Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Generation and Characterization of Monoclonal Antibodies to the Ogawa Lipopolysaccharide of Vibrio cholerae O1 from Phage-Displayed Human Synthetic Fab Library

  • Kim, Dain (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Hong, Jisu (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Choi, Yoonjoo (Medical Research Center, Chonnam National University Medical School) ;
  • Han, Jemin (Eubiologics Co., Ltd.) ;
  • Kim, Sangkyu (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Jo, Gyunghee (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Yoon, Jun-Yeol (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Chae, Heesu (Department of Systems Immunology, College of Biomedical Science, Kangwon National University) ;
  • Yoon, Hyeseon (Eubiologics Co., Ltd.) ;
  • Lee, Chankyu (Eubiologics Co., Ltd.) ;
  • Hong, Hyo Jeong (Department of Systems Immunology, College of Biomedical Science, Kangwon National University)
  • Received : 2020.05.29
  • Accepted : 2020.08.22
  • Published : 2020.11.28
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Abstract

Vibrio cholerae, cause of the life-threatening diarrheal disease cholera, can be divided into different serogroups based on the structure of its lipopolysaccharide (LPS), which consists of lipid-A, core-polysaccharide and O-antigen polysaccharide (O-PS). The O1 serogroup, the predominant cause of cholera, includes two major serotypes, Inaba and Ogawa. These serotypes are differentiated by the presence of a single 2-O-methyl group in the upstream terminal perosamine of the Ogawa O-PS, which is absent in the Inaba O-PS. To ensure the consistent quality and efficacy of the current cholera vaccines, accurate measurement and characterization of each of these two serotypes is highly important. In this study, we efficiently screened a phage-displayed human synthetic Fab library by bio-panning against Ogawa LPS and finally selected three unique mAbs (D9, E11, and F7) that specifically react with Ogawa LPS. The mAbs bound to Vibrio cholerae vaccine in a dose-dependent fashion. Sequence and structure analyses of antibody paratopes suggest that IgG D9 might have the same fine specificity as that of the murine mAbs, which were shown to bind to the upstream terminal perosamine of Ogawa O-PS, whereas IgGs F7 and E11 showed some different characteristics in the paratopes. To our knowledge, this study is the first to demonstrate the generation of Ogawa-specific mAbs using phage display technology. The mAbs will be useful for identification and quantification of Ogawa LPS in multivalent V. cholerae vaccines.

Keywords

References

  1. Johnson RA, Uddin T, Aktar A, Mohasin M, Alam MM, Chowdhury F, et al. 2012. Comparison of immune responses to the Ospecific polysaccharide and lipopolysaccharide of Vibrio cholerae O1 in Bangladeshi adult patients with cholera. Clin. Vaccine Immunol. 19: 1712-1721. https://doi.org/10.1128/CVI.00321-12
  2. Ryan ET, Calderwood SB, Qadri F. 2006. Live attenuated oral cholera vaccines. Expert. Rev. Vaccines 5: 483-494. https://doi.org/10.1586/14760584.5.4.483
  3. Stroeher UH, Karageorgos LE, Morona R, Manning PA. 1992. Serotype conversion in Vibrio cholerae O1. Proc. Natl. Acad. Sci. USA 89: 2566-2570. https://doi.org/10.1073/pnas.89.7.2566
  4. Kenne L, Lindberg B, Unger P, Gustafsson B, Holme T. 1982. Structural studies of the Vibrio cholerae O-antigen. Carbohydr. Res. 100: 341-349. https://doi.org/10.1016/S0008-6215(00)81047-2
  5. Hisatsune K, Kondo S, Isshiki Y, Iguchi T, Haishima Y. 1993. Occurrence of 2-O-methyl-N-(3-deoxy-L-glycero-tetronyl)-Dperosamine (4-amino-4,6-dideoxy-D-manno-pyranose) in lipopolysaccharide from Ogawa but not from Inaba O forms of O1 Vibrio cholerae. Biochem. Biophys. Res. Commun. 190: 302-307. https://doi.org/10.1006/bbrc.1993.1046
  6. Villeneuve S, Boutonnier A, Mulard LA, Fournier JM. 1999. Immunochemical characterization of an Ogawa-Inaba common antigenic determinant of Vibrio cholerae O1. Microbiology 145 (Pt 9): 2477-2484. https://doi.org/10.1099/00221287-145-9-2477
  7. Ito T, Higuchi T, Hirobe M, Hiramatsu K, Yokota T. 1994. Identification of a novel sugar, 4-amino-4,6-dideoxy-2-O-methylmannose in the lipopolysaccharide of Vibrio cholerae O1 serotype Ogawa. Carbohydr. Res. 256: 113-128. https://doi.org/10.1016/0008-6215(94)84231-0
  8. Wang J, Villeneuve S, Zhang J, Lei P, Miller CE, Lafaye P, et al. 1998. On the antigenic determinants of the lipopolysaccharides of Vibrio cholerae O:1, serotypes Ogawa and Inaba. J. Biol. Chem. 273: 2777-2783. https://doi.org/10.1074/jbc.273.5.2777
  9. Russo P, Ligsay AD, Olveda R, Choi SK, Kim DR, Park JY, et al. 2018. A randomized, observer-blinded, equivalence trial comparing two variations of Euvichol(R), a bivalent killed whole-cell oral cholera vaccine, in healthy adults and children in the Philippines. Vaccine 36: 4317-4324. https://doi.org/10.1016/j.vaccine.2018.05.102
  10. Adams LB, Henk MC, Siebeling RJ. 1988. Detection of Vibrio cholerae with monoclonal antibodies specific for serovar O1 lipopolysaccharide. J. Clin. Microbiol. 26: 1801-1809. https://doi.org/10.1128/jcm.26.9.1801-1809.1988
  11. Brayton PR, Tamplin ML, Huq A, Colwell RR. 1987. Enumeration of Vibrio cholerae O1 in Bangladesh waters by fluorescentantibody direct viable count. Appl. Environ. Microbiol. 53: 2862-2865. https://doi.org/10.1128/aem.53.12.2862-2865.1987
  12. Colwell RR, Hasan JA, Huq A, Loomis L, Siebeling RJ, Torres M, et al. 1992. Development and evaluation of a rapid, simple, sensitive, monoclonal antibody-based co-agglutination test for direct detection of Vibrio cholerae 01. FEMS Microbiol. Lett. 76: 215-219. https://doi.org/10.1111/j.1574-6968.1992.tb05466.x
  13. Gustafsson B, Rosen A, Holme T. 1982. Monoclonal antibodies against Vibrio cholerae lipopolysaccharide. Infect. Immun. 38: 449-454. https://doi.org/10.1128/iai.38.2.449-454.1982
  14. Gustafsson B, Holme T. 1983. Monoclonal antibodies against group- and type-specific lipopolysaccharide antigens of Vibrio cholerae O:1. J. Clin. Microbiol. 18: 480-485. https://doi.org/10.1128/jcm.18.3.480-485.1983
  15. Gustafsson B. 1984. Monoclonal antibody-based enzyme-linked immunosorbent assays for identification and serotyping of Vibrio cholerae O1. J. Clin. Microbiol. 20: 1180-1185. https://doi.org/10.1128/jcm.20.6.1180-1185.1984
  16. Ramamurthy T, Garg S, Nair GB. 1995. Monoclonal antibodies against Ogawa specific & Ogawa-Inaba common antigenic determinants of Vibrio cholerae O1 & their diagnostic utility. Indian J Med Res. 101: 10-12.
  17. Sugiyama J, Gondaira F, Matsuda J, Soga M, Terada Y. 1987. New method for serological typing of Vibrio cholerae 0:1 [corrected] using a monoclonal antibody-sensitized latex agglutination test. Microbiol. Immunol. 31: 387-391. https://doi.org/10.1111/j.1348-0421.1987.tb03100.x
  18. Dharmasena MN, Krebs SJ, Taylor RK. 2009. Characterization of a novel protective monoclonal antibody that recognizes an epitope common to Vibrio cholerae Ogawa and Inaba serotypes. Microbiology 155: 2353. https://doi.org/10.1099/mic.0.025726-0
  19. Pengsuk C, Longyant S, Rukpratanporn S, Chaivisuthangkura P, Sridulyakul P, Sithigorngul P. 2011. Differentiation among the Vibrio cholerae serotypes O1, O139, O141 and non-O1, non-O139, non-O141 using specific monoclonal antibodies with dot blotting. J. Microbiol. Methods 87: 224-233. https://doi.org/10.1016/j.mimet.2011.07.022
  20. Chaivisuthangkura P, Pengsuk C, Longyant S, Sithigorngul P. 2013. Evaluation of monoclonal antibody based immunochromatographic strip test for direct detection of Vibrio cholerae O1 contamination in seafood samples. J. Microbiol. Methods 95: 304-311. https://doi.org/10.1016/j.mimet.2013.09.013
  21. Chen W, Zhang J, Lu G, Yuan Z, Wu Q, Li J, et al. 2014. Development of an immunochromatographic lateral flow device for rapid diagnosis of Vibrio cholerae O1 serotype Ogawa. Clin. Biochem. 47: 448-454. https://doi.org/10.1016/j.clinbiochem.2013.12.022
  22. Winter G, Griffiths AD, Hawkins RE, Hoogenboom HR. 1994. Making antibodies by phage display technology. Annu. Rev. Immunol. 12: 433-455. https://doi.org/10.1146/annurev.iy.12.040194.002245
  23. Lerner RA, Kang AS, Bain JD, Burton DR, Barbas CF, 3rd. 1992. Antibodies without immunization. Science 258: 1313-1314. https://doi.org/10.1126/science.1455226
  24. Hoogenboom HR. 2005. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23: 1105-1116. https://doi.org/10.1038/nbt1126
  25. Marks JD, Hoogenboom HR, Bonnert TP, McCafferty J, Griffiths AD, Winter G. 1991. By-passing immunization. Human antibodies from V-gene libraries displayed on phage. J. Mol. Biol. 222: 581-597. https://doi.org/10.1016/0022-2836(91)90498-u
  26. Vaughan TJ, Williams AJ, Pritchard K, Osbourn JK, Pope AR, Earnshaw JC, et al. 1996. Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library. Nat. Biotechnol. 14: 309-314. https://doi.org/10.1038/nbt0396-309
  27. Huse WD, Sastry L, Iverson SA, Kang AS, Alting-Mees M, Burton DR, et al. 1989. Generation of a large combinatorial library of the immunoglobulin repertoire in phage lambda. Science 246: 1275-1281. https://doi.org/10.1126/science.2531466
  28. Hoet RM, Cohen EH, Kent RB, Rookey K, Schoonbroodt S, Hogan 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. https://doi.org/10.1038/nbt1067
  29. Knappik A, Ge L, Honegger A, Pack P, Fischer M, Wellnhofer G, et al. 2000. Fully synthetic human combinatorial antibody libraries (HuCAL) based on modular consensus frameworks and CDRs randomized with trinucleotides. J. Mol. Biol. 296: 57-86. https://doi.org/10.1006/jmbi.1999.3444
  30. Prassler J, Thiel S, Pracht C, Polzer A, Peters S, Bauer M, et al. 2011. HuCAL PLATINUM, a synthetic Fab library optimized for sequence diversity and superior performance in mammalian expression systems. J. Mol. Biol. 413: 261-278. https://doi.org/10.1016/j.jmb.2011.08.012
  31. Rothe C, Urlinger S, Lohning C, Prassler J, Stark Y, Jager U, et al. 2008. The human combinatorial antibody library HuCAL GOLD combines diversification of all six CDRs according to the natural immune system with a novel display method for efficient selection of high-affinity antibodies. J. Mol. Biol. 376: 1182-1200. https://doi.org/10.1016/j.jmb.2007.12.018
  32. Rothlisberger D, Honegger A, Pluckthun A. 2005. Domain interactions in the Fab fragment: a comparative evaluation of the singlechain Fv and Fab format engineered with variable domains of different stability. J. Mol. Biol. 347: 773-789. https://doi.org/10.1016/j.jmb.2005.01.053
  33. Jo G, Jeong MS, Wi J, Kim DH, Kim S, Kim D, et al. 2018. Generation and characterization of a neutralizing human monoclonal antibody to Hepatitis B Virus PreS1 from a phage-displayed human synthetic fab library. J. Microbiol. Biotechnol. 28: 1376-1383. https://doi.org/10.4014/jmb.1803.03056
  34. Yoon J-Y, Kim D-H, Kim S, Kim D, Jo G, Shin M-S, et al. 2017. Generation of a monoclonal antibody that has reduced binding activity to VX-inactivated butyrylcholinesterase (BuChE) compared to BuChE by phage display. Biotechnol. Bioprocess Eng. 22: 114-119. https://doi.org/10.1007/s12257-017-0110-7
  35. Kim D, Yoon H, Kim S, Wi J, Chae H, Jo G, et al. 2018. Generation of a human monoclonal antibody to cross-reactive material 197 (CRM(1)(9)(7)) and development of a sandwich ELISA for CRM(1)(9)(7) conjugate vaccines. J. Microbiol. Biotechnol. 28: 2113-2120. https://doi.org/10.4014/jmb.1810.10009
  36. Westphal O. 1965. Bacterial lipopolysaccharides extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5: 83-91.
  37. Kristensen P, Winter G. 1998. Proteolytic selection for protein folding using filamentous bacteriophages. Fold Des. 3: 321-328. https://doi.org/10.1016/S1359-0278(98)00044-3
  38. Fattom A, Schneerson R, Szu SC, Vann WF, Shiloach J, Karakawa WW, et al. 1990. Synthesis and immunologic properties in mice of vaccines composed of Staphylococcus aureus type 5 and type 8 capsular polysaccharides conjugated to Pseudomonas aeruginosa exotoxin A. Infect. Immun. 58: 2367-2374. https://doi.org/10.1128/iai.58.7.2367-2374.1990
  39. MacKenzie CR, Hirama T, Deng SJ, Bundle DR, Narang SA, Young NM. 1996. Analysis by surface plasmon resonance of the influence of valence on the ligand binding affinity and kinetics of an anti-carbohydrate antibody. J. Biol. Chem. 271: 1527-1533. https://doi.org/10.1074/jbc.271.3.1527
  40. Otamiri M, Nilsson KG. 1999. Analysis of human serum antibody-carbohydrate interaction using biosensor based on surface plasmon resonance. Int. J. Biol. Macromol. 26: 263-268. https://doi.org/10.1016/S0141-8130(99)00092-6
  41. Schatz DG. 2004. V (d) j recombination. Immunol. Rev. 200: 5-11. https://doi.org/10.1111/j.0105-2896.2004.00173.x
  42. Villeneuve S, Souchon H, Riottot MM, Mazie JC, Lei P, Glaudemans CP, et al. 2000. Crystal structure of an anti-carbohydrate antibody directed against Vibrio cholerae O1 in complex with antigen: molecular basis for serotype specificity. Proc. Natl. Acad. Sci. USA 97: 8433-8438. https://doi.org/10.1073/pnas.060022997
  43. Chatterjee S, Chaudhuri K. 2003. Lipopolysaccharides of Vibrio cholerae: I. Physical and chemical characterization. Biochimica et Biophysica Acta (BBA)-Mol. Basis Dis. 1639: 65-79. https://doi.org/10.1016/j.bbadis.2003.08.004