Molecular recognition of human ephrinB2 cell surface receptor by an emergent African henipavirus

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

Volumn 112, Issue 17, 2015, Pages E2156-E2165

  Lee, Benhur ^a   Pernet, Olivier ^b   Ahmed, Asim A ^c   Zeltina, Antra ^d   Beaty, Shannon M ^a   Bowden, Thomas A ^d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Emerging virus; Glycoprotein; Henipavirus; Structure; Viral attachment

Indexed keywords

CELL SURFACE RECEPTOR; EPHRINB2; GLYCOPROTEIN; HEMAGGLUTININ; HN PROTEIN; UNCLASSIFIED DRUG; EPHRIN B2; EPHRIN B3; VIRAL PROTEIN;

AFRICAN; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; CROSS REACTION; CRYSTAL STRUCTURE; DISULFIDE BOND; GENETIC CONSERVATION; GLYCOSYLATION; HENDRA VIRUS; HENIPAVIRUS; HUMAN; HYDROGEN BOND; MOLECULAR RECOGNITION; NIPAH VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SITE DIRECTED MUTAGENESIS; VIRUS PARTICLE; WILD TYPE; CHEMISTRY; GENETICS; HEK293 CELL LINE; HENIPAVIRUS INFECTION; METABOLISM; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; VIRUS ENTRY;

HENDRA VIRUS; HENIPAVIRUS; NIPAH VIRUS;

EPHRIN-B2; EPHRIN-B3; HEK293 CELLS; HENIPAVIRUS; HENIPAVIRUS INFECTIONS; HUMANS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84928559944     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501690112     Document Type: Article

References (72)

1. Eaton BT, Broder CC, Middleton D, Wang LF (2006) Hendra and Nipah viruses: Different and dangerous. Nat Rev Microbiol 4(1):23-35.
2. Drexler JF, et al. (2012) Bats host major mammalian paramyxoviruses. Nat Commun 3:796.
3. Marsh GA, et al. (2012) Cedar virus: A novel Henipavirus isolated from Australian bats. PLoS Pathog 8(8):e1002836.
4. Breed AC, et al. (2013) The distribution of henipaviruses in Southeast Asia and Australasia: Is Wallace's line a barrier to Nipah virus? PLoS ONE 8(4):e61316.
5. Halpin K, et al.; Henipavirus Ecology Research Group (2011) Pteropid bats are confirmed as the reservoir hosts of henipaviruses: A comprehensive experimental study of virus transmission. Am J Trop Med Hyg 85(5):946-951.
6. Chua KB, et al. (1999) Fatal encephalitis due to Nipah virus among pig-farmers in Malaysia. Lancet 354(9186):1257-1259.
7. Gurley ES, et al. (2007) Person-to-person transmission of Nipah virus in a Bangladeshi community. Emerg Infect Dis 13(7):1031-1037.
8. Blum LS, Khan R, Nahar N, Breiman RF (2009) In-depth assessment of an outbreak of Nipah encephalitis with person-to-person transmission in Bangladesh: Implications for prevention and control strategies. Am J Trop Med Hyg 80(1):96-102.
9. Wu Z, et al. (2014) Novel Henipa-like virus, Mojiang Paramyxovirus, in rats, China, 2012. Emerg Infect Dis 20(6):1064-1066.
10. Iehlé C, et al. (2007) Henipavirus and Tioman virus antibodies in pteropodid bats, Madagascar. Emerg Infect Dis 13(1):159-161.
11. Peel AJ, et al. (2013) Continent-wide panmixia of an African fruit bat facilitates transmission of potentially zoonotic viruses. Nat Commun 4:2770.
12. Pernet O, et al. (2014) Evidence for henipavirus spillover into human populations in Africa. Nat Commun 5:5342.
13. Mathers CD, Ezzati M, Lopez AD (2007) Measuring the burden of neglected tropical diseases: The global burden of disease framework. PLoS Negl Trop Dis 1(2):e114.
14. Hayman DT, et al. (2008) Evidence of henipavirus infection in West African fruit bats. PLoS ONE 3(7):e2739.
15. Lee B, Ataman ZA (2011) Modes of paramyxovirus fusion: A Henipavirus perspective. Trends Microbiol 19(8):389-399.
16. Pernet O, Wang YE, Lee B (2012) Henipavirus receptor usage and tropism. Curr Top Microbiol Immunol 359:59-78.
17. Hafner C, et al. (2004) Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin Chem 50(3):490-499.
18. Pasquale EB (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6(6):462-475.
19. Negrete OA, et al. (2006) Two key residues in ephrinB3 are critical for its use as an alternative receptor for Nipah virus. PLoS Pathog 2(2):e7.
20. Negrete OA, et al. (2005) EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436(7049):401-405.
21. Bonaparte MI, et al. (2005) Ephrin-B2 ligand is a functional receptor for Hendra virus and Nipah virus. Proc Natl Acad Sci USA 102(30):10652-10657.
22. Bowden TA, et al. (2008) Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat Struct Mol Biol 15(6):567-572.
23. Bowden TA, et al. (2008) Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: A template for antiviral and vaccine design. J Virol 82(23):11628-11636.
24. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI (2010) Dimeric architecture of the Hendra virus attachment glycoprotein: Evidence for a conserved mode of assembly. J Virol 84(12):6208-6217.
25. Bowden TA, Jones EY, Stuart DI (2011) Cells under siege: Viral glycoprotein interactions at the cell surface. J Struct Biol 175(2):120-126.
26. Xu K, et al. (2008) Host cell recognition by the henipaviruses: Crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc Natl Acad Sci USA 105(29):9953-9958.
27. Pernet O, Beaty S, Lee B (2014) Functional rectification of the newly described African henipavirus fusion glycoprotein (Gh-M74a). J Virol 88(9):5171-5176.
28. Weis M, et al. (2014) Characterization of African bat henipavirus GH-M74a glycoproteins. J Gen Virol 95(Pt 3):539-548.
29. Hurchla MA, et al. (2013) The epoxyketone-based proteasome inhibitors carfilzomib and orally bioavailable oprozomib have anti-resorptive and bone-anabolic activity in addition to anti-myeloma effects. Leukemia 27(2):430-440.
30. Welch BD, et al. (2013) Structure of the parainfluenza virus 5 (PIV5) hemagglutinin-neuraminidase (HN) ectodomain. PLoS Pathog 9(8):e1003534.
31. Yuan P, et al. (2011) Structure of the Newcastle disease virus hemagglutinin-neuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc Natl Acad Sci USA 108(36):14920-14925.
32. Crennell S, Takimoto T, Portner A, Taylor G (2000) Crystal structure of the multi-functional paramyxovirus hemagglutinin-neuraminidase. Nat Struct Biol 7(11):1068-1074.
33. Lawrence MC, et al. (2004) Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J Mol Biol 335(5):1343-1357.
34. Yuan P, et al. (2005) Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13(5):803-815.
35. Bishop KA, et al. (2008) Residues in the stalk domain of the hendra virus g glycoprotein modulate conformational changes associated with receptor binding. J Virol 82(22):11398-11409.
36. Morrison TG (1988) Structure, function, and intracellular processing of paramyxovirus membrane proteins. Virus Res 10(2-3):113-135.
37. Markwell MA, Fox CF (1980) Protein-protein interactions within paramyxoviruses identified by native disulfide bonding or reversible chemical cross-linking. J Virol 33(1):152-166.
38. Parks GD, Lamb RA (1990) Folding and oligomerization properties of a soluble and secreted form of the paramyxovirus hemagglutinin-neuraminidase glycoprotein. Virology 178(2):498-508.
39. Thompson SD, Laver WG, Murti KG, Portner A (1988) Isolation of a biologically active soluble form of the hemagglutinin-neuraminidase protein of Sendai virus. J Virol 62(12):4653-4660.
40. Yuan P, Leser GP, Demeler B, Lamb RA, Jardetzky TS (2008) Domain architecture and oligomerization properties of the paramyxovirus PIV 5 hemagglutinin-neuraminidase (HN) protein. Virology 378(2):282-291.
41. Bowden TA, Crispin M, Jones EY, Stuart DI (2010) Shared paramyxoviral glycoprotein architecture is adapted for diverse attachment strategies. Biochem Soc Trans 38(5):1349-1355.
42. Chothia C, Lesk AM (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5(4):823-826.
43. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797.
44. Negrete OA, Chu D, Aguilar HC, Lee B (2007) Single amino acid changes in the Nipah and Hendra virus attachment glycoproteins distinguish ephrinB2 from ephrinB3 usage. J Virol 81(19):10804-10814.
45. Lee B, Ataman ZA, Jin L (2008) Evil versus 'eph-ective' use of ephrin-B2. Nat Struct Mol Biol 15(6):540-542.
46. Aguilar HC, et al. (2009) A novel receptor-induced activation site in the Nipah virus attachment glycoprotein (G) involved in triggering the fusion glycoprotein (F). J Biol Chem 284(3):1628-1635.
47. Gorman JJ, Nestorowicz A, Mitchell SJ, Corino GL, Selleck PW (1988) Characterization of the sites of proteolytic activation of Newcastle disease virus membrane glycoprotein precursors. J Biol Chem 263(25):12522-12531.
48. Sakaguchi T, et al. (1989) Newcastle disease virus evolution. I. Multiple lineages defined by sequence variability of the hemagglutinin-neuraminidase gene. Virology 169(2):260-272.
49. Yuan P, Paterson RG, Leser GP, Lamb RA, Jardetzky TS (2012) Structure of the ulster strain newcastle disease virus hemagglutinin-neuraminidase reveals auto-inhibitory interactions associated with low virulence. PLoS Pathog 8(8):e1002855.
50. Yang ZR, Thomson R, McNeil P, Esnouf RM (2005) RONN: The bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 21(16):3369-3376.
51. Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15(6):655-663.
52. Ryan C, et al. (2006) Structural analysis of a designed inhibitor complexed with the hemagglutinin-neuraminidase of Newcastle disease virus. Glycoconj J 23(1-2):135-141.
53. Sabarth N, et al. (2010) Comparison of single, homologous prime-boost and heterologous prime-boost immunization strategies against H5N1 influenza virus in a mouse challenge model. Vaccine 28(3):650-656.
54. Eda Y, et al. (2006) Sequential immunization with V3 peptides from primary human immunodeficiency virus type 1 produces cross-neutralizing antibodies against primary isolates with a matching narrow-neutralization sequence motif. J Virol 80(11):5552-5562.
55. Aricescu AR, Lu W, Jones EY (2006) A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr D Biol Crystallogr 62(Pt 10):1243-1250.
56. Walter TS, et al. (2005) A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr D Biol Crystallogr 61(Pt 6):651-657.
57. Winter G (2010) xia2: An expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43:186-190.
58. Karplus PA, Diederichs K (2012) Linking crystallographic model and data quality. Science 336(6084):1030-1033.
59. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40(Pt 4):658-674.
60. Perrakis A, Harkiolaki M, Wilson KS, Lamzin VS (2001) ARP/wARP and molecular replacement. Acta Crystallogr D Biol Crystallogr 57(Pt 10):1445-1450.
61. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
62. Winn MD, Murshudov GN, Papiz MZ (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 374:300-321.
63. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62(Pt 4):439-450.
64. Davis IW, et al. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35(Web Server issue):W375-W383.
65. Garner OB, et al. (2015) Timing of galectin-1 exposure differentially modulates nipah virus entry and syncytium formation in endothelial cells. J Virol 89(5):2520-2529.
66. Stuart DI, Levine M, Muirhead H, Stammers DK (1979) Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 A. J Mol Biol 134(1):109-142.
67. Felsenstein J (1989) PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 5:164-166.
68. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
69. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725-2729.
70. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406-425.
71. Zuckerkandl E, Pauling L (1965) Evolutionary Divergence and Convergence in Proteins (Academic, New York).
72. Ren J, et al. (2009) DOG 1.0: Illustrator of protein domain structures. Cell Res 19(2):271-273.