rather than longitudinal observations of individual cells.One possible explanation for these observations is an exponential increase in ROS in individual fibroblasts with time (e.g. resulting from a vicious cycle between cellular ROS and damage). However, we demonstrate an alternative, simple hypothesis, equally consistent with these observations which does not depend on any gradual increase in ROS concentration: the Stochastic Step Model of Replicative Senescence (SSMRS). We also demonstrate that, consistent with the SSMRS, neither proliferation-competent human fibroblasts of any age, nor populations of hTERT overexpressing human fibroblasts passaged beyond the Hayflick limit, display high ROS concentrations. We conclude that longitudinal studies of single cells and their lineages are now required for testing hypotheses about roles and mechanisms of ROS increase during replicative senescence.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032117&type=printable
spellingShingle Conor Lawless
Diana Jurk
Colin S Gillespie
Daryl Shanley
Gabriele Saretzki
Thomas von Zglinicki
João F Passos
A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
PLoS ONE
title A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
title_full A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
title_fullStr A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
title_full_unstemmed A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
title_short A stochastic step model of replicative senescence explains ROS production rate in ageing cell populations.
title_sort stochastic step model of replicative senescence explains ros production rate in ageing cell populations
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032117&type=printable
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