Unraveling Molecular Interactions in Liquid–Liquid Phase Separation of Disordered Proteins by Atomistic Simulations
Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid–liquid phase separation of proteins and RNA molecules. Multiple evidence suggests that in several cases disordered proteins are structural scaffolds that drive the condensation by forming a dynamic network of i...
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| Published in | The journal of physical chemistry. B Vol. 124; no. 41; pp. 9009 - 9016 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
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United States
American Chemical Society
15.10.2020
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| Abstract | Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid–liquid phase separation of proteins and RNA molecules. Multiple evidence suggests that in several cases disordered proteins are structural scaffolds that drive the condensation by forming a dynamic network of inter- and intramolecular contacts. Despite the blooming research activity in this field, the structural characterization of these entities is very limited, and we still do not understand how the phase behavior is encoded in the amino acid sequences of the scaffolding proteins. Here we exploited explicit-solvent atomistic simulations to investigate the N-terminal disordered region of DEAD-box helicase 4 (NDDX4), which is a well-established model for phase separation. Notably, we determined NDDX4 conformational ensemble at the single-molecule level, and we relied on a “divide-and-conquer” strategy, based on simulations of various protein fragments at high concentration, to probe intermolecular interactions in conditions mimicking real condensates. Our results provide a high-resolution picture of the molecular mechanisms underlying phase separation in agreement with NMR and mutagenesis data and suggest that clusters of arginine and aromatic residues may stabilize the assembly of several condensates. |
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| AbstractList | Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid-liquid phase separation of proteins and RNA molecules. Multiple evidence suggests that in several cases disordered proteins are structural scaffolds that drive the condensation by forming a dynamic network of inter- and intramolecular contacts. Despite the blooming research activity in this field, the structural characterization of these entities is very limited, and we still do not understand how the phase behavior is encoded in the amino acid sequences of the scaffolding proteins. Here we exploited explicit-solvent atomistic simulations to investigate the N-terminal disordered region of DEAD-box helicase 4 (NDDX4), which is a well-established model for phase separation. Notably, we determined NDDX4 conformational ensemble at the single-molecule level, and we relied on a "divide-and-conquer" strategy, based on simulations of various protein fragments at high concentration, to probe intermolecular interactions in conditions mimicking real condensates. Our results provide a high-resolution picture of the molecular mechanisms underlying phase separation in agreement with NMR and mutagenesis data and suggest that clusters of arginine and aromatic residues may stabilize the assembly of several condensates. Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid-liquid phase separation of proteins and RNA molecules. Multiple evidence suggests that in several cases disordered proteins are structural scaffolds that drive the condensation by forming a dynamic network of inter- and intramolecular contacts. Despite the blooming research activity in this field, the structural characterization of these entities is very limited, and we still do not understand how the phase behavior is encoded in the amino acid sequences of the scaffolding proteins. Here we exploited explicit-solvent atomistic simulations to investigate the N-terminal disordered region of DEAD-box helicase 4 (NDDX4), which is a well-established model for phase separation. Notably, we determined NDDX4 conformational ensemble at the single-molecule level, and we relied on a "divide-and-conquer" strategy, based on simulations of various protein fragments at high concentration, to probe intermolecular interactions in conditions mimicking real condensates. Our results provide a high-resolution picture of the molecular mechanisms underlying phase separation in agreement with NMR and mutagenesis data and suggest that clusters of arginine and aromatic residues may stabilize the assembly of several condensates.Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid-liquid phase separation of proteins and RNA molecules. Multiple evidence suggests that in several cases disordered proteins are structural scaffolds that drive the condensation by forming a dynamic network of inter- and intramolecular contacts. Despite the blooming research activity in this field, the structural characterization of these entities is very limited, and we still do not understand how the phase behavior is encoded in the amino acid sequences of the scaffolding proteins. Here we exploited explicit-solvent atomistic simulations to investigate the N-terminal disordered region of DEAD-box helicase 4 (NDDX4), which is a well-established model for phase separation. Notably, we determined NDDX4 conformational ensemble at the single-molecule level, and we relied on a "divide-and-conquer" strategy, based on simulations of various protein fragments at high concentration, to probe intermolecular interactions in conditions mimicking real condensates. Our results provide a high-resolution picture of the molecular mechanisms underlying phase separation in agreement with NMR and mutagenesis data and suggest that clusters of arginine and aromatic residues may stabilize the assembly of several condensates. |
| Author | Bailly, Rémy Ciandrini, Luca Paloni, Matteo Barducci, Alessandro |
| AuthorAffiliation | Centre de Biochimie Structurale (CBS), INSERM, CNRS |
| AuthorAffiliation_xml | – name: Centre de Biochimie Structurale (CBS), INSERM, CNRS |
| Author_xml | – sequence: 1 givenname: Matteo orcidid: 0000-0003-4841-9321 surname: Paloni fullname: Paloni, Matteo – sequence: 2 givenname: Rémy surname: Bailly fullname: Bailly, Rémy – sequence: 3 givenname: Luca surname: Ciandrini fullname: Ciandrini, Luca – sequence: 4 givenname: Alessandro orcidid: 0000-0002-1911-8039 surname: Barducci fullname: Barducci, Alessandro email: alessandro.barducci@cbs.cnrs.fr |
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| Snippet | Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid–liquid phase separation of proteins and RNA molecules. Multiple... Membraneless organelles are dynamical cellular condensates formed via biomolecular liquid-liquid phase separation of proteins and RNA molecules. Multiple... |
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| SubjectTerms | Amino Acid Sequence arginine B: Biophysics; Physical Chemistry of Biological Systems and Biomolecules Chemical Sciences DEAD-box RNA helicases Intrinsically Disordered Proteins mutagenesis or physical chemistry Organelles Phase Transition RNA separation Theoretical and |
| Title | Unraveling Molecular Interactions in Liquid–Liquid Phase Separation of Disordered Proteins by Atomistic Simulations |
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