Early target cells of measles virus after aerosol infection of non-human primates
Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strain...
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| Published in | PLoS pathogens Vol. 7; no. 1; p. e1001263 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.01.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMV(KS)EGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected (EGFP(+)) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP(+) cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. |
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| AbstractList |
Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMVKSEGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected (EGFP+) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP+ cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMVKSEGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected (EGFP+) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP+ cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMV(KS)EGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected (EGFP(+)) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP(+) cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMVKSEGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n=3 per time point) and infected (EGFP+) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP+ cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles remains an important vaccine-preventable cause of morbidity and mortality in developing countries. The causative agent, measles virus (MV), is one of the most contagious viruses known. Measles has an incubation time of approximately two weeks, and surprisingly little is known about the early events after MV infection. Epithelial cells in the upper respiratory tract have long been considered as early target cells, but more recently alveolar macrophages (AM) and dendritic cells (DC) have been proposed as alternatives. We have infected cynomolgus macaques with a high dose of a recombinant EGFP-expressing MV strain via aerosol inhalation, to ensure that the virus had access to the entire respiratory tract. At 2 days post-infection, MV-infected mononuclear cells were detectable in the alveolar lumen but not in the upper respiratory tract. These infected cells migrated through the bronchus-associated lymphoid tissue to the draining tracheo-bronchial lymph node at 3 days post-infection. Systemic infection was initiated from this point, as observed in macaques euthanized 4 or 5 days post-infection. Thus, even though the aerosolized virus had access to epithelial cells and lymphoid tissues along the entire respiratory tract, AM and DC in the lungs were the first cells that sustained MV replication. Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of [rMV.sup.KS]EGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected ([EGFP.sup.+]) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., [EGFP.sup.+] cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However, epithelial cells do not express signaling lymphocyte activation molecule (CD150), which is the high-affinity cellular receptor for wild-type MV strains. We have generated a new recombinant MV strain expressing enhanced green fluorescent protein (EGFP), based on a wild-type genotype B3 virus isolate from Khartoum, Sudan (KS). Cynomolgus macaques were infected with a high dose of rMV KS EGFP by aerosol inhalation to ensure that the virus could reach the full range of potential target cells throughout the entire respiratory tract. Animals were euthanized 2, 3, 4 or 5 days post-infection (d.p.i., n = 3 per time point) and infected (EGFP + ) cells were identified at all four time points, albeit at low levels 2 and 3 d.p.i. At these earliest time points, MV-infected cells were exclusively detected in the lungs by fluorescence microscopy, histopathology and/or virus isolation from broncho-alveolar lavage cells. On 2 d.p.i., EGFP + cells were phenotypically typed as large mononuclear cells present in the alveolar lumen or lining the alveolar epithelium. One to two days later, larger clusters of MV-infected cells were detected in bronchus-associated lymphoid tissue (BALT) and in the tracheo-bronchial lymph nodes. From 4 d.p.i. onward, MV-infected cells were detected in peripheral blood and various lymphoid tissues. In spite of the possibility for the aerosolized virus to infect cells and lymphoid tissues of the upper respiratory tract, MV-infected cells were not detected in either the tonsils or the adenoids until after onset of viremia. These data strongly suggest that in our model MV entered the host at the alveolar level by infecting macrophages or dendritic cells, which traffic the virus to BALT or regional lymph nodes, resulting in local amplification and subsequent systemic dissemination by viremia. Measles remains an important vaccine-preventable cause of morbidity and mortality in developing countries. The causative agent, measles virus (MV), is one of the most contagious viruses known. Measles has an incubation time of approximately two weeks, and surprisingly little is known about the early events after MV infection. Epithelial cells in the upper respiratory tract have long been considered as early target cells, but more recently alveolar macrophages (AM) and dendritic cells (DC) have been proposed as alternatives. We have infected cynomolgus macaques with a high dose of a recombinant EGFP-expressing MV strain via aerosol inhalation, to ensure that the virus had access to the entire respiratory tract. At 2 days post-infection, MV-infected mononuclear cells were detectable in the alveolar lumen but not in the upper respiratory tract. These infected cells migrated through the bronchus-associated lymphoid tissue to the draining tracheo-bronchial lymph node at 3 days post-infection. Systemic infection was initiated from this point, as observed in macaques euthanized 4 or 5 days post-infection. Thus, even though the aerosolized virus had access to epithelial cells and lymphoid tissues along the entire respiratory tract, AM and DC in the lungs were the first cells that sustained MV replication. |
| Audience | Academic |
| Author | Kuiken, Thijs Yüksel, Selma Ludlow, Martin Rima, Bertus K Rennick, Linda J Duprex, W Paul Mesman, Annelies W Osterhaus, Albert D M E McQuaid, Stephen Geijtenbeek, Teunis B H van Amerongen, Geert de Swart, Rik L de Vries, Rory D Lemon, Ken |
| AuthorAffiliation | 1 Centre for Infection and Immunity, School of Medicine, Dentistry and Biomedical Sciences, Queen's University of Belfast, Belfast, United Kingdom 2 Department of Virology, Erasmus MC, Rotterdam, The Netherlands 3 Centre for Experimental and Molecular Medicine, Academic Medical Center, Amsterdam, The Netherlands Dalhousie University, Canada 5 Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts, United States of America 4 Tissue Pathology, Belfast Health and Social Care Trust, Queen's University of Belfast, Belfast, United Kingdom |
| AuthorAffiliation_xml | – name: 4 Tissue Pathology, Belfast Health and Social Care Trust, Queen's University of Belfast, Belfast, United Kingdom – name: Dalhousie University, Canada – name: 1 Centre for Infection and Immunity, School of Medicine, Dentistry and Biomedical Sciences, Queen's University of Belfast, Belfast, United Kingdom – name: 2 Department of Virology, Erasmus MC, Rotterdam, The Netherlands – name: 3 Centre for Experimental and Molecular Medicine, Academic Medical Center, Amsterdam, The Netherlands – name: 5 Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts, United States of America |
| Author_xml | – sequence: 1 givenname: Ken surname: Lemon fullname: Lemon, Ken organization: Centre for Infection and Immunity, School of Medicine, Dentistry and Biomedical Sciences, Queen's University of Belfast, Belfast, United Kingdom – sequence: 2 givenname: Rory D surname: de Vries fullname: de Vries, Rory D – sequence: 3 givenname: Annelies W surname: Mesman fullname: Mesman, Annelies W – sequence: 4 givenname: Stephen surname: McQuaid fullname: McQuaid, Stephen – sequence: 5 givenname: Geert surname: van Amerongen fullname: van Amerongen, Geert – sequence: 6 givenname: Selma surname: Yüksel fullname: Yüksel, Selma – sequence: 7 givenname: Martin surname: Ludlow fullname: Ludlow, Martin – sequence: 8 givenname: Linda J surname: Rennick fullname: Rennick, Linda J – sequence: 9 givenname: Thijs surname: Kuiken fullname: Kuiken, Thijs – sequence: 10 givenname: Bertus K surname: Rima fullname: Rima, Bertus K – sequence: 11 givenname: Teunis B H surname: Geijtenbeek fullname: Geijtenbeek, Teunis B H – sequence: 12 givenname: Albert D M E surname: Osterhaus fullname: Osterhaus, Albert D M E – sequence: 13 givenname: W Paul surname: Duprex fullname: Duprex, W Paul – sequence: 14 givenname: Rik L surname: de Swart fullname: de Swart, Rik L |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21304593$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2011 Public Library of Science 2011 Lemon et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G, et al. (2011) Early Target Cells of Measles Virus after Aerosol Infection of Non-Human Primates. PLoS Pathog 7(1): e1001263. doi:10.1371/journal.ppat.1001263 Lemon et al. 2011 |
| Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: 2011 Lemon et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G, et al. (2011) Early Target Cells of Measles Virus after Aerosol Infection of Non-Human Primates. PLoS Pathog 7(1): e1001263. doi:10.1371/journal.ppat.1001263 – notice: Lemon et al. 2011 |
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| Snippet | Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However,... Measles virus (MV) is highly infectious, and has long been thought to enter the host by infecting epithelial cells of the respiratory tract. However,... |
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| SubjectTerms | Aerosols Airborne infection Animals Binding sites Cell Movement Cynomolgus Dendritic Cells - cytology Dendritic Cells - virology Development and progression Disease Models, Animal Genetic aspects Green Fluorescent Proteins Immunology/Cellular Microbiology and Pathogenesis Infections Infectious Diseases/Respiratory Infections Infectious Diseases/Viral Infections Inhalation Exposure Leukocytes, Mononuclear - cytology Leukocytes, Mononuclear - virology Lung Lymph Nodes - cytology Lymph Nodes - virology Lymphocytes Macaca Macaca fascicularis Macrophages, Alveolar - cytology Macrophages, Alveolar - virology Measles virus Measles virus - genetics Measles virus - pathogenicity Pathology/Cellular Pathology Physiological aspects Primates Proteins Pulmonary Alveoli - cytology Pulmonary Alveoli - virology Receptors Recombination, Genetic Respiratory Medicine/Respiratory Infections Viral Fusion Proteins Viral Tropism Virology/Animal Models of Infection Virology/Host Invasion and Cell Entry Viruses |
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| Title | Early target cells of measles virus after aerosol infection of non-human primates |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/21304593 https://www.proquest.com/docview/1289086807 https://search.proquest.com/docview/902355188 https://pubmed.ncbi.nlm.nih.gov/PMC3029373 https://doaj.org/article/d471565451324e4198970169f73bfbaa http://dx.doi.org/10.1371/journal.ppat.1001263 |
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