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

Sara Tafoya, Shixin Liu, Juan P. Castillo, Rockney Atz, Marc Morais, Shelley Grimes, Paul J. Jardine, Carlos Bustamante

Research output: Contribution to journalArticle

1 Citation (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)7961-7966
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number31
DOIs
StatePublished - Jul 31 2018

Fingerprint

Adenosine Triphosphatases
Hydrolysis
Fingers
Arginine
Adenosine Triphosphate
DNA Packaging
GTPase-Activating Proteins
Guanine Nucleotide Exchange Factors
Monomeric GTP-Binding Proteins
Bacteriophages
Catalytic Domain
Up-Regulation
Nucleotides
DNA

Keywords

  • Intersubunit enzymatic regulation
  • Molecular switch-like regulation
  • Ring ATPases
  • Ring-shaped molecular motors
  • Single molecule DNA packaging

ASJC Scopus subject areas

  • General

Cite this

Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase. / Tafoya, Sara; Liu, Shixin; Castillo, Juan P.; Atz, Rockney; Morais, Marc; Grimes, Shelley; Jardine, Paul J.; Bustamante, Carlos.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 31, 31.07.2018, p. 7961-7966.

Research output: Contribution to journalArticle

Tafoya, Sara ; Liu, Shixin ; Castillo, Juan P. ; Atz, Rockney ; Morais, Marc ; Grimes, Shelley ; Jardine, Paul J. ; Bustamante, Carlos. / Molecular switch-like regulation enables global subunit coordination in a viral ring ATPase. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 31. pp. 7961-7966.
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AU - Morais, Marc

AU - Grimes, Shelley

AU - Jardine, Paul J.

AU - Bustamante, Carlos

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