Cargando…

The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance

Epigenetic regulation in starvation is important but not fully understood yet. Here we identified the Rpd3 gene, a Drosophila homolog of histone deacetylase 1, as a critical epigenetic regulator for acquiring starvation stress resistance. Immunostaining analyses of Drosophila fat body revealed that...

Descripción completa

Detalles Bibliográficos
Autores principales: Nakajima, Ei, Shimaji, Kouhei, Umegawachi, Takanari, Tomida, Saki, Yoshida, Hideki, Yoshimoto, Nana, Izawa, Shingo, Kimura, Hiroshi, Yamaguchi, Masamitsu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5132236/
https://www.ncbi.nlm.nih.gov/pubmed/27907135
http://dx.doi.org/10.1371/journal.pone.0167554
_version_ 1782471032725045248
author Nakajima, Ei
Shimaji, Kouhei
Umegawachi, Takanari
Tomida, Saki
Yoshida, Hideki
Yoshimoto, Nana
Izawa, Shingo
Kimura, Hiroshi
Yamaguchi, Masamitsu
author_facet Nakajima, Ei
Shimaji, Kouhei
Umegawachi, Takanari
Tomida, Saki
Yoshida, Hideki
Yoshimoto, Nana
Izawa, Shingo
Kimura, Hiroshi
Yamaguchi, Masamitsu
author_sort Nakajima, Ei
collection PubMed
description Epigenetic regulation in starvation is important but not fully understood yet. Here we identified the Rpd3 gene, a Drosophila homolog of histone deacetylase 1, as a critical epigenetic regulator for acquiring starvation stress resistance. Immunostaining analyses of Drosophila fat body revealed that the subcellular localization and levels of Rpd3 dynamically changed responding to starvation stress. In response to starvation stress, the level of Rpd3 rapidly increased, and it accumulated in the nucleolus in what appeared to be foci. These observations suggest that Rpd3 plays a role in regulation of rRNA synthesis in the nucleolus. The RT-qPCR and ChIP-qPCR analyses clarified that Rpd3 binds to the genomic region containing the rRNA promoters and activates rRNA synthesis in response to starvation stress. Polysome analyses revealed that the amount of polysomes was decreased in Rpd3 knockdown flies under starvation stress compared with the control flies. Since the autophagy-related proteins are known to be starvation stress tolerance proteins, we examined autophagy activity, and it was reduced in Rpd3 knockdown flies. Taken together, we conclude that Rpd3 accumulates in the nucleolus in the early stage of starvation, upregulates rRNA synthesis, maintains the polysome amount for translation, and finally increases stress tolerance proteins, such as autophagy-related proteins, to acquire starvation stress resistance.
format Online
Article
Text
id pubmed-5132236
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-51322362016-12-21 The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance Nakajima, Ei Shimaji, Kouhei Umegawachi, Takanari Tomida, Saki Yoshida, Hideki Yoshimoto, Nana Izawa, Shingo Kimura, Hiroshi Yamaguchi, Masamitsu PLoS One Research Article Epigenetic regulation in starvation is important but not fully understood yet. Here we identified the Rpd3 gene, a Drosophila homolog of histone deacetylase 1, as a critical epigenetic regulator for acquiring starvation stress resistance. Immunostaining analyses of Drosophila fat body revealed that the subcellular localization and levels of Rpd3 dynamically changed responding to starvation stress. In response to starvation stress, the level of Rpd3 rapidly increased, and it accumulated in the nucleolus in what appeared to be foci. These observations suggest that Rpd3 plays a role in regulation of rRNA synthesis in the nucleolus. The RT-qPCR and ChIP-qPCR analyses clarified that Rpd3 binds to the genomic region containing the rRNA promoters and activates rRNA synthesis in response to starvation stress. Polysome analyses revealed that the amount of polysomes was decreased in Rpd3 knockdown flies under starvation stress compared with the control flies. Since the autophagy-related proteins are known to be starvation stress tolerance proteins, we examined autophagy activity, and it was reduced in Rpd3 knockdown flies. Taken together, we conclude that Rpd3 accumulates in the nucleolus in the early stage of starvation, upregulates rRNA synthesis, maintains the polysome amount for translation, and finally increases stress tolerance proteins, such as autophagy-related proteins, to acquire starvation stress resistance. Public Library of Science 2016-12-01 /pmc/articles/PMC5132236/ /pubmed/27907135 http://dx.doi.org/10.1371/journal.pone.0167554 Text en © 2016 Nakajima et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Nakajima, Ei
Shimaji, Kouhei
Umegawachi, Takanari
Tomida, Saki
Yoshida, Hideki
Yoshimoto, Nana
Izawa, Shingo
Kimura, Hiroshi
Yamaguchi, Masamitsu
The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title_full The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title_fullStr The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title_full_unstemmed The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title_short The Histone Deacetylase Gene Rpd3 Is Required for Starvation Stress Resistance
title_sort histone deacetylase gene rpd3 is required for starvation stress resistance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5132236/
https://www.ncbi.nlm.nih.gov/pubmed/27907135
http://dx.doi.org/10.1371/journal.pone.0167554
work_keys_str_mv AT nakajimaei thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT shimajikouhei thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT umegawachitakanari thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT tomidasaki thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yoshidahideki thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yoshimotonana thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT izawashingo thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT kimurahiroshi thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yamaguchimasamitsu thehistonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT nakajimaei histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT shimajikouhei histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT umegawachitakanari histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT tomidasaki histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yoshidahideki histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yoshimotonana histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT izawashingo histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT kimurahiroshi histonedeacetylasegenerpd3isrequiredforstarvationstressresistance
AT yamaguchimasamitsu histonedeacetylasegenerpd3isrequiredforstarvationstressresistance