Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry

Pan Soonsawad, Lassi Paavolainen, Paula Upla, Wattana Weerachatyanukul, Nina Rintanen, Juan Espinoza, Gregory McNerney, Varpu Marjomäki, R. Holland Cheng

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Cellular uptake of clustered a2b1-integrin induces the formation of membrane compartments that subsequently mature into a multivesicular body (MVB). Enhanced internalization mediated by clustered integrins was observed upon infection by the picornavirus echovirus 1 (EVI). We elucidated the structural features of virus-induced MVBs (vMVBs) in comparison to antibody-induced control MVBs (mock infection) by means of high-pressure cryo fixation of cells followed by immuno electron tomography during early entry of the virus. Three-dimensional tomograms revealed a marked increase in the size and complexity of these vMVBs and the intraluminal vesicles (ILVs) at 2 and 3.5 hours post infection (p.i.), in contrast to the control MVBs without virus. Breakages in the membranes of vMVBs were detected from tomograms after 2 and especially after 3.5 h suggesting that these breakages could facilitate the genome release to the cytoplasm. The in situ neutral-red labeling of viral genome showed that virus uncoating starts as early as 30 min p.i., while an increase of permeability was detected in the vMVBs between 1 and 3 hours p.i., based on a confocal microscopy assay. Altogether, the data show marked morphological changes in size and permeability of the endosomes in the infectious entry pathway of this non-enveloped enterovirus and suggest that the formed breakages facilitate the transfer of the genome to the cytoplasm for replication.

Original languageEnglish (US)
Article numbere108948
JournalPLoS One
Volume9
Issue number10
DOIs
StatePublished - Oct 9 2014

Fingerprint

Picornaviridae
integrins
Viruses
Integrins
Permeability
permeability
viruses
Infection
Picornaviridae Infections
infection
Echovirus Infections
Genes
Virus Uncoating
Cytoplasm
Electron Microscope Tomography
Genome
Multivesicular Bodies
Neutral Red
genome
Virus Internalization

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Soonsawad, P., Paavolainen, L., Upla, P., Weerachatyanukul, W., Rintanen, N., Espinoza, J., ... Cheng, R. H. (2014). Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry. PLoS One, 9(10), [e108948]. https://doi.org/10.1371/journal.pone.0108948

Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry. / Soonsawad, Pan; Paavolainen, Lassi; Upla, Paula; Weerachatyanukul, Wattana; Rintanen, Nina; Espinoza, Juan; McNerney, Gregory; Marjomäki, Varpu; Cheng, R. Holland.

In: PLoS One, Vol. 9, No. 10, e108948, 09.10.2014.

Research output: Contribution to journalArticle

Soonsawad, P, Paavolainen, L, Upla, P, Weerachatyanukul, W, Rintanen, N, Espinoza, J, McNerney, G, Marjomäki, V & Cheng, RH 2014, 'Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry', PLoS One, vol. 9, no. 10, e108948. https://doi.org/10.1371/journal.pone.0108948
Soonsawad P, Paavolainen L, Upla P, Weerachatyanukul W, Rintanen N, Espinoza J et al. Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry. PLoS One. 2014 Oct 9;9(10). e108948. https://doi.org/10.1371/journal.pone.0108948
Soonsawad, Pan ; Paavolainen, Lassi ; Upla, Paula ; Weerachatyanukul, Wattana ; Rintanen, Nina ; Espinoza, Juan ; McNerney, Gregory ; Marjomäki, Varpu ; Cheng, R. Holland. / Permeability changes of integrin-containing multivesicular structures triggered by picornavirus entry. In: PLoS One. 2014 ; Vol. 9, No. 10.
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