CD300lf is the primary physiologic receptor of murine norovirus but not human norovirus

Murine norovirus (MNoV) is an important model of human norovirus (HNoV) and mucosal virus infection more broadly. Viral receptor utilization is a major determinant of cell tropism, host range, and pathogenesis. The bona fide receptor for HNoV is unknown. Recently, we identified CD300lf as a proteina...

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Published inPLoS pathogens Vol. 16; no. 4; p. e1008242
Main Authors Graziano, Vincent R, Walker, Forrest C, Kennedy, Elizabeth A, Wei, Jin, Ettayebi, Khalil, Strine, Madison S, Filler, Renata B, Hassan, Ebrahim, Hsieh, Leon L, Kim, Arthur S, Kolawole, Abimbola O, Wobus, Christiane E, Lindesmith, Lisa C, Baric, Ralph S, Estes, Mary K, Orchard, Robert C, Baldridge, Megan T, Wilen, Craig B
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.04.2020
Public Library of Science (PLoS)
Subjects
Animals
Binding sites
Biology
Biology and life sciences
Caliciviridae Infections - virology
Departments
Epidemiology
Feces
Funding
Genomes
Health aspects
HeLa Cells
Host range
Host Specificity
Host-Pathogen Interactions
Humans
Immunology
Infection
Infections
Infectious diseases
Laboratories
Lethality
Medicine
Medicine and Health Sciences
Mice
Mice, Inbred C57BL
Mice, Knockout
Mucosa
Norovirus - growth & development
Norovirus - metabolism
Pathogenesis
Polysaccharides
Receptors
Receptors, Immunologic - metabolism
Receptors, Immunologic - physiology
Receptors, Virus - metabolism
Research and analysis methods
Stat1 protein
Tropism
Viral infections
Viral Tropism
Virology
Virus diseases
Virus-like particles
Viruses
North Carolina
United States > US
Texas
Missouri
Connecticut
Ann Arbor Michigan
Michigan
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Abstract Murine norovirus (MNoV) is an important model of human norovirus (HNoV) and mucosal virus infection more broadly. Viral receptor utilization is a major determinant of cell tropism, host range, and pathogenesis. The bona fide receptor for HNoV is unknown. Recently, we identified CD300lf as a proteinaceous receptor for MNoV. Interestingly, its paralogue CD300ld was also sufficient for MNoV infection in vitro. Here we explored whether CD300lf is the sole physiologic receptor in vivo and whether HNoV can use a CD300 ortholog as an entry receptor. We report that both CD300ld and CD300lf are sufficient for infection by diverse MNoV strains in vitro. We further demonstrate that CD300lf is essential for both oral and parenteral MNoV infection and to elicit anti-MNoV humoral responses in vivo. In mice deficient in STAT1 signaling, CD300lf is required for MNoV-induced lethality. Finally, we demonstrate that human CD300lf (huCD300lf) is not essential for HNoV infection, nor does huCD300lf inhibit binding of HNoV virus-like particles to glycans. Thus, we report huCD300lf is not a receptor for HNoV.
AbstractList Murine norovirus (MNoV) is an important model of human norovirus (HNoV) and mucosal virus infection more broadly. Viral receptor utilization is a major determinant of cell tropism, host range, and pathogenesis. The bona fide receptor for HNoV is unknown. Recently, we identified CD300lf as a proteinaceous receptor for MNoV. Interestingly, its paralogue CD300ld was also sufficient for MNoV infection in vitro. Here we explored whether CD300lf is the sole physiologic receptor in vivo and whether HNoV can use a CD300 ortholog as an entry receptor. We report that both CD300ld and CD300lf are sufficient for infection by diverse MNoV strains in vitro. We further demonstrate that CD300lf is essential for both oral and parenteral MNoV infection and to elicit anti-MNoV humoral responses in vivo. In mice deficient in STAT1 signaling, CD300lf is required for MNoV-induced lethality. Finally, we demonstrate that human CD300lf (huCD300lf) is not essential for HNoV infection, nor does huCD300lf inhibit binding of HNoV virus-like particles to glycans. Thus, we report huCD300lf is not a receptor for HNoV.
Murine norovirus (MNoV) is an important model of human norovirus (HNoV) and mucosal virus infection more broadly. Viral receptor utilization is a major determinant of cell tropism, host range, and pathogenesis. The bona fide receptor for HNoV is unknown. Recently, we identified CD300lf as a proteinaceous receptor for MNoV. Interestingly, its paralogue CD300ld was also sufficient for MNoV infection in vitro . Here we explored whether CD300lf is the sole physiologic receptor in vivo and whether HNoV can use a CD300 ortholog as an entry receptor. We report that both CD300ld and CD300lf are sufficient for infection by diverse MNoV strains in vitro . We further demonstrate that CD300lf is essential for both oral and parenteral MNoV infection and to elicit anti-MNoV humoral responses in vivo . In mice deficient in STAT1 signaling, CD300lf is required for MNoV-induced lethality. Finally, we demonstrate that human CD300lf (huCD300lf) is not essential for HNoV infection, nor does huCD300lf inhibit binding of HNoV virus-like particles to glycans. Thus, we report huCD300lf is not a receptor for HNoV. Human norovirus is the leading cause of non-bacterial gastroenteritis causing up to 200,000 deaths each year. How human norovirus enters cells is unknown. Because human norovirus is difficult to grow in the laboratory and in small animals, we use mouse or murine norovirus as a model system. We recently discovered that murine norovirus can use the either CD300ld or CD300lf as a receptor in vitro . We also showed that CD300lf deficient mice were resistant to oral challenge with a single virus strain. Here we determined that CD300lf is essential for infection of diverse murine norovirus strains in cell lines and in mice with normal immune systems demonstrating it’s the primary physiologic receptor for diverse murine norovirus strains independent of infection route. Finally, we demonstrated that human CD300lf is not the elusive proteinaceous receptor for human norovirus.
Audience Academic
Author Hassan, Ebrahim
Wei, Jin
Orchard, Robert C
Wilen, Craig B
Wobus, Christiane E
Walker, Forrest C
Graziano, Vincent R
Strine, Madison S
Estes, Mary K
Ettayebi, Khalil
Hsieh, Leon L
Baric, Ralph S
Kennedy, Elizabeth A
Filler, Renata B
Kim, Arthur S
Lindesmith, Lisa C
Kolawole, Abimbola O
Baldridge, Megan T
AuthorAffiliation 3 Departments of Medicine and Molecular Virology & Microbiology, Baylor College of Medicine, Houston, Texas, United States of America
4 Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, United States of America
2 Department of Medicine, Division of Infectious Diseases, Edison Family Center for Genome Sciences & Systems Biology, Washington University School of Medicine, Saint Louis, Missouri, United States of America
1 Departments of Laboratory Medicine and Immunobiology, Yale University School of Medicine, New Haven, Connecticut, United States of America
5 Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan, United States of America
NIH, UNITED STATES
6 Department of Epidemiology, University of North Carolina, Chapel Hill, North Carolina, United States of America
7 Department of Immunology, University of Texas Southwestern Medical School, Dallas, Texas, United
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32251490$$D View this record in MEDLINE/PubMed
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Copyright COPYRIGHT 2020 Public Library of Science
2020 Graziano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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– notice: 2020 Graziano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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CBW and RCO are inventors on a patent application submitted by Washington University entitled “Receptor for norovirus and uses thereof” (U.S. Provisional Application 62/301,965).
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Snippet Murine norovirus (MNoV) is an important model of human norovirus (HNoV) and mucosal virus infection more broadly. Viral receptor utilization is a major...
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StartPage e1008242
SubjectTerms Animals
Binding sites
Biology
Biology and life sciences
Caliciviridae Infections - virology
Departments
Epidemiology
Feces
Funding
Genomes
Health aspects
HeLa Cells
Host range
Host Specificity
Host-Pathogen Interactions
Humans
Immunology
Infection
Infections
Infectious diseases
Laboratories
Lethality
Medicine
Medicine and Health Sciences
Mice
Mice, Inbred C57BL
Mice, Knockout
Mucosa
Norovirus - growth & development
Norovirus - metabolism
Pathogenesis
Polysaccharides
Receptors
Receptors, Immunologic - metabolism
Receptors, Immunologic - physiology
Receptors, Virus - metabolism
Research and analysis methods
Stat1 protein
Tropism
Viral infections
Viral Tropism
Virology
Virus diseases
Virus-like particles
Viruses
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Title CD300lf is the primary physiologic receptor of murine norovirus but not human norovirus
URI https://www.ncbi.nlm.nih.gov/pubmed/32251490
https://www.proquest.com/docview/2403776401
https://search.proquest.com/docview/2387260296
https://pubmed.ncbi.nlm.nih.gov/PMC7162533
https://doaj.org/article/c2674dd032554c20845ee5f10d202eda
http://dx.doi.org/10.1371/journal.ppat.1008242
Volume 16
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