ArticleProceedings of the National Academy of Sciences of the United States of America2012
The dynamic pause-unpackaging state, an off-translocation recovery state of a DNA packaging motor from bacteriophage T4.
Article in Proceedings of the National Academy of Sciences of the United States of America, 2012. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 27 papers.
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Who cites it
27 citing papers in PubMed.
- Something old, something new? Herpesvirus genome packaging examined in light of lessons from the tailed bacteriophages.Journal of virology · 2026Review
- Dynamics of viral self-assembly, viral genome packaging, and virus-cell interactions studied by optical tweezers.European biophysics journal : EBJ · 2026Review
- DNA/RNA hybrids avoid channel gating that leads to the continued packaging of numerous hybrids into the phi29 protein shell.Nucleic acids research · 2025Article
- Viral Genomic DNA Packaging Machinery.Sub-cellular biochemistry · 2024Review
- Optical Tweezers to Study Viruses.Sub-cellular biochemistry · 2024Review
- Revolving hexameric ATPases as asymmetric motors to translocate double-stranded DNA genome along one strand.iScience · 2023Review
- Revolving ATPase motors as asymmetrical hexamers in translocating lengthy dsDNA via conformational changes and electrostatic interactions in phi29, T7, herpesvirus, mimivirus,Exploration (Beijing, China) · 2023Review
- Review
- Bacteriophage T4 as a nanovehicle for delivery of genes and therapeutics into human cells.Current opinion in virology · 2022Review
- A viral genome packaging ring-ATPase is a flexibly coordinated pentamer.Nature communications · 2021Article
- Function of a viral genome packaging motor from bacteriophage T4 is insensitive to DNA sequence.Nucleic acids research · 2020Article
- Quantitative Study of the Chiral Organization of the Phage Genome Induced by the Packaging Motor.Biophysical journal · 2020Article
- Evidence that a catalytic glutamate and an 'Arginine Toggle' act in concert to mediate ATP hydrolysis and mechanochemical coupling in a viral DNA packaging motor.Nucleic acids research · 2019Article
- Nucleotide-dependent DNA gripping and an end-clamp mechanism regulate the bacteriophage T4 viral packaging motor.Nature communications · 2018Article
- Artificial bio-nanomachines based on protein needles derived from bacteriophage T4.Biophysical reviews · 2018Review
- Altering the speed of a DNA packaging motor from bacteriophage T4.Nucleic acids research · 2017Article
- Single-molecule measurements of viral ssRNA packaging.RNA (New York, N.Y.) · 2017Article
- Biological Nanomotors with a Revolution, Linear, or Rotation Motion Mechanism.Microbiology and molecular biology reviews : MMBR · 2016Review
- Mechanisms of DNA Packaging by Large Double-Stranded DNA Viruses.Annual review of virology · 2015Review
- The A, B, Cs of herpesvirus capsids.Viruses · 2015Review
Corrections and comments
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Authors and funding
3 authors.
Funding
Abstract
Tailed bacteriophages and herpes viruses use powerful ATP-driven molecular motors to translocate their viral genomes into a preformed capsid shell. The bacteriophage T4 motor, a pentamer of the large terminase protein (gp17) assembled at the portal vertex of the prohead, is the fastest and most powerful known, consistent with the need to package a ~170-kb viral genome in approximately 5 min. Although much is known about the mechanism of DNA translocation, very little is known about how ATP modulates motor-DNA interactions. Here, we report single-molecule measurements of the phage T4 gp17 motor by using dual-trap optical tweezers under different conditions of perturbation. Unexpectedly, the motor pauses randomly when ATP is limiting, for an average of 1 s, and then resumes translocation. During pausing, DNA is unpackaged, a phenomenon so far observed only in T4, where some of the packaged DNA is slowly released. We propose that the motor pauses whenever it encounters a subunit in the apo state with the DNA bound weakly and incorrectly. Pausing allows the subunit to capture ATP, whereas unpackaging allows scanning of DNA until a correct registry is established. Thus, the "pause-unpackaging" state is an off-translocation recovery state wherein the motor, sometimes by taking a few steps backward, can bypass the impediments encountered along the translocation path. These results lead to a four-state mechanochemical model that provides insights into the mechanisms of translocation of an intricately branched concatemeric viral genome.
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