Revolving hexameric ATPases as asymmetric motors to translocate double-stranded DNA genome along one strand
Margaret Bohmer,
Abhjeet S. Bhullar,
Tao Weitao,
Long Zhang,
Jing-Huei Lee,
Peixuan Guo
Affiliations
Margaret Bohmer
Center for RNA Nanobiotechnology and Nanomedicine, The Ohio State University, Columbus, OH, USA; College of Pharmacy, Division of Pharmaceutics and Pharmacology, The Ohio State University, Columbus, OH, USA; College of Medicine, Dorothy M. Davis Heart and Lung Research Institute and James Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
Abhjeet S. Bhullar
Center for RNA Nanobiotechnology and Nanomedicine, The Ohio State University, Columbus, OH, USA; College of Pharmacy, Division of Pharmaceutics and Pharmacology, The Ohio State University, Columbus, OH, USA; College of Medicine, Dorothy M. Davis Heart and Lung Research Institute and James Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA; Interdisciplinary Biophysics Graduate Program, College of Art and Science, The Ohio State University, Columbus, OH 43210, USA
Tao Weitao
Center for the Genetics of Host Defense UT Southwestern Medical Center, Dallas, TX, USA
Long Zhang
Center for RNA Nanobiotechnology and Nanomedicine, The Ohio State University, Columbus, OH, USA; College of Pharmacy, Division of Pharmaceutics and Pharmacology, The Ohio State University, Columbus, OH, USA; College of Medicine, Dorothy M. Davis Heart and Lung Research Institute and James Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA
Jing-Huei Lee
Department of Biomedical Engineering, College of Engineering and Applied Science, University of Cincinnati, Cincinnati, OH, USA
Peixuan Guo
Center for RNA Nanobiotechnology and Nanomedicine, The Ohio State University, Columbus, OH, USA; College of Pharmacy, Division of Pharmaceutics and Pharmacology, The Ohio State University, Columbus, OH, USA; College of Medicine, Dorothy M. Davis Heart and Lung Research Institute and James Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA; Interdisciplinary Biophysics Graduate Program, College of Art and Science, The Ohio State University, Columbus, OH 43210, USA; Corresponding author
Summary: DsDNA translocation through nanoscale pores is generally accomplished by ATPase biomotors. The discovery of the revolving dsDNA translocation mechanism, as opposed to rotation, in bacteriophage phi29 elucidated how ATPase motors move dsDNA. Revolution-driven, hexameric dsDNA motors have been reported in herpesvirus, bacterial FtsK, Streptomyces TraB, and T7 phage. This review explores the common relationship between their structure and mechanisms. Commonalities include moving along the 5′→3′ strand, inchworm sequential action leading to an asymmetrical structure, channel chirality, channel size, and 3-step channel gating for controlling motion direction. The revolving mechanism and contact with one of the dsDNA strands addresses the historic controversy of dsDNA packaging using nicked, gapped, hybrid, or chemically modified DNA. These controversies surrounding dsDNA packaging activity using modified materials can be answered by whether the modification was introduced into the 3′→5′ or 5′→3′ strand. Perspectives concerning solutions to the controversy of motor structure and stoichiometry are also discussed.
