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Title: Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase

Abstract

Subunits in multimeric ring-shaped motors must coordinate their activities to ensure correct and efficient performance of their mechanical tasks. Here, we study WT and arginine finger mutants of the pentameric bacteriophage φ29 DNA packaging motor. Our results reveal the molecular interactions necessary for the coordination of ADP–ATP exchange and ATP hydrolysis of the motor’s biphasic mechanochemical cycle. We show that two distinct regulatory mechanisms determine this coordination. In the first mechanism, the DNA up-regulates a single subunit’s catalytic activity, transforming it into a global regulator that initiates the nucleotide exchange phase and the hydrolysis phase. In the second, an arginine finger in each subunit promotes ADP–ATP exchange and ATP hydrolysis of its neighbor. Accordingly, we suggest that the subunits perform the roles described for GDP exchange factors and GTPase-activating proteins observed in small GTPases. We propose that these mechanisms are fundamental to intersubunit coordination and are likely present in other ring ATPases.

Authors:
; ; ; ; ; ; ; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1460503
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 115 Journal Issue: 31; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Tafoya, Sara, Liu, Shixin, Castillo, Juan P., Atz, Rockney, Morais, Marc C., Grimes, Shelley, Jardine, Paul J., and Bustamante, Carlos. Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase. United States: N. p., 2018. Web. doi:10.1073/pnas.1802736115.
Tafoya, Sara, Liu, Shixin, Castillo, Juan P., Atz, Rockney, Morais, Marc C., Grimes, Shelley, Jardine, Paul J., & Bustamante, Carlos. Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase. United States. doi:10.1073/pnas.1802736115.
Tafoya, Sara, Liu, Shixin, Castillo, Juan P., Atz, Rockney, Morais, Marc C., Grimes, Shelley, Jardine, Paul J., and Bustamante, Carlos. Mon . "Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase". United States. doi:10.1073/pnas.1802736115.
@article{osti_1460503,
title = {Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase},
author = {Tafoya, Sara and Liu, Shixin and Castillo, Juan P. and Atz, Rockney and Morais, Marc C. and Grimes, Shelley and Jardine, Paul J. and Bustamante, Carlos},
abstractNote = {Subunits in multimeric ring-shaped motors must coordinate their activities to ensure correct and efficient performance of their mechanical tasks. Here, we study WT and arginine finger mutants of the pentameric bacteriophage φ29 DNA packaging motor. Our results reveal the molecular interactions necessary for the coordination of ADP–ATP exchange and ATP hydrolysis of the motor’s biphasic mechanochemical cycle. We show that two distinct regulatory mechanisms determine this coordination. In the first mechanism, the DNA up-regulates a single subunit’s catalytic activity, transforming it into a global regulator that initiates the nucleotide exchange phase and the hydrolysis phase. In the second, an arginine finger in each subunit promotes ADP–ATP exchange and ATP hydrolysis of its neighbor. Accordingly, we suggest that the subunits perform the roles described for GDP exchange factors and GTPase-activating proteins observed in small GTPases. We propose that these mechanisms are fundamental to intersubunit coordination and are likely present in other ring ATPases.},
doi = {10.1073/pnas.1802736115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 31,
volume = 115,
place = {United States},
year = {2018},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1802736115

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Cited by: 1 work
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