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Robustness and evolvability of heterogeneous cell populations
Biological systems are endowed with two fundamental but seemingly contradictory properties: robustness, the ability to withstand environmental fluctuations and genetic variability; and evolvability, the ability to acquire selectable and heritable phenotypic changes. Cell populations with heterogeneo...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The American Society for Cell Biology
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994894/ https://www.ncbi.nlm.nih.gov/pubmed/29851566 http://dx.doi.org/10.1091/mbc.E18-01-0070 |
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author | Kucharavy, Andrei Rubinstein, Boris Zhu, Jin Li, Rong |
author_facet | Kucharavy, Andrei Rubinstein, Boris Zhu, Jin Li, Rong |
author_sort | Kucharavy, Andrei |
collection | PubMed |
description | Biological systems are endowed with two fundamental but seemingly contradictory properties: robustness, the ability to withstand environmental fluctuations and genetic variability; and evolvability, the ability to acquire selectable and heritable phenotypic changes. Cell populations with heterogeneous genetic makeup, such as those of infectious microbial organisms or cancer, rely on their inherent robustness to maintain viability and fitness, but when encountering environmental insults, such as drug treatment, these populations are also poised for rapid adaptation through evolutionary selection. In this study, we develop a general mathematical model that allows us to explain and quantify this fundamental relationship between robustness and evolvability of heterogeneous cell populations. Our model predicts that robustness is, in fact, essential for evolvability, especially for more adverse environments, a trend we observe in aneuploid budding yeast and breast cancer cells. Robustness also compensates for the negative impact of the systems’ complexity on their evolvability. Our model also provides a mathematical means to estimate the number of independent processes underlying a system’s performance and identify the most generally adapted subpopulation, which may resemble the multi-drug-resistant “persister” cells observed in cancer. |
format | Online Article Text |
id | pubmed-5994894 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-59948942018-08-16 Robustness and evolvability of heterogeneous cell populations Kucharavy, Andrei Rubinstein, Boris Zhu, Jin Li, Rong Mol Biol Cell Articles Biological systems are endowed with two fundamental but seemingly contradictory properties: robustness, the ability to withstand environmental fluctuations and genetic variability; and evolvability, the ability to acquire selectable and heritable phenotypic changes. Cell populations with heterogeneous genetic makeup, such as those of infectious microbial organisms or cancer, rely on their inherent robustness to maintain viability and fitness, but when encountering environmental insults, such as drug treatment, these populations are also poised for rapid adaptation through evolutionary selection. In this study, we develop a general mathematical model that allows us to explain and quantify this fundamental relationship between robustness and evolvability of heterogeneous cell populations. Our model predicts that robustness is, in fact, essential for evolvability, especially for more adverse environments, a trend we observe in aneuploid budding yeast and breast cancer cells. Robustness also compensates for the negative impact of the systems’ complexity on their evolvability. Our model also provides a mathematical means to estimate the number of independent processes underlying a system’s performance and identify the most generally adapted subpopulation, which may resemble the multi-drug-resistant “persister” cells observed in cancer. The American Society for Cell Biology 2018-06-01 /pmc/articles/PMC5994894/ /pubmed/29851566 http://dx.doi.org/10.1091/mbc.E18-01-0070 Text en © 2018 Kucharavy et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0/ This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License. |
spellingShingle | Articles Kucharavy, Andrei Rubinstein, Boris Zhu, Jin Li, Rong Robustness and evolvability of heterogeneous cell populations |
title | Robustness and evolvability of heterogeneous cell populations |
title_full | Robustness and evolvability of heterogeneous cell populations |
title_fullStr | Robustness and evolvability of heterogeneous cell populations |
title_full_unstemmed | Robustness and evolvability of heterogeneous cell populations |
title_short | Robustness and evolvability of heterogeneous cell populations |
title_sort | robustness and evolvability of heterogeneous cell populations |
topic | Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994894/ https://www.ncbi.nlm.nih.gov/pubmed/29851566 http://dx.doi.org/10.1091/mbc.E18-01-0070 |
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