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Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution

Sjouke Van Poucke UGent, John M Nicholls, Hans Nauwynck UGent and Kristien Van Reeth UGent (2010) VIROLOGY JOURNAL. 7.
abstract
Background: Throughout the history of human influenza pandemics, pigs have been considered the most likely "mixing vessel" for reassortment between human and avian influenza viruses (AIVs). However, the replication efficiencies of influenza viruses from various hosts, as well as the expression of sialic acid (Sia) receptor variants in the entire porcine respiratory tract have never been studied in detail. Therefore, we established porcine nasal, tracheal, bronchial and lung explants, which cover the entire porcine respiratory tract with maximal similarity to the in vivo situation. Subsequently, we assessed virus yields of three porcine, two human and six AIVs in these explants. Since our results on virus replication were in disagreement with the previously reported presence of putative avian virus receptors in the trachea, we additionally studied the distribution of sialic acid receptors by means of lectin histochemistry. Human (Sia alpha 2-6Gal) and avian virus receptors (Sia alpha 2-3Gal) were identified with Sambucus Nigra and Maackia amurensis lectins respectively. Results: Compared to swine and human influenza viruses, replication of the AIVs was limited in all cultures but most strikingly in nasal and tracheal explants. Results of virus titrations were confirmed by quantification of infected cells using immunohistochemistry. By lectin histochemistry we found moderate to abundant expression of the human-like virus receptors in all explant systems but minimal binding of the lectins that identify avian-like receptors, especially in the nasal, tracheal and bronchial epithelium. Conclusions: The species barrier that restricts the transmission of influenza viruses from one host to another remains preserved in our porcine respiratory explants. Therefore this system offers a valuable alternative to study virus and/or host properties required for adaptation or reassortment of influenza viruses. Our results indicate that, based on the expression of Sia receptors alone, the pig is unlikely to be a more appropriate mixing vessel for influenza viruses than humans. We conclude that too little is known on the exact mechanism and on predisposing factors for reassortment to assess the true role of the pig in the emergence of novel influenza viruses.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
HUMAN AIRWAY, PIGS, A VIRUSES, BINDING, MAACKIA-AMURENSIS LECTINS, SOUTHEASTERN CHINA, GENETIC REASSORTMENT, TRANSMISSION, INFECTION, MAMMALS
journal title
VIROLOGY JOURNAL
Virol. J.
volume
7
article_number
38
pages
14 pages
Web of Science type
Article
Web of Science id
000275095100001
JCR category
VIROLOGY
JCR impact factor
2.546 (2010)
JCR rank
16/32 (2010)
JCR quartile
3 (2010)
ISSN
1743-422X
DOI
10.1186/1743-422X-7-38
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1185737
handle
http://hdl.handle.net/1854/LU-1185737
date created
2011-03-10 13:53:54
date last changed
2011-03-17 15:29:14
@article{1185737,
  abstract     = {Background: Throughout the history of human influenza pandemics, pigs have been considered the most likely {\textacutedbl}mixing vessel{\textacutedbl} for reassortment between human and avian influenza viruses (AIVs). However, the replication efficiencies of influenza viruses from various hosts, as well as the expression of sialic acid (Sia) receptor variants in the entire porcine respiratory tract have never been studied in detail. Therefore, we established porcine nasal, tracheal, bronchial and lung explants, which cover the entire porcine respiratory tract with maximal similarity to the in vivo situation. Subsequently, we assessed virus yields of three porcine, two human and six AIVs in these explants. Since our results on virus replication were in disagreement with the previously reported presence of putative avian virus receptors in the trachea, we additionally studied the distribution of sialic acid receptors by means of lectin histochemistry. Human (Sia alpha 2-6Gal) and avian virus receptors (Sia alpha 2-3Gal) were identified with Sambucus Nigra and Maackia amurensis lectins respectively.
Results: Compared to swine and human influenza viruses, replication of the AIVs was limited in all cultures but most strikingly in nasal and tracheal explants. Results of virus titrations were confirmed by quantification of infected cells using immunohistochemistry. By lectin histochemistry we found moderate to abundant expression of the human-like virus receptors in all explant systems but minimal binding of the lectins that identify avian-like receptors, especially in the nasal, tracheal and bronchial epithelium. Conclusions: The species barrier that restricts the transmission of influenza viruses from one host to another remains preserved in our porcine respiratory explants. Therefore this system offers a valuable alternative to study virus and/or host properties required for adaptation or reassortment of influenza viruses. Our results indicate that, based on the expression of Sia receptors alone, the pig is unlikely to be a more appropriate mixing vessel for influenza viruses than humans. We conclude that too little is known on the exact mechanism and on predisposing factors for reassortment to assess the true role of the pig in the emergence of novel influenza viruses.},
  articleno    = {38},
  author       = {Van Poucke, Sjouke and Nicholls, John M and Nauwynck, Hans and Van Reeth, Kristien},
  issn         = {1743-422X},
  journal      = {VIROLOGY JOURNAL},
  keyword      = {HUMAN AIRWAY,PIGS,A VIRUSES,BINDING,MAACKIA-AMURENSIS LECTINS,SOUTHEASTERN CHINA,GENETIC REASSORTMENT,TRANSMISSION,INFECTION,MAMMALS},
  language     = {eng},
  pages        = {14},
  title        = {Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution},
  url          = {http://dx.doi.org/10.1186/1743-422X-7-38},
  volume       = {7},
  year         = {2010},
}

Chicago
Van Poucke, Sjouke, John M Nicholls, Hans Nauwynck, and Kristien Van Reeth. 2010. “Replication of Avian, Human and Swine Influenza Viruses in Porcine Respiratory Explants and Association with Sialic Acid Distribution.” Virology Journal 7.
APA
Van Poucke, Sjouke, Nicholls, J. M., Nauwynck, H., & Van Reeth, K. (2010). Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. VIROLOGY JOURNAL, 7.
Vancouver
1.
Van Poucke S, Nicholls JM, Nauwynck H, Van Reeth K. Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. VIROLOGY JOURNAL. 2010;7.
MLA
Van Poucke, Sjouke, John M Nicholls, Hans Nauwynck, et al. “Replication of Avian, Human and Swine Influenza Viruses in Porcine Respiratory Explants and Association with Sialic Acid Distribution.” VIROLOGY JOURNAL 7 (2010): n. pag. Print.