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Articles

The Late S-Phase Transcription Factor Hcm1 Is Regulated through Phosphorylation by the Cell Wall Integrity Checkpoint

Takahiro Negishi, Jiri Veis, David Hollenstein, Mizuho Sekiya, Gustav Ammerer, Yoshikazu Ohya
Takahiro Negishi
aDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba, Japan
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Jiri Veis
bDepartment of Biochemistry, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria
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David Hollenstein
bDepartment of Biochemistry, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria
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Mizuho Sekiya
aDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba, Japan
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Gustav Ammerer
bDepartment of Biochemistry, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria
cChristian Doppler Laboratory for Proteome Analysis, University of Vienna, Vienna, Austria
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Yoshikazu Ohya
aDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba, Japan
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DOI: 10.1128/MCB.00952-15
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ABSTRACT

The cell wall integrity (CWI) checkpoint in the budding yeast Saccharomyces cerevisiae coordinates cell wall construction and cell cycle progression. In this study, we showed that the regulation of Hcm1, a late-S-phase transcription factor, arrests the cell cycle via the cell wall integrity checkpoint. Although the HCM1 mRNA level remained unaffected when the cell wall integrity checkpoint was induced, the protein level decreased. The overproduction of Hcm1 resulted in the failure of the cell wall integrity checkpoint. We identified 39 Hcm1 phosphorylation sites, including 26 novel sites, by tandem mass spectrometry analysis. A mutational analysis revealed that phosphorylation of Hcm1 at S61, S65, and S66 is required for the proper onset of the cell wall integrity checkpoint by regulating the timely decrease in its protein level. Hyperactivation of the CWI mitogen-activated protein kinase (MAPK) signaling pathway significantly reduced the Hcm1 protein level, and the deletion of CWI MAPK Slt2 resulted in a failure to decrease Hcm1 protein levels in response to stress, suggesting that phosphorylation is regulated by CWI MAPK. In conclusion, we suggest that Hcm1 is regulated negatively by the cell wall integrity checkpoint through timely phosphorylation and degradation under stress to properly control budding yeast proliferation.

FOOTNOTES

    • Received 18 October 2015.
    • Returned for modification 11 November 2015.
    • Accepted 24 December 2015.
    • Accepted manuscript posted online 4 January 2016.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/MCB.00952-15.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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The Late S-Phase Transcription Factor Hcm1 Is Regulated through Phosphorylation by the Cell Wall Integrity Checkpoint
Takahiro Negishi, Jiri Veis, David Hollenstein, Mizuho Sekiya, Gustav Ammerer, Yoshikazu Ohya
Molecular and Cellular Biology Mar 2016, 36 (6) 941-953; DOI: 10.1128/MCB.00952-15

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The Late S-Phase Transcription Factor Hcm1 Is Regulated through Phosphorylation by the Cell Wall Integrity Checkpoint
Takahiro Negishi, Jiri Veis, David Hollenstein, Mizuho Sekiya, Gustav Ammerer, Yoshikazu Ohya
Molecular and Cellular Biology Mar 2016, 36 (6) 941-953; DOI: 10.1128/MCB.00952-15
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