Relating influenza virus membrane fusion kinetics to stoichiometry of neutralizing antibodies at the single-particle level

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

Volumn 111, Issue 48, 2014, Pages E5143-E5148

  Otterstrom, Jason J ^a,b   Brenburg, Boerries ^c   Koldijk, Martin H ^c   Juraszek, Jarek ^c   Tang, Chan ^c   Mashaghi, Samaneh ^b   Kwaks, Ted ^c   Goudsmit, Jaap ^c   Vogels, Ronald ^c   Friesen, Robert H E ^c,d   Van Oijen, Antoine M ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c CRUCELL HOLLAND BV   (Netherlands)

^d ICFO INSTITUT DE CIENCIES FOTONIQUES   (Spain)

Author keywords

Hemagglutinin; Influenza; Membrane fusion; Neutralization stoichiometry; Neutralizing antibody

Indexed keywords

ORTHOMYXOVIRIDAE;

IMMUNOGLOBULIN F(AB) FRAGMENT; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; PROTEIN BINDING;

DRUG EFFECTS; FLUORESCENCE MICROSCOPY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA, HUMAN; KINETICS; MEMBRANE FUSION; MONTE CARLO METHOD; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRION; VIROLOGY; VIRUS ENTRY;

ANTIBODIES, NEUTRALIZING; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; KINETICS; MEMBRANE FUSION; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MONTE CARLO METHOD; PROTEIN BINDING; VIRION; VIRUS INTERNALIZATION;

EID: 84914165942     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1411755111     Document Type: Article

References (42)

1. Han T, Marasco WA (2011) Structural basis of influenza virus neutralization. Ann N Y Acad Sci 1217:178-190.
2. Fleishman SJ, et al. (2011) Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332(6031):816-821.
3. Burton DR, Poignard P, Stanfield RL, Wilson IA (2012) Broadly neutralizing antibodies present new prospects to counter highly antigenically diverse viruses. Science 337(6091):183-186.
4. Steel J, et al. (2010) Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 1(1), 10.1128/mBio.00018-10.
5. Vanderlinden E, et al. (2010) Novel inhibitors of influenza virus fusion: Structureactivity relationship and interaction with the viral hemagglutinin. J Virol 84(9): 4277-4288.
6. Klasse PJ, Sattentau QJ (2002) Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J Gen Virol 83(Pt 9):2091-2108.
7. Klasse PJ (2008) Desk Encyclopedia of General Virology, eds Mahy BWJ, van Regenmortel MHV (Academic, Oxford), pp 404-410.
8. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289(5796):366-373.
9. Waterfield M, Scrace G, Skehel J (1981) Disulphide bonds of haemagglutinin of Asian influenza virus. Nature 289(5796):422-424.
10. Tong S, et al. (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9(10):e1003657.
11. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371(6492):37-43.
12. Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15(7):690-698.
13. Mittal A, Bentz J (2001) Comprehensive kinetic analysis of influenza hemagglutininmediated membrane fusion: Role of sialate binding. Biophys J 81(3):1521-1535.
14. Danieli T, Pelletier SL, Henis YI, White JM (1996) Membrane fusion mediated by the influenza virus hemagglutinin requires the concerted action of at least three hemagglutinin trimers. J Cell Biol 133(3):559-569.
15. Floyd DL, Ragains JR, Skehel JJ, Harrison SC, van Oijen AM (2008) Single-particle kinetics of influenza virus membrane fusion. Proc Natl Acad Sci USA 105(40): 15382-15387.
16. Ivanovic T, Choi JL, Whelan SP, van Oijen AM, Harrison SC (2013) Influenza-virus membrane fusion by cooperative fold-back of stochastically induced hemagglutinin intermediates. ELife Sciences 2:e00333.
17. Bizebard T, et al. (1995) Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376(6535):92-94.
18. Knossow M, et al. (2002) Mechanism of neutralization of influenza virus infectivity by antibodies. Virology 302(2):294-298.
19. Dreyfus C, et al. (2012) Highly conserved protective epitopes on influenza B viruses. Science 337(6100):1343-1348.
20. Ekiert DC, et al. (2012) Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489(7417):526-532.
21. Lee PS, et al. (2012) Heterosubtypic antibody recognition of the influenza virus hemagglutinin receptor binding site enhanced by avidity. Proc Natl Acad Sci USA 109(42):17040-17045.
22. Throsby M, et al. (2008) Heterosubtypic neutralizing monoclonal antibodies crossprotective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE 3(12):e3942.
23. Ekiert DC, et al. (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324(5924):246-251.
24. Ekiert DC, et al. (2011) A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333(6044):843-850.
25. Sui J, et al. (2009) Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16(3):265-273.
26. Okuno Y, Isegawa Y, Sasao F, Ueda S (1993) A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 67(5):2552-2558.
27. Corti D, et al. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333(6044):850-856.
28. Nakamura G, et al. (2013) An in vivo human-plasmablast enrichment technique allows rapid identification of therapeutic influenza A antibodies. Cell Host Microbe 14(1): 93-103.
29. Brandenburg B, et al. (2013) Mechanisms of hemagglutinin targeted influenza virus neutralization. PLoS ONE 8(12):e80034.
30. Harris AK, et al. (2013) Structure and accessibility of HA trimers on intact 2009 H1N1 pandemic influenza virus to stem region-specific neutralizing antibodies. Proc Natl Acad Sci USA 110(12):4592-4597.
31. Taylor HP, Armstrong SJ, Dimmock NJ (1987) Quantitative relationships between an influenza virus and neutralizing antibody. Virology 159(2):288-298.
32. Parren PW, Burton DR (2001) The antiviral activity of antibodies in vitro and in vivo. Adv Immunol 77:195-262.
33. Reading SA, Dimmock NJ (2007) Neutralization of animal virus infectivity by antibody. Arch Virol 152(6):1047-1059.
34. Otterstrom J, van Oijen AM (2013) Visualization of membrane fusion, one particle at a time. Biochemistry 52(10):1654-1668.
35. Tiffany JM, Blough HA (1970) Models of structure of the envelope of influenza virus. Proc Natl Acad Sci USA 65(4):1105-1112.
36. Inglis SC, Carroll AR, Lamb RA, Mahy BW (1976) Polypeptides specified by the influenza virus genome I. Evidence for eight distinct gene products specified by fowl plague virus. Virology 74(2):489-503.
37. Moulès V, et al. (2011) Importance of viral genomic composition in modulating glycoprotein content on the surface of influenza virus particles. Virology 414(1):51-62.
38. Harris A, et al. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci USA 103(50):19123-19127.
39. Floyd DL, Harrison SC, van Oijen AM (2010) Analysis of kinetic intermediates in singleparticle dwell-time distributions. Biophys J 99(2):360-366.
40. Weber T, et al. (1994) Evidence for H(+)-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. J Biol Chem 269(28):18353-18358.
41. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P (2008) Cellular proteins in influenza virus particles. PLoS Pathog 4(6):e1000085.
42. Schofield DJ, Stephenson JR, Dimmock NJ (1997) Variations in the neutralizing and haemagglutination-inhibiting activities of five influenza A virus-specific IgGs and their antibody fragments. J Gen Virol 78(Pt 10):2431-2439.