The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells

In the complex microenvironment of the human respiratory tract, different kinds of microorganisms may synergistically interact with each other resulting in viral-bacterial co-infections that are often associated with more severe diseases than the respective mono-infections. Human respiratory paramyx...

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Main Authors: Jie Tong, Yuguang Fu, Fandan Meng, Nadine Krüger, Peter Valentin-Weigand, Georg Herrler
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fcimb.2018.00280/full
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spelling doaj-d6e374bf950c454281da056fad5a881e2020-11-24T23:14:19ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882018-08-01810.3389/fcimb.2018.00280362012The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 CellsJie Tong0Yuguang Fu1Fandan Meng2Fandan Meng3Nadine Krüger4Peter Valentin-Weigand5Georg Herrler6Institute of Virology, University of Veterinary Medicine Hannover, Hanover, GermanyInstitute of Virology, University of Veterinary Medicine Hannover, Hanover, GermanyInstitute of Virology, University of Veterinary Medicine Hannover, Hanover, GermanyState Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, ChinaInstitute of Virology, University of Veterinary Medicine Hannover, Hanover, GermanyInstitute of Microbiology, University of Veterinary Medicine Hannover, Hanover, GermanyInstitute of Virology, University of Veterinary Medicine Hannover, Hanover, GermanyIn the complex microenvironment of the human respiratory tract, different kinds of microorganisms may synergistically interact with each other resulting in viral-bacterial co-infections that are often associated with more severe diseases than the respective mono-infections. Human respiratory paramyxoviruses, for example parainfluenza virus type 3 (HPIV3), are common causes of respiratory diseases both in infants and a subset of adults. HPIV3 recognizes sialic acid (SA)-containing receptors on host cells. In contrast to human influenza viruses which have a preference for α2,6-linked sialic acid, HPIV3 preferentially recognize α2,3-linked sialic acids. Group B streptococci (GBS) are colonizers in the human respiratory tract. They contain a capsular polysaccharide with terminal sialic acid residues in an α2,3-linkage. In the present study, we report that HPIV3 can recognize the α2,3-linked sialic acids present on GBS. The interaction was evident not only by the binding of virions to GBS in a co-sedimentation assay, but also in the GBS binding to HPIV3-infected cells. While co-infection by GBS and HPIV3 had a delaying effect on the virus replication, it enhanced GBS adherence to virus-infected cells. To show that other human paramyxoviruses are also able to recognize the capsular sialic acid of GBS we demonstrate that GBS attaches in a sialic acid-dependent way to transfected BHK cells expressing the HN protein of mumps virus (MuV) on their surface. Overall, our results reveal a new type of synergism in the co-infection by respiratory pathogens, which is based on the recognition of α2,3-linked sialic acids. This interaction between human paramyxoviruses and GBS enhances the bacterial adherence to airway cells and thus may result in more severe disease.https://www.frontiersin.org/article/10.3389/fcimb.2018.00280/fullsialic acidshemagglutinin-neuraminidase proteinparainfluenza virusmumps virusgroup B streptococcico-infection
collection DOAJ
language English
format Article
sources DOAJ
author Jie Tong
Yuguang Fu
Fandan Meng
Fandan Meng
Nadine Krüger
Peter Valentin-Weigand
Georg Herrler
spellingShingle Jie Tong
Yuguang Fu
Fandan Meng
Fandan Meng
Nadine Krüger
Peter Valentin-Weigand
Georg Herrler
The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
Frontiers in Cellular and Infection Microbiology
sialic acids
hemagglutinin-neuraminidase protein
parainfluenza virus
mumps virus
group B streptococci
co-infection
author_facet Jie Tong
Yuguang Fu
Fandan Meng
Fandan Meng
Nadine Krüger
Peter Valentin-Weigand
Georg Herrler
author_sort Jie Tong
title The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
title_short The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
title_full The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
title_fullStr The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
title_full_unstemmed The Sialic Acid Binding Activity of Human Parainfluenza Virus 3 and Mumps Virus Glycoproteins Enhances the Adherence of Group B Streptococci to HEp-2 Cells
title_sort sialic acid binding activity of human parainfluenza virus 3 and mumps virus glycoproteins enhances the adherence of group b streptococci to hep-2 cells
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2018-08-01
description In the complex microenvironment of the human respiratory tract, different kinds of microorganisms may synergistically interact with each other resulting in viral-bacterial co-infections that are often associated with more severe diseases than the respective mono-infections. Human respiratory paramyxoviruses, for example parainfluenza virus type 3 (HPIV3), are common causes of respiratory diseases both in infants and a subset of adults. HPIV3 recognizes sialic acid (SA)-containing receptors on host cells. In contrast to human influenza viruses which have a preference for α2,6-linked sialic acid, HPIV3 preferentially recognize α2,3-linked sialic acids. Group B streptococci (GBS) are colonizers in the human respiratory tract. They contain a capsular polysaccharide with terminal sialic acid residues in an α2,3-linkage. In the present study, we report that HPIV3 can recognize the α2,3-linked sialic acids present on GBS. The interaction was evident not only by the binding of virions to GBS in a co-sedimentation assay, but also in the GBS binding to HPIV3-infected cells. While co-infection by GBS and HPIV3 had a delaying effect on the virus replication, it enhanced GBS adherence to virus-infected cells. To show that other human paramyxoviruses are also able to recognize the capsular sialic acid of GBS we demonstrate that GBS attaches in a sialic acid-dependent way to transfected BHK cells expressing the HN protein of mumps virus (MuV) on their surface. Overall, our results reveal a new type of synergism in the co-infection by respiratory pathogens, which is based on the recognition of α2,3-linked sialic acids. This interaction between human paramyxoviruses and GBS enhances the bacterial adherence to airway cells and thus may result in more severe disease.
topic sialic acids
hemagglutinin-neuraminidase protein
parainfluenza virus
mumps virus
group B streptococci
co-infection
url https://www.frontiersin.org/article/10.3389/fcimb.2018.00280/full
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