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 »
- Authors:
-
- Miami Univ., Oxford, OH (United States)
- Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States); Chinese Academy of Medical Sciences, Tianjin (China)
- Cincinnati Children's Hospital Medical Center, Cincinnati, OH (United States)
- 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.
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
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.
@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}
}
Web of Science
Figures / Tables:

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