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Title: Glycan recognition in globally dominant human rotaviruses

Abstract

Rotaviruses (RVs) cause life-threatening diarrhea in infants and children worldwide. Recent biochemical and epidemiological studies underscore the importance of histo-blood group antigens (HBGA) as both cell attachment and susceptibility factors for the globally dominant P[4], P[6], and P[8] genotypes of human RVs. How these genotypes interact with HBGA is not known. Here, our crystal structures of P[4] and a neonate-specific P[6] VP8∗s alone and in complex with H-type I HBGA reveal a unique glycan binding site that is conserved in the globally dominant genotypes and allows for the binding of ABH HBGAs, consistent with their prevalence. Remarkably, the VP8∗ of P[6] RVs isolated from neonates displays subtle structural changes in this binding site that may restrict its ability to bind branched glycans. This provides a structural basis for the age-restricted tropism of some P[6] RVs as developmentally regulated unbranched glycans are more abundant in the neonatal gut.

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [1];  [3];  [3];  [1];  [1];  [1];  [1];  [1]
  1. Baylor College of Medicine, Houston, TX (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Emory Univ. School of Medicine, Atlanta, GA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1478359
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
[ Journal Volume: 9; Journal Issue: 1]; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hu, Liya, Sankaran, Banumathi, Laucirica, Daniel R., Patil, Ketki, Salmen, Wilhelm, Ferreon, Allan Chris M., Tsoi, Phoebe S., Lasanajak, Yi, Smith, David F., Ramani, Sasirekha, Atmar, Robert L., Estes, Mary K., Ferreon, Josephine C., and Prasad, B. V. Venkataram. Glycan recognition in globally dominant human rotaviruses. United States: N. p., 2018. Web. doi:10.1038/s41467-018-05098-4.
Hu, Liya, Sankaran, Banumathi, Laucirica, Daniel R., Patil, Ketki, Salmen, Wilhelm, Ferreon, Allan Chris M., Tsoi, Phoebe S., Lasanajak, Yi, Smith, David F., Ramani, Sasirekha, Atmar, Robert L., Estes, Mary K., Ferreon, Josephine C., & Prasad, B. V. Venkataram. Glycan recognition in globally dominant human rotaviruses. United States. doi:10.1038/s41467-018-05098-4.
Hu, Liya, Sankaran, Banumathi, Laucirica, Daniel R., Patil, Ketki, Salmen, Wilhelm, Ferreon, Allan Chris M., Tsoi, Phoebe S., Lasanajak, Yi, Smith, David F., Ramani, Sasirekha, Atmar, Robert L., Estes, Mary K., Ferreon, Josephine C., and Prasad, B. V. Venkataram. Fri . "Glycan recognition in globally dominant human rotaviruses". United States. doi:10.1038/s41467-018-05098-4. https://www.osti.gov/servlets/purl/1478359.
@article{osti_1478359,
title = {Glycan recognition in globally dominant human rotaviruses},
author = {Hu, Liya and Sankaran, Banumathi and Laucirica, Daniel R. and Patil, Ketki and Salmen, Wilhelm and Ferreon, Allan Chris M. and Tsoi, Phoebe S. and Lasanajak, Yi and Smith, David F. and Ramani, Sasirekha and Atmar, Robert L. and Estes, Mary K. and Ferreon, Josephine C. and Prasad, B. V. Venkataram},
abstractNote = {Rotaviruses (RVs) cause life-threatening diarrhea in infants and children worldwide. Recent biochemical and epidemiological studies underscore the importance of histo-blood group antigens (HBGA) as both cell attachment and susceptibility factors for the globally dominant P[4], P[6], and P[8] genotypes of human RVs. How these genotypes interact with HBGA is not known. Here, our crystal structures of P[4] and a neonate-specific P[6] VP8∗s alone and in complex with H-type I HBGA reveal a unique glycan binding site that is conserved in the globally dominant genotypes and allows for the binding of ABH HBGAs, consistent with their prevalence. Remarkably, the VP8∗ of P[6] RVs isolated from neonates displays subtle structural changes in this binding site that may restrict its ability to bind branched glycans. This provides a structural basis for the age-restricted tropism of some P[6] RVs as developmentally regulated unbranched glycans are more abundant in the neonatal gut.},
doi = {10.1038/s41467-018-05098-4},
journal = {Nature Communications},
number = [1],
volume = [9],
place = {United States},
year = {2018},
month = {7}
}

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    Works referencing / citing this record:

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    journal, November 2013


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    Modulation of allostery by protein intrinsic disorder
    journal, June 2013

    • Ferreon, Allan Chris M.; Ferreon, Josephine C.; Wright, Peter E.
    • Nature, Vol. 498, Issue 7454
    • DOI: 10.1038/nature12294

    Structural basis of glycan interaction in gastroenteric viral pathogens
    journal, August 2014


    Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution
    journal, November 2017


    Rotavirus Strain Trends During the Postlicensure Vaccine Era: United States, 2008–2013
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    • Bowen, Michael D.; Mijatovic-Rustempasic, Slavica; Esona, Mathew D.
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    • Nature Reviews Microbiology, Vol. 12, Issue 11
    • DOI: 10.1038/nrmicro3346

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    journal, April 2016

    • Tate, Jacqueline E.; Burton, Anthony H.; Boschi-Pinto, Cynthia
    • Clinical Infectious Diseases, Vol. 62, Issue suppl 2
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    Host Genetic Susceptibility to Enteric Viruses: A Systematic Review and Metaanalysis
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    • Kambhampati, Anita; Payne, Daniel C.; Costantini, Veronica
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    • DOI: 10.1093/cid/civ873

    P[8] and P[4] Rotavirus Infection Associated with Secretor Phenotypes Among Children in South China
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    • Zhang, Xu-Fu; Long, Yan; Tan, Ming
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep34591

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    • Matthijnssens, Jelle; Ciarlet, Max; McDonald, Sarah M.
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    • DOI: 10.1038/nature10996

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    • Cellular and Molecular Gastroenterology and Hepatology, Vol. 2, Issue 3
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    • Laskowski, Roman A.; Swindells, Mark B.
    • Journal of Chemical Information and Modeling, Vol. 51, Issue 10
    • DOI: 10.1021/ci200227u

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    Histo–Blood Group Antigen Phenotype Determines Susceptibility to Genotype-Specific Rotavirus Infections and Impacts Measures of Rotavirus Vaccine Efficacy
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    • Hu, Liya; Ramani, Sasirekha; Czako, Rita
    • Nature Communications, Vol. 6, Issue 1
    • DOI: 10.1038/ncomms9346

    Host–pathogen co-evolution and glycan interactions
    journal, August 2014


    Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7
    journal, June 2008

    • Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S.
    • Nature Protocols, Vol. 3, Issue 7
    • DOI: 10.1038/nprot.2008.91

    Sialic acid dependence in rotavirus host cell invasion
    journal, December 2008

    • Haselhorst, Thomas; Fleming, Fiona E.; Dyason, Jeffrey C.
    • Nature Chemical Biology, Vol. 5, Issue 2
    • DOI: 10.1038/nchembio.134

    Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion
    journal, January 2015

    • Böhm, Raphael; Fleming, Fiona E.; Maggioni, Andrea
    • Nature Communications, Vol. 6, Issue 1
    • DOI: 10.1038/ncomms6907

    Binding of recombinant norovirus like particle to histo-blood group antigen on cells in the lumen of pig duodenum
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    Predominance of unusual rotavirus G1P[6] strain in North India: An evidence from hospitalized children and adult diarrheal patients
    journal, December 2016


    A FUT2 Gene Common Polymorphism Determines Resistance to Rotavirus A of the P[8] Genotype
    journal, November 2013

    • Imbert-Marcille, Berthe-Marie; Barbé, Laure; Dupé, Mathilde
    • The Journal of Infectious Diseases, Vol. 209, Issue 8
    • DOI: 10.1093/infdis/jit655

    NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy
    journal, December 2014


    Rotaviruses: From Pathogenesis to Vaccination
    journal, May 2009


    Both Lewis and Secretor Status Mediate Susceptibility to Rotavirus Infections in a Rotavirus Genotype–Dependent Manner
    journal, August 2014

    • Nordgren, Johan; Sharma, Sumit; Bucardo, Filemon
    • Clinical Infectious Diseases, Vol. 59, Issue 11
    • DOI: 10.1093/cid/ciu633

    A paradox of transcriptional and functional innate interferon responses of human intestinal enteroids to enteric virus infection
    journal, January 2017

    • Saxena, Kapil; Simon, Lukas M.; Zeng, Xi-Lei
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 4
    • DOI: 10.1073/pnas.1615422114

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    journal, November 2015


    UCSF Chimera?A visualization system for exploratory research and analysis
    journal, January 2004

    • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
    • Journal of Computational Chemistry, Vol. 25, Issue 13
    • DOI: 10.1002/jcc.20084

    Carbohydrate Structure Suite (CSS): analysis of carbohydrate 3D structures derived from the PDB
    journal, December 2004

    • Lutteke, T.
    • Nucleic Acids Research, Vol. 33, Issue Database issue
    • DOI: 10.1093/nar/gki013

    Human P[6] Rotaviruses From Sub-Saharan Africa and Southeast Asia Are Closely Related to Those of Human P[4] and P[8] Rotaviruses Circulating Worldwide
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    • Heylen, Elisabeth; Zeller, Mark; Ciarlet, Max
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    • DOI: 10.1093/infdis/jiw247