Animal cell differentiation patterns suppress somatic evolution.

Cell differentiation in multicellular organisms has the obvious function during development of creating new cell types. However, in long-lived organisms with extensive cell turnover, cell differentiation often continues after new cell types are no longer needed or produced. Here, we address the ques...

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Autores principales: John W Pepper, Kathleen Sprouffske, Carlo C Maley
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Publicado: Public Library of Science (PLoS) 2007
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spelling oai:doaj.org-article:e92bc3900cc9476091d166f2981968c22021-11-25T05:41:28ZAnimal cell differentiation patterns suppress somatic evolution.1553-734X1553-735810.1371/journal.pcbi.0030250https://doaj.org/article/e92bc3900cc9476091d166f2981968c22007-12-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.0030250https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Cell differentiation in multicellular organisms has the obvious function during development of creating new cell types. However, in long-lived organisms with extensive cell turnover, cell differentiation often continues after new cell types are no longer needed or produced. Here, we address the question of why this is true. It is believed that multicellular organisms could not have arisen or been evolutionarily stable without possessing mechanisms to suppress somatic selection among cells within organisms, which would otherwise disrupt organismal integrity. Here, we propose that one such mechanism is a specific pattern of ongoing cell differentiation commonly found in metazoans with cell turnover, which we call "serial differentiation." This pattern involves a sequence of differentiation stages, starting with self-renewing somatic stem cells and proceeding through several (non-self-renewing) transient amplifying cell stages before ending with terminally differentiated cells. To test the hypothesis that serial differentiation can suppress somatic evolution, we used an agent-based computer simulation of cell population dynamics and evolution within tissues. The results indicate that, relative to other, simpler patterns, tissues organized into serial differentiation experience lower rates of detrimental cell-level evolution. Self-renewing cell populations are susceptible to somatic evolution, while those that are not self-renewing are not. We find that a mutation disrupting differentiation can create a new self-renewing cell population that is vulnerable to somatic evolution. These results are relevant not only to understanding the evolutionary origins of multicellularity, but also the causes of pathologies such as cancer and senescence in extant metazoans, including humans.John W PepperKathleen SprouffskeCarlo C MaleyPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 3, Iss 12, p e250 (2007)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
John W Pepper
Kathleen Sprouffske
Carlo C Maley
Animal cell differentiation patterns suppress somatic evolution.
description Cell differentiation in multicellular organisms has the obvious function during development of creating new cell types. However, in long-lived organisms with extensive cell turnover, cell differentiation often continues after new cell types are no longer needed or produced. Here, we address the question of why this is true. It is believed that multicellular organisms could not have arisen or been evolutionarily stable without possessing mechanisms to suppress somatic selection among cells within organisms, which would otherwise disrupt organismal integrity. Here, we propose that one such mechanism is a specific pattern of ongoing cell differentiation commonly found in metazoans with cell turnover, which we call "serial differentiation." This pattern involves a sequence of differentiation stages, starting with self-renewing somatic stem cells and proceeding through several (non-self-renewing) transient amplifying cell stages before ending with terminally differentiated cells. To test the hypothesis that serial differentiation can suppress somatic evolution, we used an agent-based computer simulation of cell population dynamics and evolution within tissues. The results indicate that, relative to other, simpler patterns, tissues organized into serial differentiation experience lower rates of detrimental cell-level evolution. Self-renewing cell populations are susceptible to somatic evolution, while those that are not self-renewing are not. We find that a mutation disrupting differentiation can create a new self-renewing cell population that is vulnerable to somatic evolution. These results are relevant not only to understanding the evolutionary origins of multicellularity, but also the causes of pathologies such as cancer and senescence in extant metazoans, including humans.
format article
author John W Pepper
Kathleen Sprouffske
Carlo C Maley
author_facet John W Pepper
Kathleen Sprouffske
Carlo C Maley
author_sort John W Pepper
title Animal cell differentiation patterns suppress somatic evolution.
title_short Animal cell differentiation patterns suppress somatic evolution.
title_full Animal cell differentiation patterns suppress somatic evolution.
title_fullStr Animal cell differentiation patterns suppress somatic evolution.
title_full_unstemmed Animal cell differentiation patterns suppress somatic evolution.
title_sort animal cell differentiation patterns suppress somatic evolution.
publisher Public Library of Science (PLoS)
publishDate 2007
url https://doaj.org/article/e92bc3900cc9476091d166f2981968c2
work_keys_str_mv AT johnwpepper animalcelldifferentiationpatternssuppresssomaticevolution
AT kathleensprouffske animalcelldifferentiationpatternssuppresssomaticevolution
AT carlocmaley animalcelldifferentiationpatternssuppresssomaticevolution
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