Identification of new meningococcal serogroup B surface antigens through a systematic analysis of neisserial genomes

Vaccine

Volumn 28, Issue 2, 2009, Pages 532-541

  Pajon, Rolando ^a   Yero, Daniel ^a,b   Niebla, Olivia ^a   Climent, Yanet ^a,b   Sardiñas, Gretel ^a   García, Darién ^a   Perera, Yasser ^a   Llanes, Alejandro ^a   Delgado, Maité ^a   Cobas, Karem ^a   Caballero, Evelin ^a   Taylor, Stephen ^c   Brookes, Charlotte ^c   Gorringe, Andrew ^c  

^a CENTER FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Cuba)

^b FINLAY INSTITUTE   (Cuba)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

BamC; Curli; Genomics; Neisseria meningitidis; Positive selection; Proteomics; Vaccine

Indexed keywords

MENINGOCOCCUS VACCINE; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; GENETIC CODE; GENETIC VARIABILITY; GENOME ANALYSIS; HIGH THROUGHPUT SCREENING; IMMUNE RESPONSE; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UNINDEXED SEQUENCE;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, BACTERIAL; COMPUTATIONAL BIOLOGY; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENOME, BACTERIAL; MENINGOCOCCAL VACCINES; MICE; MICE, INBRED BALB C; NEISSERIA MENINGITIDIS, SEROGROUP B; POLYMERASE CHAIN REACTION; RATS;

EID: 70849130929     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.09.128     Document Type: Article

References (73)

1. Perrett K.P., and Pollard A.J. Towards an improved serogroup B Neisseria meningitidis vaccine. Expert Opin Biol Ther 5 12 (2005) 1611-1625
2. Cartwright K.A., Stuart J.M., Jones D.M., and Noah N.D. The Stonehouse survey: nasopharyngeal carriage of meningococci and Neisseria lactamica. Epidemiol Infect 99 3 (1987) 591-601
3. Pollard A.J. Global epidemiology of meningococcal disease and vaccine efficacy. Pediatr Infect Dis J 23 12 Suppl. (2004) S274-S279
4. Mitka M. New vaccine should ease meningitis fears. JAMA 293 12 (2005) 1433-1434
5. Stephens D.S. Conquering the meningococcus. FEMS Microbiol Rev 31 1 (2007) 3-14
6. Finne J., Leinonen M., and Makela P.H. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet 2 8346 (1983) 355-357
7. Fredriksen J.H., Rosenqvist E., Wedege E., Bryn K., Bjune G., Froholm L.O., et al. Production, characterization and control of MenB-vaccine "Folkehelsa": an outer membrane vesicle vaccine against group B meningococcal disease. NIPH Ann 14 2 (1991) 67-79
8. Sierra G.V., Campa H.C., Varcacel N.M., Garcia I.L., Izquierdo P.L., Sotolongo P.F., et al. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann 14 2 (1991) 195-207
9. Bjune G., Hoiby E.A., Gronnesby J.K., Arnesen O., Fredriksen J.H., Halstensen A., et al. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet 338 8775 (1991) 1093-1096
10. Tappero J.W., Lagos R., Ballesteros A.M., Plikaytis B., Williams D., Dykes J., et al. Immunogenicity of 2 serogroup B outer-membrane protein meningococcal vaccines: a randomized controlled trial in Chile. JAMA 281 16 (1999) 1520-1527
11. Holst J., Feiring B., Naess L.M., Norheim G., Kristiansen P., Hoiby E.A., et al. The concept of "tailor-made", protein-based, outer membrane vesicle vaccines against meningococcal disease. Vaccine 23 17-18 (2005) 2202-2205
12. Perkins B.A., Jonsdottir K., Briem H., Griffiths E., Plikaytis B.D., Hoiby E.A., et al. Immunogenicity of two efficacious outer membrane protein-based serogroup B meningococcal vaccines among young adults in Iceland. J Infect Dis 177 3 (1998) 683-691
13. Grifantini R., Bartolini E., Muzzi A., Draghi M., Frigimelica E., Berger J., et al. Previously unrecognized vaccine candidates against group B meningococcus identified by DNA microarrays. Nat Biotechnol 20 9 (2002) 914-921
14. Hotopp J.C., Grifantini R., Kumar N., Tzeng Y.L., Fouts D., Frigimelica E., et al. Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 152 Pt 12 (2006) 3733-3749
15. Pizza M., Scarlato V., Masignani V., Giuliani M.M., Arico B., Comanducci M., et al. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 287 5459 (2000) 1816-1820
16. Wheeler J.X., Vipond C., and Feavers I.M. Exploring the proteome of meningococcal outer membrane vesicles vaccines. Proteomics Clin Appl 1 (2007) 1198-1210
17. Litt D.J., Savino S., Beddek A., Comanducci M., Sandiford C., Stevens J., et al. Putative vaccine antigens from Neisseria meningitidis recognized by serum antibodies of young children convalescing after meningococcal disease. J Infect Dis 190 8 (2004) 1488-1497
18. Yero D., Pajon R., Perez Y., Farinas M., Cobas K., Diaz D., et al. Identification by genomic immunization of a pool of DNA vaccine candidates that confer protective immunity in mice against Neisseria meningitidis serogroup B. Vaccine 25 28 (2007) 5175-5188
19. Ferrari G., Garaguso I., Adu-Bobie J., Doro F., Taddei A.R., Biolchi A., et al. Outer membrane vesicles from group B Neisseria meningitidis delta gna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 6 6 (2006) 1856-1866
20. Giuliani M.M., Adu-Bobie J., Comanducci M., Arico B., Savino S., Santini L., et al. A universal vaccine for serogroup B meningococcus. Proc Natl Acad Sci USA 103 29 (2006) 10834-10839
21. Parkhill J., Achtman M., James K.D., Bentley S.D., Churcher C., Klee S.R., et al. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404 6777 (2000) 502-506
22. Bentley S.D., Vernikos G.S., Snyder L.A., Churcher C., Arrowsmith C., Chillingworth T., et al. Meningococcal genetic variation mechanisms viewed through comparative analysis of serogroup C strain FAM18. PLoS Genet 3 2 (2007) e23
23. Peng J., Yang L., Yang F., Yang J., Yan Y., Nie H., et al. Characterization of ST-4821 complex, a unique Neisseria meningitidis clone. Genomics 91 1 (2008) 78-87
24. Serruto D., Serino L., Masignani V., and Pizza M. Genome-based approaches to develop vaccines against bacterial pathogens. Vaccine (2009)
25. Bernardini G., Renzone G., Comanducci M., Mini R., Arena S., D'Ambrosio C., et al. Proteome analysis of Neisseria meningitidis serogroup A. Proteomics 4 10 (2004) 2893-2926
26. Mignogna G., Giorgi A., Stefanelli P., Neri A., Colotti G., Maras B., et al. Inventory of the proteins in Neisseria meningitidis serogroup B strain MC58. J Proteome Res 4 4 (2005) 1361-1370
27. Vipond C., Suker J., Jones C., Tang C., Feavers I.M., and Wheeler J.X. Proteomic analysis of a meningococcal outer membrane vesicle vaccine prepared from the group B strain NZ98/254. Proteomics 6 11 (2006) 3400-3413
28. Uli L., Castellanos-Serra L., Betancourt L., Dominguez F., Barbera R., Sotolongo F., et al. Outer membrane vesicles of the VA-MENGOC-BC(R) vaccine against serogroup B of Neisseria meningitidis: analysis of protein components by two-dimensional gel electrophoresis and mass spectrometry. Proteomics 6 11 (2006) 3389-3399
29. Vaughan T.E., Skipp P.J., O'Connor C.D., Hudson M.J., Vipond R., Elmore M.J., et al. Proteomic analysis of Neisseria lactamica and Neisseria meningitidis outer membrane vesicle vaccine antigens. Vaccine 24 25 (2006) 5277-5293
30. Yero D., Pajon R., Niebla O., Sardinas G., Vivar I., Perera Y., et al. Bicistronic expression plasmid for the rapid production of recombinant fused proteins in Escherichia coli. Biotechnol Appl Biochem 44 Pt 1 (2006) 27-34
31. Aggarwal G., and Ramaswamy R. Ab initio gene identification: prokaryote genome annotation with GeneScan and GLIMMER. J Biosci 27 1 Suppl. 1 (2002) 7-14
32. Garrow A.G., Agnew A., and Westhead D.R. TMB-Hunt: a web server to screen sequence sets for transmembrane beta-barrel proteins. Nucleic Acids Res 33 Web Server issue (2005) W188-W192
33. Pajon R., Yero D., Lage A., Llanes A., and Borroto C.J. Computational identification of beta-barrel outer-membrane proteins in Mycobacterium tuberculosis predicted proteomes as putative vaccine candidates. Tuberculosis (Edinb) 86 3-4 (2006) 290-302
34. Waterhouse A.M., Procter J.B., Martin D.M., Clamp M., and Barton G.J. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 9 (2009) 1189-1191
35. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 5 (2003) 696-704
36. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5 2 (2004) 150-163
37. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 8 (2007) 1586-1591
38. Pond S.L., and Frost S.D. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21 10 (2005) 2531-2533
39. Rosenqvist E., Wedege E., Hoiby E.A., and Froholm L.O. Serogroup determination of Neisseria meningitidis by whole-cell ELISA, dot-blotting and agglutination. APMIS 98 6 (1990) 501-506
40. Maslanka S.E., Gheesling L.L., Libutti D.E., Donaldson K.B., Harakeh H.S., Dykes J.K., et al. Standardization and a multilaboratory comparison of Neisseria meningitidis serogroup A and C serum bactericidal assays. The Multilaboratory Study Group. Clin Diagn Lab Immunol 4 2 (1997) 156-167
41. Yero C.D., Pajon F.R., Caballero M.E., Cobas A.K., Lopez H.Y., Farinas M.M., et al. Immunization of mice with Neisseria meningitidis serogroup B genomic expression libraries elicits functional antibodies and reduces the level of bacteremia in an infant rat infection model. Vaccine 23 7 (2005) 932-939
42. Snyder L.A., Butcher S.A., and Saunders N.J. Comparative whole-genome analyses reveal over 100 putative phase-variable genes in the pathogenic Neisseria spp. Microbiology 147 Pt 8 (2001) 2321-2332
43. Delgado M., Yero D., Niebla O., Gonzalez S., Climent Y., Perez Y., et al. Lipoprotein NMB0928 from Neisseria meningitidis serogroup B as a novel vaccine candidate. Vaccine 25 50 (2007) 8420-8431
44. Niebla O., Alvarez A., Martin A., Rodriguez A., Delgado M., Falcon V., et al. Immunogenicity of recombinant class 1 protein from Neisseria meningitidis refolded into phospholipid vesicles and detergent. Vaccine 19 25-26 (2001) 3568-3574
45. Musacchio A., Carmenate T., Delgado M., and Gonzalez S. Recombinant Opc meningococcal protein, folded in vitro, elicits bactericidal antibodies after immunization. Vaccine 15 6-7 (1997) 751-758
46. Urwin R., Holmes E.C., Fox A.J., Derrick J.P., and Maiden M.C. Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. Mol Biol Evol 19 10 (2002) 1686-1694
47. Andrews T.D., and Gojobori T. Strong positive selection and recombination drive the antigenic variation of the PilE protein of the human pathogen Neisseria meningitidis. Genetics 166 1 (2004) 25-32
48. Yang Z., Wong W.S., and Nielsen R. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22 4 (2005) 1107-1118
49. Charo J., Geluk A., Sundback M., Mirzai B., Diehl A.D., Malmberg K.J., et al. The identification of a common pathogen-specific HLA class I A*0201-restricted cytotoxic T cell epitope encoded within the heat shock protein 65. Eur J Immunol 31 12 (2001) 3602-3611
50. Koebnik R., Locher K.P., and Van G.P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37 2 (2000) 239-253
51. Masignani V., Balducci E., Serruto D., Veggi D., Arico B., Comanducci M., et al. In silico identification of novel bacterial ADP-ribosyltransferases. Int J Med Microbiol 293 7-8 (2004) 471-478
52. Cantini F., Veggi D., Dragonetti S., Savino S., Scarselli M., Romagnoli G., et al. Solution structure of the factor H-binding protein, a survival factor and protective antigen of Neisseria meningitidis. J Biol Chem 284 14 (2009) 9022-9026
53. Pajon R., Chinea G., Marrero E., Gonzalez D., and Guillen G. Sequence analysis of the structural tbpA gene: protein topology and variable regions within neisserial receptors for transferrin iron acquisition. Microb Pathog 23 2 (1997) 71-84
54. Sardinas G., Yero D., Climent Y., Caballero E., Cobas K., and Niebla O. Neisseria meningitidis antigen NMB0088: sequence variability, protein topology and vaccine potential. J Med Microbiol 58 Pt 2 (2009) 196-208
55. Lin H.H., Zhang G.L., Tongchusak S., Reinherz E.L., and Brusic V. Evaluation of MHC-II peptide binding prediction servers: applications for vaccine research. BMC Bioinformatics 9 Suppl. 12 (2008) S22
56. Dieckman L., Gu M., Stols L., Donnelly M.I., and Collart F.R. High throughput methods for gene cloning and expression. Protein Expr Purif 25 1 (2002) 1-7
57. Misra R. First glimpse of the crystal structure of YaeT's POTRA domains. ACS Chem Biol 2 10 (2007) 649-651
58. Onufryk C., Crouch M.L., Fang F.C., and Gross C.A. Characterization of six lipoproteins in the sigmaE regulon. J Bacteriol 187 13 (2005) 4552-4561
59. Rizzitello A.E., Harper J.R., and Silhavy T.J. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183 23 (2001) 6794-6800
60. Bouvier J., Pugsley A.P., and Stragier P. A gene for a new lipoprotein in the dapA-purC interval of the Escherichia coli chromosome. J Bacteriol 173 17 (1991) 5523-5531
61. Malinverni J.C., Werner J., Kim S., Sklar J.G., Kahne D., Misra R., et al. YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61 1 (2006) 151-164
62. Yokota N., Kuroda T., Matsuyama S., and Tokuda H. Characterization of the LolA-LolB system as the general lipoprotein localization mechanism of Escherichia coli. J Biol Chem 274 43 (1999) 30995-30999
63. Vemulapalli R., Duncan A.J., Boyle S.M., Sriranganathan N., Toth T.E., and Schurig G.G. Cloning and sequencing of yajC and secD homologs of Brucella abortus and demonstration of immune responses to YajC in mice vaccinated with B. abortus RB51. Infect Immun 66 12 (1998) 5684-5691
64. Soto G.E., and Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181 4 (1999) 1059-1071
65. Martin D., Cadieux N., Hamel J., and Brodeur B.R. Highly conserved Neisseria meningitidis surface protein confers protection against experimental infection. J Exp Med 185 7 (1997) 1173-1183
66. Prochazkova K., Osicka R., Linhartova I., Halada P., Sulc M., and Sebo P. The Neisseria meningitidis outer membrane lipoprotein FrpD binds the RTX protein FrpC. J Biol Chem 280 5 (2005) 3251-3258
67. Masignani V., Comanducci M., Giuliani M.M., Bambini S., Adu-Bobie J., Arico B., et al. Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J Exp Med 197 6 (2003) 789-799
68. Comanducci M., Bambini S., Brunelli B., Adu-Bobie J., Arico B., Capecchi B., et al. NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 195 11 (2002) 1445-1454
69. Jacobsson S., Thulin S., Mölling P., Unemo M., Comanducci M., Rappuoli R., et al. Sequence constancies and variations in genes encoding three new meningococcal vaccine candidate antigens. Vaccine 24 12 (2006) 2161-2168
70. Fletcher L.D., Bernfield L., Barniak V., Farley J.E., Howell A., Knauf M., et al. Vaccine potential of the Neisseria meningitidis 2086 lipoprotein. Infect Immun 72 4 (2004) 2088-2100
71. Comanducci M., Bambini S., Caugant D.A., Mora M., Brunelli B., Capecchi B., et al. NadA diversity and carriage in Neisseria meningitidis. Infect Immun 72 7 (2004) 4217-4223
72. Arenas J., Abel A., Sanchez S., Marzoa J., Berron S., van der L.P., et al. A cross-reactive neisserial antigen encoded by the NMB0035 locus shows high sequence conservation but variable surface accessibility. J Med Microbiol 57 Pt 1 (2008) 80-87
73. Borrow R., Carlone G.M., Rosenstein N., Blake M., Feavers I., Martin D., et al. Neisseria meningitidis group B correlates of protection and assay standardization-international meeting report Emory University, Atlanta, Georgia, United States, 16-17 March 2005. Vaccine 24 24 (2006) 5093-5107