The origin of minus-end directionality and mechanochemistry of Ncd motors.

Adaptation of molecular structure to the ligand chemistry and interaction with the cytoskeletal filament are key to understanding the mechanochemistry of molecular motors. Despite the striking structural similarity with kinesin-1, which moves towards plus-end, Ncd motors exhibit minus-end directiona...

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Main Authors: Biman Jana, Changbong Hyeon, José N Onuchic
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002783&type=printable
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author Biman Jana
Changbong Hyeon
José N Onuchic
author_facet Biman Jana
Changbong Hyeon
José N Onuchic
author_sort Biman Jana
collection DOAJ
description Adaptation of molecular structure to the ligand chemistry and interaction with the cytoskeletal filament are key to understanding the mechanochemistry of molecular motors. Despite the striking structural similarity with kinesin-1, which moves towards plus-end, Ncd motors exhibit minus-end directionality on microtubules (MTs). Here, by employing a structure-based model of protein folding, we show that a simple repositioning of the neck-helix makes the dynamics of Ncd non-processive and minus-end directed as opposed to kinesin-1. Our computational model shows that Ncd in solution can have both symmetric and asymmetric conformations with disparate ADP binding affinity, also revealing that there is a strong correlation between distortion of motor head and decrease in ADP binding affinity in the asymmetric state. The nucleotide (NT) free-ADP (φ-ADP) state bound to MTs favors the symmetric conformation whose coiled-coil stalk points to the plus-end. Upon ATP binding, an enhanced flexibility near the head-neck junction region, which we have identified as the important structural element for directional motility, leads to reorienting the coiled-coil stalk towards the minus-end by stabilizing the asymmetric conformation. The minus-end directionality of the Ncd motor is a remarkable example that demonstrates how motor proteins in the kinesin superfamily diversify their functions by simply rearranging the structural elements peripheral to the catalytic motor head domain.
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spelling doaj-art-67a825934d4a48dab41c442b063e70632025-08-20T03:11:57ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582012-01-01811e100278310.1371/journal.pcbi.1002783The origin of minus-end directionality and mechanochemistry of Ncd motors.Biman JanaChangbong HyeonJosé N OnuchicAdaptation of molecular structure to the ligand chemistry and interaction with the cytoskeletal filament are key to understanding the mechanochemistry of molecular motors. Despite the striking structural similarity with kinesin-1, which moves towards plus-end, Ncd motors exhibit minus-end directionality on microtubules (MTs). Here, by employing a structure-based model of protein folding, we show that a simple repositioning of the neck-helix makes the dynamics of Ncd non-processive and minus-end directed as opposed to kinesin-1. Our computational model shows that Ncd in solution can have both symmetric and asymmetric conformations with disparate ADP binding affinity, also revealing that there is a strong correlation between distortion of motor head and decrease in ADP binding affinity in the asymmetric state. The nucleotide (NT) free-ADP (φ-ADP) state bound to MTs favors the symmetric conformation whose coiled-coil stalk points to the plus-end. Upon ATP binding, an enhanced flexibility near the head-neck junction region, which we have identified as the important structural element for directional motility, leads to reorienting the coiled-coil stalk towards the minus-end by stabilizing the asymmetric conformation. The minus-end directionality of the Ncd motor is a remarkable example that demonstrates how motor proteins in the kinesin superfamily diversify their functions by simply rearranging the structural elements peripheral to the catalytic motor head domain.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002783&type=printable
spellingShingle Biman Jana
Changbong Hyeon
José N Onuchic
The origin of minus-end directionality and mechanochemistry of Ncd motors.
PLoS Computational Biology
title The origin of minus-end directionality and mechanochemistry of Ncd motors.
title_full The origin of minus-end directionality and mechanochemistry of Ncd motors.
title_fullStr The origin of minus-end directionality and mechanochemistry of Ncd motors.
title_full_unstemmed The origin of minus-end directionality and mechanochemistry of Ncd motors.
title_short The origin of minus-end directionality and mechanochemistry of Ncd motors.
title_sort origin of minus end directionality and mechanochemistry of ncd motors
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002783&type=printable
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