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A genetically-encoded crosslinker screen identifies SERBP1 as a PKCε substrate influencing translation and cell division

Author

Listed:
  • Silvia Martini

    (Protein Phosphorylation Laboratory, The Francis Crick Institute)

  • Khalil Davis

    (Protein Phosphorylation Laboratory, The Francis Crick Institute)

  • Rupert Faraway

    (RNA Network Laboratory, The Francis Crick Institute
    UCL Queen Square Institute of Neurology, Queen Square)

  • Lisa Elze

    (Radboud University Medical Center)

  • Nicola Lockwood

    (Protein Phosphorylation Laboratory, The Francis Crick Institute)

  • Andrew Jones

    (Cell Cycle Laboratory, The Francis Crick Institute)

  • Xiao Xie

    (Synthetic and Functional Biomolecules Center, Beijing National Laboratory for Molecular Sciences, College of Chemistry and Molecular Engineering, Peking University)

  • Neil Q. McDonald

    (Signalling and Structural Biology Laboratory, The Francis Crick Institute)

  • David J. Mann

    (Imperial College London)

  • Alan Armstrong

    (Imperial College)

  • Jernej Ule

    (RNA Network Laboratory, The Francis Crick Institute
    UCL Queen Square Institute of Neurology, Queen Square)

  • Peter J. Parker

    (Protein Phosphorylation Laboratory, The Francis Crick Institute
    School of Cancer and Pharmaceutical Sciences, King’s College London, Guy’s Campus)

Abstract

The PKCε-regulated genome protective pathway provides transformed cells a failsafe to successfully complete mitosis. Despite the necessary role for Aurora B in this programme, it is unclear whether its requirement is sufficient or if other PKCε cell cycle targets are involved. To address this, we developed a trapping strategy using UV-photocrosslinkable amino acids encoded in the PKCε kinase domain. The validation of the mRNA binding protein SERBP1 as a PKCε substrate revealed a series of mitotic events controlled by the catalytic form of PKCε. PKCε represses protein translation, altering SERBP1 binding to the 40 S ribosomal subunit and promoting the assembly of ribonucleoprotein granules containing SERBP1, termed M-bodies. Independent of Aurora B, SERBP1 is shown to be necessary for chromosome segregation and successful cell division, correlating with M-body formation. This requirement for SERBP1 demonstrates that Aurora B acts in concert with translational regulation in the PKCε-controlled pathway exerting genome protection.

Suggested Citation

  • Silvia Martini & Khalil Davis & Rupert Faraway & Lisa Elze & Nicola Lockwood & Andrew Jones & Xiao Xie & Neil Q. McDonald & David J. Mann & Alan Armstrong & Jernej Ule & Peter J. Parker, 2021. "A genetically-encoded crosslinker screen identifies SERBP1 as a PKCε substrate influencing translation and cell division," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27189-5
    DOI: 10.1038/s41467-021-27189-5
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    References listed on IDEAS

    as
    1. Nicola Brownlow & Tanya Pike & Daniel Zicha & Lucy Collinson & Peter J. Parker, 2014. "Mitotic catenation is monitored and resolved by a PKCε-regulated pathway," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    2. Jason Ptacek & Geeta Devgan & Gregory Michaud & Heng Zhu & Xiaowei Zhu & Joseph Fasolo & Hong Guo & Ghil Jona & Ashton Breitkreutz & Richelle Sopko & Rhonda R. McCartney & Martin C. Schmidt & Najma Ra, 2005. "Global analysis of protein phosphorylation in yeast," Nature, Nature, vol. 438(7068), pages 679-684, December.
    3. Joanna R. Kelly & Silvia Martini & Nicola Brownlow & Dhira Joshi & Stefania Federico & Shirin Jamshidi & Svend Kjaer & Nicola Lockwood & Khondaker Miraz Rahman & Franca Fraternali & Peter J. Parker & , 2020. "The Aurora B specificity switch is required to protect from non-disjunction at the metaphase/anaphase transition," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. Andreas M. Anger & Jean-Paul Armache & Otto Berninghausen & Michael Habeck & Marion Subklewe & Daniel N. Wilson & Roland Beckmann, 2013. "Structures of the human and Drosophila 80S ribosome," Nature, Nature, vol. 497(7447), pages 80-85, May.
    5. Joanna R. Kelly & Silvia Martini & Nicola Brownlow & Dhira Joshi & Stefania Federico & Shirin Jamshidi & Svend Kjaer & Nicola Lockwood & Khondaker Miraz Rahman & Franca Fraternali & Peter J. Parker & , 2020. "Author Correction: The Aurora B specificity switch is required to protect from non-disjunction at the metaphase/anaphase transition," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
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