Literature DB >> 24766813

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

Shixin Liu1,2, Gheorghe Chistol1,3, Craig L Hetherington1,2,3, Sara Tafoya1,4, K Aathavan1,4, Joerg Schnitzbauer1,2, Shelley Grimes5, Paul J Jardine5, Carlos Bustamante1,2,3,6,7,8.   

Abstract

Multimeric, ring-shaped molecular motors rely on the coordinated action of their subunits to perform crucial biological functions. During these tasks, motors often change their operation in response to regulatory signals. Here, we investigate a viral packaging machine as it fills the capsid with DNA and encounters increasing internal pressure. We find that the motor rotates the DNA during packaging and that the rotation per base pair increases with filling. This change accompanies a reduction in the motor's step size. We propose that these adjustments preserve motor coordination by allowing one subunit to make periodic, specific, and regulatory contacts with the DNA. At high filling, we also observe the downregulation of the ATP-binding rate and the emergence of long-lived pauses, suggesting a throttling-down mechanism employed by the motor near the completion of packaging. This study illustrates how a biological motor adjusts its operation in response to changing conditions, while remaining highly coordinated.
Copyright © 2014 Elsevier Inc. All rights reserved.

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Year:  2014        PMID: 24766813      PMCID: PMC4003460          DOI: 10.1016/j.cell.2014.02.034

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  42 in total

Review 1.  Reverse engineering a protein: the mechanochemistry of ATP synthase.

Authors:  G Oster; H Wang
Journal:  Biochim Biophys Acta       Date:  2000-05-31

2.  Structural transitions and elasticity from torque measurements on DNA.

Authors:  Zev Bryant; Michael D Stone; Jeff Gore; Steven B Smith; Nicholas R Cozzarelli; Carlos Bustamante
Journal:  Nature       Date:  2003-07-17       Impact factor: 49.962

3.  A single-molecule Hershey-Chase experiment.

Authors:  David Van Valen; David Wu; Yi-Ju Chen; Hannah Tuson; Paul Wiggins; Rob Phillips
Journal:  Curr Biol       Date:  2012-06-21       Impact factor: 10.834

Review 4.  The bacteriophage DNA packaging motor.

Authors:  Venigalla B Rao; Michael Feiss
Journal:  Annu Rev Genet       Date:  2008       Impact factor: 16.830

5.  Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules.

Authors:  S B Smith; Y Cui; C Bustamante
Journal:  Science       Date:  1996-02-09       Impact factor: 47.728

Review 6.  Intersubunit coordination and cooperativity in ring-shaped NTPases.

Authors:  Ryota Iino; Hiroyuki Noji
Journal:  Curr Opin Struct Biol       Date:  2013-02-08       Impact factor: 6.809

7.  Helical repeat of DNA in solution.

Authors:  J C Wang
Journal:  Proc Natl Acad Sci U S A       Date:  1979-01       Impact factor: 11.205

Review 8.  DNA packaging by the double-stranded DNA bacteriophages.

Authors:  W C Earnshaw; S R Casjens
Journal:  Cell       Date:  1980-09       Impact factor: 41.582

9.  Role of the CCA bulge of prohead RNA of bacteriophage ø29 in DNA packaging.

Authors:  Wei Zhao; Marc C Morais; Dwight L Anderson; Paul J Jardine; Shelley Grimes
Journal:  J Mol Biol       Date:  2008-08-29       Impact factor: 5.469

10.  Revolution rather than rotation of AAA+ hexameric phi29 nanomotor for viral dsDNA packaging without coiling.

Authors:  Chad Schwartz; Gian Marco De Donatis; Hui Zhang; Huaming Fang; Peixuan Guo
Journal:  Virology       Date:  2013-06-12       Impact factor: 3.616

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  70 in total

Review 1.  Energy coupling mechanisms of MFS transporters.

Authors:  Xuejun C Zhang; Yan Zhao; Jie Heng; Daohua Jiang
Journal:  Protein Sci       Date:  2015-09-18       Impact factor: 6.725

Review 2.  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 3.  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

4.  Experimental comparison of forces resisting viral DNA packaging and driving DNA ejection.

Authors:  Nicholas Keller; Zachary T Berndsen; Paul J Jardine; Douglas E Smith
Journal:  Phys Rev E       Date:  2017-05-17       Impact factor: 2.529

5.  Continuous allosteric regulation of a viral packaging motor by a sensor that detects the density and conformation of packaged DNA.

Authors:  Zachary T Berndsen; Nicholas Keller; Douglas E Smith
Journal:  Biophys J       Date:  2015-01-20       Impact factor: 4.033

6.  Structure and mechanism of the ATPase that powers viral genome packaging.

Authors:  Brendan J Hilbert; Janelle A Hayes; Nicholas P Stone; Caroline M Duffy; Banumathi Sankaran; Brian A Kelch
Journal:  Proc Natl Acad Sci U S A       Date:  2015-07-06       Impact factor: 11.205

Review 7.  Interplay between the electrostatic membrane potential and conformational changes in membrane proteins.

Authors:  Xuejun C Zhang; Hang Li
Journal:  Protein Sci       Date:  2019-01-10       Impact factor: 6.725

8.  Kinetics of DNA uptake during transformation provide evidence for a translocation ratchet mechanism.

Authors:  Christof Hepp; Berenike Maier
Journal:  Proc Natl Acad Sci U S A       Date:  2016-10-17       Impact factor: 11.205

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

Authors:  Stephen C Harvey
Journal:  J Struct Biol       Date:  2014-12-05       Impact factor: 2.867

Review 10.  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

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