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Long-term recovery from acute cold shock in Caenorhabditis elegans

BACKGROUND: Animals are exposed to a wide range of environmental stresses that can cause potentially fatal cellular damage. The ability to survive the period of stress as well as to repair any damage incurred is essential for fitness. Exposure to 2 °C for 24 h or longer is rapidly fatal to the nemat...

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Autores principales: Robinson, Joseph D., Powell, Jennifer R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4709947/
https://www.ncbi.nlm.nih.gov/pubmed/26754108
http://dx.doi.org/10.1186/s12860-015-0079-z
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author Robinson, Joseph D.
Powell, Jennifer R.
author_facet Robinson, Joseph D.
Powell, Jennifer R.
author_sort Robinson, Joseph D.
collection PubMed
description BACKGROUND: Animals are exposed to a wide range of environmental stresses that can cause potentially fatal cellular damage. The ability to survive the period of stress as well as to repair any damage incurred is essential for fitness. Exposure to 2 °C for 24 h or longer is rapidly fatal to the nematode Caenorhabditis elegans, but the process of recovery from a shorter, initially non-lethal, cold shock is poorly understood. RESULTS: We report that cold shock of less than 12-hour duration does not initially kill C. elegans, but these worms experience a progression of devastating phenotypes over the next 96 h that correlate with their eventual fate: successful recovery from the cold shock and survival, or failure to recover and death. Cold-shocked worms experience a marked loss of pigmentation, decrease in the size of their intestine and gonads, and disruption to the vulva. Those worms who will successfully recover from the cold shock regain their pigmentation and much of the integrity of their intestine and gonads. Those who will die do so with a distinct phenotype from worms dying during or immediately following cold shock, suggesting independent mechanisms. Worms lacking the G-protein coupled receptor FSHR-1 are resistant to acute death from longer cold shocks, and are more successful in their recovery from shorter sub-lethal cold shocks. CONCLUSIONS: We have defined two distinct phases of death associated with cold shock and described a progression of phenotypes that accompanies the course of recovery from that cold shock. The G-protein coupled receptor FSHR-1 antagonizes these novel processes of damage and recovery. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12860-015-0079-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-47099472016-01-13 Long-term recovery from acute cold shock in Caenorhabditis elegans Robinson, Joseph D. Powell, Jennifer R. BMC Cell Biol Research Article BACKGROUND: Animals are exposed to a wide range of environmental stresses that can cause potentially fatal cellular damage. The ability to survive the period of stress as well as to repair any damage incurred is essential for fitness. Exposure to 2 °C for 24 h or longer is rapidly fatal to the nematode Caenorhabditis elegans, but the process of recovery from a shorter, initially non-lethal, cold shock is poorly understood. RESULTS: We report that cold shock of less than 12-hour duration does not initially kill C. elegans, but these worms experience a progression of devastating phenotypes over the next 96 h that correlate with their eventual fate: successful recovery from the cold shock and survival, or failure to recover and death. Cold-shocked worms experience a marked loss of pigmentation, decrease in the size of their intestine and gonads, and disruption to the vulva. Those worms who will successfully recover from the cold shock regain their pigmentation and much of the integrity of their intestine and gonads. Those who will die do so with a distinct phenotype from worms dying during or immediately following cold shock, suggesting independent mechanisms. Worms lacking the G-protein coupled receptor FSHR-1 are resistant to acute death from longer cold shocks, and are more successful in their recovery from shorter sub-lethal cold shocks. CONCLUSIONS: We have defined two distinct phases of death associated with cold shock and described a progression of phenotypes that accompanies the course of recovery from that cold shock. The G-protein coupled receptor FSHR-1 antagonizes these novel processes of damage and recovery. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12860-015-0079-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-01-12 /pmc/articles/PMC4709947/ /pubmed/26754108 http://dx.doi.org/10.1186/s12860-015-0079-z Text en © Robinson and Powell. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Robinson, Joseph D.
Powell, Jennifer R.
Long-term recovery from acute cold shock in Caenorhabditis elegans
title Long-term recovery from acute cold shock in Caenorhabditis elegans
title_full Long-term recovery from acute cold shock in Caenorhabditis elegans
title_fullStr Long-term recovery from acute cold shock in Caenorhabditis elegans
title_full_unstemmed Long-term recovery from acute cold shock in Caenorhabditis elegans
title_short Long-term recovery from acute cold shock in Caenorhabditis elegans
title_sort long-term recovery from acute cold shock in caenorhabditis elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4709947/
https://www.ncbi.nlm.nih.gov/pubmed/26754108
http://dx.doi.org/10.1186/s12860-015-0079-z
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