Structure and stabilization of the Hendra virus F glycoprotein in its prefusion form

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

Volumn 113, Issue 4, 2016, Pages 1056-1061

  Wong, Joyce J W ^a   Paterson, Reay G ^b   Lamb, Robert A ^b   Jardetzky, Theodore S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

F protein atomic structure; Hendra virus; Membrane fusion; Metastable F protein stabilization; Paramyxovirus F protein

Indexed keywords

GLYCOPROTEIN; HENDRA VIRUS F GLYCOPROTEIN; UNCLASSIFIED DRUG; DISULFIDE; VIRUS FUSION PROTEIN;

ANTIGENICITY; ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DISULFIDE BOND; HENDRA VIRUS; HENDRA VIRUS F; HUMAN RESPIRATORY SYNCYTIAL VIRUS; HYDROPHOBICITY; MOLECULAR WEIGHT; NONHUMAN; PARAINFLUENZA VIRUS 5; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; SHELF LIFE; THERMOSTABILITY; X RAY DIFFRACTION; AMINO ACID SEQUENCE; CHEMISTRY; HEK293 CELL LINE; HUMAN; MOLECULAR GENETICS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; HEK293 CELLS; HENDRA VIRUS; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STABILITY; VIRAL FUSION PROTEINS;

EID: 84955495688     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523303113     Document Type: Article

References (47)

1. Rota PA, Lo MK (2012) Molecular virology of the henipaviruses. Curr Top Microbiol Immunol 359:41-58.
2. Field H, et al. (2001) The natural history of Hendra and Nipah viruses. Microbes Infect 3(4):307-314.
3. Marsh GA, et al. (2012) Cedar virus: A novel Henipavirus isolated from Australian bats. PLoS Pathog 8(8):e1002836.
4. Drexler JF, et al. (2012) Bats host major mammalian paramyxoviruses. Nat Commun 3:796.
5. Mahalingam S, et al. (2012) Hendra virus: An emerging paramyxovirus in Australia. Lancet Infect Dis 12(10):799-807.
6. Clayton BA, Wang LF, Marsh GA (2013) Henipaviruses: An updated review focusing on the pteropid reservoir and features of transmission. Zoonoses Public Health 60(1):69-83.
7. Hyatt AD, Zaki SR, Goldsmith CS, Wise TG, Hengstberger SG (2001) Ultrastructure of Hendra virus and Nipah virus within cultured cells and host animals. Microbes Infect 3(4):297-306.
8. Bossart KN, Fusco DL, Broder CC (2013) Paramyxovirus entry. Adv ExpMed Biol 790:95-127.
9. Jardetzky TS, Lamb RA (2014) Activation of paramyxovirus membrane fusion and virus entry. Curr Opin Virol 5:24-33.
10. Liu Q, et al. (2013) Unraveling a three-step spatiotemporal mechanism of triggering of receptor-induced Nipah virus fusion and cell entry. PLoS Pathog 9(11):e1003770.
11. Liu Q, et al. (2015) Nipah virus attachment glycoprotein stalk C-terminal region links receptor binding to fusion triggering. J Virol 89(3):1838-1850.
12. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS (2006) Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439(7072):38-44.
13. Apte-Sengupta S, et al. (2012) Base of the measles virus fusion trimer head receives the signal that triggers membrane fusion. J Biol Chem 287(39):33026-33035.
14. Bose S, et al. (2013) Mutations in the parainfluenza virus 5 fusion protein reveal domains important for fusion triggering and metastability. J Virol 87(24):13520-13531.
15. Pager CT, Dutch RE (2005) Cathepsin L is involved in proteolytic processing of the Hendra virus fusion protein. J Virol 79(20):12714-12720.
16. Moll M, Diederich S, Klenk HD, Czub M, Maisner A (2004) Ubiquitous activation of the Nipah virus fusion protein does not require a basic amino acid at the cleavage site. J Virol 78(18):9705-9712.
17. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS (2005) Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci USA 102(26):9288-9293.
18. McLellan JS, et al. (2013) Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340(6136):1113-1117.
19. Lee B, Ataman ZA (2011) Modes of paramyxovirus fusion: A Henipavirus perspective. Trends Microbiol 19(8):389-399.
20. Hayward S, Kitao A, Berendsen HJ (1997) Model-free methods of analyzing domain motions in proteins from simulation: A comparison of normal mode analysis and molecular dynamics simulation of lysozyme. Proteins 27(3):425-437.
21. Carter JR, Pager CT, Fowler SD, Dutch RE (2005) Role of N-linked glycosylation of the Hendra virus fusion protein. J Virol 79(12):7922-7925.
22. Bagai S, Lamb RA (1995) Individual roles of N-linked oligosaccharide chains in intracellular transport of the paramyxovirus SV5 fusion protein. Virology 209(1):250-256.
23. Garten W, et al. (1994) Processing of viral glycoproteins by the subtilisin-like endoprotease furin and its inhibition by specific peptidylchloroalkylketones. Biochimie 76(3-4):217-225.
24. Dahms SO, et al. (2014) X-ray structures of human furin in complex with competitive inhibitors. ACS Chem Biol 9(5):1113-1118.
25. Adams-Cioaba MA, Krupa JC, Xu C, Mort JS, Min J (2011) Structural basis for the recognition and cleavage of histone H3 by cathepsin L. Nat Commun 2:197.
26. Asaad N, et al. (2009) Dipeptidyl nitrile inhibitors of Cathepsin L. Bioorg Med Chem Lett 19(15):4280-4283.
27. Guncar G, Pungercic G, Klemencic I, Turk V, Turk D (1999) Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J 18(4):793-803.
28. Ljunggren A, et al. (2007) Crystal structure of the parasite protease inhibitor chagasin in complex with a host target cysteine protease. J Mol Biol 371(1):137-153.
29. Dombkowski AA (2003) Disulfide by Design: A computational method for the rational design of disulfide bonds in proteins. Bioinformatics 19(14):1852-1853.
30. Chan YP, et al. (2012) Biochemical, conformational, and immunogenic analysis of soluble trimeric forms of henipavirus fusion glycoproteins. J Virol 86(21):11457-11471.
31. Dormitzer PR, Ulmer JB, Rappuoli R (2008) Structure-based antigen design: A strategy for next generation vaccines. Trends Biotechnol 26(12):659-667.
32. Cozzi R, Scarselli M, Ferlenghi I (2013) Structural vaccinology: A three-dimensional view for vaccine development. Curr Top Med Chem 13(20):2629-2637.
33. Magro M, et al. (2012) Neutralizing antibodies against the preactive form of respiratory syncytial virus fusion protein offer unique possibilities for clinical intervention. Proc Natl Acad Sci USA 109(8):3089-3094.
34. Lee JK, Prussia A, Snyder JP, Plemper RK (2007) Reversible inhibition of the fusion activity of measles virus F protein by an engineered intersubunit disulfide bridge. J Virol 81(16):8821-8826.
35. Zokarkar A, Connolly SA, Jardetzky TS, Lamb RA (2012) Reversible inhibition of fusion activity of a paramyxovirus fusion protein by an engineered disulfide bond in the membrane-proximal external region. J Virol 86(22):12397-12401.
36. McLellan JS, et al. (2013) Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342(6158):592-598.
37. Kemble GW, Bodian DL, Rosé J, Wilson IA, White JM (1992) Intermonomer disulfide bonds impair the fusion activity of influenza virus hemagglutinin. J Virol 66(8):4940-4950.
38. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA (2006) Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc Natl Acad Sci USA 103(47):17903-17908.
39. Comstedt P, Hanner M, Schüler W, Meinke A, Lundberg U (2014) Design and development of a novel vaccine for protection against Lyme borreliosis. PLoS One 9(11):e113294.
40. Compton JR, Legler PM, Clingan BV, Olson MA, Millard CB (2011) Introduction of a disulfide bond leads to stabilization and crystallization of a ricin immunogen. Proteins 79(4):1048-1060.
41. Backliwal G, Hildinger M, Hasija V, Wurm FM (2008) High-density transfection with HEK-293 cells allows doubling of transient titers and removes need for a priori DNA complex formation with PEI. Biotechnol Bioeng 99(3):721-727.
42. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
43. Vagin A, Teplyakov A (2010) Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66(Pt 1):22-25.
44. Brünger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921.
45. Murshudov GN, et al. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67(Pt 4):355-367.
46. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
47. Jones TA, Zou J-Y, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47(Pt 2):110-119.