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UFMylation regulates translational homeostasis and cell cycle progression

Igor A. Gak, Djordje Vasiljevic, Thomas Zerjatke, Lu Yu, Mario Brosch, Theodoros I. Roumeliotis, Cindy Horenburg, Nancy Klemm, Gábor Bakos, Alexander Herrmann, Jochen Hampe, Ingmar Glauche, Jyoti S. Choudhary, View ORCID ProfileJörg Mansfeld
doi: https://doi.org/10.1101/2020.02.03.931196
Igor A. Gak
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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Djordje Vasiljevic
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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Thomas Zerjatke
2Institute for Medical Informatics and Biometry, Carl Gustav Carus Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany
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Lu Yu
3Functional Proteomics Group, The Institute of Cancer Research, London, SW3 6JB, UK
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Mario Brosch
4Center for Regenerative Therapies Dresden (CRTD), Technische Universität Dresden, 01307 Dresden, Germany
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Theodoros I. Roumeliotis
3Functional Proteomics Group, The Institute of Cancer Research, London, SW3 6JB, UK
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Cindy Horenburg
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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Nancy Klemm
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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Gábor Bakos
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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Alexander Herrmann
4Center for Regenerative Therapies Dresden (CRTD), Technische Universität Dresden, 01307 Dresden, Germany
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Jochen Hampe
4Center for Regenerative Therapies Dresden (CRTD), Technische Universität Dresden, 01307 Dresden, Germany
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Ingmar Glauche
2Institute for Medical Informatics and Biometry, Carl Gustav Carus Faculty of Medicine, Technische Universität Dresden, 01307 Dresden, Germany
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Jyoti S. Choudhary
3Functional Proteomics Group, The Institute of Cancer Research, London, SW3 6JB, UK
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Jörg Mansfeld
1Cell Cycle, Biotechnology Center, Technische Universität Dresden, 01307 Dresden, Germany
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  • ORCID record for Jörg Mansfeld
  • For correspondence: joerg.mansfeld@tu-dresden.de
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Summary

UFMylation, the posttranslational modification of proteins with ubiquitin fold modifier 1 (UFM1) is essential for metazoan life and is associated with multiple human diseases. Although UFMylation has been linked to endoplasmic reticulum (ER) stress, its biological functions and relevant cellular targets beyond the ER are obscure. Here, we show that UFMylation directly controls translation and cell division in a manner otherwise known for cellular homeostasis-sensing pathways such as mTOR. By combining cell cycle analyses, mass spectrometry and ribosome profiling we demonstrate that UFMylation is required for eIF4F translation initiation complex assembly and recruitment of the ribosome. Interference with UFMylation shuts down global translation, which is sensed by cyclin D1 and halts the cell cycle independently of integrated stress response signalling. Our findings establish UFMylation as a key regulator of translation and uncover a pathway that couples translational homeostasis to cell cycle progression via a ubiquitin-like modification.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 03, 2020.
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UFMylation regulates translational homeostasis and cell cycle progression
Igor A. Gak, Djordje Vasiljevic, Thomas Zerjatke, Lu Yu, Mario Brosch, Theodoros I. Roumeliotis, Cindy Horenburg, Nancy Klemm, Gábor Bakos, Alexander Herrmann, Jochen Hampe, Ingmar Glauche, Jyoti S. Choudhary, Jörg Mansfeld
bioRxiv 2020.02.03.931196; doi: https://doi.org/10.1101/2020.02.03.931196
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UFMylation regulates translational homeostasis and cell cycle progression
Igor A. Gak, Djordje Vasiljevic, Thomas Zerjatke, Lu Yu, Mario Brosch, Theodoros I. Roumeliotis, Cindy Horenburg, Nancy Klemm, Gábor Bakos, Alexander Herrmann, Jochen Hampe, Ingmar Glauche, Jyoti S. Choudhary, Jörg Mansfeld
bioRxiv 2020.02.03.931196; doi: https://doi.org/10.1101/2020.02.03.931196

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