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

Nature Communications

Volumn 6, Issue , 2015, Pages

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

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; PROTEIN VP4; PROTEIN VP8; UNCLASSIFIED DRUG; VIRUS PROTEIN; POLYSACCHARIDE; VIRAL PROTEIN; VIRUS RECEPTOR;

CELLS AND CELL COMPONENTS; CHILD HEALTH; DISEASE TRANSMISSION; GASTROENTERITIS; GENETIC VARIATION; GENOTYPE; MILK; NEONATE; POLYSACCHARIDE; PROTEIN; UNGULATE; VIRUS;

ARTICLE; BINDING SITE; BREAST MILK; CELL ADHESION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC REASSORTMENT; GENETIC VARIABILITY; HOST RANGE; HUMAN; HYDROGEN BOND; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PURIFICATION; ROTAVIRUS; TROPISM; ANIMAL; BOVINE; CATTLE DISEASE; CHEMISTRY; GASTROENTERITIS; GENETICS; METABOLISM; ROTAVIRUS INFECTION; SPECIES DIFFERENCE; VETERINARY; VIROLOGY;

BOVINAE; ROTAVIRUS;

ANIMALS; CATTLE; CATTLE DISEASES; GASTROENTERITIS; HUMANS; POLYSACCHARIDES; REASSORTANT VIRUSES; RECEPTORS, VIRUS; ROTAVIRUS; ROTAVIRUS INFECTIONS; SPECIES SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84942888046     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9346     Document Type: Article

References (50)

1. Stencel-Baerenwald, J. E., Reiss, K., Reiter, D. M., Stehle, T., Dermody, T. S. The sweet spot: defining virus-sialic acid interactions. Nat. Rev. Microbiol. 12, 739-749 (2014).
2. Smith, D. F., Cummings, R. D. Investigating virus-glycan interactions using glycan microarrays. Curr. Opin. Virol. 7, 79-87 (2014).
3. Tate, J. E. et al. 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. Lancet Infect. Dis. 12, 136-141 (2012).
4. Estes, M. K., Greenberg, H. B. in Fields Virology (eds Knipe, D. M. et al.) 1347-1401 (Lippincott Williams & Wilkins, 2013).
5. Martella, V., Banyai, K., Matthijnssens, J., Buonavoglia, C., Ciarlet, M. Zoonotic aspects of rotaviruses. Vet. Microbiol. 140, 246-255 (2010).
6. Midgley, S. E., Hjulsager, C. K., Larsen, L. E., Falkenhorst, G., Bottiger, B. Suspected zoonotic transmission of rotavirus group A in Danish adults. Epidemiol. Infect. 140, 1-5 (2011).
7. Angel, J., Franco, M. A., Greenberg, H. B. Rotavirus vaccines: recent developments and future considerations. Nat. Rev. Microbiol. 5, 529-539 (2007).
8. Matthijnssens, J. et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch. Virol. 156, 1397-1413 (2011).
9. Trojnar, E. et al. Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J. Gen. Virol. 94, 136-142 (2013).
10. Haselhorst, T. et al. Sialic acid dependence in rotavirus host cell invasion. Nat. Chem. Biol. 5, 91-93 (2009).
11. Blanchard, H., Yu, X., Coulson, B. S., von Itzstein, M. Insight into host cell carbohydrate-recognition by human and porcine rotavirus from crystal structures of the virion spike associated carbohydrate-binding domain (VP8∗). J. Mol. Biol. 367, 1215-1226 (2007).
12. Dormitzer, P. R., Sun, Z. Y., Wagner, G., Harrison, S. C. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 21, 885-897 (2002).
13. Bohm, R. et al. Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat. Commun. 6, 5907 (2015).
14. Hu, L. et al. Cell attachment protein VP8∗of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485, 256-259 (2012).
15. Huang, P. et al. Spike protein VP8∗of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 86, 4833-4843 (2012).
16. Nordgren, J. et al. Both lewis and secretor status mediate susceptibility to rotavirus infections in a rotavirus genotype-dependent manner. Clin. Infect. Dis. 59, 1567-1573 (2014).
17. Imbert-Marcille, B. M. et al. A FUT2 gene common polymorphism determines resistance to rotavirus A of the P[8] genotype. J. Infect. Dis. 209, 1227-1230 (2014).
18. Ramani, S. et al. Rotavirus infection in the neonatal nurseries of a tertiary care hospital in India. Pediatr. Infect. Dis. J. 27, 719-723 (2008).
19. Ramani, S. et al. Comparison of viral load and duration of virus shedding in symptomatic and asymptomatic neonatal rotavirus infections. J. Med. Virol. 82, 1803-1807 (2010).
20. Travasso, C. First rotavirus vaccine made in India is launched. BMJ 350, h1475 (2015).
21. Ramani, S. et al. The VP8∗domain of neonatal rotavirus strain G10P[11] binds to type II precursor glycans. J. Virol. 87, 7255-7264 (2013).
22. Liu, Y. et al. Poly-LacNAc as an age-specific ligand for rotavirus P[11] in neonates and infants. PLoS One 8, e78113 (2013).
23. Yu, Y. et al. Human milk contains novel glycans that are potential decoy receptors for neonatal rotaviruses. Mol. Cell. Proteomics 13, 2944-2960 (2014).
24. Ashline, D. J. et al. Structural characterization by multistage mass spectrometry (MSn) of human milk glycans recognized by human rotaviruses. Mol. Cell. Proteomics 13, 2961-2974 (2014).
25. Etzold, S., Bode, L. Glycan-dependent viral infection in infants and the role of human milk oligosaccharides. Curr. Opin. Virol. 7C, 101-107 (2014).
26. Stanley, P., Cummings, R. Structures Common to Different Glycans: Essentials of Glycobiology (Cold Spring Harbor Laboratory, 2009).
27. Monnier, N. et al. High-resolution molecular and antigen structure of the VP8∗core of a sialic acid-independent human rotavirus strain. J. Virol. 80, 1513-1523 (2006).
28. Ramani, S. et al. 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. J. Clin. Virol. 45, 237-244 (2009).
29. Morris, G. M. et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791 (2009).
30. Yu, X. et al. Novel structural insights into rotavirus recognition of ganglioside glycan receptors. J. Mol. Biol. 413, 929-939 (2011).
31. Smilowitz, J. T., Lebrilla, C. B., Mills, D. A., German, J. B., Freeman, S. L. Breast milk oligosaccharides: structure-function relationships in the neonate. Annu. Rev. Nutr. 34, 143-169 (2014).
32. Urashima, T. et al. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv. Nutr. 3, 473S-482SS (2012).
33. Urashima, T., Taufik, E., Fukuda, K., Asakuma, S. Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci. Biotechnol. Biochem. 77, 455-466 (2013).
34. Muglia, C. et al. The glycan-binding protein galectin-1 controls survival of epithelial cells along the crypt-villus axis of small intestine. Cell Death Dis. 2, e163 (2011).
35. Krzeslak, A., Lipinska, A. Galectin-3 as a multifunctional protein. Cell Mol. Biol. Lett. 9, 305-328 (2004).
36. Collins, P. M., Bum-Erdene, K., Yu, X., Blanchard, H. Galectin-3 interactions with glycosphingolipids. J. Mol. Biol. 426, 1439-1451 (2013).
37. Baum, L. G., Garner, O. B., Schaefer, K., Lee, B. Microbe-host interactions are positively and negatively regulated by galectin-glycan interactions. Front. Immunol. 5, 284 (2014).
38. Ouellet, M., St-Pierre, C., Tremblay, M. J., Sato, S. Effect of galectins on viral transmission. Methods Mol. Biol. 1207, 397-420 (2015).
39. Wilkins, M. R. et al. Protein identification and analysis tools in the ExPASy server. Methods Mol. Biol. 112, 531-552 (1999).
40. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
41. Evans, P. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62, 72-82 (2006).
42. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
43. Morris, R. J., Perrakis, A., Lamzin, V. S. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol. 374, 229-244 (2003).
44. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
45. Emsley, P., Lohkamp, B., Scott, W. G., Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
46. Bohne, A., Lang, E., von der Lieth, C. W. SWEET-WWW-based rapid 3D construction of oligo-and polysaccharides. Bioinformatics 15, 767-768 (1999).
47. Lutteke, T., Frank, M., von der Lieth, C. W. Carbohydrate Structure Suite (CSS): analysis of carbohydrate 3D structures derived from the PDB. Nucleic Acids Res. 33, D242-D246 (2005).
48. Wallace, A. C., Laskowski, R. A., Thornton, J. M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-134 (1995).
49. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
50. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., Barton, G. J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191 (2009).