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Research Article
Deubiquitylases USP5 and USP13 are recruited to and regulate heat-induced stress granules through their deubiquitylating activities
Xuan Xie, Shunsuke Matsumoto, Akinori Endo, Toshiaki Fukushima, Hiroyuki Kawahara, Yasushi Saeki, Masayuki Komada
J Cell Sci 2018 131: jcs210856 doi: 10.1242/jcs.210856 Published 12 April 2018
Xuan Xie
Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8501, JapanDepartment of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
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  • ORCID record for Xuan Xie
Shunsuke Matsumoto
Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
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  • ORCID record for Shunsuke Matsumoto
Akinori Endo
Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8501, Japan
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Toshiaki Fukushima
Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8501, JapanDepartment of Life Science and Technology, School of Life Science and Technology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
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  • For correspondence: tofu@bio.titech.ac.jpmakomada@bio.titech.ac.jp
Hiroyuki Kawahara
Department of Biological Sciences, Tokyo Metropolitan University, Tokyo 192-0397, Japan
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Yasushi Saeki
Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Tokyo 156-8506, Japan
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  • ORCID record for Yasushi Saeki
Masayuki Komada
Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama 226-8501, JapanDepartment of Life Science and Technology, School of Life Science and Technology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
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  • For correspondence: tofu@bio.titech.ac.jpmakomada@bio.titech.ac.jp
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ABSTRACT

Stress granules are transient cytoplasmic foci induced by various stresses that contain translation-stalled mRNAs and RNA-binding proteins. They are proposed to modulate mRNA translation and stress responses. Here, we show that the deubiquitylases USP5 and USP13 are recruited to heat-induced stress granules. Heat-induced stress granules also contained K48- and K63-linked ubiquitin chains. Depletion of USP5 or USP13 resulted in elevated ubiquitin chain levels and accelerated assembly of heat-induced stress granules, suggesting that these enzymes regulate the stability of the stress granules through their ubiquitin isopeptidase activity. Moreover, disassembly of heat-induced stress granules after returning the cells to normal temperatures was markedly repressed by individual depletion of USP5 or USP13. Finally, overexpression of a ubiquitin mutant lacking the C-terminal diglycine motif caused the accumulation of unanchored ubiquitin chains and the repression of the disassembly of heat-induced stress granules. As unanchored ubiquitin chains are preferred substrates for USP5, we suggest that USP5 regulates the assembly and disassembly of heat-induced stress granules by mediating the hydrolysis of unanchored ubiquitin chains while USP13 regulates stress granules through deubiquitylating protein-conjugated ubiquitin chains.

This article has an associated First Person interview with the first author of the paper.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: X.X., S.M., A.E., T.F., M.K.; Methodology: X.X., S.M., A.E., T.F., M.K.; Validation: X.X., S.M., A.E., T.F., M.K.; Investigation: X.X., S.M., A.E., M.K.; Resources: H.K.; Writing - original draft: X.X., M.K.; Writing - review & editing: A.E., T.F., Y.S., M.K.; Visualization: X.X., M.K.; Supervision: T.F., M.K.; Funding acquisition: M.K.

  • Funding

    This work was supported by the Japan Society for the Promotion of Science [KAKENHI JP24112003 to M.K.].

  • Supplementary information

    Supplementary information available online at http://jcs.biologists.org/lookup/doi/10.1242/jcs.210856.supplemental

  • Received September 13, 2017.
  • Accepted March 16, 2018.
  • © 2018. Published by The Company of Biologists Ltd
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Keywords

  • Ubiquitin
  • Deubiquitylase
  • Stress granule
  • USP5
  • USP13

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Deubiquitylases USP5 and USP13 are recruited to and regulate heat-induced stress granules through their deubiquitylating activities
Xuan Xie, Shunsuke Matsumoto, Akinori Endo, Toshiaki Fukushima, Hiroyuki Kawahara, Yasushi Saeki, Masayuki Komada
J Cell Sci 2018 131: jcs210856 doi: 10.1242/jcs.210856 Published 12 April 2018
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Deubiquitylases USP5 and USP13 are recruited to and regulate heat-induced stress granules through their deubiquitylating activities
Xuan Xie, Shunsuke Matsumoto, Akinori Endo, Toshiaki Fukushima, Hiroyuki Kawahara, Yasushi Saeki, Masayuki Komada
J Cell Sci 2018 131: jcs210856 doi: 10.1242/jcs.210856 Published 12 April 2018

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