The breadth of cross sub-type neutralisation activity of a single domain antibody to influenza hemagglutinin can be increased by antibody valency

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Hufton, Simon E ^a   Risley, Paul ^a   Ball, Christina R ^a   Major, Diane ^a   Engelhardt, Othmar G ^a   Poole, Stephen ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; INFLUENZA VIRUS HEMAGGLUTININ; NANOBODY; NEUTRALIZING ANTIBODY; R1A A5 ANTIBODY; R1A B6 ANTIBODY; R1A C5 ANTIBODY; R1A E5 ANTIBODY; R1A E6 ANTIBODY; R1A F4 ANTIBODY; R1A F5 ANTIBODY; R1A G5 ANTIBODY; R1A G6 ANTIBODY; R2A B9 ANTIBODY; R2A E8 ANTIBODY; R2A F9 ANTIBODY; R2A G8 ANTIBODY; R2A G9 ANTIBODY; R2A H9 ANTIBODY; R2B D8 ANTIBODY; R2B D9 ANTIBODY; R2B E8 ANTIBODY; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS ANTIGEN;

ACIDITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H9N2; JUVENILE ANIMAL; MALE; NONHUMAN; VIRUS ATTACHMENT; VIRUS HEMAGGLUTINATION; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ARTIODACTYLA; CELL SURFACE DISPLAY; CHEMISTRY; CLASSIFICATION; CROSS REACTION; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; SERODIAGNOSIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; CAMELIDS, NEW WORLD; CELL SURFACE DISPLAY TECHNIQUES; CROSS REACTIONS; EPITOPES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MALE; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; SEQUENCE ALIGNMENT; SINGLE-DOMAIN ANTIBODIES;

EID: 84905472558     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103294     Document Type: Article

References (77)

1. Webster RG, Laver WG, Air GM, Schild GC (1982) Molecular mechanisms of variation in influenza viruses. Nature 296: 115-121. (Pubitemid 12160907)
2. Girard MP, Tam JS, Assossou OM, Kieny MP (2010) The 2009 A (H1N1) influenza virus pandemic: A review. Vaccine 28: 4895-4902.
3. Johnson NP, Mueller J (2002) Updating the accounts: global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull Hist Med 76: 105-115.
4. de J (2008) H5N1 transmission and disease: observations from the frontlines. Pediatr Infect Dis J 27: S54-S56.
5. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de WE, et al. (2012) Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336: 1534-1541. 336/6088/1534 [pii];10.1126/science.1213362 [doi].
6. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, et al. (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486: 420-428. nature10831 [pii];10.1038/nature10831 [doi].
7. Hayden FG (2006) Antiviral resistance in influenza viruses - implications for management and pandemic response. N Engl J Med 354: 785-788.
8. Lowen AC, Palese P (2007) Influenza virus transmission: basic science and implications for the use of antiviral drugs during a pandemic. Infect Disord Drug Targets 7: 318-328.
9. Nabel GJ, Fauci AS (2010) Induction of unnatural immunity: prospects for a broadly protective universal influenza vaccine. Nat Med 16: 1389-1391.
10. Marasco WA, Sui J (2007) The growth and potential of human antiviral monoclonal antibody therapeutics. Nat Biotechnol 25: 1421-1434. (Pubitemid 350233138)
11. Martinez O, Tsibane T, Basler CF (2009) Neutralizing anti-influenza virus monoclonal antibodies: therapeutics and tools for discovery. Int Rev Immunol 28: 69-92.
12. Luke TC, Kilbane EM, Jackson JL, Hoffman SL (2006) Meta-analysis: convalescent blood products for Spanish influenza pneumonia: a future H5N1 treatment? Ann Intern Med 145: 599-609. (Pubitemid 46780940)
13. Zhou B, Zhong N, Guan Y (2007) Treatment with convalescent plasma for influenza A (H5N1) infection. N Engl J Med 357: 1450-1451. (Pubitemid 47535608)
14. Lachmann P (2009) Anti-infective antibodies-reviving an old paradigm. Vaccine 27 Suppl 6: G33-G37. S0264-410X(09)01497-2 [pii];10.1016/j.vaccine.2009. 09.137 [doi].
15. Epstein SL, Lo CY, Misplon JA, Lawson CM, Hendrickson BA, et al. (1997) Mechanisms of heterosubtypic immunity to lethal influenza A virus infection in fully immunocompetent, T cell-depleted, beta2-microglobulin-deficient, and J chain-deficient mice. J Immunol 158: 1222-1230. (Pubitemid 127469945)
16. Sui J, Hwang WC, Perez S, Wei G, Aird D, et al. (2009) Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16: 265-273.
17. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, et al. (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324: 246-251.
18. Throsby M, van den BE, Jongeneelen M, Poon LL, Alard P, et al. (2008) Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE 3: e3942.
19. Kashyap AK, Steel J, Oner AF, Dillon MA, Swale RE, et al. (2008) Combinatorial antibody libraries from survivors of the Turkish H5N1 avian influenza outbreak reveal virus neutralization strategies. Proc Natl Acad Sci U S A 105: 5986-5991. (Pubitemid 351758386)
20. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, et al. (2011) A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333: 843-850.
21. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, et al. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333: 850-856.
22. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, et al. (2012) Highly conserved protective epitopes on influenza B viruses. Science 337: 1343-1348. science.1222908 [pii];10.1126/science.1222908 [doi].
23. Nakamura G, Chai N, Park S, Chiang N, Lin Z, et al. (2013) An in vivo human-plasmablast enrichment technique allows rapid identification of therapeutic influenza A antibodies. Cell Host Microbe 14: 93-103. S1931-3128(13)00220-5 [pii];10.1016/j.chom.2013.06.004 [doi].
24. Wang R, Song A, Levin J, Dennis D, Zhang NJ, et al. (2008) Therapeutic potential of a fully human monoclonal antibody against influenza A virus M2 protein. Antiviral Res 80: 168-177.
25. Beerli RR, Bauer M, Schmitz N, Buser RB, Gwerder M, et al. (2009) Prophylactic and therapeutic activity of fully human monoclonal antibodies directed against influenza A M2 protein. Virol J 6: 224.
26. Russell RJ, Haire LF, Stevens DJ, Collins PJ, Lin YP, et al. (2006) The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443: 45-49. (Pubitemid 44344043)
27. Lamere MW, Lam HT, Moquin A, Haynes L, Lund FE, et al. (2011) Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus. J Immunol 186: 4331-4339.
28. Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69: 531-569.
29. Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR, et al. (2008) Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci U S A 105: 17736-17741.
30. Russell RJ, Gamblin SJ, Haire LF, Stevens DJ, Xiao B, et al. (2004) H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes. Virology 325: 287-296. 10.1016/j.virol.2004.04.040 [doi];S004268220400282X [pii].
31. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, et al. (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79: 2814-2822. 79/5/2814 [pii];10.1128/JVI.79.5.2814-2822.2005 [doi].
32. Corti D, Suguitan AL, Jr., Pinna D, Silacci C, Fernandez-Rodriguez BM, et al. (2010) Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 120: 1663-1673.
33. Kwong PD, Wilson IA (2009) HIV-1 and influenza antibodies: seeing antigens in new ways. Nat Immunol 10: 573-578.
34. Zhou T, Xu L, Dey B, Hessell AJ, Van RD, et al. (2007) Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737. (Pubitemid 46279718)
35. Sui J, Sheehan J, Hwang WC, Bankston LA, Burchett SK, et al. (2011) Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies. Clin Infect Dis 52: 1003-1009. cir121 [pii];10.1093/cid/cir121 [doi].
36. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, et al. (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208: 181-193. jem.20101352 [pii];10.1084/jem.20101352 [doi].
37. Arbabi GM, Desmyter A, Wyns L, Hamers R, Muyldermans S (1997) Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett 414: 521-526. (Pubitemid 27390659)
38. Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, et al. (1993) Naturally occurring antibodies devoid of light chains. Nature 363: 446-448. (Pubitemid 23179389)
39. Coppieters K, Dreier T, Silence K, de HH, Lauwereys M, et al. (2006) Formatted anti-tumor necrosis factor alpha VHH proteins derived from camelids show superior potency and targeting to inflamed joints in a murine model of collagen-induced arthritis. Arthritis Rheum 54: 1856-1866. 10.1002/art.21827 [doi]. (Pubitemid 43877935)
40. Muyldermans S, Baral TN, Retamozzo VC, De BP, De GE, et al. (2009) Camelid immunoglobulins and nanobody technology. Vet Immunol Immunopathol 128: 178-183.
41. Robertson JS, Engelhardt OG (2010) Developing vaccines to combat pandemic influenza. Viruses 2: 532-546. 10.3390/v2020532 [doi];viruses-02-00532 [pii].
42. Maass DR, Sepulveda J, Pernthaner A, Shoemaker CB (2007) Alpaca (Lama pacos) as a convenient source of recombinant camelid heavy chain antibodies (VHHs). J Immunol Methods 324: 13-25. (Pubitemid 47001424)
43. Harmsen MM, de Haard HJ (2007) Properties, production, and applications of camelid single-domain antibody fragments. Appl Microbiol Biotechnol 77: 13-22. (Pubitemid 47573319)
44. de Haard HJ, van NN, Reurs A, Hufton SE, Roovers RC, et al. (1999) A large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J Biol Chem 274: 18218-18230.
45. Hoet RM, Cohen EH, Kent RB, Rookey K, Schoonbroodt S, et al. (2005) Generation of high-affinity human antibodies by combining donor-derived and synthetic complementarity-determining-region diversity. Nat Biotechnol 23: 344-348. (Pubitemid 41094423)
46. Finlay WJ, Cunningham O, Lambert MA, Darmanin-Sheehan A, Liu X, et al. (2009) Affinity maturation of a humanized rat antibody for anti-RAGE therapy: comprehensive mutagenesis reveals a high level of mutational plasticity both inside and outside the complementarity-determining regions. J Mol Biol 388: 541-558.
47. Harmon MW, Rota PA, Walls HH, Kendal AP (1988) Antibody response in humans to influenza virus type B host-cell-derived variants after vaccination with standard (egg-derived) vaccine or natural infection. J Clin Microbiol 26: 333-337. (Pubitemid 18054955)
48. Heyndrickx L, Heath A, Sheik-Khalil E, Alcami J, Bongertz V, et al. (2012) International network for comparison of HIV neutralization assays: the NeutNet report II. PLoS ONE 7: e36438. 10.1371/journal.pone.0036438 [doi];PONE-D-11-25421 [pii].
49. Karlsson R, Katsamba PS, Nordin H, Pol E, Myszka DG (2006) Analyzing a kinetic titration series using affinity biosensors. Anal Biochem 349: 136-147. (Pubitemid 43129567)
50. Sakabe S, Iwatsuki-Horimoto K, Horimoto T, Nidom CA, Le M, et al. (2010) A cross-reactive neutralizing monoclonal antibody protects mice from H5N1 and pandemic (H1N1) 2009 virus infection. Antiviral Res 88: 249-255. S0166-3542(10)00725-4 [pii];10.1016/j.antiviral.2010.09.007 [doi].
51. 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: 2552-2558. (Pubitemid 23118850)
52. Feshchenko E, Rhodes DG, Felberbaum R, McPherson C, Rininger JA, et al. (2012) Pandemic influenza vaccine: characterization of A/California/07/2009 (H1N1) recombinant hemagglutinin protein and insights into H1N1 antigen stability. BMC Biotechnol 12: 77. 1472-6750-12-77 [pii];10.1186/1472-6750-12-77 [doi].
53. Harmsen MM, Ruuls RC, Nijman IJ, Niewold TA, Frenken LG, et al. (2000) Llama heavy-chain V regions consist of at least four distinct subfamilies revealing novel sequence features. Mol Immunol 37: 579-590. (Pubitemid 32052527)
54. Nguyen VK, Hamers R, Wyns L, Muyldermans S (2000) Camel heavy-chain antibodies: diverse germline V(H)H and specific mechanisms enlarge the antigen-binding repertoire. EMBO J 19: 921-930. (Pubitemid 30119818)
55. Weis W, Brown JH, Cusack S, Paulson JC, Skehel JJ, et al. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333: 426-431. 10.1038/333426a0 [doi].
56. Wilson IA, Ladner RC, Skehel JJ, Wiley DC (1983) The structure and role of the carbohydrate moieties of influenza virus haemagglutinin. Biochem Soc Trans 11 Pt 2: 145-147.
57. Hoag H (2013) A universal problem. Nat Med 19: 12-14. nm0113-12 [pii];10.1038/nm0113-12 [doi].
58. Lee PS, Yoshida R, Ekiert DC, Sakai N, Suzuki Y, et al. (2012) Heterosubtypic antibody recognition of the influenza virus hemagglutinin receptor binding site enhanced by avidity. Proc Natl Acad Sci U S A 109: 17040-17045. 1212371109 [pii];10.1073/pnas.1212371109 [doi].
59. 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. (Pubitemid 27469983)
60. Gigant B, Fleury D, Bizebard T, Skehel JJ, Knossow M (1995) Crystallization and preliminary X-ray diffraction studies of complexes between an influenza hemagglutinin and Fab fragments of two different monoclonal antibodies. Proteins 23: 115-117. 10.1002/prot.340230113 [doi].
61. Hultberg A, Temperton NJ, Rosseels V, Koenders M, Gonzalez-Pajuelo M, et al. (2011) Llama-derived single domain antibodies to build multivalent, superpotent and broadened neutralizing anti-viral molecules. PLoS ONE 6: e17665.
62. Stijlemans B, Conrath K, Cortez-Retamozo V, Van XH, Wyns L, et al. (2004) Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. J Biol Chem 279: 1256-1261. (Pubitemid 38082649)
63. Collis AV, Brouwer AP, Martin AC (2003) Analysis of the antigen combining site: correlations between length and sequence composition of the hypervariable loops and the nature of the antigen. J Mol Biol 325: 337-354. S0022283602012226 [pii].
64. Ekiert DC, Kashyap AK, Steel J, Rubrum A, Bhabha G, et al. (2012) Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489: 526-532. nature11414 [pii];10.1038/nature11414 [doi].
65. Sriwilaijaroen N, Suzuki Y (2012) Molecular basis of the structure and function of H1 hemagglutinin of influenza virus. Proc Jpn Acad Ser B Phys Biol Sci 88: 226-249. DN/JST.JSTAGE/pjab/88.226 [pii].
66. Chen J, Wharton SA, Weissenhorn W, Calder LJ, Hughson FM, et al. (1995) A soluble domain of the membrane-anchoring chain of influenza virus hemagglutinin (HA2) folds in Escherichia coli into the low-pH-induced conformation. Proc Natl Acad Sci U S A 92: 12205-12209. (Pubitemid 26014039)
67. Forsman A, Beirnaert E, asa-Chapman MM, Hoorelbeke B, Hijazi K, et al. (2008) Llama antibody fragments with cross-subtype human immunodeficiency virus type 1 (HIV-1)-neutralizing properties and high affinity for HIV-1 gp120. J Virol 82: 12069-12081.
68. Garaicoechea L, Olichon A, Marcoppido G, Wigdorovitz A, Mozgovoj M, et al. (2008) Llama-derived single-chain antibody fragments directed to rotavirus VP6 protein possess broad neutralizing activity in vitro and confer protection against diarrhea in mice. J Virol 82: 9753-9764.
69. van d, V, Pant N, Wolvers D, Bezemer S, Hermans PW, et al. (2006) Reduction in morbidity of rotavirus induced diarrhoea in mice by yeast produced monovalent llama-derived antibody fragments. Vaccine 24: 4130-4137.
70. Serruys B, Van HF, Verbrugghe P, Leroux-Roels G, Vanlandschoot P (2009) Llama-derived single-domain intrabodies inhibit secretion of hepatitis B virions in mice. Hepatology 49: 39-49. 10.1002/hep.22609 [doi].
71. Ibanez LI, De FM, Hultberg A, Verrips T, Temperton N, et al. (2011) Nanobodies With In Vitro Neutralizing Activity Protect Mice Against H5N1 Influenza Virus Infection. J Infect Dis 203: 1063-1072.
72. Dumoulin M, Conrath K, Van MA, Meersman F, Heremans K, et al. (2002) Single-domain antibody fragments with high conformational stability. Protein Sci 11: 500-515. (Pubitemid 34171255)
73. Dolk E, van d, V, Lutje HD, Vriend G, de HH, et al. (2005) Isolation of llama antibody fragments for prevention of dandruff by phage display in shampoo. Appl Environ Microbiol 71: 442-450.
74. Vincke C, Loris R, Saerens D, Martinez-Rodriguez S, Muyldermans S, et al. (2009) General strategy to humanize a camelid single-domain antibody and identification of a universal humanized nanobody scaffold. J Biol Chem 284: 3273-3284. M806889200 [pii];10.1074/jbc.M806889200 [doi].
75. Shen J, Vil MD, Jimenez X, Iacolina M, Zhang H, et al. (2006) Single variable domain-IgG fusion. A novel recombinant approach to Fc domain-containing bispecific antibodies. J Biol Chem 281: 10706-10714. M513415200 [pii];10.1074/jbc.M513415200 [doi].
76. Chun S, Li C, Van DG, Wang J, Farnsworth A, et al. (2008) Universal antibodies and their applications to the quantitative determination of virtually all subtypes of the influenza A viral hemagglutinins. Vaccine 26: 6068-6076. S0264-410X(08)01232-2 [pii];10.1016/j.vaccine.2008.09.015 [doi].
77. Khurana S, Suguitan AL, Jr., Rivera Y, Simmons CP, Lanzavecchia A, et al. (2009) Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med 6: e1000049.