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Structure and Assembly | Spotlight

Structural Insights into Human Bocaparvoviruses

Mario Mietzsch, Shweta Kailasan, Jamie Garrison, Maria Ilyas, Paul Chipman, Kalle Kantola, Mandy E. Janssen, John Spear, Duncan Sousa, Robert McKenna, Kevin Brown, Maria Söderlund-Venermo, Timothy Baker, Mavis Agbandje-McKenna
Rozanne M. Sandri-Goldin, Editor
Mario Mietzsch
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Shweta Kailasan
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Jamie Garrison
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Maria Ilyas
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Paul Chipman
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Kalle Kantola
bDepartment of Virology, University of Helsinki, Helsinki, Finland
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Mandy E. Janssen
cDepartment of Chemistry and Biochemistry and Division of Biological Sciences, University of California—San Diego, San Diego, California, USA
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John Spear
dBiological Science Imaging Resource, Department of Biological Sciences, The Florida State University, Tallahassee, Florida, USA
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Duncan Sousa
dBiological Science Imaging Resource, Department of Biological Sciences, The Florida State University, Tallahassee, Florida, USA
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Robert McKenna
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Kevin Brown
eVirus Reference Department, National Infection Service, Public Health England, London, United Kingdom
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Maria Söderlund-Venermo
bDepartment of Virology, University of Helsinki, Helsinki, Finland
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Timothy Baker
cDepartment of Chemistry and Biochemistry and Division of Biological Sciences, University of California—San Diego, San Diego, California, USA
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Mavis Agbandje-McKenna
aDepartment of Biochemistry and Molecular Biology, Center for Structural Biology, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida, USA
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Rozanne M. Sandri-Goldin
University of California, Irvine
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DOI: 10.1128/JVI.00261-17
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ABSTRACT

Bocaparvoviruses are emerging pathogens of the Parvoviridae family. Human bocavirus 1 (HBoV1) causes severe respiratory infections and HBoV2 to HBoV4 cause gastrointestinal infections in young children. Recent reports of life-threatening cases, lack of direct treatment or vaccination, and a limited understanding of their disease mechanisms highlight the need to study these pathogens on a molecular and structural level for the development of therapeutics. Toward this end, the capsid structures of HBoV1, HBoV3, and HBoV4 were determined to a resolution of 2.8 to 3.0 Å by cryo-electron microscopy and three-dimensional image reconstruction. The bocaparvovirus capsids, which display different tissue tropisms, have features in common with other parvoviruses, such as depressions at the icosahedral 2-fold symmetry axis and surrounding the 5-fold symmetry axis, protrusions surrounding the 3-fold symmetry axis, and a channel at the 5-fold symmetry axis. However, unlike other parvoviruses, densities extending the 5-fold channel into the capsid interior are conserved among the bocaparvoviruses and are suggestive of a genus-specific function. Additionally, their major viral protein 3 contains loops with variable regions at their apexes conferring capsid surface topologies different from those of other parvoviruses. Structural comparisons at the strain (HBoV) and genus (bovine parvovirus and HBoV) levels identified differences in surface loops that are functionally important in host/tissue tropism, pathogenicity, and antigenicity in other parvoviruses and likely play similar roles in these viruses. This study thus provides a structural framework to characterize determinants of host/tissue tropism, pathogenicity, and antigenicity for the development of antiviral strategies to control human bocavirus infections.

IMPORTANCE Human bocaviruses are one of only a few members of the Parvoviridae family pathogenic to humans, especially young children and immunocompromised adults. There are currently no treatments or vaccines for these viruses or the related enteric bocaviruses. This study obtained the first high-resolution structures of three human bocaparvoviruses determined by cryo-reconstruction. HBoV1 infects the respiratory tract, and HBoV3 and HBoV4 infect the gastrointestinal tract, tissues that are likely targeted by the capsid. Comparison of these viruses provides information on conserved bocaparvovirus-specific features and variable regions resulting in unique surface topologies that can serve as guides to characterize HBoV determinants of tissue tropism and antigenicity in future experiments. Based on the comparison to other existing parvovirus capsid structures, this study suggests capsid regions that likely control successful infection, including determinants of receptor attachment, host cell trafficking, and antigenic reactivity. Overall, these observations could impact efforts to design antiviral strategies and vaccines for HBoVs.

  • Copyright © 2017 American Society for Microbiology.

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Structural Insights into Human Bocaparvoviruses
Mario Mietzsch, Shweta Kailasan, Jamie Garrison, Maria Ilyas, Paul Chipman, Kalle Kantola, Mandy E. Janssen, John Spear, Duncan Sousa, Robert McKenna, Kevin Brown, Maria Söderlund-Venermo, Timothy Baker, Mavis Agbandje-McKenna
Journal of Virology May 2017, 91 (11) e00261-17; DOI: 10.1128/JVI.00261-17

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Structural Insights into Human Bocaparvoviruses
Mario Mietzsch, Shweta Kailasan, Jamie Garrison, Maria Ilyas, Paul Chipman, Kalle Kantola, Mandy E. Janssen, John Spear, Duncan Sousa, Robert McKenna, Kevin Brown, Maria Söderlund-Venermo, Timothy Baker, Mavis Agbandje-McKenna
Journal of Virology May 2017, 91 (11) e00261-17; DOI: 10.1128/JVI.00261-17
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KEYWORDS

capsid
human bocavirus
capsid
cryo-EM
gastrointestinal infection
HBoV
human bocaviruses
parvovirus
respiratory infection

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