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Research Article
Sequestration of the PKC ortholog Pck2 in stress granules as a feedback mechanism of MAPK signaling in fission yeast
Yuki Kanda, Ryosuke Satoh, Teruaki Takasaki, Naofumi Tomimoto, Kiko Tsuchiya, Chun An Tsai, Taemi Tanaka, Shu Kyomoto, Kozo Hamada, Toshinobu Fujiwara, Reiko Sugiura
Journal of Cell Science 2021 134: jcs250191 doi: 10.1242/jcs.250191 Published 26 January 2021
Yuki Kanda
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Ryosuke Satoh
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Teruaki Takasaki
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Naofumi Tomimoto
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Kiko Tsuchiya
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Chun An Tsai
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Taemi Tanaka
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Shu Kyomoto
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Kozo Hamada
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Toshinobu Fujiwara
2Laboratory of Biochemistry, Department of Pharmacy, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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Reiko Sugiura
1Laboratory of Molecular Pharmacogenomics, Department of Pharmaceutical Sciences, Faculty of Pharmacy, Kindai University, Osaka 577-8502, Japan
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  • ORCID record for Reiko Sugiura
  • For correspondence: sugiurar@phar.kindai.ac.jp

Handling Editor: John Heath

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ABSTRACT

Protein kinase C (PKC) signaling is a highly conserved signaling module that plays a central role in a myriad of physiological processes, ranging from cell proliferation to cell death, via various signaling pathways, including MAPK signaling. Stress granules (SGs) are non-membranous cytoplasmic foci that aggregate in cells exposed to environmental stresses. Here, we explored the role of SGs in PKC/MAPK signaling activation in fission yeast. High-heat stress (HHS) induced Pmk1 MAPK activation and Pck2 translocation from the cell tips into poly(A)-binding protein (Pabp)-positive SGs. Pck2 dispersal from the cell tips required Pck2 kinase activity, and constitutively active Pck2 exhibited increased translocation to SGs. Importantly, Pmk1 deletion impaired Pck2 recruitment to SGs, indicating that MAPK activation stimulates Pck2 SG translocation. Consistently, HHS-induced SGs delayed Pck2 relocalization at the cell tips, thereby blocking subsequent Pmk1 reactivation after recovery from HHS. HHS partitioned Pck2 into the Pabp-positive SG-containing fraction, which resulted in reduced Pck2 abundance and kinase activity in the soluble fraction. Taken together, these results indicate that MAPK-dependent Pck2 SG recruitment serves as a feedback mechanism to intercept PKC/MAPK activation induced by HHS, which might underlie PKC-related diseases.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: Y.K., R. Satoh, T. Takasaki, K.H., T.F., R. Sugiura; Methodology: Y.K., R. Satoh, T. Takasaki, K.H., T.F., R. Sugiura; Validation: Y.K., R. Satoh, T. Takasaki, K.H., R. Sugiura; Formal analysis: Y.K., R. Satoh, T. Takasaki, N.T., K.T., C.A.T., T. Tanaka, S.K., K.H., R. Sugiura; Investigation: Y.K., N.T., K.T., C.A.T., T. Tanaka, S.K.; Resources: R. Sugiura; Data curation: Y.K.; Writing - original draft: Y.K., R. Sugiura; Writing - review & editing: Y.K., R. Satoh, T. Takasaki, K.H., T.F., R. Sugiura; Visualization: Y.K., R. Sugiura; Supervision: R. Sugiura; Project administration: R. Sugiura; Funding acquisition: R. Sugiura.

  • Funding

    This study was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT)-Supported Program for the Strategic Research Foundation at Private Universities, 2014–2018 [JPS1411037 (R. Sugiura)], a Grant-in-Aid for scientific research from the Japan Society for the Promotion of Science (JSPS) KAKENHI [JP19H03376 (R. Sugiura)], a JSPS Fellowship [JP20J15403 (Y.K.)] and a grant by the Antiaging Project for Private Universities (R. Sugiura).

  • Supplementary information

    Supplementary information available online at https://jcs.biologists.org/lookup/doi/10.1242/jcs.250191.supplemental

  • Received June 16, 2020.
  • Accepted November 23, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • PKC
  • Stress granules
  • MAPK Signaling
  • Spatiotemporal regulation
  • Heat stress
  • Phase separation

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Research Article
Sequestration of the PKC ortholog Pck2 in stress granules as a feedback mechanism of MAPK signaling in fission yeast
Yuki Kanda, Ryosuke Satoh, Teruaki Takasaki, Naofumi Tomimoto, Kiko Tsuchiya, Chun An Tsai, Taemi Tanaka, Shu Kyomoto, Kozo Hamada, Toshinobu Fujiwara, Reiko Sugiura
Journal of Cell Science 2021 134: jcs250191 doi: 10.1242/jcs.250191 Published 26 January 2021
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Research Article
Sequestration of the PKC ortholog Pck2 in stress granules as a feedback mechanism of MAPK signaling in fission yeast
Yuki Kanda, Ryosuke Satoh, Teruaki Takasaki, Naofumi Tomimoto, Kiko Tsuchiya, Chun An Tsai, Taemi Tanaka, Shu Kyomoto, Kozo Hamada, Toshinobu Fujiwara, Reiko Sugiura
Journal of Cell Science 2021 134: jcs250191 doi: 10.1242/jcs.250191 Published 26 January 2021

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