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Title: Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens

Abstract

Initial cell attachment of rotavirus (RV) to specific cell surface glycan receptors, which is the essential first step in RV infection, is mediated by the VP8* domain of the spike protein VP4. Recently, human histo-blood group antigens (HBGAs) have been identified as receptors or attachment factors for human RV strains. RV strains in the P[4] and P[8] genotypes of the P[II] genogroup share common recognition of the Lewis b (Leb) and H type 1 antigens, however, the molecular basis of receptor recognition by the major human P[8] RVs remains unknown due to lack of experimental structural information. Here, we used nuclear magnetic resonance (NMR) spectroscopy-based titration experiments and NMR-derived high ambiguity driven docking (HADDOCK) methods to elucidate the molecular basis for P[8] VP8* recognition of the Leb (LNDFH I) and type 1 HBGAs. We also used X-ray crystallography to determine the molecular details underlying P[6] recognition of H type 1 HBGAs. Unlike P[6]/P[19] VP8*s that recognize H type 1 HBGAs in a binding surface composed of an α-helix and a β-sheet, referred as the “βα binding site”, the P[8] and P[4] VP8*s bind Leb HBGAs in a previously undescribed pocket formed by the edges of two β-sheets, referred to asmore » the “ββ binding site”. Importantly, the P[8] and P[4] VP8*s retain binding capability to non-Leb type 1 HBGAs using the βα binding site. The presence of two distinct binding sites for Leb and non-Leb HBGA glycans in the P[8] and P[4] VP8* domains suggests host-pathogen co-evolution under structural and functional adaptation of RV pathogens to host glycan polymorphisms. Assessment and understanding of the precise impact of this co-evolutionary process in determining RV host ranges and cross-species RV transmission should facilitate improved RV vaccine development and prediction of future RV strain emergence and epidemics.« less

Authors:
 [1]; ORCiD logo [1]; ORCiD logo [1];  [1];  [2];  [3]; ORCiD logo [3];  [3];  [3];  [4]; ORCiD logo [1]
+ Show Author Affiliations
  1. Miami Univ., Oxford, OH (United States)
  2. Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States); Chinese Academy of Medical Sciences, Tianjin (China)
  3. Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States)
  4. Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States); Univ. of Cincinnati, OH (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1618487
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 16; Journal Issue: 3; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Xu, Shenyuan, Ahmed, Luay U., Stuckert, Michael Robert, McGinnis, Kristen Rose, Liu, Yang, Tan, Ming, Huang, Pengwei, Zhong, Weiming, Zhao, Dandan, Jiang, Xi, and Kennedy, Michael A. Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens. United States: N. p., 2020. Web. doi:10.1371/journal.ppat.1008386.
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Xu, Shenyuan, Ahmed, Luay U., Stuckert, Michael Robert, McGinnis, Kristen Rose, Liu, Yang, Tan, Ming, Huang, Pengwei, Zhong, Weiming, Zhao, Dandan, Jiang, Xi, & Kennedy, Michael A. Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens. United States. https://doi.org/10.1371/journal.ppat.1008386
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Xu, Shenyuan, Ahmed, Luay U., Stuckert, Michael Robert, McGinnis, Kristen Rose, Liu, Yang, Tan, Ming, Huang, Pengwei, Zhong, Weiming, Zhao, Dandan, Jiang, Xi, and Kennedy, Michael A. Tue . "Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens". United States. https://doi.org/10.1371/journal.ppat.1008386. https://www.osti.gov/servlets/purl/1618487.
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@article{osti_1618487,
title = {Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens},
author = {Xu, Shenyuan and Ahmed, Luay U. and Stuckert, Michael Robert and McGinnis, Kristen Rose and Liu, Yang and Tan, Ming and Huang, Pengwei and Zhong, Weiming and Zhao, Dandan and Jiang, Xi and Kennedy, Michael A.},
abstractNote = {Initial cell attachment of rotavirus (RV) to specific cell surface glycan receptors, which is the essential first step in RV infection, is mediated by the VP8* domain of the spike protein VP4. Recently, human histo-blood group antigens (HBGAs) have been identified as receptors or attachment factors for human RV strains. RV strains in the P[4] and P[8] genotypes of the P[II] genogroup share common recognition of the Lewis b (Leb) and H type 1 antigens, however, the molecular basis of receptor recognition by the major human P[8] RVs remains unknown due to lack of experimental structural information. Here, we used nuclear magnetic resonance (NMR) spectroscopy-based titration experiments and NMR-derived high ambiguity driven docking (HADDOCK) methods to elucidate the molecular basis for P[8] VP8* recognition of the Leb (LNDFH I) and type 1 HBGAs. We also used X-ray crystallography to determine the molecular details underlying P[6] recognition of H type 1 HBGAs. Unlike P[6]/P[19] VP8*s that recognize H type 1 HBGAs in a binding surface composed of an α-helix and a β-sheet, referred as the “βα binding site”, the P[8] and P[4] VP8*s bind Leb HBGAs in a previously undescribed pocket formed by the edges of two β-sheets, referred to as the “ββ binding site”. Importantly, the P[8] and P[4] VP8*s retain binding capability to non-Leb type 1 HBGAs using the βα binding site. The presence of two distinct binding sites for Leb and non-Leb HBGA glycans in the P[8] and P[4] VP8* domains suggests host-pathogen co-evolution under structural and functional adaptation of RV pathogens to host glycan polymorphisms. Assessment and understanding of the precise impact of this co-evolutionary process in determining RV host ranges and cross-species RV transmission should facilitate improved RV vaccine development and prediction of future RV strain emergence and epidemics.},
doi = {10.1371/journal.ppat.1008386},
journal = {PLoS Pathogens},
number = 3,
volume = 16,
place = {United States},
year = {2020},
month = {3}
}
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https://doi.org/10.1371/journal.ppat.1008386
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Figures / Tables:

Fig. 1 Fig. 1: Schematic representation of VP8* from P[II] genogroup with its corresponding binding glycan structures. (a) Schematic representation of P[8] VP8* and its binding glycan structures, Leb tetra-saccharide and LNDFH I. (b) Schematic representation of P[4] VP8* and its binding glycan structures, LNDFH I and LNFP I. (c) Schematic representationmore » of P[6] VP8* and its binding glycan structures, LNT and LNFP I. (d) Schematic representation of P[19] VP8* and its binding glycan structures, LNT and LNFP I. The red boxes encircle Leb glycans and the blue boxes encircle non Leb glycans. (e) Inhibition of rotavirus Wa strain replication in HT29 cells. Left) Representative indirect immunofluorescence assay (IFA) microscopy image of P[8] RV Wa strain replication focuses in HT29 cells. Right) Quantitation of viral replication focus reductions observed in wells incubated with LNDFH1-BSA and H type 1-biotin-PAA in compared with cell culture wells with media only. Ley-PAA is a negative ligand control.« less
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