Trisaccharide containing α2,3-linked sialic acid is a receptor for mumps virus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 41, 2016, Pages 11579-11584

  Kubota, Marie ^a   Takeuchi, Kaoru ^b   Watanabe, Shumpei ^a   Ohno, Shinji ^a   Matsuoka, Rei ^c   Kohda, Daisuke ^c   Nakakita, Shin Ichi ^d   Hiramatsu, Hiroaki ^e   Suzuki, Yasuo ^e   Nakayama, Tetsuo ^f   Terada, Tohru ^g   Shimizu, Kentaro ^g   Shimizu, Nobutaka ^h   Shiroishi, Mitsunori ^c   Yanagi, Yusuke ^a   Hashiguchi, Takao ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d KAGAWA UNIVERSITY   (Japan)

^e CHUBU UNIVERSITY   (Japan)

^f KITASATO UNIVERSITY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h INSTITUTE OF MATERIALS STRUCTURE SCIENCE   (Japan)

Author keywords

Entry; Infection; Paramyxovirus; Receptor; Structure

Indexed keywords

ALANINE; ALPHA 2,3 LINKED SIALIC ACID; GLYCAN; HEMAGGLUTININ; HN PROTEIN; NEUTRALIZING ANTIBODY; SIALIC ACID DERIVATIVE; SIALIDASE; SUGAR; TRISACCHARIDE; UNCLASSIFIED DRUG; VIRUS RECEPTOR; EPITOPE; LACTOSE; MUTANT PROTEIN; N ACETYLNEURAMINIC ACID; PROTEIN BINDING; VIRAL PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BINDING ASSAY; CALCULATION; CELL FUSION; CENTRAL NERVOUS SYSTEM; CRYSTAL STRUCTURE; ENERGY; FEMALE; GENOTYPE; GLAND TISSUE; HUMAN; HUMAN CELL; ISOTHERMAL TITRATION CALORIMETRY; MUMPS VIRUS; NONHUMAN; PARAMYXOVIRIDAE; PRIORITY JOURNAL; TROPISM; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; HEK293 CELL LINE; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; THERMODYNAMICS; VERO CELL LINE; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIBODIES, NEUTRALIZING; CELL FUSION; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CRYSTALLOGRAPHY, X-RAY; EPITOPES; HEK293 CELLS; HUMANS; LACTOSE; MODELS, MOLECULAR; MUMPS VIRUS; MUTANT PROTEINS; N-ACETYLNEURAMINIC ACID; PROTEIN BINDING; PROTEIN DOMAINS; RECEPTORS, VIRUS; THERMODYNAMICS; TRISACCHARIDES; VERO CELLS; VIRAL PROTEINS;

EID: 84991493933     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1608383113     Document Type: Article

References (44)

1. Rubin SA, Sauder CJ, Carbone KM (2013) Mumps virus. Fields Virology, eds Knipe DM, et al. (Lippincott Williams & Wilkins, Philadelphia), 6th Ed, Vol I, pp 1024-1041.
2. Griffin DE (2013) Measles virus. Fields Virology, eds Knipe DM, et al. (Lippincott Williams & Wilkins, Philadelphia), 6th Ed, Vol I, pp 1042-1069.
3. Cong H, Jiang Y, Tien P (2011) Identification of the myelin oligodendrocyte glycoprotein as a cellular receptor for rubella virus. J Virol 85(21):11038-11047.
4. DuBois RM, et al. (2013) Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature 493(7433):552-556.
5. Latner DR, Hickman CJ (2015) Remembering mumps. PLoS Pathog 11(5):e1004791.
6. Yoshida N, et al. (2008) Mumps virus reinfection is not a rare event confirmed by reverse transcription loop-mediated isothermal amplification. J Med Virol 80(3):517-523.
7. Rubin SA, et al. (2012) Recent mumps outbreaks in vaccinated populations: No evidence of immune escape. J Virol 86(1):615-620.
8. Örvell C, Alsheikhly AR, Kalantari M, Johansson B (1997) Characterization of genotype-specific epitopes of the HN protein of mumps virus. J Gen Virol 78(Pt 12):3187-3193.
9. Rydbeck R, Löve A, Örvell C, Norrby E (1986) Antigenic variation of envelope and internal proteins of mumps virus strains detected with monoclonal antibodies. J Gen Virol 67(Pt 2):281-287.
10. Lamb RA, Parks GD (2013) Paramyxoviridae. Fields Virology, eds Knipe DM, et al. (Lippincott Williams & Wilkins, Philadelphia), 6th Ed, Vol I, pp 957-995.
11. Wright PF, Neumann G, Kawaoka Y (2013) Orthomyxoviruses. Fields Virology, eds Knipe DM, et al. (Lippincott Williams & Wilkins, Philadelphia), 6th Ed, Vol I, pp 1186-1243.
12. Reeves PJ, Callewaert N, Contreras R, Khorana HG (2002) Structure and function in rhodopsin: High-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci USA 99(21):13419-13424.
13. Walter TS, et al. (2006) Lysine methylation as a routine rescue strategy for protein crystallization. Structure 14(11):1617-1622.
14. Crennell S, Takimoto T, Portner A, Taylor G (2000) Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 7(11):1068-1074.
15. Hashiguchi T, et al. (2007) Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc Natl Acad Sci USA 104(49):19535-19540.
16. Yuan P, et al. (2005) Structural studies of the parainfluenza virus 5 hemagglutininneuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13(5):803-815.
17. Lawrence MC, et al. (2004) Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 335(5):1343-1357.
18. Colman PM, Hoyne PA, Lawrence MC (1993) Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J Virol 67(6):2972-2980.
19. Nakakita S, Hirabayashi J (2016) Preparation of glycan arrays using pyridylaminated glycans. Methods Mol Biol 1368:225-235.
20. Imamura T, et al. (2014) Antigenic and receptor binding properties of enterovirus 68. J Virol 88(5):2374-2384.
21. Walther T, et al. (2013) Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection. PLoS Pathog 9(3):e1003223.
22. Tateno H, et al. (2008) Glycoconjugate microarray based on an evanescent-field fluorescence-assisted detection principle for investigation of glycan-binding proteins. Glycobiology 18(10):789-798.
23. Inou Y, et al. (2004) Molecular epidemiology of mumps virus in Japan and proposal of two new genotypes. J Med Virol 73(1):97-104.
24. Totani K, et al. (2003) Chemoenzymatic synthesis and application of glycopolymers containing multivalent sialyloligosaccharides with a poly (L-glutamic acid) backbone for inhibition of infection by influenza viruses. Glycobiology 13(5):315-326.
25. Varki A, et al. (2009) Essentials of Glycobiology (Cold Spring Harbor, New York), 2nd Ed.
26. Kövamees J, Rydbeck R, Orvell C, Norrby E (1990) Hemagglutinin-neuraminidase (HN) amino acid alterations in neutralization escape mutants of Kilham mumps virus. Virus Res 17(2):119-129.
27. Cusi MG, et al. (2001) Localization of a new neutralizing epitope on the mumps virus hemagglutinin-neuraminidase protein. Virus Res 74(1-2):133-137.
28. Ziegler D, et al. (1996) Protection against measles virus encephalitis by monoclonal antibodies binding to a cystine loop domain of the H protein mimicked by peptides which are not recognized by maternal antibodies. J Gen Virol 77(Pt 10):2479-2489.
29. Hashiguchi T, et al. (2011) Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat Struct Mol Biol 18(2):135-141.
30. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4(3):435-447.
31. Ninomiya K, et al. (2009) Amino acid substitution at position 464 in the haemagglutinin-neuraminidase protein of a mumps virus Urabe strain enhanced the virus growth in neuroblastoma SH-SY5Y cells. Vaccine 27(44):6160-6165.
32. Rawling J, García-Barreno B, Melero JA (2008) Insertion of the two cleavage sites of the respiratory syncytial virus fusion protein in Sendai virus fusion protein leads to enhanced cell-cell fusion and a decreased dependency on the HN attachment protein for activity. J Virol 82(12):5986-5998.
33. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
34. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674.
35. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
36. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
37. Case DA, et al. (2012) AMBER 12 Reference Manual (University of California San Francisco, San Francisco).
38. Kirschner KN, et al. (2008) GLYCAM06: A generalizable biomolecular force field. Carbohydrates. J Comput Chem 29(4):622-655.
39. Bennett CH (1976) Efficient estimation of free energy differences from Monte Carlo data. J Comput Phys 22(2):245-268.
40. Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126(1):0-4101.
41. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81(8):3684-3690.
42. Hess B (2008) P-LINCS: A parallel linear constraint solver for molecular simulation. J Chem Theory Comput 4(1):116-122.
43. Essmann U, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103(19):8577-8593.
44. Yamada A, Takeuchi K, Hishiyama M (1988) Intracellular processing of mumps virus glycoproteins. Virology 165(1):268-273.