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Solid-to-fluid-like DNA transition in viruses facilitates infection.

Liu, Ting; Sae-Ueng, Udom; Li, Dong; Lander, Gabriel C; Zuo, Xiaobing; Jönsson, Bengt LU ; Rau, Donald; Shefer, Ivetta and Evilevitch, Alex LU (2014) In Proceedings of the National Academy of Sciences 111(41). p.14675-14680
Abstract
Releasing the packaged viral DNA into the host cell is an essential process to initiate viral infection. In many double-stranded DNA bacterial viruses and herpesviruses, the tightly packaged genome is hexagonally ordered and stressed in the protein shell, called the capsid. DNA condensed in this state inside viral capsids has been shown to be trapped in a glassy state, with restricted molecular motion in vitro. This limited intracapsid DNA mobility is caused by the sliding friction between closely packaged DNA strands, as a result of the repulsive interactions between the negative charges on the DNA helices. It had been unclear how this rigid crystalline structure of the viral genome rapidly ejects from the capsid, reaching rates of 60,000... (More)
Releasing the packaged viral DNA into the host cell is an essential process to initiate viral infection. In many double-stranded DNA bacterial viruses and herpesviruses, the tightly packaged genome is hexagonally ordered and stressed in the protein shell, called the capsid. DNA condensed in this state inside viral capsids has been shown to be trapped in a glassy state, with restricted molecular motion in vitro. This limited intracapsid DNA mobility is caused by the sliding friction between closely packaged DNA strands, as a result of the repulsive interactions between the negative charges on the DNA helices. It had been unclear how this rigid crystalline structure of the viral genome rapidly ejects from the capsid, reaching rates of 60,000 bp/s. Through a combination of single-molecule and bulk techniques, we determined how the structure and energy of the encapsidated DNA in phage λ regulates the mobility required for its ejection. Our data show that packaged λ-DNA undergoes a solid-to-fluid-like disordering transition as a function of temperature, resulting locally in less densely packed DNA, reducing DNA-DNA repulsions. This process leads to a significant increase in genome mobility or fluidity, which facilitates genome release at temperatures close to that of viral infection (37 °C), suggesting a remarkable physical adaptation of bacterial viruses to the environment of Escherichia coli cells in a human host. (Less)
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author
organization
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type
Contribution to journal
publication status
published
subject
in
Proceedings of the National Academy of Sciences
volume
111
issue
41
pages
14675 - 14680
publisher
National Acad Sciences
external identifiers
  • pmid:25271319
  • wos:000342922000028
  • scopus:84907942361
ISSN
1091-6490
DOI
10.1073/pnas.1321637111
language
English
LU publication?
yes
id
b1851417-f3a0-431e-b9f5-e64919333961 (old id 4738615)
date added to LUP
2014-11-17 11:32:40
date last changed
2017-01-01 04:12:45
@article{b1851417-f3a0-431e-b9f5-e64919333961,
  abstract     = {Releasing the packaged viral DNA into the host cell is an essential process to initiate viral infection. In many double-stranded DNA bacterial viruses and herpesviruses, the tightly packaged genome is hexagonally ordered and stressed in the protein shell, called the capsid. DNA condensed in this state inside viral capsids has been shown to be trapped in a glassy state, with restricted molecular motion in vitro. This limited intracapsid DNA mobility is caused by the sliding friction between closely packaged DNA strands, as a result of the repulsive interactions between the negative charges on the DNA helices. It had been unclear how this rigid crystalline structure of the viral genome rapidly ejects from the capsid, reaching rates of 60,000 bp/s. Through a combination of single-molecule and bulk techniques, we determined how the structure and energy of the encapsidated DNA in phage λ regulates the mobility required for its ejection. Our data show that packaged λ-DNA undergoes a solid-to-fluid-like disordering transition as a function of temperature, resulting locally in less densely packed DNA, reducing DNA-DNA repulsions. This process leads to a significant increase in genome mobility or fluidity, which facilitates genome release at temperatures close to that of viral infection (37 °C), suggesting a remarkable physical adaptation of bacterial viruses to the environment of Escherichia coli cells in a human host.},
  author       = {Liu, Ting and Sae-Ueng, Udom and Li, Dong and Lander, Gabriel C and Zuo, Xiaobing and Jönsson, Bengt and Rau, Donald and Shefer, Ivetta and Evilevitch, Alex},
  issn         = {1091-6490},
  language     = {eng},
  number       = {41},
  pages        = {14675--14680},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences},
  title        = {Solid-to-fluid-like DNA transition in viruses facilitates infection.},
  url          = {http://dx.doi.org/10.1073/pnas.1321637111},
  volume       = {111},
  year         = {2014},
}