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A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus

Xiaoyun Yang, Lennert Steukers, Katrien Forier UGent, Ranhua Xiong UGent, Kevin Braeckmans UGent, Kristien Van Reeth UGent and Hans Nauwynck UGent (2014) PLOS ONE. 9(10).
abstract
Swine influenza virus (SIV) has a strong tropism for pig respiratory mucosa, which consists of a mucus layer, epithelium, basement membrane and lamina propria. Sialic acids present on the epithelial surface have long been considered to be determinants of influenza virus tropism. However, mucus which is also rich in sialic acids may serve as the first barrier of selection. It was investigated how influenza virus interacts with the mucus to infect epithelial cells. Two techniques were applied to track SIV H1N1 in porcine mucus. The microscopic diffusion of SIV particles in the mucus was analyzed by single particle tracking (SPT), and the macroscopic penetration of SIV through mucus was studied by a virus in-capsule-mucus penetration system, followed by visualizing the translocation of the virions with time by immunofluorescence staining. Furthermore, the effects of neuraminidase on SIV getting through or binding to the mucus were studied by using zanamivir, a neuraminidase inhibitor (NAI), and Arthrobacter ureafaciens neuraminidase. The distribution of the diffusion coefficient shows that 70% of SIV particles were entrapped, while the rest diffused freely in the mucus. Additionally, SIV penetrated the porcine mucus with time, reaching a depth of 65 mm at 30 min post virus addition, 2 fold of that at 2 min. Both the microscopic diffusion and macroscopic penetration were largely diminished by NAI, while were clearly increased by the effect of exogenous neuraminidase. Moreover, the exogenous neuraminidase sufficiently prevented the binding of SIV to mucus which was reversely enhanced by effect of NAI. These findings clearly show that the neuraminidase helps SIV move through the mucus, which is important for the virus to reach and infect epithelial cells and eventually become shed into the lumen of the respiratory tract.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
SURFACTANT PROTEIN-D, SINGLE-PARTICLE TRACKING, INFECTION, SIALIC ACIDS, VIRAL PROTEIN, PROTECTIVE ROLE, AIRWAY EPITHELIUM, A VIRUSES, RECEPTOR SPECIFICITY, SUBSTRATE-SPECIFICITY
journal title
PLOS ONE
PLoS One
volume
9
issue
10
article number
e110026
pages
11 pages
Web of Science type
Article
Web of Science id
000346766200079
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.234 (2014)
JCR rank
9/57 (2014)
JCR quartile
1 (2014)
ISSN
1932-6203
DOI
10.1371/journal.pone.0110026
project
Center for nano- and biophotonics (NB-Photonics)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
5816381
handle
http://hdl.handle.net/1854/LU-5816381
date created
2015-01-23 15:18:59
date last changed
2016-12-21 15:42:49
@article{5816381,
  abstract     = {Swine influenza virus (SIV) has a strong tropism for pig respiratory mucosa, which consists of a mucus layer, epithelium, basement membrane and lamina propria. Sialic acids present on the epithelial surface have long been considered to be determinants of influenza virus tropism. However, mucus which is also rich in sialic acids may serve as the first barrier of selection. It was investigated how influenza virus interacts with the mucus to infect epithelial cells. Two techniques were applied to track SIV H1N1 in porcine mucus. The microscopic diffusion of SIV particles in the mucus was analyzed by single particle tracking (SPT), and the macroscopic penetration of SIV through mucus was studied by a virus in-capsule-mucus penetration system, followed by visualizing the translocation of the virions with time by immunofluorescence staining. Furthermore, the effects of neuraminidase on SIV getting through or binding to the mucus were studied by using zanamivir, a neuraminidase inhibitor (NAI), and Arthrobacter ureafaciens neuraminidase. The distribution of the diffusion coefficient shows that 70\% of SIV particles were entrapped, while the rest diffused freely in the mucus. Additionally, SIV penetrated the porcine mucus with time, reaching a depth of 65 mm at 30 min post virus addition, 2 fold of that at 2 min. Both the microscopic diffusion and macroscopic penetration were largely diminished by NAI, while were clearly increased by the effect of exogenous neuraminidase. Moreover, the exogenous neuraminidase sufficiently prevented the binding of SIV to mucus which was reversely enhanced by effect of NAI. These findings clearly show that the neuraminidase helps SIV move through the mucus, which is important for the virus to reach and infect epithelial cells and eventually become shed into the lumen of the respiratory tract.},
  articleno    = {e110026},
  author       = {Yang, Xiaoyun and Steukers, Lennert and Forier, Katrien and Xiong, Ranhua and Braeckmans, Kevin and Van Reeth, Kristien and Nauwynck, Hans},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {SURFACTANT PROTEIN-D,SINGLE-PARTICLE TRACKING,INFECTION,SIALIC ACIDS,VIRAL PROTEIN,PROTECTIVE ROLE,AIRWAY EPITHELIUM,A VIRUSES,RECEPTOR SPECIFICITY,SUBSTRATE-SPECIFICITY},
  language     = {eng},
  number       = {10},
  pages        = {11},
  title        = {A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus},
  url          = {http://dx.doi.org/10.1371/journal.pone.0110026},
  volume       = {9},
  year         = {2014},
}

Chicago
Yang, Xiaoyun, Lennert Steukers, Katrien Forier, Ranhua Xiong, Kevin Braeckmans, Kristien Van Reeth, and Hans Nauwynck. 2014. “A Beneficiary Role for Neuraminidase in Influenza Virus Penetration Through the Respiratory Mucus.” Plos One 9 (10).
APA
Yang, Xiaoyun, Steukers, L., Forier, K., Xiong, R., Braeckmans, K., Van Reeth, K., & Nauwynck, H. (2014). A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus. PLOS ONE, 9(10).
Vancouver
1.
Yang X, Steukers L, Forier K, Xiong R, Braeckmans K, Van Reeth K, et al. A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus. PLOS ONE. 2014;9(10).
MLA
Yang, Xiaoyun, Lennert Steukers, Katrien Forier, et al. “A Beneficiary Role for Neuraminidase in Influenza Virus Penetration Through the Respiratory Mucus.” PLOS ONE 9.10 (2014): n. pag. Print.