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Co-translational assembly orchestrates competing biogenesis pathways

Author

Listed:
  • Maximilian Seidel

    (Max Planck Institute of Biophysics
    Heidelberg University)

  • Anja Becker

    (Max Planck Institute of Biophysics)

  • Filipa Pereira

    (European Molecular Biology Laboratory (EMBL)
    University of Michigan)

  • Jonathan J. M. Landry

    (European Molecular Biology Laboratory (EMBL))

  • Nayara Trevisan Doimo Azevedo

    (European Molecular Biology Laboratory (EMBL))

  • Claudia M. Fusco

    (Max Planck Institute for Brain Research)

  • Eva Kaindl

    (Max Planck Institute of Biophysics)

  • Natalie Romanov

    (Max Planck Institute of Biophysics)

  • Janina Baumbach

    (Max Planck Institute of Biophysics
    European Molecular Biology Laboratory (EMBL))

  • Julian D. Langer

    (Max Planck Institute for Brain Research
    Max Planck Institute of Biophysics
    Max Planck Institute for Brain Research)

  • Erin M. Schuman

    (Max Planck Institute for Brain Research)

  • Kiran Raosaheb Patil

    (European Molecular Biology Laboratory (EMBL)
    University of Cambridge)

  • Gerhard Hummer

    (Max Planck Institute of Biophysics
    Goethe University Frankfurt)

  • Vladimir Benes

    (European Molecular Biology Laboratory (EMBL))

  • Martin Beck

    (Max Planck Institute of Biophysics
    European Molecular Biology Laboratory (EMBL))

Abstract

During the co-translational assembly of protein complexes, a fully synthesized subunit engages with the nascent chain of a newly synthesized interaction partner. Such events are thought to contribute to productive assembly, but their exact physiological relevance remains underexplored. Here, we examine structural motifs contained in nucleoporins for their potential to facilitate co-translational assembly. We experimentally test candidate structural motifs and identify several previously unknown co-translational interactions. We demonstrate by selective ribosome profiling that domain invasion motifs of beta-propellers, coiled-coils, and short linear motifs may act as co-translational assembly domains. Such motifs are often contained in proteins that are members of multiple complexes (moonlighters) and engage with closely related paralogs. Surprisingly, moonlighters and paralogs assemble co-translationally in only some but not all of the relevant biogenesis pathways. Our results highlight the regulatory complexity of assembly pathways.

Suggested Citation

  • Maximilian Seidel & Anja Becker & Filipa Pereira & Jonathan J. M. Landry & Nayara Trevisan Doimo Azevedo & Claudia M. Fusco & Eva Kaindl & Natalie Romanov & Janina Baumbach & Julian D. Langer & Erin M, 2022. "Co-translational assembly orchestrates competing biogenesis pathways," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28878-5
    DOI: 10.1038/s41467-022-28878-5
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    References listed on IDEAS

    as
    1. Seung Joong Kim & Javier Fernandez-Martinez & Ilona Nudelman & Yi Shi & Wenzhu Zhang & Barak Raveh & Thurston Herricks & Brian D. Slaughter & Joanna A. Hogan & Paula Upla & Ilan E. Chemmama & Riccardo, 2018. "Integrative structure and functional anatomy of a nuclear pore complex," Nature, Nature, vol. 555(7697), pages 475-482, March.
    2. Elijah L. Mena & Predrag Jevtić & Basil J. Greber & Christine L. Gee & Brandon G. Lew & David Akopian & Eva Nogales & John Kuriyan & Michael Rape, 2020. "Structural basis for dimerization quality control," Nature, Nature, vol. 586(7829), pages 452-456, October.
    3. Ivanka Kamenova & Pooja Mukherjee & Sascha Conic & Florian Mueller & Farrah El-Saafin & Paul Bardot & Jean-Marie Garnier & Doulaye Dembele & Simona Capponi & H. T. Marc Timmers & Stéphane D. Vincent &, 2019. "Co-translational assembly of mammalian nuclear multisubunit complexes," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Ayala Shiber & Kristina Döring & Ulrike Friedrich & Kevin Klann & Dorina Merker & Mostafa Zedan & Frank Tippmann & Günter Kramer & Bernd Bukau, 2018. "Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling," Nature, Nature, vol. 561(7722), pages 268-272, September.
    5. Matteo Allegretti & Christian E. Zimmerli & Vasileios Rantos & Florian Wilfling & Paolo Ronchi & Herman K. H. Fung & Chia-Wei Lee & Wim Hagen & Beata Turoňová & Kai Karius & Mandy Börmel & Xiaojie Zha, 2020. "In-cell architecture of the nuclear pore and snapshots of its turnover," Nature, Nature, vol. 586(7831), pages 796-800, October.
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    Cited by:

    1. Johannes Venezian & Hagit Bar-Yosef & Hila Ben-Arie Zilberman & Noam Cohen & Oded Kleifeld & Juan Fernandez-Recio & Fabian Glaser & Ayala Shiber, 2024. "Diverging co-translational protein complex assembly pathways are governed by interface energy distribution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Maximilian Seidel & Natalie Romanov & Agnieszka Obarska-Kosinska & Anja Becker & Nayara Trevisan Doimo de Azevedo & Jan Provaznik & Sankarshana R. Nagaraja & Jonathan J. M. Landry & Vladimir Benes & M, 2023. "Co-translational binding of importins to nascent proteins," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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