Literature DB >> 25486612

The scrunchworm hypothesis: transitions between A-DNA and B-DNA provide the driving force for genome packaging in double-stranded DNA bacteriophages.

Stephen C Harvey1.   

Abstract

Double-stranded DNA bacteriophages have motors that drive the genome into preformed capsids, using the energy released by hydrolysis of ATP to overcome the forces opposing DNA packaging. Viral packaging motors are the strongest of all biological motors, but it is not known how they generate these forces. Several models for the process of mechanochemical force generation have been put forward, but there is no consensus on which, if any, of these is correct. All the existing models assume that protein-generated forces drive the DNA forward. The scrunchworm hypothesis proposes that the DNA molecule is the active force-generating core of the motor, not simply a substrate on which the motor operates. The protein components of the motor dehydrate a section of the DNA, converting it from the B form to the A form and shortening it by about 23%. The proteins then rehydrate the DNA, which converts back to the B form. Other regions of the motor grip and release the DNA to capture the shortening-lengthening motions of the B→A→B cycle ("scrunching"), so that DNA is pulled into the motor and pushed forward into the capsid. This DNA-centric mechanism provides a quantitative physical explanation for the magnitude of the forces generated by viral packaging motors. It also provides a simple explanation for the fact that each of the steps in the burst cycle advances the DNA by 2.5 base pairs. The scrunchworm hypothesis is consistent with a large body of published data, and it makes four experimentally testable predictions.
Copyright © 2014 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  A-DNA; B-DNA; DNA bacteriophage; Mechanochemistry; Molecular motors; Viral genome packaging

Mesh:

Substances:

Year:  2014        PMID: 25486612      PMCID: PMC4357361          DOI: 10.1016/j.jsb.2014.11.012

Source DB:  PubMed          Journal:  J Struct Biol        ISSN: 1047-8477            Impact factor:   2.867


  56 in total

1.  Sequence-dependent B<-->A transition in DNA evaluated with dimeric and trimeric scales.

Authors:  M Y Tolstorukov; V I Ivanov; G G Malenkov; R L Jernigan; V B Zhurkin
Journal:  Biophys J       Date:  2001-12       Impact factor: 4.033

2.  Detailed architecture of a DNA translocating machine: the high-resolution structure of the bacteriophage phi29 connector particle.

Authors:  Alicia Guasch; Joan Pous; Borja Ibarra; F Xavier Gomis-Rüth; José María Valpuesta; Natalia Sousa; José L Carrascosa; Miquel Coll
Journal:  J Mol Biol       Date:  2002-01-25       Impact factor: 5.469

3.  Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation.

Authors:  Erika J Mancini; Denis E Kainov; Jonathan M Grimes; Roman Tuma; Dennis H Bamford; David I Stuart
Journal:  Cell       Date:  2004-09-17       Impact factor: 41.582

4.  The conformation of double-stranded DNA inside bacteriophages depends on capsid size and shape.

Authors:  Anton S Petrov; Mustafa Burak Boz; Stephen C Harvey
Journal:  J Struct Biol       Date:  2007-08-29       Impact factor: 2.867

5.  Condensation prevails over B-A transition in the structure of DNA at low humidity.

Authors:  Silvia Hormeño; Fernando Moreno-Herrero; Borja Ibarra; José L Carrascosa; José M Valpuesta; J Ricardo Arias-Gonzalez
Journal:  Biophys J       Date:  2011-04-20       Impact factor: 4.033

Review 6.  The DNA-packaging nanomotor of tailed bacteriophages.

Authors:  Sherwood R Casjens
Journal:  Nat Rev Microbiol       Date:  2011-08-12       Impact factor: 60.633

7.  High degree of coordination and division of labor among subunits in a homomeric ring ATPase.

Authors:  Gheorghe Chistol; Shixin Liu; Craig L Hetherington; Jeffrey R Moffitt; Shelley Grimes; Paul J Jardine; Carlos Bustamante
Journal:  Cell       Date:  2012-11-21       Impact factor: 41.582

8.  The hexameric helicase DnaB adopts a nonplanar conformation during translocation.

Authors:  Ornchuma Itsathitphaisarn; Richard A Wing; William K Eliason; Jimin Wang; Thomas A Steitz
Journal:  Cell       Date:  2012-09-27       Impact factor: 41.582

9.  A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills.

Authors:  Shixin Liu; Gheorghe Chistol; Craig L Hetherington; Sara Tafoya; K Aathavan; Joerg Schnitzbauer; Shelley Grimes; Paul J Jardine; Carlos Bustamante
Journal:  Cell       Date:  2014-04-24       Impact factor: 41.582

10.  Three-dimensional structure of a viral genome-delivery portal vertex.

Authors:  Adam S Olia; Peter E Prevelige; John E Johnson; Gino Cingolani
Journal:  Nat Struct Mol Biol       Date:  2011-04-17       Impact factor: 15.369

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  26 in total

Review 1.  Biological Nanomotors with a Revolution, Linear, or Rotation Motion Mechanism.

Authors:  Peixuan Guo; Hiroyuki Noji; Christopher M Yengo; Zhengyi Zhao; Ian Grainge
Journal:  Microbiol Mol Biol Rev       Date:  2016-01-27       Impact factor: 11.056

Review 2.  Old, new, and widely true: The bacteriophage T4 DNA packaging mechanism.

Authors:  Lindsay W Black
Journal:  Virology       Date:  2015-02-27       Impact factor: 3.616

3.  May the Road Rise to Meet You: DNA Deformation May Drive DNA Translocation.

Authors:  Paul J Jardine
Journal:  Biophys J       Date:  2019-05-02       Impact factor: 4.033

4.  Phage-like packing structures with mean field sequence dependence.

Authors:  Christopher G Myers; B Montgomery Pettitt
Journal:  J Comput Chem       Date:  2017-03-27       Impact factor: 3.376

5.  Forces from the Portal Govern the Late-Stage DNA Transport in a Viral DNA Packaging Nanomotor.

Authors:  Peng Jing; Benjamin Burris; Rong Zhang
Journal:  Biophys J       Date:  2016-07-12       Impact factor: 4.033

6.  DNA Conformational Changes Play a Force-Generating Role during Bacteriophage Genome Packaging.

Authors:  Kim A Sharp; Xiang-Jun Lu; Gino Cingolani; Stephen C Harvey
Journal:  Biophys J       Date:  2019-04-30       Impact factor: 4.033

Review 7.  Mechanisms of DNA Packaging by Large Double-Stranded DNA Viruses.

Authors:  Venigalla B Rao; Michael Feiss
Journal:  Annu Rev Virol       Date:  2015-09-10       Impact factor: 10.431

8.  Walker-A Motif Acts to Coordinate ATP Hydrolysis with Motor Output in Viral DNA Packaging.

Authors:  Damian delToro; David Ortiz; Mariam Ordyan; Jean Sippy; Choon-Seok Oh; Nicholas Keller; Michael Feiss; Carlos E Catalano; Douglas E Smith
Journal:  J Mol Biol       Date:  2016-04-30       Impact factor: 5.469

9.  Transitions of Double-Stranded DNA Between the A- and B-Forms.

Authors:  James T Waters; Xiang-Jun Lu; Rodrigo Galindo-Murillo; James C Gumbart; Harold D Kim; Thomas E Cheatham; Stephen C Harvey
Journal:  J Phys Chem B       Date:  2016-05-11       Impact factor: 2.991

10.  Functional Dissection of a Viral DNA Packaging Machine's Walker B Motif.

Authors:  Damian delToro; David Ortiz; Mariam Ordyan; Joshua Pajak; Jean Sippy; Alexis Catala; Choon-Seok Oh; Amber Vu; Gaurav Arya; Douglas E Smith; Carlos E Catalano; Michael Feiss
Journal:  J Mol Biol       Date:  2019-08-30       Impact factor: 5.469

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