Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography

Hu, Liya; Salmen, Wilhelm; Sankaran, Banumathi; Lasanajak, Yi; Smith, David F.; Crawford, Sue E.; Estes, Mary K.; Prasad, B. V. Venkataram

doi:10.1038/s42003-022-03357-1

Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography

Journal Article · Thu May 05 00:00:00 EDT 2022 · Communications Biology

DOI:https://doi.org/10.1038/s42003-022-03357-1· OSTI ID:1880816

^[1]; Salmen, Wilhelm ^[1]; ^[2]; Lasanajak, Yi ^[3]; Smith, David F. ^[3]; Crawford, Sue E. ^[1]; ^[1]; ^[1]

Baylor College of Medicine, Houston, TX (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Emory Univ. School of Medicine, Atlanta, GA (United States)

The VP8* domain of spike protein VP4 in group A and C rotaviruses, which cause epidemic gastroenteritis in children, exhibits a conserved galectin-like fold for recognizing glycans during cell entry. In group B rotavirus, which causes significant diarrheal outbreaks in adults, the VP8* domain (VP8*B) surprisingly lacks sequence similarity with VP8* of group A or group C rotavirus. Here, by using the recently developed AlphaFold2 for ab initio structure prediction and validating the predicted model by determining a 1.3-Å crystal structure, we show that VP8*B exhibits a novel fold distinct from the galectin fold. This fold with a β-sheet clasping an α-helix represents a new fold for glycan recognition based on glycan array screening, which shows that VP8*B recognizes glycans containing N-acetyllactosamine moiety. Although uncommon, our study illustrates how evolution can incorporate structurally distinct folds with similar functionality in a homologous protein within the same virus genus.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Institute of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1880816

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 5; ISSN 2399-3642

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Tracking N-Acetyllactosamine on Cell-Surface Glycans In Vivo Zheng, Tianqing; Jiang, Hao; Gros, Marilyn Angewandte Chemie International Edition, Vol. 50, Issue 18 https://doi.org/10.1002/anie.201100265	journal	March 2011
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
AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility Morris, Garrett M.; Huey, Ruth; Lindstrom, William Journal of Computational Chemistry, Vol. 30, Issue 16 https://doi.org/10.1002/jcc.21256	journal	December 2009
Detection of group B rotavirus in an adult with acute gastroenteritis in Yangon, Myanmar Aung, Tin Sabai; Kobayashi, Nobumichi; Nagashima, Shigeo Journal of Medical Virology, Vol. 81, Issue 11 https://doi.org/10.1002/jmv.21613	journal	November 2009
Using Dali for Protein Structure Comparison Holm, Liisa Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-0270-6_3	book	January 2020
Coding assignments of the genome of adult diarrhea rotavirus Fang, Z. -Y.; Monroe, S. S.; Dong, H. Archives of Virology, Vol. 125, Issue 1-4 https://doi.org/10.1007/BF01309628	journal	March 1992
VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation Matthijnssens, Jelle; Otto, Peter H.; Ciarlet, Max Archives of Virology, Vol. 157, Issue 6 https://doi.org/10.1007/s00705-012-1273-3	journal	March 2012
Three-dimensional visualization of the rotavirus hemagglutinin structure Shaw, A. L.; Rothnagel, R.; Chen, D. Cell, Vol. 74, Issue 4 https://doi.org/10.1016/0092-8674(93)90516-S	journal	August 1993
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Emergence of adult diarrhoea rotavirus in Calcutta, India Krishnan, T.; Sen, A.; Choudhury, J. Sinha The Lancet, Vol. 353, Issue 9150 https://doi.org/10.1016/S0140-6736(05)74954-0	journal	January 1999
Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis Lahon, Anismrita; Chitambar, Shobha D. Asian Pacific Journal of Tropical Medicine, Vol. 4, Issue 11 https://doi.org/10.1016/S1995-7645(11)60206-X	journal	November 2011
Diversity in Rotavirus–Host Glycan Interactions: A “Sweet” Spectrum Ramani, Sasirekha; Hu, Liya; Venkataram Prasad, B. V. Cellular and Molecular Gastroenterology and Hepatology, Vol. 2, Issue 3 https://doi.org/10.1016/j.jcmgh.2016.03.002	journal	May 2016
Novel Structural Insights into Rotavirus Recognition of Ganglioside Glycan Receptors Yu, Xing; Coulson, Barbara S.; Fleming, Fiona E. Journal of Molecular Biology, Vol. 413, Issue 5 https://doi.org/10.1016/j.jmb.2011.09.005	journal	November 2011
Candidate new rotavirus species in Schreiber's bats, Serbia Bányai, Krisztián; Kemenesi, Gábor; Budinski, Ivana Infection, Genetics and Evolution, Vol. 48 https://doi.org/10.1016/j.meegid.2016.12.002	journal	March 2017
LigPlot+: Multiple Ligand–Protein Interaction Diagrams for Drug Discovery Laskowski, Roman A.; Swindells, Mark B. Journal of Chemical Information and Modeling, Vol. 51, Issue 10 https://doi.org/10.1021/ci200227u	journal	October 2011
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
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
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 I-TASSER Suite: protein structure and function prediction Yang, Jianyi; Yan, Renxiang; Roy, Ambrish Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3213	journal	December 2014
Rotavirus infection Crawford, Sue E.; Ramani, Sasirekha; Tate, Jacqueline E. Nature Reviews Disease Primers, Vol. 3, Issue 1 https://doi.org/10.1038/nrdp.2017.83	journal	November 2017
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
Functional refolding of the penetration protein on a non-enveloped virus Herrmann, Tobias; Torres, Raúl; Salgado, Eric N. Nature, Vol. 590, Issue 7847 https://doi.org/10.1038/s41586-020-03124-4	journal	January 2021
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Highly accurate protein structure prediction for the human proteome Tunyasuvunakool, Kathryn; Adler, Jonas; Wu, Zachary Nature, Vol. 596, Issue 7873 https://doi.org/10.1038/s41586-021-03828-1	journal	July 2021
Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa Viana, Raquel; Moyo, Sikhulile; Amoako, Daniel G. Nature, Vol. 603, Issue 7902 https://doi.org/10.1038/s41586-022-04411-y	journal	January 2022
Porcine rotavirus B as primary causative agent of diarrhea outbreaks in newborn piglets Miyabe, Flavia Megumi; Dall Agnol, Alais Maria; Leme, Raquel Arruda Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-78797-y	journal	December 2020
Improved protein structure prediction using predicted interresidue orientations Yang, Jianyi; Anishchenko, Ivan; Park, Hahnbeom Proceedings of the National Academy of Sciences, Vol. 117, Issue 3 https://doi.org/10.1073/pnas.1914677117	journal	January 2020
Structural basis of P[II] rotavirus evolution and host ranges under selection of histo-blood group antigens Xu, Shenyuan; McGinnis, Kristen Rose; Liu, Yang Proceedings of the National Academy of Sciences, Vol. 118, Issue 36 https://doi.org/10.1073/pnas.2107963118	journal	September 2021
GlycoGlyph: a glycan visualizing, drawing and naming application Mehta, Akul Y.; Cummings, Richard D. Bioinformatics, Vol. 36, Issue 11 https://doi.org/10.1093/bioinformatics/btaa190	journal	March 2020
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
ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules Ashkenazy, Haim; Abadi, Shiran; Martz, Eric Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw408	journal	May 2016
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
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Human Group B Rotavirus Infections Cause Severe Diarrhea in Children and Adults in Bangladesh Sanekata, Takeshi; Ahmed, Muzahed Uddin; Kader, Abdul Journal of Clinical Microbiology, Vol. 41, Issue 5 https://doi.org/10.1128/JCM.41.5.2187-2190.2003	journal	May 2003
Human Group C Rotavirus VP8*s Recognize Type A Histo-Blood Group Antigens as Ligands Sun, Xiaoman; Wang, Lihong; Qi, Jianxun Journal of Virology, Vol. 92, Issue 11 https://doi.org/10.1128/JVI.00442-18	journal	June 2018
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
Prevalence of antibody to group B (atypical) rotavirus in humans and animals Brown, D. W.; Beards, G. M.; Chen, G. M. Journal of Clinical Microbiology, Vol. 25, Issue 2 https://doi.org/10.1128/jcm.25.2.316-319.1987	journal	February 1987
Detection of antibody to group B adult diarrhea rotaviruses in humans Nakata, S.; Estes, M. K.; Graham, D. Y. Journal of Clinical Microbiology, Vol. 25, Issue 5 https://doi.org/10.1128/jcm.25.5.812-818.1987	journal	May 1987
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
Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens Xu, Shenyuan; Ahmed, Luay U.; Stuckert, Michael Robert PLOS Pathogens, Vol. 16, Issue 3 https://doi.org/10.1371/journal.ppat.1008386	journal	March 2020
Species H Rotavirus Detected in Piglets with Diarrhea, Brazil, 2012 Molinari, Bruna L. D.; Lorenzetti, Elis; Otonel, Rodrigo A. A. Emerging Infectious Diseases, Vol. 20, Issue 6 https://doi.org/10.3201/eid2006.130776	journal	June 2014
Identification of a Ruminant Origin Group B Rotavirus Associated with Diarrhea Outbreaks in Foals Uprety, Tirth; Sreenivasan, Chithra C.; Hause, Ben M. Viruses, Vol. 13, Issue 7 https://doi.org/10.3390/v13071330	journal	July 2021

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