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Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding.
Mol Immunol. 2015 May; 65(1):1-16.MI

Abstract

The continued threat of worldwide influenza pandemics, together with the yearly emergence of antigenically drifted influenza A virus (IAV) strains, underscore the urgent need to elucidate not only the mechanisms of influenza virulence, but also those mechanisms that predispose influenza patients to increased susceptibility to subsequent infection with Streptococcus pneumoniae. Glycans displayed on the surface of epithelia that are exposed to the external environment play important roles in microbial recognition, adhesion, and invasion. It is well established that the IAV hemagglutinin and pneumococcal adhesins enable their attachment to the host epithelia. Reciprocally, the recognition of microbial glycans by host carbohydrate-binding proteins (lectins) can initiate innate immune responses, but their relevance in influenza or pneumococcal infections is poorly understood. Galectins are evolutionarily conserved lectins characterized by affinity for β-galactosides and a unique sequence motif, with critical regulatory roles in development and immune homeostasis. In this study, we examined the possibility that galectins expressed in the airway epithelial cells might play a significant role in viral or pneumococcal adhesion to airway epithelial cells. Our results in a mouse model for influenza and pneumococcal infection revealed that the murine lung expresses a diverse galectin repertoire, from which selected galectins, including galectin 1 (Gal1) and galectin 3 (Gal3), are released to the bronchoalveolar space. Further, the results showed that influenza and subsequent S. pneumoniae infections significantly alter the glycosylation patterns of the airway epithelial surface and modulate galectin expression. In vitro studies on the human airway epithelial cell line A549 were consistent with the observations made in the mouse model, and further revealed that both Gal1 and Gal3 bind strongly to IAV and S. pneumoniae, and that exposure of the cells to viral neuraminidase or influenza infection increased galectin-mediated S. pneumoniae adhesion to the cell surface. Our results suggest that upon influenza infection, pneumococcal adhesion to the airway epithelial surface is enhanced by an interplay among the host galectins and viral and pneumococcal neuraminidases. The observed enhancement of pneumococcal adhesion may be a contributing factor to the observed hypersusceptibility to pneumonia of influenza patients.

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Authors+Show Affiliations

Nita-Lazar M
Department of Microbiology and Immunology, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA; Institute of Marine and Environmental Technology, Columbus Center, 701 East Pratt Street, Baltimore, MD 21202, USA.
Banerjee A
Department of Microbiology and Immunology, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA; Institute of Marine and Environmental Technology, Columbus Center, 701 East Pratt Street, Baltimore, MD 21202, USA.
Feng C
Department of Microbiology and Immunology, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA; Institute of Marine and Environmental Technology, Columbus Center, 701 East Pratt Street, Baltimore, MD 21202, USA.
Amin MN
Institute of Human Virology and Department of Biochemistry & Molecular Biology, University of Maryland School of Medicine, 725 West Lombard Street, Baltimore, MD 21201, USA.
Frieman MB
Department of Microbiology and Immunology, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA.
Chen WH
Center for Vaccine Development, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA.
Cross AS
Center for Vaccine Development, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA.
Wang LX
Institute of Human Virology and Department of Biochemistry & Molecular Biology, University of Maryland School of Medicine, 725 West Lombard Street, Baltimore, MD 21201, USA.
Vasta GR
Department of Microbiology and Immunology, University of Maryland School of Medicine, 685 West Baltimore Street, Baltimore, MD 21201, USA; Institute of Marine and Environmental Technology, Columbus Center, 701 East Pratt Street, Baltimore, MD 21202, USA. Electronic address: GVasta@som.umaryland.edu.

MeSH

Adhesins, BacterialAnimalsApoptosisBacterial AdhesionCell LineDisease SusceptibilityEpithelial CellsGalectin 1Galectin 3Hemagglutinin Glycoproteins, Influenza VirusHumansInfluenza A virusMiceMice, Inbred C57BLNeuraminidaseOrthomyxoviridae InfectionsPneumococcal InfectionsProtein BindingRespiratory MucosaStreptococcus pneumoniae

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

25597246

Citation

Nita-Lazar, Mihai, et al. "Desialylation of Airway Epithelial Cells During Influenza Virus Infection Enhances Pneumococcal Adhesion Via Galectin Binding." Molecular Immunology, vol. 65, no. 1, 2015, pp. 1-16.
Nita-Lazar M, Banerjee A, Feng C, et al. Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. Mol Immunol. 2015;65(1):1-16.
Nita-Lazar, M., Banerjee, A., Feng, C., Amin, M. N., Frieman, M. B., Chen, W. H., Cross, A. S., Wang, L. X., & Vasta, G. R. (2015). Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. Molecular Immunology, 65(1), 1-16. https://doi.org/10.1016/j.molimm.2014.12.010
Nita-Lazar M, et al. Desialylation of Airway Epithelial Cells During Influenza Virus Infection Enhances Pneumococcal Adhesion Via Galectin Binding. Mol Immunol. 2015;65(1):1-16. PubMed PMID: 25597246.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Desialylation of airway epithelial cells during influenza virus infection enhances pneumococcal adhesion via galectin binding. AU - Nita-Lazar,Mihai, AU - Banerjee,Aditi, AU - Feng,Chiguang, AU - Amin,Mohammed N, AU - Frieman,Matthew B, AU - Chen,Wilbur H, AU - Cross,Alan S, AU - Wang,Lai-Xi, AU - Vasta,Gerardo R, Y1 - 2015/01/16/ PY - 2014/10/21/received PY - 2014/12/18/revised PY - 2014/12/19/accepted PY - 2015/1/20/entrez PY - 2015/1/20/pubmed PY - 2015/5/2/medline KW - Airway A549 cells KW - Galectin KW - Influenza KW - Neuraminidase KW - Pneumococcus pneumoniae SP - 1 EP - 16 JF - Molecular immunology JO - Mol Immunol VL - 65 IS - 1 N2 - The continued threat of worldwide influenza pandemics, together with the yearly emergence of antigenically drifted influenza A virus (IAV) strains, underscore the urgent need to elucidate not only the mechanisms of influenza virulence, but also those mechanisms that predispose influenza patients to increased susceptibility to subsequent infection with Streptococcus pneumoniae. Glycans displayed on the surface of epithelia that are exposed to the external environment play important roles in microbial recognition, adhesion, and invasion. It is well established that the IAV hemagglutinin and pneumococcal adhesins enable their attachment to the host epithelia. Reciprocally, the recognition of microbial glycans by host carbohydrate-binding proteins (lectins) can initiate innate immune responses, but their relevance in influenza or pneumococcal infections is poorly understood. Galectins are evolutionarily conserved lectins characterized by affinity for β-galactosides and a unique sequence motif, with critical regulatory roles in development and immune homeostasis. In this study, we examined the possibility that galectins expressed in the airway epithelial cells might play a significant role in viral or pneumococcal adhesion to airway epithelial cells. Our results in a mouse model for influenza and pneumococcal infection revealed that the murine lung expresses a diverse galectin repertoire, from which selected galectins, including galectin 1 (Gal1) and galectin 3 (Gal3), are released to the bronchoalveolar space. Further, the results showed that influenza and subsequent S. pneumoniae infections significantly alter the glycosylation patterns of the airway epithelial surface and modulate galectin expression. In vitro studies on the human airway epithelial cell line A549 were consistent with the observations made in the mouse model, and further revealed that both Gal1 and Gal3 bind strongly to IAV and S. pneumoniae, and that exposure of the cells to viral neuraminidase or influenza infection increased galectin-mediated S. pneumoniae adhesion to the cell surface. Our results suggest that upon influenza infection, pneumococcal adhesion to the airway epithelial surface is enhanced by an interplay among the host galectins and viral and pneumococcal neuraminidases. The observed enhancement of pneumococcal adhesion may be a contributing factor to the observed hypersusceptibility to pneumonia of influenza patients. SN - 1872-9142 UR - https://www.unboundmedicine.com/medline/citation/25597246/Desialylation_of_airway_epithelial_cells_during_influenza_virus_infection_enhances_pneumococcal_adhesion_via_galectin_binding_ DB - PRIME DP - Unbound Medicine ER -