Isolation of panels of llama single-domain antibody fragments binding all nine neuraminidase subtypes of influenza a virus

Antibodies

Volumn 2, Issue 2, 2013, Pages 168-192

  Harmsen, Michiel M ^a   Blokker, Juliette C ^a   Pritz Verschuren, Sylvia B ^a   Bartelink, Willem ^a,b   van der Burg, Herman ^a   Koch, Guus ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Antigenic site; Enzymatic activity; Nanobody; Phage display; Recombinant neuraminidase; Single domain antibody

Indexed keywords

IMMUNOGLOBULIN HEAVY CHAIN; RECOMBINANT PROTEIN; VIRUS HEMAGGLUTININ; VIRUS SIALIDASE;

AMINO ACID SEQUENCE; ANTIBODY ISOLATION; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; ARTIODACTYLA; AVIAN INFLUENZA VIRUS; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; INFLUENZA VIRUS A; LLAMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGE DISPLAY; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; YEAST;

EID: 84903878121     PISSN: 20734468     EISSN: None     Source Type: Journal    
DOI: 10.3390/antib2020168     Document Type: Article

References (43)

1. Bouvier, N. M.; Palese, P. The biology of influenza viruses. Vaccine 2008, 26 (Suppl. 4), D49-D53.
2. Tong, S.; Li, Y.; Rivailler, P.; Conrardy, C.; Castillo, D. A.; Chen, L. M.; Recuenco, S.; Ellison, J. A.; Davis, C. T.; York, I. A.; et al. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 2012, 109, 4269-4274.
3. Fouchier, R. A.; Schneeberger, P. M.; Rozendaal, F. W.; Broekman, J. M.; Kemink, S. A.; Munster, V.; Kuiken, T.; Rimmelzwaan, G. F.; Schutten, M.; et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl. Acad. Sci. USA 2004, 101, 1356-1361.
4. Capua, I.; Cattoli, G. Diagnosing avian influenza infection in vaccinated populations by systems for differentiating infected from vaccinated animals (DIVA). Dev. Biol. 2007, 130, 137-143.
5. Kim, J. N.; Byun, S. H.; Kang, S. Y.; Mo, I. P. Evaluation of neuraminidase antigen based competitive enzyme-linked immunosorbent assay in chickens vaccinated with avian influenza inactivated vaccine. Avian Dis. 2010, 54, 682-685.
6. Liu, Y.; Mundt, E.; Mundt, A.; Sylte, M.; Suarez, D. L.; Swayne, D. E.; Garcia, M. Development and evaluation of an avian influenza, neuraminidase subtype 1, indirect enzyme-linked immunosorbent assay for poultry using the differentiation of infected from vaccinated animals control strategy. Avian Dis. 2010, 54, 613-621.
7. Moreno, A.; Brocchi, E.; Lelli, D.; Gamba, D.; Tranquillo, M.; Cordioli, P. Monoclonal antibody based ELISA tests to detect antibodies against neuraminidase subtypes 1, 2 and 3 of avian influenza viruses in avian sera. Vaccine 2009, 27, 4967-4974.
8. Gamblin, S. J.; Skehel, J. J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J. Biol. Chem. 2010, 285, 28403-28409.
9. Marcelin, G.; Sandbulte, M. R.; Webby, R. J. Contribution of antibody production against neuraminidase to the protection afforded by influenza vaccines. Rev. Med. Virol. 2012, 22, 267-279.
10. Johansson, B. E.; Bucher, D. J.; Kilbourne, E. D. Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J. Virol. 1989, 63, 1239-1246.
11. Bosch, B. J.; Bodewes, R.; de Vries, R. P.; Kreijtz, J. H.; Bartelink, W.; van Amerongen, G.; Rimmelzwaan, G. F.; de Haan, C. A.; Osterhaus, A. D.; Rottier, P. J. Recombinant soluble, Multimeric HA and NA exhibit distinctive types of protection against pandemic swine-origin 2009 A(H1N1) influenza virus infection in ferrets. J. Virol. 2010, 84, 10366-10374.
12. Gravel, C.; Li, C.; Wang, J.; Hashem, A. M.; Jaentschke, B.; Xu, K. W.; Lorbetskie, B.; Gingras, G.; Aubin, Y.; Van Domselaar, G.; et al. Qualitative and quantitative analyses of virtually all subtypes of influenza A and B viral neuraminidases using antibodies targeting the universally conserved sequences. Vaccine 2010, 28, 5774-5784.
13. Sandbulte, M. R.; Westgeest, K. B.; Gao, J.; Xu, X.; Klimov, A. I.; Russell, C. A.; Burke, D. F.; Smith, D. J.; Fouchier, R. A.; Eichelberger, M. C. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses. Proc. Natl. Acad. Sci. USA 2011, 108, 20748-20753.
14. Harmsen, M. M.; De Haard, H. J. Properties, Production, and applications of camelid singledomain antibody fragments. Appl. Microbiol. Biotechnol. 2007, 77, 13-22.
15. Huang, L.; Muyldermans, S.; Saerens, D. Nanobodies(R): Proficient tools in diagnostics. Expert Rev. Mol. Diagn. 2010, 10, 777-785.
16. Hamers-Casterman, C.; Atarhouch, T.; Muyldermans, S.; Robinson, G.; Hamers, C.; Songa, E. B.; Bendahman, N.; Hamers, R. Naturally occurring antibodies devoid of light chains. Nature 1993, 363, 446-448.
17. Hultberg, A.; Temperton, N. J.; Rosseels, V.; Koenders, M.; Gonzalez-Pajuelo, M.; Schepens, B.; Ibanez, L. I.; Vanlandschoot, P.; Schillemans, J.; Saunders, M.; et al. Llama-derived single domain antibodies to build multivalent, superpotent and broadened neutralizing anti-viral molecules. PLoS One 2011, 6, e17665.
18. Jahnichen, S.; Blanchetot, C.; Maussang, D.; Gonzalez-Pajuelo, M.; Chow, K. Y.; Bosch, L.; De Vrieze, S.; Serruys, B.; Ulrichts, H.; Vandevelde, W.; et al. CXCR4 nanobodies (VHH-based single variable domains) potently inhibit chemotaxis and HIV-1 replication and mobilize stem cells. Proc. Natl. Acad. Sci. USA 2010, 107, 20565-20570.
19. Harmsen, M. M.; Van Solt, C. B.; Fijten, H. P. D.; Van Setten, M. C. Prolonged in vivo residence times of llama single-domain antibody fragments in pigs by binding to porcine immunoglobulins. Vaccine 2005, 23, 4926-4934.
20. Harmsen, M. M.; Ruuls, R. C.; Nijman, I. J.; Niewold, T. A.; Frenken, L. G. J.; de Geus, B. Llama heavy-chain V regions consist of at least four distinct subfamilies revealing novel sequence features. Mol. Immunol. 2000, 37, 579-590.
21. Lu, J.; Sloan, S. R. An alternating selection strategy for cloning phage display antibodies. J. Immunol. Methods 1999, 228, 109-119.
22. Wu, R.; Hu, S.; Xiao, Y.; Li, Z.; Shi, D.; Bi, D. Development of indirect enzyme-linked immunosorbent assay with nucleoprotein as antigen for detection and quantification of antibodies against avian influenza virus. Vet. Res. Commun. 2007, 31, 631-641.
23. Ekiert, D. C.; Bhabha, G.; Elsliger, M. A.; Friesen, R. H.; Jongeneelen, M.; Throsby, M.; Goudsmit, J.; Wilson, I. A. Antibody recognition of a highly conserved influenza virus epitope. Science 2009, 324, 246-251.
24. Ekiert, D. C.; Friesen, R. H.; Bhabha, G.; Kwaks, T.; Jongeneelen, M.; Yu, W.; Ophorst, C.; Cox, F.; Korse, H. J.; Brandenburg, B.; et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 2011, 333, 843-850.
25. Throsby, M.; van den Brink, E.; Jongeneelen, M.; Poon, L. L.; Alard, P.; Cornelissen, L.; Bakker, A.; Cox, F.; van Deventer, E.; Guan, Y.; et al. Heterosubtypic Neutralizing Monoclonal Antibodies Cross-Protective against H5N1 and H1N1 Recovered from Human IgM Memory B Cells. PLoS ONE 2008, 3, e3942.
26. Marks, J. D.; Ouwehand, W. H.; Bye, J. M.; Finnern, R.; Gorick, B. D.; Voak, D.; Thorpe, S. J.; Hughes-Jones, N. C.; Winter, G. Human antibody fragments specific for human blood group antigens from a phage display library. Biotechnology 1993, 11, 1145-1149.
27. Desselberger, U. Preparation-conditioned changes of the antigenicity of influenza virus neuraminidases. Arch. Virol. 1977, 53, 335-349.
28. Lauwereys, M.; Arbabi Ghahroudi, M.; Desmyter, A.; Kinne, J.; Holzer, W.; De Genst, E.; Wyns, L.; Muyldermans, S. Potent enzyme inhibitors derived from dromedary heavy-chain antibodies. EMBO J. 1998, 17, 3512-3520.
29. Stijlemans, B.; Conrath, K.; Cortez-Retamozo, V.; Van Xong, H.; Wyns, L.; Senter, P.; Revets, H.; De Baetselier, P.; Muyldermans, S.; Magez, S. Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies. African trypanosomes as paradigm. J. Biol. Chem. 2004, 279, 1256-1261.
30. Kalbfuss, B.; Knochlein, A.; Krober, T.; Reichl, U. Monitoring influenza virus content in vaccine production: precise assays for the quantitation of hemagglutination and neuraminidase activity. Biologicals 2008, 36, 145-161.
31. Lambré, C. R.; Terzidis, H.; Greffard, A.; Webster, R. G. An enzyme-linked lectin assay for sialidase. Clin. Chim. Acta 1991, 198, 183-193.
32. van Wielink, R.; Kant-Eenbergen, H. C.; Harmsen, M. M.; Martens, D. E.; Wijffels, R. H.; Coco-Martin, J. M. Adaptation of a Madin-Darby canine kidney cell line to suspension growth in serumfree media and comparison of its ability to produce avian influenza virus to Vero and BHK21 cell lines. J. Virol. Methods 2011, 171, 53-60.
33. Arora, D. J.; Tremblay, P.; Bourgault, R.; Boileau, S. Concentration and purification of influenza virus from allantoic fluid. Anal. Biochem. 1985, 144, 189-192.
34. McCafferty, J.; Johnson, K. S. Construction and screening of antibody display libraries. In Phage Display of Peptides and Proteins; Kay, B. K., Winter, J., McCafferty, J., Eds.; Academic Press: San Diego, CA, USA, 1996; pp. 79-111.
35. Lefranc, M. P. IMGT, The International ImMunoGeneTics Information System, http://imgt. cines. fr. Methods Mol. Biol. 2004, 248, 27-49.
36. Dereeper, A.; Guignon, V.; Blanc, G.; Audic, S.; Buffet, S.; Chevenet, F.; Dufayard, J. F.; Guindon, S.; Lefort, V.; Lescot, M.; et al. Phylogeny. fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36, W465-W469.
37. Harmsen, M. M.; Van Solt, C. B.; Fijten, H. P. D.; Van Keulen, L.; Rosalia, R. A.; Weerdmeester, K.; Cornelissen, A. H. M.; De Bruin, M. G. M.; Eblé, P. L.; Dekker, A. Passive immunization of guinea-pigs with llama single-domain antibody fragments against foot-and-mouth disease. Vet. Microbiol. 2007, 120, 193-206.
38. Conway, J. O.; Sherwood, L. J.; Collazo, M. T.; Garza, J. A.; Hayhurst, A. Llama single domain antibodies specific for the 7 botulinum neurotoxin serotypes as heptaplex immunoreagents. PLoS One 2010, 5, e8818.
39. Verheesen, P.; ten Haaft, M. R.; Lindner, N.; Verrips, C. T.; de Haard, J. J. Beneficial properties of single-domain antibody fragments for application in immunoaffinity purification and immunoperfusion chromatography. Biochim. Biophys. Acta 2003, 1624, 21-28.
40. Wang, T. T.; Tan, G. S.; Hai, R.; Pica, N.; Petersen, E.; Moran, T. M.; Palese, P. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathogens 2010, 6, e1000796.
41. Shoji, Y.; Chichester, J. A.; Palmer, G. A.; Farrance, C. E.; Stevens, R.; Stewart, M.; Goldschmidt, L.; Deyde, V.; Gubareva, L.; Klimov, A.; et al. An influenza N1 neuraminidase-specific monoclonal antibody with broad neuraminidase inhibition activity against H5N1 HPAI viruses. Human Vac. 2011, 7, 199-204.
42. Ibanez, L. I.; De Filette, M.; Hultberg, A.; Verrips, T.; Temperton, N.; Weiss, R. A.; Vandevelde, W.; Schepens, B.; Vanlandschoot, P.; Saelens, X. Nanobodies with in vitro neutralizing activity protect mice against H5N1 influenza virus infection. J. Infect. Dis. 2011, 203, 1063-1072.
43. Tillib, S. V.; Ivanova, T. I.; Vasilev, L. A.; Rutovskaya, M. V.; Saakyan, S. A.; Gribova, I. Y.; Tutykhina, I. L.; Sedova, E. S.; Lysenko, A. A.; Shmarov, M. M.; et al. Formatted single-domain antibodies can protect mice against infection with influenza virus (H5N2). Antiviral Res. 2013, 97, 245-254.