Growth and characterization of different human rhinovirus C types in three-dimensional human airway epithelia reconstituted in vitro

Tapparel, Caroline; Sobo, Komla; Constant, Samuel; Huang, Song; Belle, Sandra Van; Kaiser, Laurent

doi:10.1016/j.virol.2013.06.031

Cited by 63 publications

(64 citation statements)

References 45 publications

(60 reference statements)

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“…The recently discovered HRV-C clade [73], [74] is often associated with severe symptoms and asthma attacks [17]. Although the receptor for HRV-C is as of yet unidentified, the results of this study and our previous study on the Rac/TLR3/IFN axis [40] suggest several testable hypotheses.…”

Section: Discussionmentioning

confidence: 62%

Major and Minor Group Rhinoviruses Elicit Differential Signaling and Cytokine Responses as a Function of Receptor-Mediated Signal Transduction

Schuler

Schreiber

et al. 2014

PLoS ONE

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Major- and minor-group human rhinoviruses (HRV) enter their host by binding to the cell surface molecules ICAM-1 and LDL-R, respectively, which are present on both macrophages and epithelial cells. Although epithelial cells are the primary site of productive HRV infection, previous studies have implicated macrophages in establishing the cytokine dysregulation that occurs during rhinovirus-induced asthma exacerbations. Analysis of the transcriptome of primary human macrophages exposed to major- and minor-group HRV demonstrated differential gene expression. Alterations in gene expression were traced to differential mitochondrial activity and signaling pathway activation between two rhinovirus serotypes, HRV16 (major-group) and HRV1A (minor-group), upon initial HRV binding. Variances in phosphorylation of kinases (p38, JNK, ERK5) and transcription factors (ATF-2, CREB, CEBP-alpha) were observed between the major- and minor-group HRV treatments. Differential activation of signaling pathways led to changes in the production of the asthma-relevant cytokines CCL20, CCL2, and IL-10. This is the first report of genetically similar viruses eliciting dissimilar cytokine release, transcription factor phosphorylation, and MAPK activation from macrophages, suggesting that receptor use is a mechanism for establishing the inflammatory microenvironment in the human airway upon exposure to rhinovirus.

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Section: Discussionmentioning

confidence: 62%

Major and Minor Group Rhinoviruses Elicit Differential Signaling and Cytokine Responses as a Function of Receptor-Mediated Signal Transduction

Schuler

Schreiber

et al. 2014

PLoS ONE

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“…Mounting evidence supports the view that RV can replicate in the airways of the lung in some cases, including demonstration of RV in lung biopsies of experimentally infected subjects and in patients with asthma (30-32). Explanations to support the idea that rhinoviruses can replicate in lung airways have included the observation that temperatures in the large airways of the lung may reach temperatures in the permissive range for RV infection and the finding that RV strains vary in the extent to which they exhibit temperature dependence (33)(34)(35)(36)). An additional possibility is that restriction factors responsible for diminished viral replication at body temperature are not intrinsic to the biology of the virus but also reflect the biology of the host and therefore may vary from host to host.…”

Section: Discussionmentioning

confidence: 99%

Temperature-dependent innate defense against the common cold virus limits viral replication at warm temperature in mouse airway cells

Foxman

Storer²,

Fitzgerald

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

218

208

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Most isolates of human rhinovirus, the common cold virus, replicate more robustly at the cool temperatures found in the nasal cavity (33-35°C) than at core body temperature (37°C). To gain insight into the mechanism of temperature-dependent growth, we compared the transcriptional response of primary mouse airway epithelial cells infected with rhinovirus at 33°C vs. 37°C. Mouse airway cells infected with mouse-adapted rhinovirus 1B exhibited a striking enrichment in expression of antiviral defense response genes at 37°C relative to 33°C, which correlated with significantly higher expression levels of type I and type III IFN genes and IFNstimulated genes (ISGs) at 37°C. Temperature-dependent IFN induction in response to rhinovirus was dependent on the MAVS protein, a key signaling adaptor of the RIG-I-like receptors (RLRs). Stimulation of primary airway cells with the synthetic RLR ligand poly I:C led to greater IFN induction at 37°C relative to 33°C at early time points poststimulation and to a sustained increase in the induction of ISGs at 37°C relative to 33°C. Recombinant type I IFN also stimulated more robust induction of ISGs at 37°C than at 33°C. Genetic deficiency of MAVS or the type I IFN receptor in infected airway cells permitted higher levels of viral replication, particularly at 37°C, and partially rescued the temperature-dependent growth phenotype. These findings demonstrate that in mouse airway cells, rhinovirus replicates preferentially at nasal cavity temperature due, in part, to a less efficient antiviral defense response of infected cells at cool temperature.is the most frequent cause of the common cold and has recently been recognized as the most frequent cause of exacerbations of asthma, a disease affecting ∼10% of the US population (1, 2). RV is also increasingly recognized to be a major cause of lung symptoms in patients with other chronic respiratory diseases and in young children (3). Previously, RV was thought to cause disease primarily in the nasal cavity, consistent with the observation that most RV strains replicate more robustly at the cooler temperatures found in the nasal cavity (33-35°C) than at lung temperature (37°C) (4, 5). However, the recent recognition that RV is an important cause of disease in the lung (2, 3) compels further investigation of the mechanisms that control the optimal replication temperature of this virus, which are unknown.Previous studies of the replication machinery of RV have not identified a virus-intrinsic reason for temperature-dependent growth, including studies of cell entry, uncoating, and polymerase activity (6, 7). Therefore, we considered the possibility that other factors, such as temperature-dependent host antiviral responses, might contribute to this phenotype. To investigate this possibility, we examined the effect of incubation temperature on the response to RV infection by the infected host cell. Using a mouse primary airway cell infection model, we observed that incubating cells at the lower temperature of the nasal cavity (33°C) greatly dim...

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“…Rhinovirus (RV) A16 and B14 were purchased from American Type Culture Collection (Manassas, USA), while Rhinovirus C15, EV-D68, HCoV-OC43, influenza A(H1N1) and influenza A(H3N2) were isolated directly on MucilAir™ from clinical specimen as previously described (Essaidi-Laziosi et al, 2017;Tapparel et al, 2013). Influenza lineage was determined by PCR, hemagglutination inhibition assay and partial sequencing for A/Switzerland/7717739/2013(H1N1), which is very close to the reference strain A/California/07/09 and for A/Switzerland/8004462/2013(H3N2).…”

Section: Viruses and Inoculationmentioning

confidence: 99%

Antiviral drug screening by assessing epithelial functions and innate immune responses in human 3D airway epithelium model

et al. 2018

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Respiratory viral infections cause mild to severe diseases, such as common cold, bronchiolitis and pneumonia and are associated with substantial burden for society. To test new molecules for shortening, alleviating the diseases or to develop new therapies, relevant human in vitro models are mandatory. MucilAir™, a human standardized air-liquid interface 3D airway epithelial culture holds in vitro specific mechanisms to counter invaders comparable to the in vivo situation, such as mucus production, mucociliary clearance, and secretion of defensive molecules. The objective of this study was to test the relevance of such a model for the discovery and validation of antiviral drugs. Fully differentiated 3D nasal epithelium cultures were inoculated with picornaviruses, a coronavirus and influenza A viruses in the absence or in the presence of reference antiviral drugs. Results showed that, rupintrivir efficiently inhibits the replication of respiratory picornaviruses in a dose dependent manner and prevents the impairment of the mucociliary clearance. Similarly, oseltamivir reduced the replication of influenza A viruses in a dose dependent manner and prevented the impairment of the epithelial barrier function and cytotoxicity until 4 days of infection. In addition we found that Rhinovirus B14, C15 and influenza A(H1N1) induce significant increase of β Defensins 2 and Cathelicidin release with different time course. These results reveal that a large panel of epithelial functions is modified upon viral infection and validate MucilAir™ as a pertinent tool for pre-clinical antiviral drug testing.

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Growth and characterization of different human rhinovirus C types in three-dimensional human airway epithelia reconstituted in vitro

Cited by 63 publications

References 45 publications

Major and Minor Group Rhinoviruses Elicit Differential Signaling and Cytokine Responses as a Function of Receptor-Mediated Signal Transduction

Major and Minor Group Rhinoviruses Elicit Differential Signaling and Cytokine Responses as a Function of Receptor-Mediated Signal Transduction

Temperature-dependent innate defense against the common cold virus limits viral replication at warm temperature in mouse airway cells

Antiviral drug screening by assessing epithelial functions and innate immune responses in human 3D airway epithelium model

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