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A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase

Populations often display consistent developmental phenotypes across individuals despite inevitable biological stochasticity. Nevertheless, developmental robustness has limits, and systems can fail upon change in the environment or the genetic background. We use here the seam cells, a population of...

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Autores principales: Hintze, Mark, Koneru, Sneha L., Gilbert, Sophie P. R., Katsanos, Dimitris, Lambert, Julien, Barkoulas, Michalis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153939/
https://www.ncbi.nlm.nih.gov/pubmed/31988193
http://dx.doi.org/10.1534/genetics.119.302896
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author Hintze, Mark
Koneru, Sneha L.
Gilbert, Sophie P. R.
Katsanos, Dimitris
Lambert, Julien
Barkoulas, Michalis
author_facet Hintze, Mark
Koneru, Sneha L.
Gilbert, Sophie P. R.
Katsanos, Dimitris
Lambert, Julien
Barkoulas, Michalis
author_sort Hintze, Mark
collection PubMed
description Populations often display consistent developmental phenotypes across individuals despite inevitable biological stochasticity. Nevertheless, developmental robustness has limits, and systems can fail upon change in the environment or the genetic background. We use here the seam cells, a population of epidermal stem cells in Caenorhabditis elegans, to study the influence of temperature change and genetic variation on cell fate. Seam cell development has mostly been studied so far in the laboratory reference strain (N2), grown at 20° temperature. We demonstrate that an increase in culture temperature to 25° introduces variability in the wild-type seam cell lineage, with a proportion of animals showing an increase in seam cell number. We map this increase to lineage-specific symmetrization events of normally asymmetric cell divisions at the fourth larval stage, leading to the retention of seam cell fate in both daughter cells. Using genetics and single-molecule imaging, we demonstrate that this symmetrization occurs via changes in the Wnt asymmetry pathway, leading to aberrant Wnt target activation in anterior cell daughters. We find that intrinsic differences in the Wnt asymmetry pathway already exist between seam cells at 20° and this may sensitize cells toward a cell fate switch at increased temperature. Finally, we demonstrate that wild isolates of C. elegans display variation in seam cell sensitivity to increased culture temperature, although their average seam cell number is comparable at 20°. Our results highlight how temperature can modulate cell fate decisions in an invertebrate model of stem cell patterning.
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spelling pubmed-71539392020-04-19 A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase Hintze, Mark Koneru, Sneha L. Gilbert, Sophie P. R. Katsanos, Dimitris Lambert, Julien Barkoulas, Michalis Genetics Investigations Populations often display consistent developmental phenotypes across individuals despite inevitable biological stochasticity. Nevertheless, developmental robustness has limits, and systems can fail upon change in the environment or the genetic background. We use here the seam cells, a population of epidermal stem cells in Caenorhabditis elegans, to study the influence of temperature change and genetic variation on cell fate. Seam cell development has mostly been studied so far in the laboratory reference strain (N2), grown at 20° temperature. We demonstrate that an increase in culture temperature to 25° introduces variability in the wild-type seam cell lineage, with a proportion of animals showing an increase in seam cell number. We map this increase to lineage-specific symmetrization events of normally asymmetric cell divisions at the fourth larval stage, leading to the retention of seam cell fate in both daughter cells. Using genetics and single-molecule imaging, we demonstrate that this symmetrization occurs via changes in the Wnt asymmetry pathway, leading to aberrant Wnt target activation in anterior cell daughters. We find that intrinsic differences in the Wnt asymmetry pathway already exist between seam cells at 20° and this may sensitize cells toward a cell fate switch at increased temperature. Finally, we demonstrate that wild isolates of C. elegans display variation in seam cell sensitivity to increased culture temperature, although their average seam cell number is comparable at 20°. Our results highlight how temperature can modulate cell fate decisions in an invertebrate model of stem cell patterning. Genetics Society of America 2020-04 2020-01-27 /pmc/articles/PMC7153939/ /pubmed/31988193 http://dx.doi.org/10.1534/genetics.119.302896 Text en Copyright © 2020 by the Genetics Society of America Available freely online through the author-supported open access option.
spellingShingle Investigations
Hintze, Mark
Koneru, Sneha L.
Gilbert, Sophie P. R.
Katsanos, Dimitris
Lambert, Julien
Barkoulas, Michalis
A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title_full A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title_fullStr A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title_full_unstemmed A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title_short A Cell Fate Switch in the Caenorhabditis elegans Seam Cell Lineage Occurs Through Modulation of the Wnt Asymmetry Pathway in Response to Temperature Increase
title_sort cell fate switch in the caenorhabditis elegans seam cell lineage occurs through modulation of the wnt asymmetry pathway in response to temperature increase
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153939/
https://www.ncbi.nlm.nih.gov/pubmed/31988193
http://dx.doi.org/10.1534/genetics.119.302896
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