Exploiting chimeric human antibodies to characterize a protective epitope of Neisseria adhesin A, one of the Bexsero vaccine components

FASEB Journal

Volumn 30, Issue 1, 2016, Pages 93-101

  Bertoldi, Isabella ^a   Faleri, Agnese ^a   Galli, Barbara ^a   Lo Surdo, Paola ^a   Liguori, Alessia ^a   Norais, Nathalie ^a   Santini, Laura ^a   Masignani, Vega ^a   Pizza, Mariagrazia ^a   Giuliani, Marzia Monica ^a  

^a GSK   (Italy)

Author keywords

Bactericidal epitope; Epitope mapping; Hydrogen deuterium exchange; MenB vaccine; Meningococcal antigen

Indexed keywords

ADHESIN; CHIMERIC ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G3; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 6E3; NEISSERIA ADHESIN A; UNCLASSIFIED DRUG; 4CMENB VACCINE; BACTERIUM ANTIBODY; EPITOPE; MENINGOCOCCUS VACCINE;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; IMMUNOGENICITY; MASS SPECTROMETRY; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; ANIMAL; EPITOPE MAPPING; HUMAN; IMMUNOLOGY; MENINGOCOCCOSIS; NEISSERIA; PROCEDURES;

ADHESINS, BACTERIAL; ANIMALS; ANTIBODIES, BACTERIAL; DEUTERIUM EXCHANGE MEASUREMENT; EPITOPE MAPPING; EPITOPES; HUMANS; MENINGOCOCCAL INFECTIONS; MENINGOCOCCAL VACCINES; MICE; NEISSERIA;

EID: 84973512766     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-273813     Document Type: Article

References (36)

1. Giuliani, M. M., Adu-Bobie, J., Comanducci, M., Aricò, B., Savino, S., Santini, L., Brunelli, B., Bambini, S., Biolchi, A., Capecchi, B., Cartocci, E., Ciucchi, L., Di Marcello, F., Ferlicca, F., Galli, B., Luzzi, E., Masignani, V., Serruto, D., Veggi, D., Contorni, M., Morandi, M., Bartalesi, A., Cinotti, V., Mannucci, D., Titta, F., Ovidi, E., Welsch, J. A., Granoff, D., Rappuoli, R., and Pizza, M. (2006) A universal vaccine for serogroup B meningococcus. Proc. Natl. Acad. Sci. USA 103, 10834-10839
2. Comanducci, M., Bambini, S., Brunelli, B., Adu-Bobie, J., Aricò, B., Capecchi, B., Giuliani, M. M., Masignani, V., Santini, L., Savino, S., Granoff, D. M., Caugant, D. A., Pizza, M., Rappuoli, R., and Mora, M. (2002) NadA, a novel vaccine candidate of Neisseria meningitidis. J. Exp. Med. 195, 1445-1454
3. Capecchi, B., Adu-Bobie, J., Di Marcello, F., Ciucchi, L., Masignani, V., Taddei, A., Rappuoli, R., Pizza, M., and Aricò, B. (2005) Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol. Microbiol. 55, 687-698
4. Metruccio, M. M., Pigozzi, E., Roncarati, D., Berlanda Scorza, F., Norais, N., Hill, S. A., Scarlato, V., and Delany, I. (2009) A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements. PLoS Pathog. 5, e1000710
5. Fagnocchi, L., Biolchi, A., Ferlicca, F., Boccadifuoco, G., Brunelli, B., Brier, S., Norais, N., Chiarot, E., Bensi, G., Kroll, J. S., Pizza, M., Donnelly, J., Giuliani, M. M., and Delany, I. (2013) Transcriptional regulation of the nadA gene in Neisseria meningitidis impacts the prediction of coverage of a multicomponent meningococcal serogroup B vaccine. Infect. Immun. 81, 560-569
6. Litt, D. J., Savino, S., Beddek, A., Comanducci, M., Sandiford, C., Stevens, J., Levin, M., Ison, C., Pizza, M., Rappuoli, R., and Kroll, J. S. (2004) Putative vaccine antigens from Neisseria meningitidis recognized by serum antibodies of young children convalescing after meningococcal disease. J. Infect. Dis. 190, 1488-1497
7. Bowe, F., Lavelle, E. C., McNeela, E. A., Hale, C., Clare, S., Arico, B., Giuliani, M. M., Rae, A., Huett, A., Rappuoli, R., Dougan, G., and Mills, K. H. (2004) Mucosal vaccination against serogroup B meningococci: induction of bactericidal antibodies and cellular immunity following intranasal immunization with NadA of Neisseria meningitidis and mutants of Escherichia coli heat-labile enterotoxin. Infect. Immun. 72, 4052-4060
8. Ciabattini, A., Giomarelli, B., Parigi, R., Chiavolini, D., Pettini, E., Aricò, B., Giuliani, M. M., Santini, L., Medaglini, D., and Pozzi, G. (2008) Intranasal immunization of mice with recombinant Streptococcus gordonii expressing NadA of Neisseria meningitidis induces systemic bactericidal antibodies and local IgA. Vaccine 26, 4244-4250
9. Comanducci, M., Bambini, S., Caugant, D. A., Mora, M., Brunelli, B., Capecchi, B., Ciucchi, L., Rappuoli, R., and Pizza, M. (2004) NadA diversity and carriage in Neisseria meningitidis. Infect. Immun. 72, 4217-4223
10. Bambini, S., De Chiara, M., Muzzi, A., Mora, M., Lucidarme, J., Brehony, C., Borrow, R., Masignani, V., Comanducci, M., Maiden, M. C., Rappuoli, R., Pizza, M., and Jolley, K. A. (2014) Neisseria adhesin A variation and revised nomenclature scheme. Clin. Vaccine Immunol. 21, 966-971
11. Bambini, S., Muzzi, A., Olcen, P., Rappuoli, R., Pizza, M., and Comanducci, M. (2009) Distribution and genetic variability of three vaccine components in a panel of strains representative of the diversity of serogroup B meningococcus. Vaccine 27, 2794-2803
12. Lucidarme, J., Comanducci, M., Findlow, J., Gray, S. J., Kaczmarski, E. B., Guiver, M., Kugelberg, E., Vallely, P. J., Oster, P., Pizza, M., Bambini, S., Muzzi, A., Tang, C. M., and Borrow, R. (2009) Characterization of fHbp, nhba (gna2132), nadA, porA, sequence type (ST), and genomic presence of IS1301 in group B meningococcal ST269 clonal complex isolates from England and Wales. J. Clin. Microbiol. 47, 3577-3585
13. Lucidarme, J., Comanducci, M., Findlow, J., Gray, S. J., Kaczmarski, E. B., Guiver, M., Vallely, P. J., Oster, P., Pizza, M., Bambini, S., Muzzi, A., and Borrow, R. (2010) Characterization of fHbp, nhba (gna2132), nadA, porA, and sequence type in group B meningococcal case isolates collected in England and Wales during January 2008 and potential coverage of an investigational group B meningococcal vaccine. Clin. Vaccine Immunol. 17, 919-929
14. Malito, E., Biancucci, M., Faleri, A., Ferlenghi, I., Scarselli, M., Maruggi, G., Lo Surdo, P., Veggi, D., Liguori, A., Santini, L., Bertoldi, I., Petracca, R., Marchi, S., Romagnoli, G., Cartocci, E., Vercellino, I., Savino, S., Spraggon, G., Norais, N., Pizza, M., Rappuoli, R., Masignani, V., and Bottomley, M. J. (2014) Structure of the meningococcal vaccine antigen NadA and epitope mapping of a bactericidal antibody. Proc. Natl. Acad. Sci. USA 111, 17128-17133
15. Morrison, S. L., Johnson, M. J., Herzenberg, L. A., and Oi, V. T. (1984) Chimeric human-antibody molecules: mouse antigen-binding domains with human constant region domains. Proc. Natl. Acad. Sci. USA 81, 6851-6855
16. Waldmann, T. A., and Morris, J. C. (2006) Development of antibodies and chimeric molecules for cancer immunotherapy. Adv. Immunol. 90, 83-131
17. Loo, L., Robinson, M. K., and Adams, G. P. (2008) Antibody engineering principles and applications. Cancer J. 14, 149-153
18. Pillay, V., Gan, H. K., and Scott, A. M. (2011) Antibodies in oncology. N. Biotechnol. 28, 518-529
19. Weis, D. D., Engen, J. R., and Kass, I. J. (2006) Semi-automated data processing of hydrogen exchange mass spectra using HX-Express. J. Am. Soc. Mass Spectrom. 17, 1700-1703
20. Magagnoli, C., Bardotti, A., De Conciliis, G., Galasso, R., Tomei, M., Campa, C., Pennatini, C., Cerchioni, M., Fabbri, B., Giannini, S., Mattioli, G. L., Biolchi, A., D'Ascenzi, S., and Helling, F. (2009) Structural organization of NadADelta(351-405), a recombinant MenB vaccine component, by its physico-chemical characterization at drug substance level. Vaccine 27, 2156-2170
21. Karlsson, R., Katsamba, P. S., Nordin, H., Pol, E., and Myszka, D. G. (2006) Analyzing a kinetic titration series using affinity biosensors. Anal. Biochem. 349, 136-147
22. Wang, Z., Raifu, M., Howard, M., Smith, L., Hansen, D., Goldsby, R., and 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
23. Giuliani, M. M., Santini, L., Brunelli, B., Biolchi, A., Aricò, B., Di Marcello, F., Cartocci, E., Comanducci, M., Masignani, V., Lozzi, L., Savino, S., Scarselli, M., Rappuoli, R., and Pizza, M. (2005) The region comprising amino acids 100 to 255 of Neisseria meningitidis lipoprotein GNA 1870 elicits bactericidal antibodies. Infect. Immun. 73, 1151-1160
24. Borrow, R., Aaberge, I. S., Santos, G. F., Eudey, T. L., Oster, P., Glennie, A., Findlow, J., Høiby, E. A., Rosenqvist, E., Balmer, P., and Martin, D. (2005) Interlaboratory standardization of the measurement of serum bactericidal activity by using human complement against meningococcal serogroup b, strain 44/76-SL, before and after vaccination with the Norwegian MenBvac outer membrane vesicle vaccine. Clin. Diagn. Lab. Immunol. 12, 970-976
25. Hager-Braun, C., and Tomer, K. B. (2005) Determination of protein-derived epitopes by mass spectrometry. Expert Rev. Proteomics 2, 745-756
26. Malito, E., Faleri, A., Lo Surdo, P., Veggi, D., Maruggi, G., Grassi, E., Cartocci, E., Bertoldi, I., Genovese, A., Santini, L., Romagnoli, G., Borgogni, E., Brier, S., Lo Passo, C., Domina, M., Castellino, F., Felici, F., van der Veen, S., Johnson, S., Lea, S. M., Tang, C. M., Pizza, M., Savino, S., Norais, N., Rappuoli, R., Bottomley, M. J., and Masignani, V. (2013) Defining a protective epitope on factor H binding protein, a key meningococcal virulence factor and vaccine antigen. Proc. Natl. Acad. Sci. USA 110, 3304-3309
27. Brier, S., Fagnocchi, L., Donnarumma, D., Scarselli, M., Rappuoli, R., Nissum, M., Delany, I., and Norais, N. (2012) Structural insight into the mechanism of DNA-binding attenuation of the Neisserial adhesin repressor NadR by the small natural ligand 4-hydroxyphenylacetic acid. Biochemistry 51, 6738-6752
28. Scarselli, M., Aricò, B., Brunelli, B., Savino, S., Di Marcello, F., Palumbo, E., Veggi, D., Ciucchi, L., Cartocci, E., Bottomley, M. J., Malito, E., Lo Surdo, P., Comanducci, M., Giuliani, M. M., Cantini, F., Dragonetti, S., Colaprico, A., Doro, F., Giannetti, P., Pallaoro, M., Brogioni, B., Tontini, M., Hilleringmann, M., Nardi-Dei, V., Banci, L., Pizza, M., and Rappuoli, R. (2011) Rational design of a meningococcal antigen inducing broad protective immunity. Sci. Transl. Med. 3, 91ra62
29. Lux, A., and Nimmerjahn, F. (2013) Of mice and men: the need for humanized mouse models to study human IgG activity in vivo. J. Clin. Immunol. 33(Suppl 1), S4-S8
30. Schroeder, Jr., H. W., and Cavacini, L. (2010) Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125(2, Suppl 2)S41-S52
31. Giuntini, S., Reason, D. C., and Granoff, D. M. (2012) Combined roles of human IgG subclass, alternative complement pathway activation, and epitope density in the bactericidal activity of antibodies to meningococcal factor h binding protein. Infect. Immun. 80, 187-194
32. Kilár, F., Simon, I., Lakatos, S., Vonderviszt, F., Medgyesi, G. A., and Závodszky, P. (1985) Conformation of human IgG subclasses in solution. Small-angle X-ray scattering and hydrodynamic studies. Eur. J. Biochem. 147, 17-25
33. Normansell, D. E. (1987) Human immunoglobulin subclasses. Diagn. Clin. Immunol. 5, 115-128
34. Brekke, O. H., Michaelsen, T. E., and Sandlie, I. (1995) The structural requirements for complement activation by IgG: does it hinge on the hinge? Immunol. Today 16, 85-90
35. Fagnocchi, L., Pigozzi, E., Scarlato, V., and Delany, I. (2012) In the NadR regulon, adhesins and diverse meningococcal functions are regulated in response to signals in human saliva. J. Bacteriol. 194, 460-474
36. Mani, A. R., Ippolito, S., Moreno, J. C., Visser, T. J., and Moore, K. P. (2007) The metabolism and dechlorination of chlorotyrosine in vivo. J. Biol. Chem. 282, 29114-29121