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

Liu, Yang; Xu, Shenyuan; Woodruff, Andrew L.; Xia, Ming; Tan, Ming; Kennedy, Michael A.; Jiang, Xi; Zhou, Z. Hong

doi:10.1371/journal.ppat.1006707

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

Journal Article · Tue Nov 14 00:00:00 EST 2017 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1006707· OSTI ID:1627915

Liu, Yang ^[1]; ^[2]; ^[2]; Xia, Ming ^[3]; Tan, Ming ^[4]; ^[2]; ^[4]; Zhou, Z. Hong

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; DOE/OSTI
Miami University, Oxford, OH (United States). Department of Chemistry and Biochemistry
Cincinnati Children’s Hospital Medical Center, Cincinnati, OH (United States). Division of Infectious Diseases
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

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.

View Accepted Manuscript (DOE)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1627915

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 11 Vol. 13; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin Fiore, Lucia; Greenberg, Harry B.; Mackow, Erich R. Virology, Vol. 181, Issue 2 https://doi.org/10.1016/0042-6822(91)90888-i	journal	April 1991
Insight into Host Cell Carbohydrate-recognition by Human and Porcine Rotavirus from Crystal Structures of the Virion Spike Associated Carbohydrate-binding Domain (VP8*) Blanchard, Helen; Yu, Xing; Coulson, Barbara S. Journal of Molecular Biology, Vol. 367, Issue 4 https://doi.org/10.1016/j.jmb.2007.01.028	journal	April 2007
Nosocomial rotavirus infections: A systematic review Chandran, Aruna; Heinzen, Rebekah R.; Santosham, Mathuram The Journal of Pediatrics, Vol. 149, Issue 4 https://doi.org/10.1016/j.jpeds.2006.04.054	journal	October 2006
The first identification of rare human group A rotavirus strain G3P[10] with severe infantile diarrhea in eastern India Mukherjee, Anupam; Mullick, Satarupa; Kobayashi, Nobumichi Infection, Genetics and Evolution, Vol. 12, Issue 8 https://doi.org/10.1016/j.meegid.2012.08.009	journal	December 2012
Whole-genome characterization of a Peruvian alpaca rotavirus isolate expressing a novel VP4 genotype Rojas, Miguel; Gonçalves, Jorge Luiz S.; Dias, Helver G. Veterinary Microbiology, Vol. 196 https://doi.org/10.1016/j.vetmic.2016.10.005	journal	November 2016
Binding specificity of P[8] VP8* proteins of rotavirus vaccine strains with histo-blood group antigens Sun, Xiaoman; Guo, Nijun; Li, Dandi Virology, Vol. 495 https://doi.org/10.1016/j.virol.2016.05.010	journal	August 2016
Updating prevaccination rotavirus-associated mortality Desselberger, Ulrich The Lancet Infectious Diseases, Vol. 12, Issue 2 https://doi.org/10.1016/s1473-3099(11)70288-2	journal	February 2012
Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen Hu, Liya; Crawford, Sue E.; Czako, Rita Nature, Vol. 485, Issue 7397 https://doi.org/10.1038/nature10996	journal	April 2012
Sialic acid dependence in rotavirus host cell invasion Haselhorst, Thomas; Fleming, Fiona E.; Dyason, Jeffrey C. Nature Chemical Biology, Vol. 5, Issue 2 https://doi.org/10.1038/nchembio.134	journal	December 2008
Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion Böhm, Raphael; Fleming, Fiona E.; Maggioni, Andrea Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6907	journal	January 2015
Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus Hu, Liya; Ramani, Sasirekha; Czako, Rita Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9346	journal	September 2015
The sweet spot: defining virus–sialic acid interactions Stencel-Baerenwald, Jennifer E.; Reiss, Kerstin; Reiter, Dirk M. Nature Reviews Microbiology, Vol. 12, Issue 11 https://doi.org/10.1038/nrmicro3346	journal	September 2014
Human Milk Contains Novel Glycans That Are Potential Decoy Receptors for Neonatal Rotaviruses Yu, Ying; Lasanajak, Yi; Song, Xuezheng Molecular & Cellular Proteomics, Vol. 13, Issue 11 https://doi.org/10.1074/mcp.m114.039875	journal	July 2014
The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site Dormitzer, P. R. The EMBO Journal, Vol. 21, Issue 5 https://doi.org/10.1093/emboj/21.5.885	journal	March 2002
Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses Reetz, Jochen; Twardziok, Sven; Sachsenröder, Jana Journal of General Virology, Vol. 94, Issue 1 https://doi.org/10.1099/vir.0.047381-0	journal	January 2013
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/s0021889807021206	journal	July 2007
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/s0907444905036693	journal	December 2005
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/s0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/s0907444996012255	journal	May 1997
Glycan Specificity of P[19] Rotavirus and Comparison with Those of Related P Genotypes Liu, Yang; Ramelot, Theresa A.; Huang, Pengwei Journal of Virology, Vol. 90, Issue 21 https://doi.org/10.1128/jvi.01494-16	journal	August 2016
Functional and Structural Characterization of P[19] Rotavirus VP8* Interaction with Histo-blood Group Antigens Sun, Xiaoman; Li, Dandi; Peng, Ruchao Journal of Virology, Vol. 90, Issue 21 https://doi.org/10.1128/jvi.01566-16	journal	August 2016
The VP8* Domain of Neonatal Rotavirus Strain G10P[11] Binds to Type II Precursor Glycans Ramani, S.; Cortes-Penfield, N. W.; Hu, L. Journal of Virology, Vol. 87, Issue 13 https://doi.org/10.1128/jvi.03518-12	journal	April 2013
Glycosphingolipid Binding Specificities of Rotavirus: Identification of a Sialic Acid-Binding Epitope Delorme, Cécile; Brüssow, Harald; Sidoti, Josette Journal of Virology, Vol. 75, Issue 5 https://doi.org/10.1128/jvi.75.5.2276-2287.2001	journal	March 2001
Specificity and Affinity of Sialic Acid Binding by the Rhesus Rotavirus VP8* Core Dormitzer, Philip R.; Sun, Zhen-Yu J.; Blixt, Ola Journal of Virology, Vol. 76, Issue 20 https://doi.org/10.1128/jvi.76.20.10512-10517.2002	journal	October 2002
High-Resolution Molecular and Antigen Structure of the VP8* Core of a Sialic Acid-Independent Human Rotavirus Strain Monnier, N.; Higo-Moriguchi, K.; Sun, Z. -Y. J. Journal of Virology, Vol. 80, Issue 3 https://doi.org/10.1128/jvi.80.3.1513-1523.2006	journal	January 2006
Poly-LacNAc as an Age-Specific Ligand for Rotavirus P[11] in Neonates and Infants Liu, Yang; Huang, Pengwei; Jiang, Baoming PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078113	journal	November 2013
Both Lewis and Secretor Status Mediate Susceptibility to Rotavirus Infections in a Rotavirus Genotype–Dependent Manner Sylvia, Becker-Dreps,; W., Nitiema, Leon; Jacques, Simpore, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/g9xr-kj03	text	January 2014
Rotavirus and Severe Childhood Diarrhea Parashar, Umesh D.; Gibson, Christopher J.; Bresee, Joseph S. Emerging Infectious Diseases, Vol. 12, Issue 2 https://doi.org/10.3201/eid1202.050006	journal	February 2006
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Molecular characterization of VP4, VP6, VP7, NSP4, and NSP5/6 genes identifies an unusual G3P[10] human rotavirus strain: Characterization of G3P[10] Rotavirus Strain Khamrin, Pattara; Maneekarn, Niwat; Peerakome, Supatra Journal of Medical Virology, Vol. 81, Issue 1 https://doi.org/10.1002/jmv.21336	journal	November 2008
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
The VP8 fragment of VP4 is the rhesus rotavirus hemagglutinin Fiore, Lucia; Greenberg, Harry B.; Mackow, Erich R. Virology, Vol. 181, Issue 2 https://doi.org/10.1016/0042-6822(91)90888-I	journal	April 1991
Global burden of childhood pneumonia and diarrhoea Walker, Christa L. Fischer; Rudan, Igor; Liu, Li The Lancet, Vol. 381, Issue 9875 https://doi.org/10.1016/S0140-6736(13)60222-6	journal	April 2013
2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis Tate, Jacqueline E.; Burton, Anthony H.; Boschi-Pinto, Cynthia The Lancet Infectious Diseases, Vol. 12, Issue 2 https://doi.org/10.1016/S1473-3099(11)70253-5	journal	February 2012
New rotavirus vaccines: Renewed optimism O’Ryan, Miguel; Matson, David O. The Journal of Pediatrics, Vol. 149, Issue 4 https://doi.org/10.1016/j.jpeds.2006.07.018	journal	October 2006
Global distribution of group A rotavirus strains in horses: A systematic review Papp, Hajnalka; Matthijnssens, Jelle; Martella, Vito Vaccine, Vol. 31, Issue 48 https://doi.org/10.1016/j.vaccine.2013.08.045	journal	November 2013
Atomic model of an infectious rotavirus particle: Atomic model of an infectious rotavirus particle Settembre, Ethan C.; Chen, James Z.; Dormitzer, Philip R. The EMBO Journal, Vol. 30, Issue 2 https://doi.org/10.1038/emboj.2010.322	journal	December 2010
Histo-blood group antigens as receptors for rotavirus, new understanding on rotavirus epidemiology and vaccine strategy: Rotavirus host receptor and vaccine strategy Jiang, Xi; Liu, Yang; Tan, Ming Emerging Microbes & Infections, Vol. 6, Issue 1 https://doi.org/10.1038/emi.2017.30	journal	January 2017
'Sialidase sensitivity' of rotaviruses revisited Banda, Kalyan; Kang, Gagandeep; Varki, Ajit Nature Chemical Biology, Vol. 5, Issue 2 https://doi.org/10.1038/nchembio0209-71	journal	February 2009
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Human Milk Contains Novel Glycans That Are Potential Decoy Receptors for Neonatal Rotaviruses Yu, Ying; Lasanajak, Yi; Song, Xuezheng Molecular & Cellular Proteomics, Vol. 13, Issue 11 https://doi.org/10.1074/mcp.M114.039875	journal	July 2014
Both Lewis and Secretor Status Mediate Susceptibility to Rotavirus Infections in a Rotavirus Genotype–Dependent Manner Nordgren, Johan; Sharma, Sumit; Bucardo, Filemon Clinical Infectious Diseases, Vol. 59, Issue 11 https://doi.org/10.1093/cid/ciu633	journal	August 2014
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Scaling and assessment of data quality Evans, Philip Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82 https://doi.org/10.1107/S0907444905036693	journal	December 2005
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
The Rossmann Fourier autoindexing algorithm in MOSFLM Powell, Harold R. Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 10 https://doi.org/10.1107/S0907444999009506	journal	October 1999
Rotavirus VP8*: Phylogeny, Host Range, and Interaction with Histo-Blood Group Antigens Liu, Yang; Huang, Pengwei; Tan, Ming Journal of Virology, Vol. 86, Issue 18 https://doi.org/10.1128/JVI.00979-12	journal	July 2012
Glycan Specificity of P[19] Rotavirus and Comparison with Those of Related P Genotypes Liu, Yang; Ramelot, Theresa A.; Huang, Pengwei Journal of Virology, Vol. 90, Issue 21 https://doi.org/10.1128/JVI.01494-16	journal	August 2016
Functional and Structural Characterization of P[19] Rotavirus VP8* Interaction with Histo-blood Group Antigens Sun, Xiaoman; Li, Dandi; Peng, Ruchao Journal of Virology, Vol. 90, Issue 21 https://doi.org/10.1128/JVI.01566-16	journal	August 2016
The VP8* Domain of Neonatal Rotavirus Strain G10P[11] Binds to Type II Precursor Glycans Ramani, S.; Cortes-Penfield, N. W.; Hu, L. Journal of Virology, Vol. 87, Issue 13 https://doi.org/10.1128/JVI.03518-12	journal	April 2013
Spike Protein VP8* of Human Rotavirus Recognizes Histo-Blood Group Antigens in a Type-Specific Manner Huang, P.; Xia, M.; Tan, M. Journal of Virology, Vol. 86, Issue 9 https://doi.org/10.1128/JVI.05507-11	journal	February 2012
Glycosphingolipid Binding Specificities of Rotavirus: Identification of a Sialic Acid-Binding Epitope Delorme, Cécile; Brüssow, Harald; Sidoti, Josette Journal of Virology, Vol. 75, Issue 5 https://doi.org/10.1128/JVI.75.5.2276-2287.2001	journal	March 2001
Specificity and Affinity of Sialic Acid Binding by the Rhesus Rotavirus VP8* Core Dormitzer, Philip R.; Sun, Zhen-Yu J.; Blixt, Ola Journal of Virology, Vol. 76, Issue 20 https://doi.org/10.1128/JVI.76.20.10512-10517.2002	journal	October 2002
Initial Interaction of Rotavirus Strains with N-Acetylneuraminic (Sialic) Acid Residues on the Cell Surface Correlates with VP4 Genotype, Not Species of Origin Ciarlet, M.; Ludert, J. E.; Iturriza-Gomara, M. Journal of Virology, Vol. 76, Issue 8 https://doi.org/10.1128/JVI.76.8.4087-4095.2002	journal	April 2002
High-Resolution Molecular and Antigen Structure of the VP8* Core of a Sialic Acid-Independent Human Rotavirus Strain Monnier, N.; Higo-Moriguchi, K.; Sun, Z. -Y. J. Journal of Virology, Vol. 80, Issue 3 https://doi.org/10.1128/JVI.80.3.1513-1523.2006	journal	January 2006
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011

Cited By (5)

Glycan recognition in globally dominant human rotaviruses Hu, Liya; Sankaran, Banumathi; Laucirica, Daniel R. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05098-4	journal	July 2018
Unraveling the role of the secretor antigen in human rotavirus attachment to histo-blood group antigens Gozalbo-Rovira, Roberto; Ciges-Tomas, J. Rafael; Vila-Vicent, Susana PLOS Pathogens, Vol. 15, Issue 6 https://doi.org/10.1371/journal.ppat.1007865	journal	June 2019
Structural Basis of Glycan Recognition in Globally Predominant Human P[8] Rotavirus Sun, Xiaoman; Dang, Lei; Li, Dandi Virologica Sinica, Vol. 35, Issue 2 https://doi.org/10.1007/s12250-019-00164-7	journal	October 2019
Saliva as a source of reagent to study human susceptibility to avian influenza H7N9 virus infection Tan, Ming; Cui, Lunbiao; Huo, Xiang Emerging Microbes & Infections, Vol. 7, Issue 1 https://doi.org/10.1038/s41426-018-0160-8	journal	September 2018
Conformations of the type-1 lacto- N -biose I unit in protein complex structures Fushinobu, Shinya Acta Crystallographica Section F Structural Biology Communications, Vol. 74, Issue 8 https://doi.org/10.1107/s2053230x18006568	journal	July 2018

Similar Records

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

Journal Article · Mon Mar 23 20:00:00 EDT 2020 · PLoS Pathogens · OSTI ID:1618487

Glycan recognition in globally dominant human rotaviruses

Journal Article · Thu Jul 05 20:00:00 EDT 2018 · Nature Communications · OSTI ID:1478359

Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus

Journal Article · Tue Sep 29 20:00:00 EDT 2015 · Nature Communications · OSTI ID:1256040

Related Subjects

Microbiology
Parasitology
Virology

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

Citation Formats

References (60)

Cited By (5)

Similar Records

Related Subjects