Recombinant soluble respiratory syncytial virus F protein that lacks heptad repeat B, contains a GCN4 trimerization motif and is not cleaved displays prefusion-like characteristics

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Widjaja, Ivy ^a,b   Rigter, Alan ^a,b   Jacobino, Shamir ^c   Van Kuppeveld, Frank J M ^a   Leenhouts, Kees ^b   Palomo, Concepcion ^d   Melero, Jose A ^d   Leusen, Jeanette H W ^c   Haijema, Bert Jan ^b   Rottier, Peter J M ^a   De Haan, Cornelis A M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Mucosis BV Meditech Center   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; EPITOPE; FURIN; FUSION PROTEIN F; HEPTAD REPEAT B; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; NEUTRALIZING ANTIBODY; PROTEIN BINDING; RECOMBINANT PROTEIN; VIRUS ANTIBODY;

ANTIBODY SPECIFICITY; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; HUMAN RESPIRATORY SYNCYTIAL VIRUS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STABILITY; RESIDUE ANALYSIS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMISTRY; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR MODEL; PATHOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RESPIRATORY MUCOSA; TUMOR CELL LINE; VIROLOGY;

RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; CELL LINE, TUMOR; EPITHELIAL CELLS; GENE EXPRESSION; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RESPIRATORY MUCOSA; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; VIRAL FUSION PROTEINS;

EID: 84939158617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130829     Document Type: Article

References (37)

1. Collins PL, Melero JA (2011) Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res 162:80-99. doi:10.1016/j.virusres.2011.09.020 PMID:21963675
2. Del Vecchio A, Ferrara T, Maglione M, Capasso L, Raimondi F (2013) New perspectives in Respiratory Syncitial Virus infection. J Matern Fetal Neonatal Med 26 Suppl 2:55-59. doi:10.3109/14767058. 2013.831282 PMID:24059554
3. Chang A, Dutch RE (2012) Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 4:613-636. doi:10.3390/v4040613 PMID:22590688
4. Gonzalez-Reyes L, Ruiz-Arguello MB, Garcia-Barreno B, Calder L, Lopez JA, Albar JP, et al. (2001) Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc Natl Acad Sci U S A 98:9859-9864. PMID:11493675
5. Krzyzaniak MA, Zumstein MT, Gerez JA, Picotti P, Helenius A (2013) Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the F protein. PLoS Pathog 9:e1003309. doi:10.1371/journal.ppat.1003309 PMID:23593008
6. Zimmer G, Budz L, Herrler G (2001) Proteolytic activation of respiratory syncytial virus fusion protein. Cleavage at two furin consensus sequences. J Biol Chem 276:31642-31650. PMID:11418598
7. Schlender J, Zimmer G, Herrler G, Conzelmann KK (2003) Respiratory syncytial virus (RSV) fusion protein subunit F2, not attachment protein G, determines the specificity of RSV infection. J Virol 77:4609-4616. PMID:12663767
8. McLellan JS, Chen M, Leung S, Graepel KW, Du X, Yang Y, et al. (2013) Structure of RSV Fusion Glycoprotein Trimer Bound to a Prefusion-Specific Neutralizing Antibody. Science 340:1113-1117. doi:10.1126/science.1234914 PMID:23618766
9. 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. doi:10.1128/JVI.00555-11 PMID:21613394
10. Swanson KA, Settembre EC, Shaw CA, Dey AK, Rappuoli R, Mandl CW, 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 U S A 108:9619-9624. doi:10.1073/pnas.1106536108 PMID:21586636
11. Plattet P, Plemper RK (2013) Envelope protein dynamics in paramyxovirus entry. MBio 4.
12. Techaarpornkul S, Barretto N, Peeples ME (2001) Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J Virol 75:6825-6834. PMID:11435561
13. Liljeroos L, Krzyzaniak MA, Helenius A, Butcher SJ (2013) Architecture of respiratory syncytial virus revealed by electron cryotomography. Proc Natl Acad Sci U S A 110:11133-11138. doi:10.1073/pnas.1309070110 PMID:23776214
14. Rigter A, Widjaja I, Versantvoort H, Coenjaerts FE, Van Roosmalen M, Leenhouts K, et al. (2013) A protective and safe intranasal RSV vaccine based on a recombinant prefusion-like form of the F protein bound to bacterium-like particles. PLoS One 8:e71072. doi:10.1371/journal.pone.0071072 PMID:23951084
15. Ruiz-Arguello MB, Gonzalez-Reyes L, Calder LJ, Palomo C, Martin D, Saiz MJ, et al. (2002) Effect of proteolytic processing at two distinct sites on shape and aggregation of an anchorless fusion protein of human respiratory syncytial virus and fate of the intervening segment. Virology 298:317-326. PMID:12127793
16. Ruiz-Arguello MB, Martin D, Wharton SA, Calder LJ, Martin SR, Cano O, et al. (2004) Thermostability of the human respiratory syncytial virus fusion protein before and after activation: implications for the membrane-fusion mechanism. J Gen Virol 85:3677-3687. PMID:15557241
17. Magro M, Mas V, Chappell K, Vazquez M, Cano O, Luque D, 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 U S A 109:3089-3094. doi:10.1073/pnas.1115941109 PMID:22323598
18. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, et al. (2013) Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342:592-598. doi:10. 1126/science.1243283 PMID:24179220
19. Beaumont T, Bakker AQ, Yasuda E (2012) RSV specific binding molecule. US patent application US/2012/0070446 A1.
20. Kwakkenbos MJ, Diehl SA, Yasuda E, Bakker AQ, Van Geelen CM, Lukens MV, et al. (2010) Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nat Med 16:123-128. doi:10.1038/nm.2071 PMID:20023635
21. Spits H, Beaumont T, Yasuda E, Kwakkenbos MJ (2008) RSV-specific binding molecules and means for producing them. International patent WO/2008/147196.
22. Palomo C, Mas V, Vazquez M, Cano O, Luque D, Terron MC, et al. (2014) Polyclonal and monoclonal antibodies specific for the six-helix bundle of the human respiratory syncytial virus fusion glycoprotein as probes of the protein post-fusion conformation. Virology 460-461:119-127. doi:10.1016/j.virol. 2014.05.001 PMID:25010277
23. Russell CJ, Jardetzky TS, Lamb RA (2001) Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J 20:4024-4034. PMID:11483506
24. Lamb RA, Jardetzky TS (2007) Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 17:427-436. PMID:17870467
25. 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 U S A 102:9288-9293. PMID:15964978
26. 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 U S A 103:17903-17908. PMID:17093041
27. Russell CJ, Kantor KL, Jardetzky TS, Lamb RA (2003) A dual-functional paramyxovirus F protein regulatory switch segment: activation and membrane fusion. J Cell Biol 163:363-374. PMID:14581458
28. Paterson RG, Russell CJ, Lamb RA (2000) Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30. PMID:10772976
29. Poor TA, Song AS, Welch BD, Kors CA, Jardetzky TS, Lamb RA (2015) On the stability of parainfluenza virus 5 F proteins. J Virol 89:3438-3441. doi:10.1128/JVI.03221-14 PMID:25589638
30. Anderson LJ, Bingham P, Hierholzer JC (1988) Neutralization of respiratory syncytial virus by individual and mixtures of F and G protein monoclonal antibodies. J Virol 62:4232-4238. PMID:2459412
31. Tsui P, Tornetta MA, Ames RS, Bankosky BC, Griego S, Silverman C, et al. (1996) Isolation of a neutralizing human RSV antibody from a dominant, non-neutralizing immune repertoire by epitope-blocked panning. J Immunol 157:772-780. PMID:8752928
32. Sakurai H, Williamson RA, Crowe JE, Beeler JA, Poignard P, Bastidas RB, et al. (1999) Human antibody responses to mature and immature forms of viral envelope in respiratory syncytial virus infection: significance for subunit vaccines. J Virol 73:2956-2962. PMID:10074145
33. Tan L, Lemey P, Houspie L, Viveen MC, Jansen NJ, Van Loon AM, et al. (2012) Genetic Variability among Complete Human Respiratory Syncytial Virus Subgroup A Genomes: Bridging Molecular Evolutionary Dynamics and Epidemiology. PLoS One 7:e51439. doi:10.1371/journal.pone.0051439 PMID:23236501
34. Eckert DM, Kim PS (2001) Design of potent inhibitors of HIV-1 entry from the gp41 N-peptide region. Proc Natl Acad Sci U S A 98:11187-11192. PMID:11572974
35. Van Roosmalen ML, Kanninga R, El Khattabi M, Neef J, Audouy S, Bosma T, et al. (2006) Mucosal vaccine delivery of antigens tightly bound to an adjuvant particle made from food-grade bacteria. Methods 38:144-149. PMID:16414272
36. Johnson S, Oliver C, Prince GA, Hemming VG, Pfarr DS, Wang SC, et al. (1997) Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J Infect Dis 176:1215-1224. PMID:9359721
37. Hallak LK, Spillmann D, Collins PL, Peeples ME (2000) Glycosaminoglycan sulfation requirements for respiratory syncytial virus infection. J Virol 74:10508-10513. PMID:11044095