Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein

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

Volumn 109, Issue 41, 2012, Pages 16672-16677

  Welch, Brett D ^a   Liu, Yuanyuan ^a   Kors, Christopher A ^a   Leser, George P ^a   Jardetzky, Theodore S ^b   Lamb, Robert A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cleavage activation; F protein structure; Paramyxoviruses

Indexed keywords

HYBRID PROTEIN; PARAINFLUENZA VIRUS 5 FUSION PROTEIN; PROTEINASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EBOLA VIRUS; HYDROPHOBICITY; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; VIRUS INFECTIVITY;

ANIMALS; ARGININE; BINDING SITES; CELLS, CULTURED; CRYSTALLOGRAPHY, X-RAY; HN PROTEIN; MEMBRANE FUSION; MODELS, MOLECULAR; PARAMYXOVIRINAE; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SF9 CELLS; TRYPSIN; VIRAL FUSION PROTEINS;

EID: 84867351430     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213802109     Document Type: Article

References (45)

1. Lamb RA, Parks GD (2007) Paramyxoviridae: The viruses and their replication. Fields Virology, eds Knipe DM, Howley PM (Lippincott Williams & Wilkins, Philadelphia), 5th Ed, pp 1449-1496.
2. Lamb RA, Jardetzky TS (2007) Structural basis of viral invasion: Lessons from paramyxovirus F. Curr Opin Struct Biol 17:427-436. (Pubitemid 47451774)
3. Russell CJ, Luque LE (2006) The structural basis of paramyxovirus invasion. Trends Microbiol 14:243-246. (Pubitemid 43825730)
4. Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15:690-698.
5. Jardetzky TS, Lamb RA (2004) Virology: A class act. Nature 427:307-308.
6. Scheid A, Choppin PW (1974) Identification of biological activities of paramyxovirus glycoproteins: Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology 57:475-490.
7. Homma M, Ouchi M (1973) Trypsin action on the growth of Sendai virus in tissue culture cells, 3: Structural difference of Sendai viruses grown in eggs and tissue culture cells. J Virol 12:1457-1465.
8. Nagai Y, Klenk HD, Rott R (1976) Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72:494-508.
9. Bousse T, Takimoto T, Gorman WL, Takahashi T, Portner A (1994) Regions on the hemagglutinin-neuraminidase proteins of human parainfluenza virus type-1 and Sendai virus important for membrane fusion. Virology 204:506-514. (Pubitemid 24330854)
10. Deng R, et al. (1999) Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 253:43-54. (Pubitemid 29391557)
11. Deng R, Wang Z, Mirza AM, Iorio RM (1995) Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 209:457-469.
12. Lee JK, et al. (2008) Functional interaction between paramyxovirus fusion and attachment proteins. J Biol Chem 283:16561-16572.
13. Tanabayashi K, Compans RW (1996) Functional interaction of paramyxovirus glycoproteins: Identification of a domain in Sendai virus HN which promotes cell fusion. J Virol 70:6112-6118. (Pubitemid 26266827)
14. Tsurudome M, et al. (1995) Identification of regions on the hemagglutinin-neuraminidase protein of human parainfluenza virus type 2 important for promoting cell fusion. Virology 213:190-203.
15. Wang Z, Mirza AM, Li J, Mahon PJ, Iorio RM (2004) An oligosaccharide at the C-terminus of the F-specific domain in the stalk of the human parainfluenza virus 3 hemagglutinin-neuraminidase modulates fusion. Virus Res 99:177-185. (Pubitemid 38121666)
16. Bose S, et al. (2011) Structure and mutagenesis of the parainfluenza virus 5 hemagglutinin-neuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J Virol 85:12855-12866.
17. 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 108:14920-14925.
18. Russell CJ, Jardetzky TS, Lamb RA (2001) Membrane fusion machines of paramyxoviruses: Capture of intermediates of fusion. EMBO J 20:4024-4034. (Pubitemid 32751819)
19. Kim YH, et al. (2011) Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc Natl Acad Sci USA 108:20992-20997.
20. 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 439:38-44. (Pubitemid 43053622)
21. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37-43. (Pubitemid 24277462)
22. Yin H-S, 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 102:9288-9293. (Pubitemid 40923556)
23. Swanson K, et al. (2010) Structure of the Newcastle disease virus F protein in the postfusion conformation. Virology 402:372-379.
24. Swanson KA, et al. (2011) Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc Natl Acad Sci USA 108:9619-9624.
25. McLellan JS, Yang Y, Graham BS, Kwong PD (2011) Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 85:7788-7796.
26. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373.
27. Lee JE, et al. (2008) Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454:177-182. (Pubitemid 351969896)
28. Chen J, et al. (1998) Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95:409- 417.
29. Dutch RE, Hagglund RN, Nagel MA, Paterson RG, Lamb RA (2001) Paramyxovirus fusion (F) protein: A conformational change on cleavage activation. Virology 281:138-150. (Pubitemid 32911534)
30. 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 103:17903-17908. (Pubitemid 44852258)
31. Hirst GK (1941) Agglutination of red cells by allantoic fluid of chick embryos infected with influenza virus. Science 94:22-23.
32. Carette JE, et al. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477:340-343.
33. White J, Matlin K, Helenius A (1981) Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J Cell Biol 89:674-679. (Pubitemid 11035975)
34. Brecher M, et al. (2012) Cathepsin cleavage potentiates the Ebola virus glycoprotein to undergo a subsequent fusion-relevant conformational change. J Virol 86:364-372.
35. Palese P, Shaw ML (2007) Orthomyxoviridae: The viruses and their replication. Fields Virology, eds Knipe DM, Howley PM (Lippincott Williams & Wilkins, Philadelphia).
36. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM (2005) Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643-1645. (Pubitemid 40807517)
37. Bale S, et al. (2011) Ebola virus glycoprotein needs an additional trigger, beyond proteolytic priming for membrane fusion. PLoS Negl Trop Dis 5:e1395.
38. Paterson RG, Russell CJ, Lamb RA (2000) Fusion protein of the paramyxovirus SV5: Destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30. (Pubitemid 30256536)
39. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology, eds Carter CW, Sweet RM (Academic, San Diego), pp 307-326.
40. Strong M, et al. (2006) Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103:8060-8065. (Pubitemid 43801052)
41. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132. (Pubitemid 41742764)
42. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221.
43. Chen VB, et al. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12-21.
44. Weis WI, Brünger AT, Skehel JJ, Wiley DC (1990) Refinement of the influenza virus hemagglutinin by simulated annealing. J Mol Biol 212:737-761.
45. Steinhauer DA (1999) Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 258:1-20.