Identifying Sequence Perturbations to an Intrinsically Disordered Protein that Determine Its Phase Separation Behavior Article Swipe
Benjamin S. Schuster
,
Gregory L. Dignon
,
Wai Shing Tang
,
Fleurie M. Kelley
,
Aishwarya Kanchi Ranganath
,
Craig N. Jahnke
,
Alison G. Simpkins
,
Roshan Mammen Regy
,
Daniel A. Hammer
,
Matthew C. Good
,
Jeetain Mittal
·
YOU?
·
· 2020
· Open Access
·
· DOI: https://doi.org/10.1101/2020.01.06.894576
YOU?
·
· 2020
· Open Access
·
· DOI: https://doi.org/10.1101/2020.01.06.894576
Phase separation of intrinsically disordered proteins (IDPs) commonly underlies the formation of membraneless organelles, which compartmentalize molecules intracellularly in the absence of a lipid membrane. Identifying the protein sequence features responsible for IDP phase separation is critical for understanding physiological roles and pathological consequences of biomolecular condensation, as well as for harnessing phase separation for applications in bio-inspired materials design. To expand our knowledge of sequence determinants of IDP phase separation, we characterized variants of the intrinsically disordered RGG domain from LAF-1, a model protein involved in phase separation and a key component of P granules. Based on a predictive coarse-grained IDP model, we identified a region of the RGG domain that has high contact probability and is highly conserved between species; deletion of this region significantly disrupts phase separation in vitro and in vivo. We determined the effects of charge patterning on phase behavior through sequence shuffling. By altering the wild-type sequence, which contains well-mixed charged residues, to increase charge segregation, we designed sequences with significantly increased phase separation propensity. This result indicates the natural sequence is under negative selection to moderate this mode of interaction. We measured the contributions of tyrosine and arginine residues to phase separation experimentally through mutagenesis studies and computationally through direct interrogation of different modes of interaction using all-atom simulations. Finally, we show that in spite of these sequence perturbations, the RGG-derived condensates remain liquid-like. Together, these studies advance a predictive framework and identify key biophysical principles of sequence features important to phase separation. Significance Statement Membraneless organelles are assemblies of highly concentrated biomolecules that form through a liquid-liquid phase separation process. These assemblies are often enriched in intrinsically disordered proteins, which play an important role in driving phase separation. Understanding the sequence-to-phase behavior relationship of these disordered proteins is important for understanding the biochemistry of membraneless organelles, as well as for designing synthetic organelles and biomaterials. In this work, we explore a model protein, the disordered N-terminal domain of LAF-1, and highlight how three key features of the sequence control the protein’s propensity to phase separate. Combining predictive simulations with experiments, we find that phase behavior of this model IDP is dictated by the presence of a short conserved domain, charge patterning, and arginine-tyrosine interactions.
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- Type
- preprint
- Language
- en
- Landing Page
- https://doi.org/10.1101/2020.01.06.894576
- https://www.biorxiv.org/content/biorxiv/early/2020/01/06/2020.01.06.894576.full.pdf
- OA Status
- green
- Cited By
- 25
- References
- 77
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W2998532901
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https://openalex.org/W2998532901Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1101/2020.01.06.894576Digital Object Identifier
- Title
-
Identifying Sequence Perturbations to an Intrinsically Disordered Protein that Determine Its Phase Separation BehaviorWork title
- Type
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preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
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2020Year of publication
- Publication date
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2020-01-06Full publication date if available
- Authors
-
Benjamin S. Schuster, Gregory L. Dignon, Wai Shing Tang, Fleurie M. Kelley, Aishwarya Kanchi Ranganath, Craig N. Jahnke, Alison G. Simpkins, Roshan Mammen Regy, Daniel A. Hammer, Matthew C. Good, Jeetain MittalList of authors in order
- Landing page
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https://doi.org/10.1101/2020.01.06.894576Publisher landing page
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https://www.biorxiv.org/content/biorxiv/early/2020/01/06/2020.01.06.894576.full.pdfDirect link to full text PDF
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YesWhether a free full text is available
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greenOpen access status per OpenAlex
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https://www.biorxiv.org/content/biorxiv/early/2020/01/06/2020.01.06.894576.full.pdfDirect OA link when available
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Intrinsically disordered proteins, Sequence (biology), Phase (matter), Chemical physics, Biophysics, Mutagenesis, Biology, Chemistry, Mutation, Genetics, Gene, Organic chemistryTop concepts (fields/topics) attached by OpenAlex
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25Total citation count in OpenAlex
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2025: 2, 2024: 2, 2023: 2, 2022: 6, 2021: 5Per-year citation counts (last 5 years)
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77Number of works referenced by this work
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10Other works algorithmically related by OpenAlex
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