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

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

Abstract

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.

Authors:

^[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)

Publication Date:: Thu May 05 00:00:00 EDT 2022

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

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

OSTI Identifier:: 1880816

Grant/Contract Number:: AC02-05CH11231; AI36040; P30 DK56338; P30 GM124169-01

Resource Type:: Accepted Manuscript

Journal Name:: Communications Biology

Additional Journal Information:: Journal Volume: 5; Journal Issue: 1; Journal ID: ISSN 2399-3642

Publisher:: Springer Nature

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Biochemistry; X-ray crystallography

Citation Formats


                    Hu, Liya, Salmen, Wilhelm, Sankaran, Banumathi, Lasanajak, Yi, Smith, David F., Crawford, Sue E., Estes, Mary K., and Prasad, B. V. Venkataram. Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography.  United States: N. p., 2022. 
Web.  doi:10.1038/s42003-022-03357-1.

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                    Hu, Liya, Salmen, Wilhelm, Sankaran, Banumathi, Lasanajak, Yi, Smith, David F., Crawford, Sue E., Estes, Mary K., & Prasad, B. V. Venkataram. Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography.  United States.  https://doi.org/10.1038/s42003-022-03357-1

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                    Hu, Liya, Salmen, Wilhelm, Sankaran, Banumathi, Lasanajak, Yi, Smith, David F., Crawford, Sue E., Estes, Mary K., and Prasad, B. V. Venkataram. Thu .  
"Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography".  United States.  https://doi.org/10.1038/s42003-022-03357-1.  https://www.osti.gov/servlets/purl/1880816.

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@article{osti_1880816,

  title        = {Novel fold of rotavirus glycan-binding domain predicted by AlphaFold2 and determined by X-ray crystallography},

  author       = {Hu, Liya and Salmen, Wilhelm and Sankaran, Banumathi and Lasanajak, Yi and Smith, David F. and Crawford, Sue E. and Estes, Mary K. and Prasad, B. V. Venkataram},

  abstractNote = {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.},

  doi          = {10.1038/s42003-022-03357-1},

  journal      = {Communications Biology},

  number       = 1,

  volume       = 5,

  place        = {United States},

  year         = {Thu May 05 00:00:00 EDT 2022},

  month        = {Thu May 05 00:00:00 EDT 2022}

}

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Works referenced in this record:

Rotavirus infection
journal, November 2017

Crawford, Sue E.; Ramani, Sasirekha; Tate, Jacqueline E.
Nature Reviews Disease Primers, Vol. 3, Issue 1
DOI: 10.1038/nrdp.2017.83

Detection of antibody to group B adult diarrhea rotaviruses in humans
journal, May 1987

Nakata, S.; Estes, M. K.; Graham, D. Y.
Journal of Clinical Microbiology, Vol. 25, Issue 5
DOI: 10.1128/jcm.25.5.812-818.1987

Emergence of adult diarrhoea rotavirus in Calcutta, India
journal, January 1999

Krishnan, T.; Sen, A.; Choudhury, J. Sinha
The Lancet, Vol. 353, Issue 9150
DOI: 10.1016/S0140-6736(05)74954-0

Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus
journal, September 2015

Hu, Liya; Ramani, Sasirekha; Czako, Rita
Nature Communications, Vol. 6, Issue 1
DOI: 10.1038/ncomms9346

VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation
journal, March 2012

Matthijnssens, Jelle; Otto, Peter H.; Ciarlet, Max
Archives of Virology, Vol. 157, Issue 6
DOI: 10.1007/s00705-012-1273-3

Overview of the CCP 4 suite and current developments
journal, March 2011

Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
DOI: 10.1107/S0907444910045749

AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
journal, December 2009

Morris, Garrett M.; Huey, Ruth; Lindstrom, William
Journal of Computational Chemistry, Vol. 30, Issue 16
DOI: 10.1002/jcc.21256

Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen
journal, April 2012

Hu, Liya; Crawford, Sue E.; Czako, Rita
Nature, Vol. 485, Issue 7397
DOI: 10.1038/nature10996

Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens
journal, March 2020

Xu, Shenyuan; Ahmed, Luay U.; Stuckert, Michael Robert
PLOS Pathogens, Vol. 16, Issue 3
DOI: 10.1371/journal.ppat.1008386

Structural basis of P[II] rotavirus evolution and host ranges under selection of histo-blood group antigens
journal, September 2021

Xu, Shenyuan; McGinnis, Kristen Rose; Liu, Yang
Proceedings of the National Academy of Sciences, Vol. 118, Issue 36
DOI: 10.1073/pnas.2107963118

Coding assignments of the genome of adult diarrhea rotavirus
journal, March 1992

Fang, Z. -Y.; Monroe, S. S.; Dong, H.
Archives of Virology, Vol. 125, Issue 1-4
DOI: 10.1007/BF01309628

Glycan recognition in globally dominant human rotaviruses
journal, July 2018

Hu, Liya; Sankaran, Banumathi; Laucirica, Daniel R.
Nature Communications, Vol. 9, Issue 1
DOI: 10.1038/s41467-018-05098-4

Tracking N-Acetyllactosamine on Cell-Surface Glycans In Vivo
journal, March 2011

Zheng, Tianqing; Jiang, Hao; Gros, Marilyn
Angewandte Chemie International Edition, Vol. 50, Issue 18
DOI: 10.1002/anie.201100265

Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa
journal, January 2022

Viana, Raquel; Moyo, Sikhulile; Amoako, Daniel G.
Nature, Vol. 603, Issue 7902
DOI: 10.1038/s41586-022-04411-y

Functional refolding of the penetration protein on a non-enveloped virus
journal, January 2021

Herrmann, Tobias; Torres, Raúl; Salgado, Eric N.
Nature, Vol. 590, Issue 7847
DOI: 10.1038/s41586-020-03124-4

Unraveling the role of the secretor antigen in human rotavirus attachment to histo-blood group antigens
journal, June 2019

Gozalbo-Rovira, Roberto; Ciges-Tomas, J. Rafael; Vila-Vicent, Susana
PLOS Pathogens, Vol. 15, Issue 6
DOI: 10.1371/journal.ppat.1007865

Features and development of Coot
journal, March 2010

Emsley, P.; Lohkamp, B.; Scott, W. G.
Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
DOI: 10.1107/S0907444910007493

Atomic model of an infectious rotavirus particle: Atomic model of an infectious rotavirus particle
journal, December 2010

Settembre, Ethan C.; Chen, James Z.; Dormitzer, Philip R.
The EMBO Journal, Vol. 30, Issue 2
DOI: 10.1038/emboj.2010.322

Highly accurate protein structure prediction for the human proteome
journal, July 2021

Tunyasuvunakool, Kathryn; Adler, Jonas; Wu, Zachary
Nature, Vol. 596, Issue 7873
DOI: 10.1038/s41586-021-03828-1

Human Group C Rotavirus VP8*s Recognize Type A Histo-Blood Group Antigens as Ligands
journal, June 2018

Sun, Xiaoman; Wang, Lihong; Qi, Jianxun
Journal of Virology, Vol. 92, Issue 11
DOI: 10.1128/JVI.00442-18

Candidate new rotavirus species in Schreiber's bats, Serbia
journal, March 2017

Bányai, Krisztián; Kemenesi, Gábor; Budinski, Ivana
Infection, Genetics and Evolution, Vol. 48
DOI: 10.1016/j.meegid.2016.12.002

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
journal, October 2019

Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L.
Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10
DOI: 10.1107/S2059798319011471

Porcine rotavirus B as primary causative agent of diarrhea outbreaks in newborn piglets
journal, December 2020

Miyabe, Flavia Megumi; Dall Agnol, Alais Maria; Leme, Raquel Arruda
Scientific Reports, Vol. 10, Issue 1
DOI: 10.1038/s41598-020-78797-y

Three-dimensional visualization of the rotavirus hemagglutinin structure
journal, August 1993

Shaw, A. L.; Rothnagel, R.; Chen, D.
Cell, Vol. 74, Issue 4
DOI: 10.1016/0092-8674(93)90516-S

Highly accurate protein structure prediction with AlphaFold
journal, July 2021

Jumper, John; Evans, Richard; Pritzel, Alexander
Nature
DOI: 10.1038/s41586-021-03819-2

Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis
journal, November 2011

Lahon, Anismrita; Chitambar, Shobha D.
Asian Pacific Journal of Tropical Medicine, Vol. 4, Issue 11
DOI: 10.1016/S1995-7645(11)60206-X

Using Dali for Protein Structure Comparison
book, January 2020

Holm, Liisa
Methods in Molecular Biology
DOI: 10.1007/978-1-0716-0270-6_3

Improved protein structure prediction using predicted interresidue orientations
journal, January 2020

Yang, Jianyi; Anishchenko, Ivan; Park, Hahnbeom
Proceedings of the National Academy of Sciences, Vol. 117, Issue 3
DOI: 10.1073/pnas.1914677117

Diversity in Rotavirus–Host Glycan Interactions: A “Sweet” Spectrum
journal, May 2016

Ramani, Sasirekha; Hu, Liya; Venkataram Prasad, B. V.
Cellular and Molecular Gastroenterology and Hepatology, Vol. 2, Issue 3
DOI: 10.1016/j.jcmgh.2016.03.002

Identification of a Ruminant Origin Group B Rotavirus Associated with Diarrhea Outbreaks in Foals
journal, July 2021

Uprety, Tirth; Sreenivasan, Chithra C.; Hause, Ben M.
Viruses, Vol. 13, Issue 7
DOI: 10.3390/v13071330

The I-TASSER Suite: protein structure and function prediction
journal, December 2014

Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
Nature Methods, Vol. 12, Issue 1
DOI: 10.1038/nmeth.3213

GlycoGlyph: a glycan visualizing, drawing and naming application
journal, March 2020

Mehta, Akul Y.; Cummings, Richard D.
Bioinformatics, Vol. 36, Issue 11
DOI: 10.1093/bioinformatics/btaa190

Novel Structural Insights into Rotavirus Recognition of Ganglioside Glycan Receptors
journal, November 2011

Yu, Xing; Coulson, Barbara S.; Fleming, Fiona E.
Journal of Molecular Biology, Vol. 413, Issue 5
DOI: 10.1016/j.jmb.2011.09.005

ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules
journal, May 2016

Ashkenazy, Haim; Abadi, Shiran; Martz, Eric
Nucleic Acids Research, Vol. 44, Issue W1
DOI: 10.1093/nar/gkw408

LigPlot+: Multiple Ligand–Protein Interaction Diagrams for Drug Discovery
journal, October 2011

Laskowski, Roman A.; Swindells, Mark B.
Journal of Chemical Information and Modeling, Vol. 51, Issue 10
DOI: 10.1021/ci200227u

The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site
journal, March 2002

Dormitzer, P. R.
The EMBO Journal, Vol. 21, Issue 5
DOI: 10.1093/emboj/21.5.885

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

Human Group B Rotavirus Infections Cause Severe Diarrhea in Children and Adults in Bangladesh
journal, May 2003

Sanekata, Takeshi; Ahmed, Muzahed Uddin; Kader, Abdul
Journal of Clinical Microbiology, Vol. 41, Issue 5
DOI: 10.1128/JCM.41.5.2187-2190.2003

[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997

Otwinowski, Zbyszek; Minor, Wladek
Macromolecular Crystallography Part A, 307-326
DOI: 10.1016/S0076-6879(97)76066-X

Prevalence of antibody to group B (atypical) rotavirus in humans and animals
journal, February 1987

Brown, D. W.; Beards, G. M.; Chen, G. M.
Journal of Clinical Microbiology, Vol. 25, Issue 2
DOI: 10.1128/jcm.25.2.316-319.1987

Species H Rotavirus Detected in Piglets with Diarrhea, Brazil, 2012
journal, June 2014

Molinari, Bruna L. D.; Lorenzetti, Elis; Otonel, Rodrigo A. A.
Emerging Infectious Diseases, Vol. 20, Issue 6
DOI: 10.3201/eid2006.130776

Detection of group B rotavirus in an adult with acute gastroenteritis in Yangon, Myanmar
journal, November 2009

Aung, Tin Sabai; Kobayashi, Nobumichi; Nagashima, Shigeo
Journal of Medical Virology, Vol. 81, Issue 11
DOI: 10.1002/jmv.21613

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

Abstract

Citation Formats

Rotavirus infection journal, November 2017

Detection of antibody to group B adult diarrhea rotaviruses in humans journal, May 1987

Emergence of adult diarrhoea rotavirus in Calcutta, India journal, January 1999

Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus journal, September 2015

VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation journal, March 2012

Overview of the CCP 4 suite and current developments journal, March 2011

AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility journal, December 2009

Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen journal, April 2012

Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens journal, March 2020

Structural basis of P[II] rotavirus evolution and host ranges under selection of histo-blood group antigens journal, September 2021

Coding assignments of the genome of adult diarrhea rotavirus journal, March 1992

Glycan recognition in globally dominant human rotaviruses journal, July 2018

Tracking N-Acetyllactosamine on Cell-Surface Glycans In Vivo journal, March 2011

Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa journal, January 2022

Functional refolding of the penetration protein on a non-enveloped virus journal, January 2021

Unraveling the role of the secretor antigen in human rotavirus attachment to histo-blood group antigens journal, June 2019

Features and development of Coot journal, March 2010

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Highly accurate protein structure prediction for the human proteome journal, July 2021

Human Group C Rotavirus VP8*s Recognize Type A Histo-Blood Group Antigens as Ligands journal, June 2018

Candidate new rotavirus species in Schreiber's bats, Serbia journal, March 2017

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Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis journal, November 2011

Using Dali for Protein Structure Comparison book, January 2020

Improved protein structure prediction using predicted interresidue orientations journal, January 2020

Diversity in Rotavirus–Host Glycan Interactions: A “Sweet” Spectrum journal, May 2016

Identification of a Ruminant Origin Group B Rotavirus Associated with Diarrhea Outbreaks in Foals journal, July 2021

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GlycoGlyph: a glycan visualizing, drawing and naming application journal, March 2020

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LigPlot+: Multiple Ligand–Protein Interaction Diagrams for Drug Discovery journal, October 2011

The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site journal, March 2002

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

Human Group B Rotavirus Infections Cause Severe Diarrhea in Children and Adults in Bangladesh journal, May 2003

[20] Processing of X-ray diffraction data collected in oscillation mode book, January 1997

Prevalence of antibody to group B (atypical) rotavirus in humans and animals journal, February 1987

Species H Rotavirus Detected in Piglets with Diarrhea, Brazil, 2012 journal, June 2014

Detection of group B rotavirus in an adult with acute gastroenteritis in Yangon, Myanmar journal, November 2009

Rotavirus infection
journal, November 2017

Detection of antibody to group B adult diarrhea rotaviruses in humans
journal, May 1987

Emergence of adult diarrhoea rotavirus in Calcutta, India
journal, January 1999

Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus
journal, September 2015

VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation
journal, March 2012

Overview of the CCP 4 suite and current developments
journal, March 2011

AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility
journal, December 2009

Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen
journal, April 2012

Molecular basis of P[II] major human rotavirus VP8* domain recognition of histo-blood group antigens
journal, March 2020

Structural basis of P[II] rotavirus evolution and host ranges under selection of histo-blood group antigens
journal, September 2021

Coding assignments of the genome of adult diarrhea rotavirus
journal, March 1992

Glycan recognition in globally dominant human rotaviruses
journal, July 2018

Tracking N-Acetyllactosamine on Cell-Surface Glycans In Vivo
journal, March 2011

Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa
journal, January 2022

Functional refolding of the penetration protein on a non-enveloped virus
journal, January 2021

Unraveling the role of the secretor antigen in human rotavirus attachment to histo-blood group antigens
journal, June 2019

Features and development of Coot
journal, March 2010

Atomic model of an infectious rotavirus particle: Atomic model of an infectious rotavirus particle
journal, December 2010

Highly accurate protein structure prediction for the human proteome
journal, July 2021

Human Group C Rotavirus VP8*s Recognize Type A Histo-Blood Group Antigens as Ligands
journal, June 2018

Candidate new rotavirus species in Schreiber's bats, Serbia
journal, March 2017

Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix
journal, October 2019

Porcine rotavirus B as primary causative agent of diarrhea outbreaks in newborn piglets
journal, December 2020

Three-dimensional visualization of the rotavirus hemagglutinin structure
journal, August 1993

Highly accurate protein structure prediction with AlphaFold
journal, July 2021

Molecular characterization of VP4, VP6, VP7 and NSP4 genes of group B rotavirus strains from outbreaks of gastroenteritis
journal, November 2011

Using Dali for Protein Structure Comparison
book, January 2020

Improved protein structure prediction using predicted interresidue orientations
journal, January 2020

Diversity in Rotavirus–Host Glycan Interactions: A “Sweet” Spectrum
journal, May 2016

Identification of a Ruminant Origin Group B Rotavirus Associated with Diarrhea Outbreaks in Foals
journal, July 2021

The I-TASSER Suite: protein structure and function prediction
journal, December 2014

GlycoGlyph: a glycan visualizing, drawing and naming application
journal, March 2020

Novel Structural Insights into Rotavirus Recognition of Ganglioside Glycan Receptors
journal, November 2011

ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules
journal, May 2016

LigPlot+: Multiple Ligand–Protein Interaction Diagrams for Drug Discovery
journal, October 2011

The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site
journal, March 2002

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

Human Group B Rotavirus Infections Cause Severe Diarrhea in Children and Adults in Bangladesh
journal, May 2003

[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997

Prevalence of antibody to group B (atypical) rotavirus in humans and animals
journal, February 1987

Species H Rotavirus Detected in Piglets with Diarrhea, Brazil, 2012
journal, June 2014

Detection of group B rotavirus in an adult with acute gastroenteritis in Yangon, Myanmar
journal, November 2009