Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.

Ras mediates signaling pathways controlling cell proliferation and development by cycling between GTP- and GDP-bound active and inactive conformational states. Understanding the complete reaction path of this conformational change and its intermediary structures is critical to understanding Ras sign...

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Main Authors: Barry J Grant, Alemayehu A Gorfe, J Andrew McCammon
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-03-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1000325&type=printable
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author Barry J Grant
Alemayehu A Gorfe
J Andrew McCammon
author_facet Barry J Grant
Alemayehu A Gorfe
J Andrew McCammon
author_sort Barry J Grant
collection DOAJ
description Ras mediates signaling pathways controlling cell proliferation and development by cycling between GTP- and GDP-bound active and inactive conformational states. Understanding the complete reaction path of this conformational change and its intermediary structures is critical to understanding Ras signaling. We characterize nucleotide-dependent conformational transition using multiple-barrier-crossing accelerated molecular dynamics (aMD) simulations. These transitions, achieved for the first time for wild-type Ras, are impossible to observe with classical molecular dynamics (cMD) simulations due to the large energetic barrier between end states. Mapping the reaction path onto a conformer plot describing the distribution of the crystallographic structures enabled identification of highly populated intermediate structures. These structures have unique switch orientations (residues 25-40 and 57-75) intermediate between GTP and GDP states, or distinct loop3 (46-49), loop7 (105-110), and alpha5 C-terminus (159-166) conformations distal from the nucleotide-binding site. In addition, these barrier-crossing trajectories predict novel nucleotide-dependent correlated motions, including correlations of alpha2 (residues 66-74) with alpha3-loop7 (93-110), loop2 (26-37) with loop10 (145-151), and loop3 (46-49) with alpha5 (152-167). The interconversion between newly identified Ras conformations revealed by this study advances our mechanistic understanding of Ras function. In addition, the pattern of correlated motions provides new evidence for a dynamic linkage between the nucleotide-binding site and the membrane interacting C-terminus critical for the signaling function of Ras. Furthermore, normal mode analysis indicates that the dominant collective motion that occurs during nucleotide-dependent conformational exchange, and captured in aMD (but absent in cMD) simulations, is a low-frequency motion intrinsic to the structure.
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spelling doaj-art-3f5abb008d9b427f994db116a166b96c2025-08-20T02:00:55ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582009-03-0153e100032510.1371/journal.pcbi.1000325Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.Barry J GrantAlemayehu A GorfeJ Andrew McCammonRas mediates signaling pathways controlling cell proliferation and development by cycling between GTP- and GDP-bound active and inactive conformational states. Understanding the complete reaction path of this conformational change and its intermediary structures is critical to understanding Ras signaling. We characterize nucleotide-dependent conformational transition using multiple-barrier-crossing accelerated molecular dynamics (aMD) simulations. These transitions, achieved for the first time for wild-type Ras, are impossible to observe with classical molecular dynamics (cMD) simulations due to the large energetic barrier between end states. Mapping the reaction path onto a conformer plot describing the distribution of the crystallographic structures enabled identification of highly populated intermediate structures. These structures have unique switch orientations (residues 25-40 and 57-75) intermediate between GTP and GDP states, or distinct loop3 (46-49), loop7 (105-110), and alpha5 C-terminus (159-166) conformations distal from the nucleotide-binding site. In addition, these barrier-crossing trajectories predict novel nucleotide-dependent correlated motions, including correlations of alpha2 (residues 66-74) with alpha3-loop7 (93-110), loop2 (26-37) with loop10 (145-151), and loop3 (46-49) with alpha5 (152-167). The interconversion between newly identified Ras conformations revealed by this study advances our mechanistic understanding of Ras function. In addition, the pattern of correlated motions provides new evidence for a dynamic linkage between the nucleotide-binding site and the membrane interacting C-terminus critical for the signaling function of Ras. Furthermore, normal mode analysis indicates that the dominant collective motion that occurs during nucleotide-dependent conformational exchange, and captured in aMD (but absent in cMD) simulations, is a low-frequency motion intrinsic to the structure.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1000325&type=printable
spellingShingle Barry J Grant
Alemayehu A Gorfe
J Andrew McCammon
Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
PLoS Computational Biology
title Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
title_full Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
title_fullStr Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
title_full_unstemmed Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
title_short Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics.
title_sort ras conformational switching simulating nucleotide dependent conformational transitions with accelerated molecular dynamics
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1000325&type=printable
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