Literature DB >> 17675351

A kinetic analysis of DNA ejection from tailed phages revealing the prerequisite activation energy.

Eric Raspaud1, Thomas Forth, Carlos São-José, Paulo Tavares, Marta de Frutos.   

Abstract

All tailed bacteriophages follow the same general scheme of infection: they bind to their specific host receptor and then transfer their genome into the bacterium. DNA translocation is thought to be initiated by the strong pressure due to DNA packing inside the capsid. However, the exact mechanism by which each phage controls its DNA ejection remains unknown. Using light scattering, we analyzed the kinetics of in vitro DNA release from phages SPP1 and lambda (Siphoviridae family) and found a simple exponential decay. The ejection characteristic time was studied as a function of the temperature and found to follow an Arrhenius law, allowing us to determine the activation energy that governs DNA ejection. A value of 25-30 kcal/mol is obtained for SPP1 and lambda, comparable to the one measured in vitro for T5 (Siphoviridae) and in vivo for T7 (Podoviridae). This suggests similar mechanisms of DNA ejection control. In all tailed phages, the opening of the connector-tail channel is needed for DNA release and could constitute the limiting step. The common value of the activation energy likely reflects the existence for all phages of an optimum value, ensuring a compromise between efficient DNA delivery and high stability of the virus.

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Year:  2007        PMID: 17675351      PMCID: PMC2084231          DOI: 10.1529/biophysj.107.111435

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  23 in total

1.  DNA packaging and ejection forces in bacteriophage.

Authors:  J Kindt; S Tzlil; A Ben-Shaul; W M Gelbart
Journal:  Proc Natl Acad Sci U S A       Date:  2001-11-13       Impact factor: 11.205

2.  Osmotic pressure inhibition of DNA ejection from phage.

Authors:  Alex Evilevitch; Laurence Lavelle; Charles M Knobler; Eric Raspaud; William M Gelbart
Journal:  Proc Natl Acad Sci U S A       Date:  2003-07-24       Impact factor: 11.205

3.  Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host.

Authors:  Petr G Leiman; Paul R Chipman; Victor A Kostyuchenko; Vadim V Mesyanzhinov; Michael G Rossmann
Journal:  Cell       Date:  2004-08-20       Impact factor: 41.582

4.  DNA ejection from bacteriophage T5: analysis of the kinetics and energetics.

Authors:  Marta de Frutos; Lucienne Letellier; Eric Raspaud
Journal:  Biophys J       Date:  2004-11-12       Impact factor: 4.033

5.  Real-time imaging of DNA ejection from single phage particles.

Authors:  Stéphanie Mangenot; Marion Hochrein; Joachim Rädler; Lucienne Letellier
Journal:  Curr Biol       Date:  2005-03-08       Impact factor: 10.834

6.  Virus-assisted loading of polymer nanocontainer.

Authors:  Alexandra Graff; Marc Sauer; Patrick Van Gelder; Wolfgang Meier
Journal:  Proc Natl Acad Sci U S A       Date:  2002-03-26       Impact factor: 11.205

Review 7.  First-step-transfer deoxyribonucleic acid of bacteriophage T5.

Authors:  Y T Lanni
Journal:  Bacteriol Rev       Date:  1968-09

8.  Bacteriophage infection: which end of the SP82G genome goes in first?

Authors:  W T McAllister
Journal:  J Virol       Date:  1970-02       Impact factor: 5.103

9.  Bacteriophage T7 DNA ejection into cells is initiated by an enzyme-like mechanism.

Authors:  Priscilla Kemp; Manisha Gupta; Ian J Molineux
Journal:  Mol Microbiol       Date:  2004-08       Impact factor: 3.501

10.  Structure of a viral DNA gatekeeper at 10 A resolution by cryo-electron microscopy.

Authors:  Elena V Orlova; Brent Gowen; Anja Dröge; Asita Stiege; Frank Weise; Rudi Lurz; Marin van Heel; Paulo Tavares
Journal:  EMBO J       Date:  2003-03-17       Impact factor: 11.598

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  11 in total

1.  Is the in vitro ejection of bacteriophage DNA quasistatic? A bulk to single virus study.

Authors:  N Chiaruttini; M de Frutos; E Augarde; P Boulanger; L Letellier; V Viasnoff
Journal:  Biophys J       Date:  2010-07-21       Impact factor: 4.033

2.  Energy landscape for DNA rotation and sliding through a phage portal.

Authors:  Jeremiah Nummela; Ioan Andricioaei
Journal:  Biophys J       Date:  2009-02-18       Impact factor: 4.033

3.  Langevin dynamics simulation of DNA ejection from a phage.

Authors:  J P Mahalik; B Hildebrandt; M Muthukumar
Journal:  J Biol Phys       Date:  2013-04-23       Impact factor: 1.365

Review 4.  Popping the cork: mechanisms of phage genome ejection.

Authors:  Ian J Molineux; Debabrata Panja
Journal:  Nat Rev Microbiol       Date:  2013-02-04       Impact factor: 60.633

5.  Features of membrane receptors in bacterial multiplication process and necessary conditions for phage infection of bacteria.

Authors:  Tamaz Mdzinarashvili; Irina Papukashvili; Nino Shengelia; Mariam Khvedelidze
Journal:  Curr Microbiol       Date:  2014-08-06       Impact factor: 2.188

6.  Time-resolved DNA release from an O-antigen-specific Salmonella bacteriophage with a contractile tail.

Authors:  Nina K Broeker; Yvette Roske; Angelo Valleriani; Mareike S Stephan; Dorothee Andres; Joachim Koetz; Udo Heinemann; Stefanie Barbirz
Journal:  J Biol Chem       Date:  2019-06-12       Impact factor: 5.157

7.  Influence of Internal DNA Pressure on Stability and Infectivity of Phage λ.

Authors:  D W Bauer; A Evilevitch
Journal:  J Mol Biol       Date:  2015-08-05       Impact factor: 5.469

8.  Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB.

Authors:  Catarina Baptista; Mário A Santos; Carlos São-José
Journal:  J Bacteriol       Date:  2008-05-16       Impact factor: 3.490

9.  In Vitro Studies of Lipopolysaccharide-Mediated DNA Release of Podovirus HK620.

Authors:  Nina K Broeker; Franziska Kiele; Sherwood R Casjens; Eddie B Gilcrease; Anja Thalhammer; Joachim Koetz; Stefanie Barbirz
Journal:  Viruses       Date:  2018-05-29       Impact factor: 5.048

Review 10.  Enzymes and Mechanisms Employed by Tailed Bacteriophages to Breach the Bacterial Cell Barriers.

Authors:  Sofia Fernandes; Carlos São-José
Journal:  Viruses       Date:  2018-07-27       Impact factor: 5.048

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