1887

Abstract

A novel protective monoclonal antibody (mAb) that recognizes a lipopolysaccharide (LPS) epitope common between serotypes Ogawa and Inaba of the O1 serogroup of was characterized and the potential to develop peptide mimics of this protective LPS epitope was investigated. mAb 72.1 recognizes both Ogawa and Inaba LPS and it is vibriocidal and protective in passive immunization against infection by strains of both serotypes. The cDNA-derived amino acid sequence of mAb 72.1 is closely related to the previously characterized mAb ZAC-3, which is thought to recognize an epitope in the lipid A core region of O1 LPS. In an attempt to develop a peptide mimic-based vaccine against , phage display libraries were screened with mAb 72.1 and 11 peptide mimics were identified. Remarkably, all of the peptide sequences identified from linear phage display libraries contained two cysteine residues, suggesting that mAb 72.1 preferentially binds to peptides constrained with a disulphide bond. One of the peptide mimics was immunologically characterized. Although immunization of mice with this peptide mimic conjugated to KLH elicited antibodies against the peptide itself, these antibodies did not cross-react with Ogawa or Inaba LPS. Effectiveness of a peptide mimic as a vaccine may depend on how well the peptide can mimic the carbohydrate interactions when binding to the anti-carbohydrate antibody. Thus, investigating how peptides and LPS bind to mAb 72.1 may be useful in improving current peptide mimics or designing more effective peptide mimics. Identification and characterization of novel protective anti-LPS antibodies may be useful in studying protective epitopes of LPS, which may help develop LPS-based therapeutics against .

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2009-07-01
2020-01-25
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References

  1. Adams, L. B., Henk, M. C. & Siebeling, R. J. ( 1988; ). Detection of Vibrio cholerae with monoclonal antibodies specific for serovar O1 lipopolysaccharide. J Clin Microbiol 26, 1801–1809.
    [Google Scholar]
  2. Apter, F. M., Michetti, P., Winner, L. S., III, Mack, J. A., Mekalanos, J. J. & Neutra, M. R. ( 1993; ). Analysis of the roles of antilipopolysaccharide and anti-cholera toxin immunoglobulin A (IgA) antibodies in protection against Vibrio cholerae and cholera toxin by use of monoclonal IgA antibodies in vivo. Infect Immun 61, 5279–5285.
    [Google Scholar]
  3. Bougoudogo, F., Vely, F., Nato, F., Boutonnier, A., Gounon, P., Mazie, J.-C. & Fournier, J.-M. ( 1995; ). Protective activities of serum immunoglobulin G on the mucosal surface to Vibrio cholerae O1. Bull Inst Pasteur 93, 273–283.[CrossRef]
    [Google Scholar]
  4. Boutonnier, A., Dassy, B., Dumenil, R., Guenole, A., Ratsitorahina, M., Migliani, R. & Fournier, J. M. ( 2003; ). A simple and convenient microtiter plate assay for the detection of bactericidal antibodies to Vibrio cholerae O1 and Vibrio cholerae O139. J Microbiol Methods 55, 745–753.[CrossRef]
    [Google Scholar]
  5. Brayton, P. R., Tamplin, M. L., Huq, A. & Colwell, R. R. ( 1987; ). Enumeration of Vibrio cholerae O1 in Bangladesh waters by fluorescent-antibody direct viable count. Appl Environ Microbiol 53, 2862–2865.
    [Google Scholar]
  6. Brett, P. J., Tiwana, H., Feavers, I. M. & Charalambous, B. M. ( 2002; ). Characterization of oligopeptides that cross-react with carbohydrate-specific antibodies by real time kinetics, in-solution competition enzyme-linked immunosorbent assay, and immunological analyses. J Biol Chem 277, 20468–20476.[CrossRef]
    [Google Scholar]
  7. Chatterjee, S. N. & Chaudhuri, K. ( 2003; ). Lipopolysaccharides of Vibrio cholerae. I. Physical and chemical characterization. Biochim Biophys Acta 1639, 65–79.[CrossRef]
    [Google Scholar]
  8. Chatterjee, S. N. & Chaudhuri, K. ( 2006; ). Lipopolysaccharides of Vibrio cholerae: III. Biological functions. Biochim Biophys Acta 1762, 1–16.[CrossRef]
    [Google Scholar]
  9. Chernyak, A., Kondo, S., Wade, T. K., Meeks, M. D., Alzari, P. M., Fournier, J. M., Taylor, R. K., Kovac, P. & Wade, W. F. ( 2002; ). Induction of protective immunity by synthetic Vibrio cholerae hexasaccharide derived from V. cholerae O1 Ogawa lipopolysaccharide bound to a protein carrier. J Infect Dis 185, 950–962.[CrossRef]
    [Google Scholar]
  10. Colwell, R. R., Hasan, J. A., Huq, A., Loomis, L., Siebeling, R. J., Torres, M., Galvez, S., Islam, S., Tamplin, M. T. & Bernstein, D. ( 1992; ). Development and evaluation of a rapid, simple, sensitive, monoclonal antibody-based co-agglutination test for direct detection of Vibrio cholerae O1. FEMS Microbiol Lett 76, 215–219.
    [Google Scholar]
  11. Coulon, S., Metais, J. Y., Chartier, M., Briand, J. P. & Baty, D. ( 2004; ). Cyclic peptides selected by phage display mimic the natural epitope recognized by a monoclonal anti-colicin A antibody. J Pept Sci 10, 648–658.[CrossRef]
    [Google Scholar]
  12. Dalsgaard, A., Skov, M. N., Serichantalergs, O., Echeverria, P., Meza, R. & Taylor, D. N. ( 1997; ). Molecular evolution of Vibrio cholerae O1 strains isolated in Lima, Peru, from 1991 to 1995. J Clin Microbiol 35, 1151–1156.
    [Google Scholar]
  13. De Bolle, X., Laurent, T., Tibor, A., Godfroid, F., Weynants, V., Letesson, J. J. & Mertens, P. ( 1999; ). Antigenic properties of peptidic mimics for epitopes of the lipopolysaccharide from Brucella. J Mol Biol 294, 181–191.[CrossRef]
    [Google Scholar]
  14. Dharmasena, M. N., Jewell, D. A. & Taylor, R. K. ( 2007; ). Development of peptide mimics of a protective epitope of Vibrio cholerae Ogawa O-antigen and investigation of the structural basis of peptide mimicry. J Biol Chem 282, 33805–33816.[CrossRef]
    [Google Scholar]
  15. Garg, P., Nandy, R. K., Chaudhury, P., Chowdhury, N. R., De, K., Ramamurthy, T., Yamasaki, S., Bhattacharya, S. K., Takeda, Y. & Nair, G. B. ( 2000; ). Emergence of Vibrio cholerae O1 biotype El Tor serotype Inaba from the prevailing O1 Ogawa serotype strains in India. J Clin Microbiol 38, 4249–4253.
    [Google Scholar]
  16. Gupta, R. K., Szu, S. C., Finkelstein, R. A. & Robbins, J. B. ( 1992; ). Synthesis, characterization, and some immunological properties of conjugates composed of the detoxified lipopolysaccharide of Vibrio cholerae O1 serotype Inaba bound to cholera toxin. Infect Immun 60, 3201–3208.
    [Google Scholar]
  17. Gupta, R. K., Taylor, D. N., Bryla, D. A., Robbins, J. B. & Szu, S. C. ( 1998; ). Phase 1 evaluation of Vibrio cholerae O1, serotype Inaba, polysaccharide-cholera toxin conjugates in adult volunteers. Infect Immun 66, 3095–3099.
    [Google Scholar]
  18. Gustafsson, B. ( 1984; ). Monoclonal antibody-based enzyme-linked immunosorbent assays for identification and serotyping of Vibrio cholerae O1. J Clin Microbiol 20, 1180–1185.
    [Google Scholar]
  19. 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.
    [Google Scholar]
  20. Gustafsson, B., Rosen, A. & Holme, T. ( 1982; ). Monoclonal antibodies against Vibrio cholerae lipopolysaccharide. Infect Immun 38, 449–454.
    [Google Scholar]
  21. Hill, D. R., Ford, L. & Lalloo, D. G. ( 2006; ). Oral cholera vaccines: use in clinical practice. Lancet Infect Dis 6, 361–373.[CrossRef]
    [Google Scholar]
  22. Lauvrak, V., Berntzen, G., Heggelund, U., Herstad, T. K., Sandin, R. H., Dalseg, R., Rosenqvist, E., Sandlie, I. & Michaelsen, T. E. ( 2004; ). Selection and characterization of cyclic peptides that bind to a monoclonal antibody against meningococcal L3,7,9 lipopolysaccharides. Scand J Immunol 59, 373–384.[CrossRef]
    [Google Scholar]
  23. Lesinski, G. B., Smithson, S. L., Srivastava, N., Chen, D., Widera, G. & Westerink, M. A. ( 2001; ). A DNA vaccine encoding a peptide mimic of Streptococcus pneumoniae serotype 4 capsular polysaccharide induces specific anti-carbohydrate antibodies in Balb/c mice. Vaccine 19, 1717–1726.[CrossRef]
    [Google Scholar]
  24. Lullau, E., Heyse, S., Vogel, H., Marison, I., von Stockar, U., Kraehenbuhl, J. P. & Corthesy, B. ( 1996; ). Antigen binding properties of purified immunoglobulin A and reconstituted secretory immunoglobulin A antibodies. J Biol Chem 271, 16300–16309.[CrossRef]
    [Google Scholar]
  25. Luo, P., Canziani, G., Cunto-Amesty, G. & Kieber-Emmons, T. ( 2000; ). A molecular basis for functional peptide mimicry of a carbohydrate antigen. J Biol Chem 275, 16146–16154.[CrossRef]
    [Google Scholar]
  26. Meeks, M. D., Saksena, R., Ma, X., Wade, T. K., Taylor, R. K., Kovac, P. & Wade, W. F. ( 2004; ). Synthetic fragments of Vibrio cholerae O1 Inaba O-specific polysaccharide bound to a protein carrier are immunogenic in mice but do not induce protective antibodies. Infect Immun 72, 4090–4101.[CrossRef]
    [Google Scholar]
  27. Miller, V. L., DiRita, V. J. & Mekalanos, J. J. ( 1989; ). Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. J Bacteriol 171, 1288–1293.
    [Google Scholar]
  28. Moe, G. R., Tan, S. & Granoff, D. M. ( 1999; ). Molecular mimetics of polysaccharide epitopes as vaccine candidates for prevention of Neisseria meningitidis serogroup B disease. FEMS Immunol Med Microbiol 26, 209–226.[CrossRef]
    [Google Scholar]
  29. Monzavi-Karbassi, B., Hennings, L. J., Artaud, C., Liu, T., Jousheghany, F., Pashov, A., Murali, R., Hutchins, L. F. & Kieber-Emmons, T. ( 2007; ). Preclinical studies of carbohydrate mimetic peptide vaccines for breast cancer and melanoma. Vaccine 25, 3022–3031.[CrossRef]
    [Google Scholar]
  30. Phalipon, A., Folgori, A., Arondel, J., Sgaramella, G., Fortugno, P., Cortese, R., Sansonetti, P. J. & Felici, F. ( 1997; ). Induction of anti-carbohydrate antibodies by phage library-selected peptide mimics. Eur J Immunol 27, 2620–2625.[CrossRef]
    [Google Scholar]
  31. Pincus, S. H., Smith, M. J., Jennings, H. J., Burritt, J. B. & Glee, P. M. ( 1998; ). Peptides that mimic the group B streptococcal type III capsular polysaccharide antigen. J Immunol 160, 293–298.
    [Google Scholar]
  32. Qadri, F., Chowdhury, M. I., Faruque, S. M., Salam, M. A., Ahmed, T., Begum, Y. A., Saha, A., Alam, M. S. & Zaman, K. ( 2005; ). Randomized, controlled study of the safety and immunogenicity of Peru-15, a live attenuated oral vaccine candidate for cholera, in adult volunteers in Bangladesh. J Infect Dis 192, 573–579.[CrossRef]
    [Google Scholar]
  33. Ramamurthy, T., Garg, S. & Nair, G. B. ( 1995; ). Monoclonal antibodies against Ogawa specific and Ogawa-Inaba common antigenic determinants of Vibrio cholerae O1 and their diagnostic utility. Indian J Med Res 101, 10–12.
    [Google Scholar]
  34. Reidl, J. & Klose, K. E. ( 2002; ). Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev 26, 125–139.[CrossRef]
    [Google Scholar]
  35. Ryan, E. T., Calderwood, S. B. & Qadri, F. ( 2006; ). Live attenuated oral cholera vaccines. Expert Rev Vaccines 5, 483–494.[CrossRef]
    [Google Scholar]
  36. Shin, J. S., Yu, J., Lin, J., Zhong, L., Bren, K. L. & Nahm, M. H. ( 2002; ). Peptide mimotopes of pneumococcal capsular polysaccharide of 6B serotype: a peptide mimotope can bind to two unrelated antibodies. J Immunol 168, 6273–6278.[CrossRef]
    [Google Scholar]
  37. 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.[CrossRef]
    [Google Scholar]
  38. Sun, D. X., Mekalanos, J. J. & Taylor, R. K. ( 1990; ). Antibodies directed against the toxin-coregulated pilus isolated from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J Infect Dis 161, 1231–1236.[CrossRef]
    [Google Scholar]
  39. Taylor, R. K., Kirn, T. J., Bose, N., Stonehouse, E., Tripathi, S. A., Kovac, P. & Wade, W. F. ( 2004; ). Progress towards development of a cholera subunit vaccine. Chem Biodivers 1, 1036–1057.[CrossRef]
    [Google Scholar]
  40. Tiwana, H., Clow, K. J., Hall, C., Feavers, I. M. & Charalambous, B. M. ( 2005; ). The immunogenicity of a conformationally restricted peptide mimetic of meningococcal lipooligosaccharide. Scand J Immunol 62, 385–392.[CrossRef]
    [Google Scholar]
  41. Valadon, P., Nussbaum, G., Boyd, L. F., Margulies, D. H. & Scharff, M. D. ( 1996; ). Peptide libraries define the fine specificity of anti-polysaccharide antibodies to Cryptococcus neoformans. J Mol Biol 261, 11–22.[CrossRef]
    [Google Scholar]
  42. Valadon, P., Nussbaum, G., Oh, J. & Scharff, M. D. ( 1998; ). Aspects of antigen mimicry revealed by immunization with a peptide mimetic of Cryptococcus neoformans polysaccharide. J Immunol 161, 1829–1836.
    [Google Scholar]
  43. Villeneuve, S., Boutonnier, A., Mulard, L. A. & Fournier, J. M. ( 1999; ). Immunochemical characterization of an Ogawa-Inaba common antigenic determinant of Vibrio cholerae O1. Microbiology 145, 2477–2484.
    [Google Scholar]
  44. Wang, J., Villeneuve, S., Zhang, J., Lei, P., Miller, C. E., Lafaye, P., Nato, F., Szu, S. C., Karpas, A. & other authors ( 1998; ). On the antigenic determinants of the lipopolysaccharides of Vibrio cholerae O : 1, serotypes Ogawa and Inaba. J Biol Chem 273, 2777–2783.[CrossRef]
    [Google Scholar]
  45. Wang, Z., Raifu, M., Howard, M., Smith, L., Hansen, D., Goldsby, R. & Ratner, D. ( 2000; ). Universal PCR amplification of mouse immunoglobulin gene variable regions: the design of degenerate primers and an assessment of the effect of DNA polymerase 3′ to 5′ exonuclease activity. J Immunol Methods 233, 167–177.[CrossRef]
    [Google Scholar]
  46. WHO ( 2001; ). Weekly epidemiological record. Bulletin 76, 117–124.
    [Google Scholar]
  47. Winner, L., III, Mack, J., Weltzin, R., Mekalanos, J. J., Kraehenbuhl, J. P. & Neutra, M. R. ( 1991; ). New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A from hybridoma tumors protects against Vibrio cholerae infection. Infect Immun 59, 977–982.
    [Google Scholar]
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