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Designer protein assemblies with tunable phase diagrams in living cells

Meta Heidenreich, Joseph M. Georgeson, Emanuele Locatelli, View ORCID ProfileLorenzo Rovigatti, Saroj Kumar Nandi, Avital Steinberg, Yotam Nadav, Eyal Shimoni, View ORCID ProfileSamuel A. Safran, View ORCID ProfileJonathan P. K. Doye, View ORCID ProfileEmmanuel D. Levy
doi: https://doi.org/10.1101/2020.06.03.131433
Meta Heidenreich
1Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
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Joseph M. Georgeson
1Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
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Emanuele Locatelli
6Faculty of Physics, University of Vienna, Vienna, Austria
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Lorenzo Rovigatti
4Physical & Theoretical Chemistry Laboratory, Department of Chemistry, University of Oxford, South Parks Road, Oxford, OX1 3QZ, UK
5Department of Physics, Sapienza Università di Roma, Rome, Italy
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  • ORCID record for Lorenzo Rovigatti
Saroj Kumar Nandi
2Department of Chemical and Biological Physics, Weizmann Institute of Science, Rehovot, Israel
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Avital Steinberg
1Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
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Yotam Nadav
1Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
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Eyal Shimoni
3Department of Chemical Research Support, Weizmann Institute of Science, Rehovot, Israel
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Samuel A. Safran
2Department of Chemical and Biological Physics, Weizmann Institute of Science, Rehovot, Israel
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  • ORCID record for Samuel A. Safran
Jonathan P. K. Doye
4Physical & Theoretical Chemistry Laboratory, Department of Chemistry, University of Oxford, South Parks Road, Oxford, OX1 3QZ, UK
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Emmanuel D. Levy
1Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
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  • ORCID record for Emmanuel D. Levy
  • For correspondence: emmanuel.levy@weizmann.ac.il
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Abstract

The self-organization of proteins into specific assemblies is a hallmark of biological systems. Principles governing protein-protein interactions have long been known. However, principles by which such nanoscale interactions generate diverse phenotypes of mesoscale assemblies, including phase-separated compartments, remains challenging to characterize and understand. To illuminate such principles, we create a system of two proteins designed to interact and form mesh-like assemblies in living cells. We devise a novel strategy to map high-resolution phase diagrams in vivo, which provide mesoscale self-assembly signatures of our system. The structural modularity of the two protein components allows straightforward modification of their molecular properties, enabling us to characterize how point mutations that change their interaction affinity impact the phase diagram and material state of the assemblies in vivo. Both, the phase diagrams and their dependence on interaction affinity were captured by theory and simulations, including out-of-equilibrium effects seen in growing cells. Applying our system to interrogate biological mechanisms of self-assembly, we find that co-translational protein binding suffices to recruit an mRNA to the designed micron-scale structures.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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 June 03, 2020.
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Designer protein assemblies with tunable phase diagrams in living cells
Meta Heidenreich, Joseph M. Georgeson, Emanuele Locatelli, Lorenzo Rovigatti, Saroj Kumar Nandi, Avital Steinberg, Yotam Nadav, Eyal Shimoni, Samuel A. Safran, Jonathan P. K. Doye, Emmanuel D. Levy
bioRxiv 2020.06.03.131433; doi: https://doi.org/10.1101/2020.06.03.131433
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Designer protein assemblies with tunable phase diagrams in living cells
Meta Heidenreich, Joseph M. Georgeson, Emanuele Locatelli, Lorenzo Rovigatti, Saroj Kumar Nandi, Avital Steinberg, Yotam Nadav, Eyal Shimoni, Samuel A. Safran, Jonathan P. K. Doye, Emmanuel D. Levy
bioRxiv 2020.06.03.131433; doi: https://doi.org/10.1101/2020.06.03.131433

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