Nonlinear feedback drives homeostatic plasticity in H2O2 stress response
Homeostatic systems that rely on genetic regulatory networks are intrinsically limited by the transcriptional response time, which may restrict a cell’s ability to adapt to unanticipated environmental challenges. To bypass this limitation, cells have evolved mechanisms whereby exposure to mild stres...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/23971 |
| _version_ | 1811181436462432256 |
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| author | Youlian Goulev Sandrine Morlot Audrey Matifas Bo Huang Mikael Molin Michel B Toledano Gilles Charvin |
| author_facet | Youlian Goulev Sandrine Morlot Audrey Matifas Bo Huang Mikael Molin Michel B Toledano Gilles Charvin |
| author_sort | Youlian Goulev |
| collection | DOAJ |
| description | Homeostatic systems that rely on genetic regulatory networks are intrinsically limited by the transcriptional response time, which may restrict a cell’s ability to adapt to unanticipated environmental challenges. To bypass this limitation, cells have evolved mechanisms whereby exposure to mild stress increases their resistance to subsequent threats. However, the mechanisms responsible for such adaptive homeostasis remain largely unknown. Here, we used live-cell imaging and microfluidics to investigate the adaptive response of budding yeast to temporally controlled H2O2 stress patterns. We demonstrate that acquisition of tolerance is a systems-level property resulting from nonlinearity of H2O2 scavenging by peroxiredoxins and our study reveals that this regulatory scheme induces a striking hormetic effect of extracellular H2O2 stress on replicative longevity. Our study thus provides a novel quantitative framework bridging the molecular architecture of a cellular homeostatic system to the emergence of nonintuitive adaptive properties. |
| first_indexed | 2024-04-11T09:17:38Z |
| format | Article |
| id | doaj.art-f0fb90f0ac82471381c61cfa499ed5cd |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:17:38Z |
| publishDate | 2017-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-f0fb90f0ac82471381c61cfa499ed5cd2022-12-22T04:32:17ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.23971Nonlinear feedback drives homeostatic plasticity in H2O2 stress responseYoulian Goulev0https://orcid.org/0000-0003-0370-4567Sandrine Morlot1Audrey Matifas2Bo Huang3https://orcid.org/0000-0001-5945-7601Mikael Molin4Michel B Toledano5Gilles Charvin6https://orcid.org/0000-0002-6852-6952Developmental Biology and Stem Cells Department, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, France; Centre National de la Recherche Scientifique, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, Illkirch, France; Université de Strasbourg, Illkirch, FranceDevelopmental Biology and Stem Cells Department, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, France; Centre National de la Recherche Scientifique, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, Illkirch, France; Université de Strasbourg, Illkirch, FranceDevelopmental Biology and Stem Cells Department, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, France; Centre National de la Recherche Scientifique, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, Illkirch, France; Université de Strasbourg, Illkirch, FranceOxidative Stress and Cancer, IBITECS, SBIGEM, CEA-Saclay, Gif-sur-Yvette, FranceDepartment of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, SwedenOxidative Stress and Cancer, IBITECS, SBIGEM, CEA-Saclay, Gif-sur-Yvette, FranceDevelopmental Biology and Stem Cells Department, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Strasbourg, France; Centre National de la Recherche Scientifique, Illkirch, France; Institut National de la Santé et de la Recherche Médicale, Illkirch, France; Université de Strasbourg, Illkirch, FranceHomeostatic systems that rely on genetic regulatory networks are intrinsically limited by the transcriptional response time, which may restrict a cell’s ability to adapt to unanticipated environmental challenges. To bypass this limitation, cells have evolved mechanisms whereby exposure to mild stress increases their resistance to subsequent threats. However, the mechanisms responsible for such adaptive homeostasis remain largely unknown. Here, we used live-cell imaging and microfluidics to investigate the adaptive response of budding yeast to temporally controlled H2O2 stress patterns. We demonstrate that acquisition of tolerance is a systems-level property resulting from nonlinearity of H2O2 scavenging by peroxiredoxins and our study reveals that this regulatory scheme induces a striking hormetic effect of extracellular H2O2 stress on replicative longevity. Our study thus provides a novel quantitative framework bridging the molecular architecture of a cellular homeostatic system to the emergence of nonintuitive adaptive properties.https://elifesciences.org/articles/23971H2O2 homeostasisacquired stress resistancehormesisnonlinear feedbackadaptation |
| spellingShingle | Youlian Goulev Sandrine Morlot Audrey Matifas Bo Huang Mikael Molin Michel B Toledano Gilles Charvin Nonlinear feedback drives homeostatic plasticity in H2O2 stress response eLife H2O2 homeostasis acquired stress resistance hormesis nonlinear feedback adaptation |
| title | Nonlinear feedback drives homeostatic plasticity in H2O2 stress response |
| title_full | Nonlinear feedback drives homeostatic plasticity in H2O2 stress response |
| title_fullStr | Nonlinear feedback drives homeostatic plasticity in H2O2 stress response |
| title_full_unstemmed | Nonlinear feedback drives homeostatic plasticity in H2O2 stress response |
| title_short | Nonlinear feedback drives homeostatic plasticity in H2O2 stress response |
| title_sort | nonlinear feedback drives homeostatic plasticity in h2o2 stress response |
| topic | H2O2 homeostasis acquired stress resistance hormesis nonlinear feedback adaptation |
| url | https://elifesciences.org/articles/23971 |
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