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Article

Genome-Wide Role of HSF1 in Transcriptional Regulation of Desiccation Tolerance in the Anhydrobiotic Cell Line, Pv11

1
Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa 277-8562, Japan
2
Division of Biotechnology, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Tsukuba 305-0851, Japan
3
Extreme Biology Laboratory, Institute of Fundamental Medicine and Biology, Kazan Federal University, 420008 Kazan, Russia
4
Department of Biosciences and Informatics, Keio University, Yokohama 223-8522, Japan
5
Institute for Advanced Biosciences, Keio University, Tsuruoka 997-0017, Japan
6
Systems Biology Program, Graduate School of Media and Governance, Keio University, Fujisawa 252-8520, Japan
7
Laboratory for Transcriptome Technology, RIKEN Center for Integrative Medical Sciences, RIKEN, Yokohama 230-0045, Japan
*
Author to whom correspondence should be addressed.
Contributed equally to this work.
Academic Editor: T. G. Emyr Davies
Int. J. Mol. Sci. 2021, 22(11), 5798; https://doi.org/10.3390/ijms22115798
Received: 16 April 2021 / Revised: 24 May 2021 / Accepted: 24 May 2021 / Published: 28 May 2021
(This article belongs to the Section Molecular Biology)
The Pv11, an insect cell line established from the midge Polypedilum vanderplanki, is capable of extreme hypometabolic desiccation tolerance, so-called anhydrobiosis. We previously discovered that heat shock factor 1 (HSF1) contributes to the acquisition of desiccation tolerance by Pv11 cells, but the mechanistic details have yet to be elucidated. Here, by analyzing the gene expression profiles of newly established HSF1-knockout and -rescue cell lines, we show that HSF1 has a genome-wide effect on gene regulation in Pv11. The HSF1-knockout cells exhibit a reduced desiccation survival rate, but this is completely restored in HSF1-rescue cells. By comparing mRNA profiles of the two cell lines, we reveal that HSF1 induces anhydrobiosis-related genes, especially genes encoding late embryogenesis abundant proteins and thioredoxins, but represses a group of genes involved in basal cellular processes, thus promoting an extreme hypometabolism state in the cell. In addition, HSF1 binding motifs are enriched in the promoters of anhydrobiosis-related genes and we demonstrate binding of HSF1 to these promoters by ChIP-qPCR. Thus, HSF1 directly regulates the transcription of anhydrobiosis-related genes and consequently plays a pivotal role in the induction of anhydrobiotic ability in Pv11 cells. View Full-Text
Keywords: CRISPR/Cas9; knockout; rescue; anhydrobiosis; Polypedilum vanderplanki; insect cell CRISPR/Cas9; knockout; rescue; anhydrobiosis; Polypedilum vanderplanki; insect cell
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MDPI and ACS Style

Tokumoto, S.; Miyata, Y.; Deviatiiarov, R.; Yamada, T.G.; Hiki, Y.; Kozlova, O.; Yoshida, Y.; Cornette, R.; Funahashi, A.; Shagimardanova, E.; Gusev, O.; Kikawada, T. Genome-Wide Role of HSF1 in Transcriptional Regulation of Desiccation Tolerance in the Anhydrobiotic Cell Line, Pv11. Int. J. Mol. Sci. 2021, 22, 5798. https://doi.org/10.3390/ijms22115798

AMA Style

Tokumoto S, Miyata Y, Deviatiiarov R, Yamada TG, Hiki Y, Kozlova O, Yoshida Y, Cornette R, Funahashi A, Shagimardanova E, Gusev O, Kikawada T. Genome-Wide Role of HSF1 in Transcriptional Regulation of Desiccation Tolerance in the Anhydrobiotic Cell Line, Pv11. International Journal of Molecular Sciences. 2021; 22(11):5798. https://doi.org/10.3390/ijms22115798

Chicago/Turabian Style

Tokumoto, Shoko, Yugo Miyata, Ruslan Deviatiiarov, Takahiro G. Yamada, Yusuke Hiki, Olga Kozlova, Yuki Yoshida, Richard Cornette, Akira Funahashi, Elena Shagimardanova, Oleg Gusev, and Takahiro Kikawada. 2021. "Genome-Wide Role of HSF1 in Transcriptional Regulation of Desiccation Tolerance in the Anhydrobiotic Cell Line, Pv11" International Journal of Molecular Sciences 22, no. 11: 5798. https://doi.org/10.3390/ijms22115798

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