Phage display approaches for the isolation of monoclonal antibodies against dengue virus envelope domain III from human and mouse derived libraries

International Journal of Molecular Sciences

Volumn 13, Issue 3, 2012, Pages 2618-2635

  Moreland, Nicole J ^a   Susanto, Patricia ^a   Lim, Elfin ^a   Tay, Moon Y F ^a   Rajamanonmani, Ravikumar ^a   Hanson, Brendon J ^b   Vasudevan, Subhash G ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b DSO NATIONAL LABORATORIES   (Singapore)

Author keywords

Dengue; Domain III; E protein; Fab; Hybridoma; Phage display

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIBODY DETECTION; ANTIBODY ISOLATION; ANTIGEN RECOGNITION; ARTICLE; BIOPANNING; CIRCULAR DICHROISM; CONTROLLED STUDY; CROSS REACTION; DATA BASE; DENGUE VIRUS; ENZYME SPECIFICITY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGE DISPLAY; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MODIFICATION; VIRUS ENVELOPE; VIRUS NEUTRALIZATION; ANIMAL; CELL SURFACE DISPLAY; CHEMISTRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; MOUSE; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

DENGUE VIRUS; MURINAE;

IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; CELL SURFACE DISPLAY TECHNIQUES; DENGUE VIRUS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOGLOBULIN G; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS;

EID: 84858959575     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms13032618     Document Type: Article

References (43)

1. Lindenbach, B.D.; Thiel, H.J.; Rice, C.M. Flaviviridae: the viruses and their replication. In Fields Virology, 5th ed.; Lippincott William: Philadelphia, PA, USA, 2007; pp. 1101-1151.
2. Halstead, S.B. Dengue. Lancet 2007, 370, 1644-1652.
3. Fink, J.; Gu, F.; Vasudevan, S.G. Role of T cells, cytokines and antibody in dengue fever and dengue haemorrhagic fever. Rev. Med. Virol. 2006, 16, 263-275.
4. Falconar, A.K. Identification of an epitope on the dengue virus membrane (M) protein defined by cross-protective monoclonal antibodies: design of an improved epitope sequence based on common determinants present in both envelope (E and M) proteins. Arch. Virol. 1999, 144, 2313-2330.
5. Falconar, A.K. Antibody responses are generated to immunodominant ELK/KLE-type motifs on the nonstructural-1 glycoprotein during live dengue virus infections in mice and humans: implications for diagnosis, pathogenesis, and vaccine design. Clin. Vaccine Immunol. 2007, 14, 493-504.
6. Huang, K.J.; Yang, Y.C.; Lin, Y.S.; Huang, J.H.; Liu, H.S.; Yeh, T.M.; Chen, S.H.; Liu, C.C.; Lei, H.Y. The dual-specific binding of dengue virus and target cells for the antibody-dependent enhancement of dengue virus infection. J. Immunol. 2006, 176, 2825-2832.
7. Modis, Y.; Ogata, S.; Clements, D.; Harrison, S.C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 2003, 100, 6986-6991.
8. Chin, J.F.; Chu, J.J.; Ng, M.L. The envelope glycoprotein domain III of dengue virus serotypes 1 and 2 inhibit virus entry. Microbes Infect. 2007, 9, 1-6.
9. Bhardwaj, S.; Holbrook, M.; Shope, R.E.; Barrett, A.D.; Watowich, S.J. Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein. J. Virol. 2001, 75, 4002-4007.
10. Volk, D.E.; Beasley, D.W.; Kallick, D.A.; Holbrook, M.R.; Barrett, A.D.; Gorenstein, D.G. Solution structure and antibody binding studies of the envelope protein domain III from the New York strain of West Nile virus. J. Biol. Chem. 2004, 279, 38755-38761.
11. Modis, Y.; Ogata, S.; Clements, D.; Harrison, S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427, 313-319.
12. Gromowski, G.D.; Barrett, N.D.; Barrett, A.D.T. Characterization of dengue virus complex-specific neutralizing epitopes on envelope protein domain III of dengue 2 virus. J. Virol. 2008, 82, 8828-8837.
13. Shrestha, B.; Brien, J.D.; Sukupolvi-Petty, S.; Austin, S.K.; Edeling, M.A.; Kim, T.; O'Brien, K.M.; Nelson, C.A.; Johnson, S.; Fremont, D.H.; Diamond, M.S. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 2010, 6, e1000823.
14. Sukupolvi-Petty, S.; Austin, S.K.; Engle, M.; Brien, J.D.; Dowd, K.A.; Williams, K.L.; Johnson, S.; Rico-Hesse, R.; Harris, E.; Pierson, T.C.; Fremont, D.H.; Diamond, M.S. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 2010, 84, 9227-9239.
15. Sukupolvi-Petty, S.; Austin, S.K.; Purtha, W.E.; Oliphant, T.; Nybakken, G.E.; Schlesinger, J.J.; Roehrig, J.T.; Gromowski, G.D.; Barrett, A.D.; Fremont, D.H.; Diamond, M.S. Type- and subcomplex-specific neutralizing antibodies against domain III of dengue virus type 2 envelope protein recognize adjacent epitopes. J. Virol. 2007, 81, 12816-12826.
16. Wahala, W.M.P.B.; Kraus, A.A.; Haymore, L.B.; Accavitti-Loper, M.A.; de Silva, A.M. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 2009, 392, 103-113.
17. Crill, W.D.; Hughes, H.R.; Delorey, M.J.; Chang, G.-J.J. Humoral immune responses of dengue fever patients using epitope-specific serotype-2 virus-like particle antigens. PLoS One 2009, 4, e4991.
18. Midgley, C.M.; Bajwa-Joseph, M.; Vasanawathana, S.; Limpitikul, W.; Wills, B.; Flanagan, A.; Waiyaiya, E.; Tran, H.B.; Cowper, A.E.; Chotiyarnwon, P.; Grimes, J.M.; Yoksan, S.; Malasit, P.; Simmons, C.P.; Mongkolsapaya, J.; Screaton, G.R. An in-depth analysis of original antigenic sin in dengue virus infection. J. Virol. 2011, 85, 410-421.
19. Beltramello, M.; Williams, K.L.; Simmons, C.P.; Macagno, A.; Simonelli, L.; Quyen, N.T.; Sukupolvi-Petty, S.; Navarro-Sanchez, E.; Young, P.R.; de Silva, A.M.; Rey, F.A.; Varani, L.; Whitehead, S.S.; Diamond, M.S.; Harris, E.; Lanzavecchia, A.; Sallusto, F. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 2010, 8, 271-283.
20. Rajamanonmani, R.; Nkenfou, C.; Clancy, P.; Yau, Y.H.; Shochat, S.G.; Sukupolvi-Petty, S.; Schul, W.; Diamond, M.S.; Vasudevan, S.G.; Lescar, J. On a mouse monoclonal antibody that neutralizes all four dengue virus serotypes. J. Gen. Virol. 2009, 90, 799-809.
21. Krebber, A.; Bornhauser, S.; Burmester, J.; Honegger, A.; Willuda, J.; Bosshard, H.R.; Plückthun, A. Reliable cloning of functional antibody variable domains from hybridomas and spleen cell repertoires employing a reengineered phage display system. J. Immunol. Methods 1997, 201, 35-55.
22. Azzazy, H.M.E.; Highsmith, W.E. Phage display technology: clinical applications and recent innovations. Clin. Biochem. 2002, 35, 425-445.
23. Xu, J.L.; Davis, M.M. Diversity in the CDR3 region of V(H) is sufficient for most antibody specificities. Immunity 2000, 13, 37-45.
24. Brochet, X.; Lefranc, M.P.; Giudicelli, V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucl. Acids Res. 2008, 36, W503-W508.
25. Barbas, C.F.; Burton, D.R.; Scott, J.K.; Silverman, G.J. Phage Display, A Laboratory Manual; Cold Spring Harbor Press: Cold Spring Harbor, NY, USA, 2001
26. Abhinandan, K.R.; Martin, A.C. Analysis and improvements to Kabat and structurally correct numbering of antibody variable domains. Mol. Immunol. 2008, 45, 3832-3839.
27. Rader, C.; Popkov, M.; Neves, J.A.; Barbas, C.F. Integrin alpha(v)beta3 targeted therapy for Kaposi's sarcoma with an in vitro evolved antibody. FASEB J. 2002, 16, 2000-2002.
28. Hofer, T.; Tangkeangsirisin, W.; Kennedy, M.G.; Mage, R.G.; Raiker, S.J.; Venkatesh, K.; Lee, H.; Giger, R.J.; Rader, C. Chimeric rabbit/human Fab and IgG specific for members of the Nogo-66 receptor family selected for species cross-reactivity with an improved phage display vector. J. Immunol. Methods 2007, 318, 75-87.
29. Hiramatsu, K.; Tadano, M.; Men, R.; Lai, C.J. Mutational analysis of a neutralization epitope on the dengue type 2 virus (DEN2) envelope protein: monoclonal antibody resistant DEN2/DEN4 chimeras exhibit reduced mouse neurovirulence. Virology 1996, 224, 437-445.
30. Nielsen, U.B.; Marks, J.D. Affinity Maturation of Phage Antibodies. In Phage Display: a Practical Approach; Clackson, T., Lowman, H.B., Eds.; Oxford University Press: Oxford, UK, 2004; pp: 289-315.
31. Schier, R.; Bye, J.; Apell, G.; McCall, A.; Adams, G.P.; Malmqvist, M.; Weiner, L.M.; Marks, J.D. Isolation of high-affinity monomeric human anti-c-erbB-2 single chain Fv using affinity-driven selection. J. Mol. Biol. 1996, 255, 28-43.
32. Bradbury, A.R.M.; Marks, J.D. Antibodies from phage antibody libraries. J. Immunol. Methods 2004, 290, 29-49.
33. Moreland, N.J.; Tay, M.Y.; Lim, E.; Paradkar, P.N.; Doan, D.N.; Yau, Y.H.; Shochat, S.G.; Vasudevan, S.G. High affinity human antibody fragments to dengue virus non-structural protein 3. PLoS Negl. Trop. Dis. 2010, 4, e881.
34. Moreland, N.J.; Tay, M.Y.; Lim, E.; Rathore, A.P.; Lim, A.P.; Hanson, B.J.; Vasudevan, S.G. Monoclonal antibodies against dengue NS2B and NS3 proteins for the study of protein interactions in the flaviviral replication complex. J. Virol. Methods 2011, 179, 97-103.
35. Lim, A.P.C.; Chan, C.E.Z.; Wong, S.K.K.; Chan, A.H.Y.; Ooi, E.E.; Hanson, B.J. Neutralizing human monoclonal antibody against H5N1 influenza HA selected from a Fab-phage display library. Virol. J. 2008, 5, 130.
36. Gould, L.H.; Sui, J.; Foellmer, H.; Oliphant, T.; Wang, T.; Ledizet, M.; Murakami, A.; Noonan, K.; Lambeth, C.; Kar, K.; Anderson, J.F.; de Silva, A.M.; Diamond, M.S.; Koski, R.A.; Marasco, W.A.; Fikrig, E. Protective and therapeutic capacity of human single-chain Fv-Fc fusion proteins against West Nile virus. J. Virol. 2005, 79, 14606-14613.
37. Throsby, M.; Geuijen, C.; Goudsmit, J.; Bakker, A.Q.; Korimbocus, J.; Kramer, R.A.; vander Clijsters Horst, M.; de Jong, M.; Jongeneelen, M.; Thijsse, S.; Smit, R.; Visser, T.J.; Bijl, N.; Marissen, W.E.; Loeb, M.; Kelvin, D.J.; Preiser, W.; ter Meulen, J.; de Kruif, J. Isolation and characterization of human monoclonal antibodies from individuals infected with West Nile Virus. J. Virol. 2006, 80, 6982-6992.
38. de Alwis, R.; Beltramello, M.; Messer, W.B.; Sukupolvi-Petty, S.; Wahala, W.M.; Kraus, A.; Olivarez, N.P.; Pham, Q.; Brien, J.D.; Tsai, W.Y.; Wang, W.K.; Halstead, S.; Kliks, S.; Diamond, M.S.; Baric, R.; Lanzavecchia, A.; Sallusto, F.; de Silva, A.M. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl. Trop. Dis. 2011, 5, e1188.
39. Pierson, T.C.; Diamond, M.S. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert Rev. Mol. Med. 2008, 10, e12.
40. de Haard, H.J.; van Neer, N.; Reurs, A.; Hufton, S.E.; Roovers, R.C.; Henderikx, P.; de Bruïne, A.P.; Arends, J.W.; Hoogenboom, H.R. A large non-immunized human Fab fragment phage library that permits rapid isolation and kinetic analysis of high affinity antibodies. J. Biol. Chem. 1999, 274, 18218-18230.
41. Collins, T.J. ImageJ for microscopy. Biotechniques 2007, 43, S25-S30.
42. Hudson, P.J.; Souriau, C. Engineered antibodies. Nat. Med. 2003, 9, 129-134.
43. Parren, P.W.; Burton, D.R. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 2001, 77, 195-262.