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Herpes simplex virus type 1 infection facilitates invasion of Staphylococcus aureus into the nasal mucosa and nasal polyp tissue

XiangDong Wang, Nan Zhang UGent, SARAH GLORIEUX UGent, Gabriële Holtappels UGent, Mario Vaneechoutte UGent, Olga Krysko UGent, Luo Zhang, DeMin Han, Hans Nauwynck UGent and Claus Bachert UGent (2012) PLOS ONE. 7(6).
abstract
Background: Staphylococcus aureus (S. aureus) plays an important role in the pathogenesis of severe chronic airway disease, such as nasal polyps. However the mechanisms underlying the initiation of damage and/or invasion of the nasal mucosa by S. aureus are not clearly understood. The aim of this study was to investigate the interaction between S. aureus and herpes simplex virus type 1 (HSV1) in the invasion of the nasal mucosa and nasal polyp tissue. Methodology/Principal Findings: Inferior turbinate and nasal polyp samples were cultured and infected with either HSV1 alone, S. aureus alone or a combination of both. Both in turbinate mucosa and nasal polyp tissue, HSV1, with or without S. aureus incubation, led to focal infection of outer epithelial cells within 48 h, and loss or damage of the epithelium and invasion of HSV1 into the lamina propria within 72 h. After pre-infection with HSV1 for 24 h or 48 h, S. aureus was able to pass the basement membrane and invade the mucosa. Epithelial damage scores were significantly higher for HSV1 and S. aureus co-infected explants compared with control explants or S. aureus only-infected explants, and significantly correlated with HSV1-invasion scores. The epithelial damage scores of nasal polyp tissues were significantly higher than those of inferior turbinate tissues upon HSV1 infection. Consequently, invasion scores of HSV1 of nasal polyp tissues were significantly higher than those of inferior turbinate mucosa in the HSV1 and co-infection groups, and invasion scores of S. aureus of nasal polyp tissues were significantly higher than those of inferior turbinate tissues in the co-infection group. Conclusions/Significance: HSV1 may lead to a significant damage of the nasal epithelium and consequently may facilitate invasion of S. aureus into the nasal mucosa. Nasal polyp tissue is more susceptible to the invasion of HSV1 and epithelial damage by HSV1 compared with inferior turbinate mucosa.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
AIRWAY EPITHELIAL-CELLS, HUMAN NASOPHARYNGEAL MUCOSA, ORGAN-CULTURE, ENTEROTOXIN-B, PROTEIN-A, RHINOVIRUS, ASTHMA, MODEL, SEROPREVALENCE, SUPERANTIGENS
journal title
PLOS ONE
PLoS One
volume
7
issue
6
article_number
e39875
pages
10 pages
Web of Science type
Article
Web of Science id
000305892100120
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.73 (2012)
JCR rank
7/56 (2012)
JCR quartile
1 (2012)
ISSN
1932-6203
DOI
10.1371/journal.pone.0039875
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
3000583
handle
http://hdl.handle.net/1854/LU-3000583
date created
2012-09-28 09:48:43
date last changed
2012-10-08 16:51:50
@article{3000583,
  abstract     = {Background: Staphylococcus aureus (S. aureus) plays an important role in the pathogenesis of severe chronic airway disease, such as nasal polyps. However the mechanisms underlying the initiation of damage and/or invasion of the nasal mucosa by S. aureus are not clearly understood. The aim of this study was to investigate the interaction between S. aureus and herpes simplex virus type 1 (HSV1) in the invasion of the nasal mucosa and nasal polyp tissue. 
Methodology/Principal Findings: Inferior turbinate and nasal polyp samples were cultured and infected with either HSV1 alone, S. aureus alone or a combination of both. Both in turbinate mucosa and nasal polyp tissue, HSV1, with or without S. aureus incubation, led to focal infection of outer epithelial cells within 48 h, and loss or damage of the epithelium and invasion of HSV1 into the lamina propria within 72 h. After pre-infection with HSV1 for 24 h or 48 h, S. aureus was able to pass the basement membrane and invade the mucosa. Epithelial damage scores were significantly higher for HSV1 and S. aureus co-infected explants compared with control explants or S. aureus only-infected explants, and significantly correlated with HSV1-invasion scores. The epithelial damage scores of nasal polyp tissues were significantly higher than those of inferior turbinate tissues upon HSV1 infection. Consequently, invasion scores of HSV1 of nasal polyp tissues were significantly higher than those of inferior turbinate mucosa in the HSV1 and co-infection groups, and invasion scores of S. aureus of nasal polyp tissues were significantly higher than those of inferior turbinate tissues in the co-infection group. 
Conclusions/Significance: HSV1 may lead to a significant damage of the nasal epithelium and consequently may facilitate invasion of S. aureus into the nasal mucosa. Nasal polyp tissue is more susceptible to the invasion of HSV1 and epithelial damage by HSV1 compared with inferior turbinate mucosa.},
  articleno    = {e39875},
  author       = {Wang, XiangDong and Zhang, Nan and GLORIEUX, SARAH and Holtappels, Gabri{\"e}le and Vaneechoutte, Mario and Krysko, Olga and Zhang, Luo and Han, DeMin and Nauwynck, Hans and Bachert, Claus},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {AIRWAY EPITHELIAL-CELLS,HUMAN NASOPHARYNGEAL MUCOSA,ORGAN-CULTURE,ENTEROTOXIN-B,PROTEIN-A,RHINOVIRUS,ASTHMA,MODEL,SEROPREVALENCE,SUPERANTIGENS},
  language     = {eng},
  number       = {6},
  pages        = {10},
  title        = {Herpes simplex virus type 1 infection facilitates invasion of Staphylococcus aureus into the nasal mucosa and nasal polyp tissue},
  url          = {http://dx.doi.org/10.1371/journal.pone.0039875},
  volume       = {7},
  year         = {2012},
}

Chicago
Wang, XiangDong, Nan Zhang, Sarah Glorieux, Gabriële Holtappels, Mario Vaneechoutte, Olga Krysko, Luo Zhang, DeMin Han, Hans Nauwynck, and Claus Bachert. 2012. “Herpes Simplex Virus Type 1 Infection Facilitates Invasion of Staphylococcus Aureus into the Nasal Mucosa and Nasal Polyp Tissue.” Plos One 7 (6).
APA
Wang, XiangDong, Zhang, N., Glorieux, S., Holtappels, G., Vaneechoutte, M., Krysko, O., Zhang, L., et al. (2012). Herpes simplex virus type 1 infection facilitates invasion of Staphylococcus aureus into the nasal mucosa and nasal polyp tissue. PLOS ONE, 7(6).
Vancouver
1.
Wang X, Zhang N, Glorieux S, Holtappels G, Vaneechoutte M, Krysko O, et al. Herpes simplex virus type 1 infection facilitates invasion of Staphylococcus aureus into the nasal mucosa and nasal polyp tissue. PLOS ONE. 2012;7(6).
MLA
Wang, XiangDong, Nan Zhang, Sarah Glorieux, et al. “Herpes Simplex Virus Type 1 Infection Facilitates Invasion of Staphylococcus Aureus into the Nasal Mucosa and Nasal Polyp Tissue.” PLOS ONE 7.6 (2012): n. pag. Print.