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      Herpes Simplex Virus Type 1 Infection Facilitates Invasion of Staphylococcus aureus into the Nasal Mucosa and Nasal Polyp Tissue

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          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.

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          Most cited references47

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          Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus

          Rhinoviruses are the major trigger of acute asthma exacerbations and asthmatic subjects are more susceptible to these infections. To investigate the underlying mechanisms of this increased susceptibility, we examined virus replication and innate responses to rhinovirus (RV)-16 infection of primary bronchial epithelial cells from asthmatic and healthy control subjects. Viral RNA expression and late virus release into supernatant was increased 50- and 7-fold, respectively in asthmatic cells compared with healthy controls. Virus infection induced late cell lysis in asthmatic cells but not in normal cells. Examination of the early cellular response to infection revealed impairment of virus induced caspase 3/7 activity and of apoptotic responses in the asthmatic cultures. Inhibition of apoptosis in normal cultures resulted in enhanced viral yield, comparable to that seen in infected asthmatic cultures. Examination of early innate immune responses revealed profound impairment of virus-induced interferon-β mRNA expression in asthmatic cultures and they produced >2.5 times less interferon-β protein. In infected asthmatic cells, exogenous interferon-β induced apoptosis and reduced virus replication, demonstrating a causal link between deficient interferon-β, impaired apoptosis and increased virus replication. These data suggest a novel use for type I interferons in the treatment or prevention of virus-induced asthma exacerbations.
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            Role of deficient type III interferon-lambda production in asthma exacerbations.

            Rhinoviruses are the major cause of asthma exacerbations, and asthmatics have increased susceptibility to rhinovirus and risk of invasive bacterial infections. Here we show deficient induction of interferon-lambdas by rhinovirus in asthmatic primary bronchial epithelial cells and alveolar macrophages, which was highly correlated with severity of rhinovirus-induced asthma exacerbation and virus load in experimentally infected human volunteers. Induction by lipopolysaccharide in asthmatic macrophages was also deficient and correlated with exacerbation severity. These results identify previously unknown mechanisms of susceptibility to infection in asthma and suggest new approaches to prevention and/or treatment of asthma exacerbations.
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              Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States.

              Herpes simplex virus type 1 (HSV-1) and type 2 are common infections worldwide. Herpes simplex virus type 2 (HSV-2) is the cause of most genital herpes and is almost always sexually transmitted. In contrast, HSV-1 is usually transmitted during childhood via nonsexual contacts. Preexisting HSV-1 antibodies can alleviate clinical manifestations of subsequently acquired HSV-2. Furthermore, HSV-1 has become an important cause of genital herpes in some developed countries. To examine trends in HSV-1 and HSV-2 seroprevalence in the United States in 1999-2004 compared with 1988-1994. Cross-sectional, nationally representative surveys (US National Health and Nutrition Examination Surveys [NHANES]), were used to compare national seroprevalence estimates from 1999-2004 with those from 1988-1994, and changes in HSV-1 and HSV-2 seroprevalence since 1976-1980 were reviewed. Persons aged 14 to 49 years were included in these analyses. Seroprevalence of HSV-1 and HSV-2 antibodies based on results from type-specific immunodot assays; diagnosis of genital herpes. The overall age-adjusted HSV-2 seroprevalence was 17.0% (95% confidence interval [CI], 15.8%-18.3%) in 1999-2004 and 21.0% (95% CI, 19.1%-23.1%) in 1988-1994, a relative decrease of 19.0% between the 2 surveys (95% CI, -28.6% to -9.5%; P<.001). Decreases in HSV-2 seroprevalence were especially concentrated in persons aged 14 to 19 years between 1988 and 2004. In adolescents aged 17 to 19 years and young adults, the decreases in HSV-2 seroprevalence were significant even after adjusting for changes in sexual behaviors. Among those infected with HSV-2, the percentage who reported having been diagnosed with genital herpes was statistically different (14.3% in 1999-2004 and 9.9% in 1988-1994; P = .02). Seroprevalence of HSV-1 decreased from 62.0% (95% CI, 59.6%-64.6%) in 1988-1994 to 57.7% (95% CI, 55.9%-59.5%) in 1999-2004, a relative decrease of 6.9% between the 2 surveys (95% CI, -11.6% to -2.3%; P = .006). Among persons infected with HSV-1 but not with HSV-2, a higher percentage reported having been diagnosed with genital herpes in 1999-2004 compared with 1988-1994 (1.8% vs 0.4%, respectively; P<.001). These data show declines in HSV-2 seroprevalence, suggesting that the trajectory of increasing HSV-2 seroprevalence in the United States has been reversed. Seroprevalence of HSV-1 decreased but the incidence of genital herpes caused by HSV-1 may be increasing.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                29 June 2012
                : 7
                : 6
                : e39875
                Affiliations
                [1 ]Upper Airways Research Laboratory, Department of Oto-Rhino-Laryngology, Ghent University Hospital, Ghent, Belgium
                [2 ]Department of Otolaryngology Head and Neck Surgery, Beijing TongRen Hospital, Capital Medical University, Beijing, People’s Republic of China
                [3 ]Laboratory of Virology, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium
                [4 ]Laboratory of Bacteriology Research, Department of Clinical Chemistry, Microbiology and Immunology, Ghent University, Ghent, Belgium
                [5 ]Key Laboratory of Otolaryngology Head and Neck Surgery (Capital Medical University), Ministry of Education, Beijing Institute of Otolaryngology, Beijing, People’s Republic of China
                National Institutes of Health, United States of America
                Author notes

                Conceived and designed the experiments: CB HJN LZ DH. Performed the experiments: XDW NZ SG. Analyzed the data: XDW NZ SG. Contributed reagents/materials/analysis tools: GH MV. Wrote the paper: XDW NZ SG. Gave technical support: OK.

                Article
                PONE-D-12-08136
                10.1371/journal.pone.0039875
                3387208
                22768151
                b02d6d71-c07a-4585-ad8e-c9e311eea9f8
                Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 18 March 2012
                : 28 May 2012
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Microbiology
                Bacterial Pathogens
                Staphylococci
                Medicine
                Infectious Diseases
                Bacterial Diseases
                Staph Infections
                Staphylococcal Infection
                Staphylococcus Aureus
                Viral Diseases
                Herpes Simplex
                Otorhinolaryngology
                Nasal Diseases
                Rhinology

                Uncategorized
                Uncategorized

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