Structural and Molecular Basis for Coordination in a Viral DNA Packaging Motor

Huzhang Mao, Mitul Saha, Emilio Reyes-Aldrete, Michael B. Sherman, Michael Woodson, Rockney Atz, Shelley Grimes, Paul J. Jardine, Marc C. Morais

Research output: Contribution to journalArticlepeer-review

30 Scopus citations

Abstract

Ring NTPases are a class of ubiquitous molecular motors involved in basic biological partitioning processes. dsDNA viruses encode ring ATPases that translocate their genomes to near-crystalline densities within pre-assembled viral capsids. Here, X-ray crystallography, cryoEM, and biochemical analyses of the dsDNA packaging motor in bacteriophage phi29 show how individual subunits are arranged in a pentameric ATPase ring and suggest how their activities are coordinated to translocate dsDNA. The resulting pseudo-atomic structure of the motor and accompanying functional analyses show how ATP is bound in the ATPase active site; identify two DNA contacts, including a potential DNA translocating loop; demonstrate that a trans-acting arginine finger is involved in coordinating hydrolysis around the ring; and suggest a functional coupling between the arginine finger and the DNA translocating loop. The ability to visualize the motor in action illuminates how the different motor components interact with each other and with their DNA substrate.

Original languageEnglish (US)
Pages (from-to)2017-2029
Number of pages13
JournalCell reports
Volume14
Issue number8
DOIs
StatePublished - Mar 1 2016

Bibliographical note

Funding Information:
This work was supported by Public Health Service grant GM095516 (to S.G. and M.C.M.) and GM059604 (to S.G.) from the National Institutes of Health. We would also like to acknowledge the Sealy Center for Structural Biology and Molecular Biophysics (SCSB) for support of the UTMB X-ray and cryoEM core facilities; the Texas Advanced Computing Center (TACC) for providing computational resources; Henry Bellamy and the Center for Advanced Microstructures and Devices (CAMD) for assistance with X-ray data collection; and Jiao Xie, Wei Zhao, and Bora Kuyomba Faulkner for technical assistance with the project.

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