Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium
Rhinovirus causes many types of respiratory illnesses, ranging from minor colds to exacerbations of asthma. Moraxella catarrhalis is an opportunistic pathogen that is increased in abundance during rhinovirus illnesses and asthma exacerbations and is associated with increased severity of illness thro...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2022.1060748/full |
| _version_ | 1797951483282456576 |
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| author | Eishika Dissanayake Rebecca A. Brockman-Schneider Reed M. Stubbendieck Britney A. Helling Zhumin Zhang Yury A. Bochkov Charmaine Kirkham Timothy F. Murphy Carole Ober Cameron R. Currie Cameron R. Currie James E. Gern |
| author_facet | Eishika Dissanayake Rebecca A. Brockman-Schneider Reed M. Stubbendieck Britney A. Helling Zhumin Zhang Yury A. Bochkov Charmaine Kirkham Timothy F. Murphy Carole Ober Cameron R. Currie Cameron R. Currie James E. Gern |
| author_sort | Eishika Dissanayake |
| collection | DOAJ |
| description | Rhinovirus causes many types of respiratory illnesses, ranging from minor colds to exacerbations of asthma. Moraxella catarrhalis is an opportunistic pathogen that is increased in abundance during rhinovirus illnesses and asthma exacerbations and is associated with increased severity of illness through mechanisms that are ill-defined. We used a co-infection model of human airway epithelium differentiated at the air-liquid interface to test the hypothesis that rhinovirus infection promotes M. catarrhalis adhesion and survival on the respiratory epithelium. Initial experiments showed that infection with M. catarrhalis alone did not damage the epithelium or induce cytokine production, but increased trans-epithelial electrical resistance, indicative of increased barrier function. In a co-infection model, infection with the more virulent rhinovirus-A and rhinovirus-C, but not the less virulent rhinovirus-B types, increased cell-associated M. catarrhalis. Immunofluorescent staining demonstrated that M. catarrhalis adhered to rhinovirus-infected ciliated epithelial cells and infected cells being extruded from the epithelium. Rhinovirus induced pronounced changes in gene expression and secretion of inflammatory cytokines. In contrast, M. catarrhalis caused minimal effects and did not enhance RV-induced responses. Our results indicate that rhinovirus-A or C infection increases M. catarrhalis survival and cell association while M. catarrhalis infection alone does not cause cytopathology or epithelial inflammation. Our findings suggest that rhinovirus and M. catarrhalis co-infection could promote epithelial damage and more severe illness by amplifying leukocyte inflammatory responses at the epithelial surface. |
| first_indexed | 2024-04-10T22:31:19Z |
| format | Article |
| id | doaj.art-f8d33749490d4a6caf34ee0a914cf831 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-10T22:31:19Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-f8d33749490d4a6caf34ee0a914cf8312023-01-17T04:57:12ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-01-011210.3389/fcimb.2022.10607481060748Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epitheliumEishika Dissanayake0Rebecca A. Brockman-Schneider1Reed M. Stubbendieck2Britney A. Helling3Zhumin Zhang4Yury A. Bochkov5Charmaine Kirkham6Timothy F. Murphy7Carole Ober8Cameron R. Currie9Cameron R. Currie10James E. Gern11Department of Pediatrics, University of Wisconsin – Madison, Madison, WI, United StatesDepartment of Pediatrics, University of Wisconsin – Madison, Madison, WI, United StatesDepartment of Bacteriology, University of Wisconsin – Madison, Madison, WI, United StatesDepartment of Human Genetics, University of Chicago, Chicago, IL, United StatesDepartment of Biostatistics and Medical Informatics, University of Wisconsin – Madison, Madison, WI, United StatesDepartment of Pediatrics, University of Wisconsin – Madison, Madison, WI, United StatesClinical and Translational Research Center, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, The State University of New York, Buffalo, NY, United StatesClinical and Translational Research Center, Jacobs School of Medicine and Biomedical Sciences, University at Buffalo, The State University of New York, Buffalo, NY, United StatesDepartment of Human Genetics, University of Chicago, Chicago, IL, United StatesDepartment of Bacteriology, University of Wisconsin – Madison, Madison, WI, United StatesMichael G. DeGroote Institute for Infectious Disease Research, David Braley Centre for Antibiotic Discovery, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, ON, CanadaDepartment of Pediatrics, University of Wisconsin – Madison, Madison, WI, United StatesRhinovirus causes many types of respiratory illnesses, ranging from minor colds to exacerbations of asthma. Moraxella catarrhalis is an opportunistic pathogen that is increased in abundance during rhinovirus illnesses and asthma exacerbations and is associated with increased severity of illness through mechanisms that are ill-defined. We used a co-infection model of human airway epithelium differentiated at the air-liquid interface to test the hypothesis that rhinovirus infection promotes M. catarrhalis adhesion and survival on the respiratory epithelium. Initial experiments showed that infection with M. catarrhalis alone did not damage the epithelium or induce cytokine production, but increased trans-epithelial electrical resistance, indicative of increased barrier function. In a co-infection model, infection with the more virulent rhinovirus-A and rhinovirus-C, but not the less virulent rhinovirus-B types, increased cell-associated M. catarrhalis. Immunofluorescent staining demonstrated that M. catarrhalis adhered to rhinovirus-infected ciliated epithelial cells and infected cells being extruded from the epithelium. Rhinovirus induced pronounced changes in gene expression and secretion of inflammatory cytokines. In contrast, M. catarrhalis caused minimal effects and did not enhance RV-induced responses. Our results indicate that rhinovirus-A or C infection increases M. catarrhalis survival and cell association while M. catarrhalis infection alone does not cause cytopathology or epithelial inflammation. Our findings suggest that rhinovirus and M. catarrhalis co-infection could promote epithelial damage and more severe illness by amplifying leukocyte inflammatory responses at the epithelial surface.https://www.frontiersin.org/articles/10.3389/fcimb.2022.1060748/fullMoraxella catarrhalisrhinovirusairway epitheliumco-infectionasthma |
| spellingShingle | Eishika Dissanayake Rebecca A. Brockman-Schneider Reed M. Stubbendieck Britney A. Helling Zhumin Zhang Yury A. Bochkov Charmaine Kirkham Timothy F. Murphy Carole Ober Cameron R. Currie Cameron R. Currie James E. Gern Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium Frontiers in Cellular and Infection Microbiology Moraxella catarrhalis rhinovirus airway epithelium co-infection asthma |
| title | Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium |
| title_full | Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium |
| title_fullStr | Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium |
| title_full_unstemmed | Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium |
| title_short | Rhinovirus increases Moraxella catarrhalis adhesion to the respiratory epithelium |
| title_sort | rhinovirus increases moraxella catarrhalis adhesion to the respiratory epithelium |
| topic | Moraxella catarrhalis rhinovirus airway epithelium co-infection asthma |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2022.1060748/full |
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