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

Hu, Liya; Ramani, Sasirekha; Czako, Rita; Sankaran, Banumathi; Yu, Ying; Smith, David F.; Cummings, Richard D.; Estes, Mary K.; Venkataram Prasad, B. V.

doi:10.1038/ncomms9346

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

Journal Article · Wed Sep 30 00:00:00 EDT 2015 · Nature Communications

DOI:https://doi.org/10.1038/ncomms9346· OSTI ID:1256040

Hu, Liya ^[1]; Ramani, Sasirekha ^[2]; Czako, Rita ^[2]; Sankaran, Banumathi ^[3]; Yu, Ying ^[4]; Smith, David F. ^[4]; Cummings, Richard D. ^[4]; Estes, Mary K. ^[2]; Venkataram Prasad, B. V. ^[5]

Baylor College of Medicine, Houston, TX (United States). Verna and Marrs McLean Department of Biochemistry and Molecular Biology
Baylor College of Medicine, Houston, TX (United States). Department of Molecular Virology and Microbiology
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Emory Univ.School of Medicine, Atlanta, GA (United States)
Baylor College of Medicine, Houston, TX (United States). Verna and Marrs McLean Department of Biochemistry and Molecular Biology; Baylor College of Medicine, Houston, TX (United States). Department of Molecular Virology and Microbiology

We report that strain-dependent variation of glycan recognition during initial cell attachment of viruses is a critical determinant of host specificity, tissue-tropism and zoonosis. Rotaviruses (RVs), which cause life-threatening gastroenteritis in infants and children, display significant genotype-dependent variations in glycan recognition resulting from sequence alterations in the VP8* domain of the spike protein VP4. The structural basis of this genotype-dependent glycan specificity, particularly in human RVs, remains poorly understood. Here, from crystallographic studies, we show how genotypic variations configure a novel binding site in the VP8* of a neonate-specific bovine-human reassortant to uniquely recognize either type I or type II precursor glycans, and to restrict type II glycan binding in the bovine counterpart. In conclusion, such a distinct glycan-binding site that allows differential recognition of the precursor glycans, which are developmentally regulated in the neonate gut and abundant in bovine and human milk provides a basis for age-restricted tropism and zoonotic transmission of G10P[11] rotaviruses.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1256040

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

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
Comparison of viral load and duration of virus shedding in symptomatic and asymptomatic neonatal rotavirus infections Ramani, Sasirekha; Sankaran, Premi; Arumugam, Rajesh Journal of Medical Virology, Vol. 82, Issue 10 https://doi.org/10.1002/jmv.21872	journal	September 2010
Investigating virus–glycan interactions using glycan microarrays Smith, David F.; Cummings, Richard D. Current Opinion in Virology, Vol. 7 https://doi.org/10.1016/j.coviro.2014.05.005	journal	August 2014
Glycan-dependent viral infection in infants and the role of human milk oligosaccharides Etzold, Sabrina; Bode, Lars Current Opinion in Virology, Vol. 7 https://doi.org/10.1016/j.coviro.2014.06.005	journal	August 2014
Whole genome characterization of reassortant G10P[11] strain (N155) from a neonate with symptomatic rotavirus infection: Identification of genes of human and animal rotavirus origin Ramani, Sasirekha; Iturriza-Gomara, Miren; Jana, Atanu Kumar Journal of Clinical Virology, Vol. 45, Issue 3 https://doi.org/10.1016/j.jcv.2009.05.003	journal	July 2009
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
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
Galectin-3 Interactions with Glycosphingolipids Collins, Patrick M.; Bum-Erdene, Khuchtumur; Yu, Xing Journal of Molecular Biology, Vol. 426, Issue 7 https://doi.org/10.1016/j.jmb.2013.12.004	journal	April 2014
Zoonotic aspects of rotaviruses Martella, V.; Bányai, Krisztián; Matthijnssens, Jelle Veterinary Microbiology, Vol. 140, Issue 3-4 https://doi.org/10.1016/j.vetmic.2009.08.028	journal	January 2010
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
Role of environmental poliovirus surveillance in global polio eradication and beyond Hovi, T.; Shulman, L. M.; Van Der Avoort, H. Epidemiology and Infection, Vol. 140, Issue 1 https://doi.org/10.1017/s095026881000316x	journal	August 2011
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
Rotavirus vaccines: recent developments and future considerations Angel, Juana; Franco, Manuel A.; Greenberg, Harry B. Nature Reviews Microbiology, Vol. 5, Issue 7 https://doi.org/10.1038/nrmicro1692	journal	July 2007
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
Structural Characterization by Multistage Mass Spectrometry (MS ⁿ ) of Human Milk Glycans Recognized by Human Rotaviruses Ashline, David J.; Yu, Ying; Lasanajak, Yi Molecular & Cellular Proteomics, Vol. 13, Issue 11 https://doi.org/10.1074/mcp.m114.039925	journal	July 2014
SWEET - WWW-based rapid 3D construction of oligo- and polysaccharides Bohne, A.; Lang, E.; von der Lieth, C. W. Bioinformatics, Vol. 15, Issue 9 https://doi.org/10.1093/bioinformatics/15.9.767	journal	September 1999
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
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
A FUT2 Gene Common Polymorphism Determines Resistance to Rotavirus A of the P[8] Genotype Imbert-Marcille, Berthe-Marie; Barbé, Laure; Dupé, Mathilde The Journal of Infectious Diseases, Vol. 209, Issue 8 https://doi.org/10.1093/infdis/jit655	journal	November 2013
Carbohydrate Structure Suite (CSS): analysis of carbohydrate 3D structures derived from the PDB Lutteke, T. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki013	journal	December 2004
Rotavirus Infection in the Neonatal Nurseries of a Tertiary Care Hospital in India Ramani, Sasirekha; Sowmyanarayanan, Thuppal V.; Gladstone, Beryl Primrose The Pediatric Infectious Disease Journal, Vol. 27, Issue 8 https://doi.org/10.1097/inf.0b013e3181715170	journal	January 2008
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
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
First rotavirus vaccine made in India is launched Travasso, C. BMJ, Vol. 350, Issue mar16 14 https://doi.org/10.1136/bmj.h1475	journal	March 2015
Breast Milk Oligosaccharides: Structure-Function Relationships in the Neonate Smilowitz, Jennifer T.; Lebrilla, Carlito B.; Mills, David A. Annual Review of Nutrition, Vol. 34, Issue 1 https://doi.org/10.1146/annurev-nutr-071813-105721	journal	July 2014
Recent Advances in Studies on Milk Oligosaccharides of Cows and Other Domestic Farm Animals Urashima, Tadasu; Taufik, Epi; Fukuda, Kenji Bioscience, Biotechnology, and Biochemistry, Vol. 77, Issue 3 https://doi.org/10.1271/bbb.120810	journal	March 2013
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
Microbeâ€“Host Interactions are Positively and Negatively Regulated by Galectinâ€“Glycan Interactions Baum, Linda G.; Garner, Omai B.; Schaefer, Katrin Frontiers in Immunology, Vol. 5 https://doi.org/10.3389/fimmu.2014.00284	journal	June 2014
The Predominance of Type I Oligosaccharides Is a Feature Specific to Human Breast Milk Urashima, Tadasu; Asakuma, Sadaki; Leo, Fiame Advances in Nutrition, Vol. 3, Issue 3 https://doi.org/10.3945/an.111.001412	journal	May 2012
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
Effect of Galectins on Viral Transmission Ouellet, Michel; St-Pierre, Christian; Tremblay, Michel J. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-1396-1_26	book	August 2014
Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG) Matthijnssens, Jelle; Ciarlet, Max; McDonald, Sarah M. Archives of Virology, Vol. 156, Issue 8 https://doi.org/10.1007/s00705-011-1006-z	journal	May 2011
ARP⧸wARP and Automatic Interpretation of Protein Electron Density Maps Morris, Richard J.; Perrakis, Anastassis; Lamzin, Victor S. Methods in Enzymology, Vol. 374, p. 229-244 https://doi.org/10.1016/S0076-6879(03)74011-7	book	February 2004
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
The glycan-binding protein galectin-1 controls survival of epithelial cells along the crypt-villus axis of small intestine Muglia, C.; Mercer, N.; Toscano, M. A. Cell Death & Disease, Vol. 2, Issue 5 https://doi.org/10.1038/cddis.2011.44	journal	May 2011
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
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
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
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Why does the Aβ peptide of Alzheimer share structural similarity with antimicrobial peptides? Pastore, Annalisa; Raimondi, Francesco; Rajendran, Lawrence Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-0865-9	journal	March 2020
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
Structural Characterization by Multistage Mass Spectrometry (MS ⁿ ) of Human Milk Glycans Recognized by Human Rotaviruses Ashline, David J.; Yu, Ying; Lasanajak, Yi Molecular & Cellular Proteomics, Vol. 13, Issue 11 https://doi.org/10.1074/mcp.M114.039925	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
LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Wallace, Andrew C.; Laskowski, Roman A.; Thornton, Janet M. "Protein Engineering, Design and Selection", Vol. 8, Issue 2 https://doi.org/10.1093/protein/8.2.127	journal	January 1995
Rotavirus Infection in the Neonatal Nurseries of a Tertiary Care Hospital in India Ramani, Sasirekha; Sowmyanarayanan, Thuppal V.; Gladstone, Beryl Primrose The Pediatric Infectious Disease Journal, Vol. 27, Issue 8 https://doi.org/10.1097/INF.0b013e3181715170	journal	January 2008
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
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
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
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
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
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
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 (14)

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
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
Human milk oligosaccharides, milk microbiome and infant gut microbiome modulate neonatal rotavirus infection Ramani, Sasirekha; Stewart, Christopher J.; Laucirica, Daniel R. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07476-4	journal	November 2018
Development and evaluation of two subunit vaccine candidates containing antigens of hepatitis E virus, rotavirus, and astrovirus Xia, Ming; Wei, Chao; Wang, Leyi Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25735	journal	May 2016
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
Structural basis of glycan specificity of P[19] VP8*: Implications for rotavirus zoonosis and evolution Liu, Yang; Xu, Shenyuan; Woodruff, Andrew L. PLOS Pathogens, Vol. 13, Issue 11 https://doi.org/10.1371/journal.ppat.1006707	journal	November 2017
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
Glycan Microarrays as Chemical Tools for Identifying Glycan Recognition by Immune Proteins Gao, Chao; Wei, Mohui; McKitrick, Tanya R. Frontiers in Chemistry, Vol. 7 https://doi.org/10.3389/fchem.2019.00833	journal	December 2019
Human Milk Oligosaccharides as Promising Antivirals Morozov, Vasily; Hansman, Grant; Hanisch, Franz-Georg Molecular Nutrition & Food Research, Vol. 62, Issue 6 https://doi.org/10.1002/mnfr.201700679	journal	March 2018
“Stuck on sugars – how carbohydrates regulate cell adhesion, recognition, and signaling” Cummings, Richard D. Glycoconjugate Journal, Vol. 36, Issue 4 https://doi.org/10.1007/s10719-019-09876-0	journal	July 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
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
P[8] and P[4] Rotavirus Infection Associated with Secretor Phenotypes Among Children in South China Zhang, Xu-Fu; Long, Yan; Tan, Ming Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34591	journal	October 2016
Generation of Infectious Recombinant Human Rotaviruses from Just 11 Cloned cDNAs Encoding the Rotavirus Genome Komoto, Satoshi; Fukuda, Saori; Kugita, Masanori Journal of Virology, Vol. 93, Issue 8 https://doi.org/10.1128/jvi.02207-18	journal	February 2019

Similar Records

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 of P[19] VP8*: Implications for rotavirus zoonosis and evolution

Journal Article · Mon Nov 13 19:00:00 EST 2017 · PLoS Pathogens · OSTI ID:1627915

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

Journal Article · Wed May 04 20:00:00 EDT 2022 · Communications Biology · OSTI ID:1880816

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (60)

Cited By (14)

Similar Records

Related Subjects