The role of peptide loops of the Bordetella pertussis protein P.69 pertactin in antibody recognition

Vaccine

Volumn 25, Issue 31, 2007, Pages 5902-5914

  Hijnen, Marcel ^a   de Voer, Richarda ^a   Mooi, Frits R ^a   Schepp, Rutger ^a   Moret, Ed E ^b   van Gageldonk, Pieter ^a   Smits, Gaby ^a   Berbers, Guy A M ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Bordetella pertussis; Conformational epitopes; Discontinuous epitopes; Epitope mapping; Immune evasion; P.69 pertactin

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; EPITOPE; MONOCLONAL ANTIBODY; PEPTIDE DERIVATIVE; PERTACTIN; PERTUSSIS VACCINE; PROTEIN P.69; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ANTIGEN RECOGNITION; ANTIGENIC VARIATION; ARTICLE; BACTERIAL STRAIN; BINDING SITE; BORDETELLA PERTUSSIS; CRYSTAL STRUCTURE; DELETION MUTANT; IMMUNE RESPONSE; MOUSE; NONHUMAN; PERTUSSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; SITE DIRECTED MUTAGENESIS;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORDETELLA PERTUSSIS; MICE; MICE, INBRED BALB C; PEPTIDES; PERTUSSIS VACCINE; VIRULENCE FACTORS, BORDETELLA;

EID: 34447261439     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2007.05.039     Document Type: Article

References (63)

1. Kerr J.R., and Matthews R.C. Bordetella pertussis infection: pathogenesis, diagnosis, management, and the role of protective immunity. Eur J Clin Microbiol Infect Dis 19 2 (2000) 77-88
2. Mooi F.R., van Loo I.H., and King A.J. Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence?. Emerg Infect Dis 7 (2001) 526-528
3. Bass J.W., and Wittler R.R. Return of epidemic pertussis in the United States. Pediatr Infect Dis J 13 5 (1994) 343-345
4. Andrews R., Herceg A., and Roberts C. Pertussis notifications in Australia, 1991 to 1997. Commun Dis Intell 21 11 (1997) 145-148
5. de Melker H.E., Schellekens J.F., Neppelenbroek S.E., Mooi F.R., Rumke H.C., and Conyn-van Spaendonck M.A. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis 6 4 (2000) 348-357
6. de Melker H.E., Conyn-van Spaendonck M.A., Rumke H.C., van Wijngaarden J.K., Mooi F.R., and Schellekens J.F. Pertussis in The Netherlands: an outbreak despite high levels of immunization with whole-cell vaccine. Emerg Infect Dis 3 2 (1997) 175-178
7. Mooi F.R., van Oirschot H., Heuvelman K., van der Heide H.G., Gaastra W., and Willems R.J. Polymorphism in the Bordetella pertussis virulence factors P.69/pertactin and pertussis toxin in The Netherlands: temporal trends and evidence for vaccine-driven evolution. Infect Immun 66 2 (1998) 670-675
8. Mastrantonio P., Spigaglia P., van Oirschot H., van der Heide H.G., Heuvelman K., Stefanelli P., et al. Antigenic variants in Bordetella pertussis strains isolated from vaccinated and unvaccinated children. Microbiology 145 Pt 8 (1999) 2069-2075
9. Mooi F.R., He Q., van Oirschot H., and Mertsola J. Variation in the Bordetella pertussis virulence factors pertussis toxin and pertactin in vaccine strains and clinical isolates in Finland. Infect Immun 67 6 (1999) 3133-3134
10. Fry N.K., Neal S., Harrison T.G., Miller E., Matthews R., and George R.C. Genotypic variation in the Bordetella pertussis virulence factors pertactin and pertussis toxin in historical and recent clinical isolates in the United Kingdom. Infect Immun 69 9 (2001) 5520-5528
11. Cassiday P., Sanden G., Heuvelman K., Mooi F., Bisgard K.M., and Popovic T. Polymorphism in Bordetella pertussis pertactin and pertussis toxin virulence factors in the United States, 1935-1999. J Infect Dis 182 5 (2000) 1402-1408
12. Gzyl A., Augustynowicz E., Gniadek G., Rabczenko D., Dulny G., and Slusarczyk J. Sequence variation in pertussis S1 subunit toxin and pertussis genes in Bordetella pertussis strains used for the whole-cell pertussis vaccine produced in Poland since 1960: efficiency of the DTwP vaccine-induced immunity against currently circulating B. pertussis isolates. Vaccine 22 17-18 (2004) 2122-2128
13. Weber C., Boursaux-Eude C., Coralie G., Caro V., and Guiso N. Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J Clin Microbiol 39 12 (2001) 4396-4403
14. Poynten M., McIntyre P.B., Mooi F.R., Heuvelman K.J., and Gilbert G.L. Temporal trends in circulating Bordetella pertussis strains in Australia. Epidemiol Infect 132 2 (2004) 185-193
15. Gzyl A., Augustynowicz E., Loo I., and Slusarczyk J. Temporal nucleotide changes in pertactin and pertussis toxin genes in Bordetella pertussis strains isolated from clinical cases in Poland. Vaccine 20 3-4 (2001) 299-303
16. Kourova N., Caro V., Weber C., Thiberge S., Chuprinina R., Tseneva G., et al. Comparison of the Bordetella pertussis and Bordetella parapertussis isolates circulating in Saint Petersburg between 1998 and 2000 with Russian vaccine strains. J Clin Microbiol 41 8 (2003) 3706-3711
17. Guiso N., Boursaux-Eude C., Weber C., Hausman S.Z., Sato H., Iwak M., et al. Analysis of Bordetella pertussis isolates collected in Japan before and after introduction of acellular pertussis vaccines. Vaccine 19 23-24 (2001) 3248-3252
18. van Loo I.H., van der Heide H.G., Nagelkerke N.J., Verhoef J., and Mooi F.R. Temporal trends in the population structure of Bordetella pertussis during 1949-1996 in a highly vaccinated population. J Infect Dis 179 4 (1999) 915-923
19. Cherry J.D., Gornbein J., Heininger U., and Stehr K. A search for serologic correlates of immunity to Bordetella pertussis cough illnesses. Vaccine 16 20 (1998) 1901-1906
20. Storsaeter J., Hallander H.O., Gustafsson L., and Olin P. Levels of anti-pertussis antibodies related to protection after household exposure to Bordetella pertussis. Vaccine 16 20 (1998) 1907-1916
21. Gustafsson L., Hallander H.O., Olin P., Reizenstein E., and Storsaeter J. A controlled trial of a two-component acellular, a five-component acellular, and a whole-cell pertussis vaccine. N Engl J Med 334 6 (1996) 349-355
22. Miller E. Overview of recent clinical trials of acellular pertussis vaccines. Biologicals 27 2 (1999) 79-86
23. Plotkin S.A., and Cadoz M. Acellular vaccine efficacy trials. Pediatr Infect Dis J 16 9 (1997) 913-914
24. King A.J., Berbers G., van Oirschot H.F., Hoogerhout P., Knipping K., and Mooi F.R. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology 147 (2001) 2885-2895
25. Kobisch M., and Novotny P. Identification of a 68-kilodalton outer membrane protein as the major protective antigen of Bordetella bronchiseptica by using specific-pathogen-free piglets. Infect Immun 58 2 (1990) 352-357
26. Hellwig S.M., Rodriguez M.E., Berbers G.A., Van De Winkel J.G., and Mooi F.R. Crucial role of antibodies to pertactin in Bordetella pertussis immunity. J Infect Dis 188 5 (2003) 738-742
27. He Q., Makinen J., Berbers G., Mooi F.R., Viljanen M.K., Arvilommi H., et al. Bordetella pertussis protein pertactin induces type-specific antibodies: one possible explanation for the emergence of antigenic variants?. J Infect Dis 187 8 (2003) 1200-1205
28. Henderson I.R., Cappello R., and Nataro J.P. Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol 8 12 (2000) 529-532
29. Henderson I.R., Navarro-Garcia F., and Nataro J.P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6 9 (1998) 370-378
30. Henderson I.R., and Nataro J.P. Virulence functions of autotransporter proteins. Infect Immun 69 3 (2001) 1231-1243
31. Charles I., Fairweather N., Pickard D., Beesley J., Anderson R., Dougan G., et al. Expression of the Bordetella pertussis P.69 pertactin adhesin in Escherichia coli: fate of the carboxy-terminal domain. Microbiology 140 (1994) 3301-3308
32. Gotto J.W., Eckhardt T., Reilly P.A., Scott J.V., Cowell J.L., Metcalf T.N., et al. Biochemical and immunological properties of two forms of pertactin, the 69,000-molecular-weight outer membrane protein of Bordetella pertussis. Infect Immun 61 5 (1993) 2211-2215
33. Emsley P., Charles I.G., Fairweather N.F., and Isaacs N.W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381 6577 (1996) 90-92
34. Mooi F.R., Hallander H., Wirsing Von Konig C.H., Hoet B., and Guiso N. Epidemiological typing of Bordetella pertussis isolates: recommendations for a standard methodology. Eur J Clin Microbiol Infect Dis 19 3 (2000) 174-181
35. Leininger E., Ewanowich C.A., Bhargava A., Peppler M.S., Kenimer J.G., and Brennan M.J. Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect Immun 60 6 (1992) 2380-2385
36. Leininger E., Roberts M., Kenimer J.G., Charles I.G., Fairweather N., Novotny P., et al. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci USA 88 2 (1991) 345-349
37. Khelef N., Danve B., Quentin-Millet M.J., and Guiso N. Bordetella pertussis and Bordetella parapertussis: two immunologically distinct species. Infect Immun 61 2 (1993) 486-490
38. Hijnen M., Mooi F.R., van Gageldonk P.G., Hoogerhout P., King A.J., and Berbers G.A. Epitope structure of the Bordetella pertussis protein P.69 pertactin, a major vaccine component and protective antigen. Infect Immun 72 7 (2004) 3716-3723
39. Berbers G.A., Marzec A.H., Bastmeijer M., van Gageldonk P.G., and Plantinga A.D. Blocking ELISA for detection of mumps virus antibodies in human sera. J Virol Met 42 2-3 (1993) 155-168
40. Malmqvist M. Biospecific interaction analysis using biosensor technology. Nature 361 6408 (1993) 186-187
41. Van Der Geld Y.M., Limburg P.C., and Kallenberg C.G. Characterization of monoclonal antibodies to proteinase 3 (PR3) as candidate tools for epitope mapping of human anti-PR3 autoantibodies. Clin Exp Immunol 118 3 (1999) 487-496
42. Johnsson B., Lofas S., and Lindquist G. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 198 2 (1991) 268-277
43. Hijnen M., van Gageldonk P.G., Berbers G.A., van Woerkom T., and Mooi F.R. The Bordetella pertussis virulence factor P.69 pertactin retains its immunological properties after overproduction in Escherichia coli. Protein Expr Purif 41 1 (2005) 106-112
44. Junker M., Schuster C.C., McDonnell A.V., Sorg K.A., Finn M.C., Berger B., et al. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc Natl Acad Sci USA 103 13 (2006) 4918-4923
45. Anttila M., Eskola J., Ahman H., and Kayhty H. Avidity of IgG for Streptococcus pneumoniae type 6B and 23F polysaccharides in infants primed with pneumococcal conjugates and boosted with polysaccharide or conjugate vaccines. J Infect Dis 177 6 (1998) 1614-1621
46. Vermont C.L., van Dijken H.H., van Limpt C.J., de G.R., van A.L., and van Den Dobbelsteen G.P. Antibody avidity and immunoglobulin G isotype distribution following immunization with a monovalent meningococcal B outer membrane vesicle vaccine. Infect Immun 70 2 (2002) 584-590
47. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The protein data bank. Nucl Acids Res 28 1 (2000) 235-242
48. Vriend G. WHAT IF: a molecular modeling and drug design program. J Mol Graph 8 1 (1990) 52-56 p. 29
49. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 15 (1997) 2714-2723
50. Fraczkiewicz R., and Braun W. Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J Comput Chem 19 3 (1998) 319-333 July 12
51. Oliver D.C., Huang G., Nodel E., Pleasance S., and Fernandez R.C. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 47 5 (2003) 1367-1383
52. Kang S.M., Quan F.S., Huang C., Guo L., Ye L., Yang C., et al. Modified HIV envelope proteins with enhanced binding to neutralizing monoclonal antibodies. Virology 331 1 (2005) 20-32
53. Koch M., Pancera M., Kwong P.D., Kolchinsky P., Grundner C., Wang L., et al. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology 313 2 (2003) 387-400
54. David S., van F.R., and Mooi F.R. Efficacies of whole cell and acellular pertussis vaccines against Bordetella parapertussis in a mouse model. Vaccine 22 15-16 (2004) 1892-1898
55. van Dolleweerd C.J., Chargelegue D., and Ma J.K. Characterization of the conformational epitope of Guy's 13, a monoclonal antibody that prevents Streptococcus mutans colonization in humans. Infect Immun 71 2 (2003) 754-765
56. Rhodin N.R., Cutalo J.M., Tomer K.B., McArthur W.P., and Brady L.J. Characterization of the Streptococcus mutans P1 epitope recognized by immunomodulatory monoclonal antibody 6-11A. Infect Immun 72 8 (2004) 4680-4688
57. Seifert T.B., Bleiweis A.S., and Brady L.J. Contribution of the alanine-rich region of Streptococcus mutans P1 to antigenicity, surface expression, and interaction with the proline-rich repeat domain. Infect Immun 72 8 (2004) 4699-4706
58. Streisinger G., and Owen J. Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4. Genetics 109 4 (1985) 633-659
59. Madoff L.C., Michel J.L., Gong E.W., Kling D.E., and Kasper D.L. Group B streptococci escape host immunity by deletion of tandem repeat elements of the alpha C protein. Proc Natl Acad Sci USA 93 9 (1996) 4131-4136
60. Hijnen M. The Bordetella pertussis protein Pertactin: role in immunity and immune evasion. Ph.D. Thesis. University of Utrecht, Utrecht, the Netherlands January 2006.
61. Diavatopoulos D.A., Hijnen M., and Mooi F.R. Adaptive evolution of the Bordetella autotransporter pertactin. J Evol Biol 19 6 (2006) 1931-1938
62. Chivian D., Kim D.E., Malmstrom L., Bradley P., Robertson T., Murphy P., et al. Automated prediction of CASP-5 structures using the Robetta server. Proteins 53 Suppl. 6 (2003) 524-533
63. Kim D.E., Chivian D., and Baker D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32 Web Server issue (2004) W526-W531