Measles Virus Infects both Polarized Epithelial and Immune Cells by Using Distinctive Receptor-Binding Sites on Its Hemagglutinin

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Published inJournal of Virology Vol. 82; no. 9; pp. 4630 - 4637
Main Authors Tahara, Maino, Takeda, Makoto, Shirogane, Yuta, Hashiguchi, Takao, Ohno, Shinji, Yanagi, Yusuke
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.05.2008
American Society for Microbiology (ASM)
Subjects
Animals
Antigens, CD
Binding Sites
Biological and medical sciences
Cell Line
Cell Polarity
Epithelial Cells - virology
Fundamental and applied biological sciences. Psychology
Hemagglutinins - metabolism
Humans
Immune System - cytology
Immune System - virology
Lymphocytes - virology
Measles virus
Measles virus - pathogenicity
Membrane Cofactor Protein
Microbiology
Miscellaneous
Receptors, Cell Surface
Receptors, Virus - metabolism
Signaling Lymphocytic Activation Molecule Family Member 1
Virology
Virus Attachment
Virus-Cell Interactions
Virus
Infection
Paramyxovirinae
Mononegavirales
Hemagglutinin
Morbillivirus
Epithelial cell
Binding site
Paramyxoviridae
Biological receptor
Virology
Measles virus
Online AccessGet full text

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Abstract Article Usage Stats Services JVI Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue Spotlights in the Current Issue JVI About JVI Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JVI RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0022-538X Online ISSN: 1098-5514 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JVI .asm.org, visit: JVI       
AbstractList Measles is one of the most contagious human infectious diseases and remains a major cause of childhood morbidity and mortality worldwide. The signaling lymphocyte activation molecule (SLAM), also called CD150, is a cellular receptor for measles virus (MV), presumably accounting for its tropism for immune cells and its immunosuppressive properties. On the other hand, pathological studies have shown that MV also infects epithelial cells at a later stage of infection, although its mechanism has so far been unknown. In this study, we show that wild-type MV can infect and produce syncytia in human polarized epithelial cell lines independently of SLAM and CD46 (a receptor for the vaccine strains of MV). Progeny viral particles are released exclusively from the apical surface of these polarized epithelial cell lines. We have also identified amino acid residues on the MV attachment protein that are likely to interact with a putative receptor on epithelial cells. All of these residues have aromatic side chains and may form a receptor-binding pocket located in a different position from the putative SLAM- and CD46-binding sites on the MV attachment protein. Thus, our results indicate that MV has an intrinsic ability to infect both polarized epithelial and immune cells by using distinctive receptor-binding sites on the attachment protein corresponding to each of their respective receptors. The ability of MV to infect polarized epithelial cells and its exclusive release from the apical surface may facilitate its efficient transmission via aerosol droplets, resulting in its highly contagious nature.Measles is one of the most contagious human infectious diseases and remains a major cause of childhood morbidity and mortality worldwide. The signaling lymphocyte activation molecule (SLAM), also called CD150, is a cellular receptor for measles virus (MV), presumably accounting for its tropism for immune cells and its immunosuppressive properties. On the other hand, pathological studies have shown that MV also infects epithelial cells at a later stage of infection, although its mechanism has so far been unknown. In this study, we show that wild-type MV can infect and produce syncytia in human polarized epithelial cell lines independently of SLAM and CD46 (a receptor for the vaccine strains of MV). Progeny viral particles are released exclusively from the apical surface of these polarized epithelial cell lines. We have also identified amino acid residues on the MV attachment protein that are likely to interact with a putative receptor on epithelial cells. All of these residues have aromatic side chains and may form a receptor-binding pocket located in a different position from the putative SLAM- and CD46-binding sites on the MV attachment protein. Thus, our results indicate that MV has an intrinsic ability to infect both polarized epithelial and immune cells by using distinctive receptor-binding sites on the attachment protein corresponding to each of their respective receptors. The ability of MV to infect polarized epithelial cells and its exclusive release from the apical surface may facilitate its efficient transmission via aerosol droplets, resulting in its highly contagious nature.
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Measles is one of the most contagious human infectious diseases and remains a major cause of childhood morbidity and mortality worldwide. The signaling lymphocyte activation molecule (SLAM), also called CD150, is a cellular receptor for measles virus (MV), presumably accounting for its tropism for immune cells and its immunosuppressive properties. On the other hand, pathological studies have shown that MV also infects epithelial cells at a later stage of infection, although its mechanism has so far been unknown. In this study, we show that wild-type MV can infect and produce syncytia in human polarized epithelial cell lines independently of SLAM and CD46 (a receptor for the vaccine strains of MV). Progeny viral particles are released exclusively from the apical surface of these polarized epithelial cell lines. We have also identified amino acid residues on the MV attachment protein that are likely to interact with a putative receptor on epithelial cells. All of these residues have aromatic side chains and may form a receptor-binding pocket located in a different position from the putative SLAM- and CD46-binding sites on the MV attachment protein. Thus, our results indicate that MV has an intrinsic ability to infect both polarized epithelial and immune cells by using distinctive receptor-binding sites on the attachment protein corresponding to each of their respective receptors. The ability of MV to infect polarized epithelial cells and its exclusive release from the apical surface may facilitate its efficient transmission via aerosol droplets, resulting in its highly contagious nature.
Author Yusuke Yanagi
Maino Tahara
Shinji Ohno
Makoto Takeda
Yuta Shirogane
Takao Hashiguchi
AuthorAffiliation Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
AuthorAffiliation_xml – name: Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
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  surname: Tahara
  fullname: Tahara, Maino
  organization: Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
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  surname: Takeda
  fullname: Takeda, Makoto
  organization: Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
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  surname: Shirogane
  fullname: Shirogane, Yuta
  organization: Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
– sequence: 4
  givenname: Takao
  surname: Hashiguchi
  fullname: Hashiguchi, Takao
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  surname: Yanagi
  fullname: Yanagi, Yusuke
  organization: Department of Virology, Faculty of Medicine, Kyushu University, Fukuoka 812-8582, Japan
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Issue 9
Keywords Virus
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Paramyxovirinae
Mononegavirales
Hemagglutinin
Morbillivirus
Epithelial cell
Binding site
Paramyxoviridae
Biological receptor
Virology
Measles virus
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Corresponding author. Mailing address: Department of Virology, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan. Phone: 81-92-642-6138. Fax: 81-92-642-6140. E-mail: mtakeda@virology.med.kyushu-u.ac.jp
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Measles is one of the most contagious human infectious diseases and remains a major cause of childhood morbidity and mortality worldwide. The signaling...
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StartPage 4630
SubjectTerms Animals
Antigens, CD
Binding Sites
Biological and medical sciences
Cell Line
Cell Polarity
Epithelial Cells - virology
Fundamental and applied biological sciences. Psychology
Hemagglutinins - metabolism
Humans
Immune System - cytology
Immune System - virology
Lymphocytes - virology
Measles virus
Measles virus - pathogenicity
Membrane Cofactor Protein
Microbiology
Miscellaneous
Receptors, Cell Surface
Receptors, Virus - metabolism
Signaling Lymphocytic Activation Molecule Family Member 1
Virology
Virus Attachment
Virus-Cell Interactions
Title Measles Virus Infects both Polarized Epithelial and Immune Cells by Using Distinctive Receptor-Binding Sites on Its Hemagglutinin
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https://www.ncbi.nlm.nih.gov/pubmed/18287234
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