Yeast Nuak1 phosphorylates histone H3 threonine 11 in low glucose stress by the cooperation of AMPK and CK2 signaling

  1. Seunghee Oh
  2. Jaehyoun Lee
  3. Selene K Swanson
  4. Laurence Florens
  5. Michael P Washburn
  6. Jerry L Workman  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
  2. Stowers Institute of Medical Research, United States

Abstract

Changes in available nutrients are inevitable events for most living organisms. Upon nutritional stress, several signaling pathways cooperate to change the transcription program through chromatin regulation to rewire cellular metabolism. In budding yeast, histone H3 threonine 11 phosphorylation (H3pT11) acts as a marker of low glucose stress and regulates the transcription of nutritional stress responsive genes. Understanding how this histone modification 'senses' external glucose changes remains elusive. Here, we show that Tda1, the yeast orthologue of human Nuak1, is a direct kinase for H3pT11 upon low glucose stress. Yeast AMPK directly phosphorylates Tda1 to govern Tda1 activity, while CK2 regulates Tda1 nuclear localization. Collectively, AMPK and CK2 signaling converge on histone kinase Tda1 to link external low glucose stress to chromatin regulation.

Data availability

Original data underlying this manuscript can be accessed from the Stowers Original Data Repository at http://www.stowers.org/research/publications/libpb-1536.

Article and author information

Author details

  1. Seunghee Oh

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6701-9473
  2. Jaehyoun Lee

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  3. Selene K Swanson

    Stowers Institute of Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  4. Laurence Florens

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
  5. Michael P Washburn

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7568-2585
  6. Jerry L Workman

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    jlw@Stowers.org
    Competing interests
    Jerry L Workman, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8163-1952

Funding

Stowers Institute for Medical Research (Workman Lab)

  • Jerry L Workman

National Institute of General Medical Sciences (R35GM118068)

  • Jerry L Workman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Xiaobing Shi, Van Andel Institute, United States

Publication history

  1. Received: November 3, 2020
  2. Accepted: December 26, 2020
  3. Accepted Manuscript published: December 29, 2020 (version 1)
  4. Version of Record published: January 4, 2021 (version 2)

Copyright

© 2020, Oh et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Seunghee Oh
  2. Jaehyoun Lee
  3. Selene K Swanson
  4. Laurence Florens
  5. Michael P Washburn
  6. Jerry L Workman
(2020)
Yeast Nuak1 phosphorylates histone H3 threonine 11 in low glucose stress by the cooperation of AMPK and CK2 signaling
eLife 9:e64588.
https://doi.org/10.7554/eLife.64588
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