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Title: Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution

Abstract

Recognition of specific cell surface glycans, mediated by the VP8* domain of the spike protein VP4, is the essential first step in rotavirus (RV) infection. Due to lack of direct structural information of virus-ligand interactions, the molecular basis of ligand-controlled host ranges of the major human RVs (P[8] and P[4]) in P[II] genogroup remains unknown. Here, through characterization of a minor P[II] RV (P[19]) that can infect both animals (pigs) and humans, we made an important advance to fill this knowledge gap by solving the crystal structures of the P[19] VP8* in complex with its ligands. Our data showed that P[19] RVs use a novel binding site that differs from the known ones of other genotypes/genogroups. This binding site is capable of interacting with two types of glycans, the mucin core and type 1 histo-blood group antigens (HBGAs) with a common GlcNAc as the central binding saccharide. The binding site is apparently shared by other P[II] RVs and possibly two genotypes (P[10] and P[12]) in P[I] as shown by their highly conserved GlcNAc-interacting residues. These data provide strong evidence of evolutionary connections among these human and animal RVs, pointing to a common ancestor in P[I] with a possible animal hostmore » origin. While the binding properties to GlcNAc-containing saccharides are maintained, changes in binding to additional residues, such as those in the polymorphic type 1 HBGAs may occur in the course of RV evolution, explaining the complex P[II] genogroup that mainly causes diseases in humans but also in some animals.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [2];  [3];  [4]; ORCiD logo [2]; ORCiD logo [4];
  1. Tianjin Key Laboratory of Molecular Nuclear Medicine, Institute of Radiation Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, China, Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, United States of America
  2. Miami University, Oxford, OH (United States). Department of Chemistry and Biochemistry
  3. Cincinnati Children’s Hospital Medical Center, Cincinnati, OH (United States). Division of Infectious Diseases
  4. Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, United States of America, University of Cincinnati College of Medicine, Cincinnati, OH, United States of America
Publication Date:
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1627915
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 13; Journal Issue: 11; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
Microbiology; Parasitology; Virology

Citation Formats

Liu, Yang, Xu, Shenyuan, Woodruff, Andrew L., Xia, Ming, Tan, Ming, Kennedy, Michael A., Jiang, Xi, and Zhou, Z. Hong. Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution. United States: N. p., 2017. Web. doi:10.1371/journal.ppat.1006707.
Liu, Yang, Xu, Shenyuan, Woodruff, Andrew L., Xia, Ming, Tan, Ming, Kennedy, Michael A., Jiang, Xi, & Zhou, Z. Hong. Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution. United States. https://doi.org/10.1371/journal.ppat.1006707
Liu, Yang, Xu, Shenyuan, Woodruff, Andrew L., Xia, Ming, Tan, Ming, Kennedy, Michael A., Jiang, Xi, and Zhou, Z. Hong. Tue . "Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution". United States. https://doi.org/10.1371/journal.ppat.1006707. https://www.osti.gov/servlets/purl/1627915.
@article{osti_1627915,
title = {Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution},
author = {Liu, Yang and Xu, Shenyuan and Woodruff, Andrew L. and Xia, Ming and Tan, Ming and Kennedy, Michael A. and Jiang, Xi and Zhou, Z. Hong},
abstractNote = {Recognition of specific cell surface glycans, mediated by the VP8* domain of the spike protein VP4, is the essential first step in rotavirus (RV) infection. Due to lack of direct structural information of virus-ligand interactions, the molecular basis of ligand-controlled host ranges of the major human RVs (P[8] and P[4]) in P[II] genogroup remains unknown. Here, through characterization of a minor P[II] RV (P[19]) that can infect both animals (pigs) and humans, we made an important advance to fill this knowledge gap by solving the crystal structures of the P[19] VP8* in complex with its ligands. Our data showed that P[19] RVs use a novel binding site that differs from the known ones of other genotypes/genogroups. This binding site is capable of interacting with two types of glycans, the mucin core and type 1 histo-blood group antigens (HBGAs) with a common GlcNAc as the central binding saccharide. The binding site is apparently shared by other P[II] RVs and possibly two genotypes (P[10] and P[12]) in P[I] as shown by their highly conserved GlcNAc-interacting residues. These data provide strong evidence of evolutionary connections among these human and animal RVs, pointing to a common ancestor in P[I] with a possible animal host origin. While the binding properties to GlcNAc-containing saccharides are maintained, changes in binding to additional residues, such as those in the polymorphic type 1 HBGAs may occur in the course of RV evolution, explaining the complex P[II] genogroup that mainly causes diseases in humans but also in some animals.},
doi = {10.1371/journal.ppat.1006707},
journal = {PLoS Pathogens},
number = 11,
volume = 13,
place = {United States},
year = {Tue Nov 14 00:00:00 EST 2017},
month = {Tue Nov 14 00:00:00 EST 2017}
}

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