1887

Abstract

One potential vaccine strategy in the fight against meningococcal disease involves the exploitation of outer-membrane components of , a commensal bacterium closely related to the meningococcus, . Although shares many surface structures with the meningococcus, little is known about the antigenic diversity of this commensal bacterium or the antigenic relationships between and . Here, the porin protein (Por) was examined and compared to the related PorB antigens of , to investigate potential involvement in anti-meningococcal immunity. Relationships among porin sequences were determined using distance-based methods and , and maximum-likelihood analyses were used to compare the selection pressures acting on the encoded proteins. These analyses demonstrated that the porin was less diverse than meningococcal PorB and although it was subject to positive selection, this was not as strong as the positive selection pressures acting on the meningococcal porin. In addition, the porin gene sequences and the protein sequences of the loop regions predicted to be exposed to the human immune system were dissimilar to the corresponding sequences in the meningococcus. This suggests that Por, contrary to previous suggestions, may have limited involvement in the development of natural immunity to meningococcal disease and might not be effective as a meningococcal vaccine component.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/015479-0
2008-05-01
2020-04-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/5/1525.html?itemId=/content/journal/micro/10.1099/mic.0.2007/015479-0&mimeType=html&fmt=ahah

References

  1. Achouak W., Heulin T., Pages J. M.. 2001; Multiple facets of bacterial porins. FEMS Microbiol Lett199:1–7
    [Google Scholar]
  2. Bennett J. S.. 2006; The relationship of Neisseria lactamica to the pathogenic Neisseria: implications for vaccine development DPhil thesis Department of Zoology, University of Oxford; Oxford:
    [Google Scholar]
  3. Bennett J. S., Griffiths D. T., McCarthy N. D., Sleeman K. L., Jolley K. A., Crook D. W., Maiden M. C.. 2005; Genetic diversity and carriage dynamics of Neisseria lactamica in infants. Infect Immun73:2424–2432
    [Google Scholar]
  4. Bennett J. S., Jolley K. A., Sparling P. F., Saunders N. J., Hart C. A., Feavers I. M., Maiden M. C.. 2007; Species status of Neisseria gonorrhoeae : evolutionary and epidemiological inferences from MLST. BMC Biol5:35
    [Google Scholar]
  5. Bjune G., Høiby E. A., Grønnesby J. K., Arnesen O., Fredriksen J. H., Halstensen A., Holten E., Lindbak A. K., Nøkleby H.. other authors 1991; Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway. Lancet338:1093–1096
    [Google Scholar]
  6. Boslego J., Garcia J., Cruz C., Zollinger W., Brandt B., Ruiz S., Martinez M., Arthur J., Underwood P.. other authors 1995; Efficacy, safety, and immunogenicity of a meningococcal group B (15 : P1.3) outer membrane protein vaccine in Iquique, Chile. Vaccine13:821–829
    [Google Scholar]
  7. Derrick J. P., Urwin R., Suker J., Feavers I. M., Maiden M. C. J.. 1999; Structural and evolutionary inference from molecular variation in Neisseria porins. Infect Immun67:2406–2413
    [Google Scholar]
  8. Feavers I. M., Maiden M. C. J.. 1998; A gonococcal porA pseudogene: implications for understanding the evolution and pathogenicity of Neisseria gonorrhoeae . Mol Microbiol30:647–656
    [Google Scholar]
  9. Finne J., Bitter Suermann D., Goridis C., Finne U.. 1987; An IgG monoclonal antibody to group B meningococci cross-reacts with developmentally regulated polysialic acid units of glycoproteins in neural and extraneural tissues. J Immunol138:4402–4407
    [Google Scholar]
  10. Finney M., Vaughan T., Taylor S., Hudson M. J., Pratt C., Wheeler J. X., Vipond C., Feavers I., Jones C.. other authors 2007; Characterization of the key antigenic components and pre-clinical immune responses to a meningococcal disease vaccine based on Neisseria lactamica outer membrane vesicles. Hum Vaccin3:
    [Google Scholar]
  11. Gill M. J., Simjee S., Al-Hattawi K., Robertson B. D., Easmon C. S., Ison C. A.. 1998; Gonococcal resistance to β -lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob Agents Chemother42:2799–2803
    [Google Scholar]
  12. Gold R., Goldschneider I., Lepow M. L., Draper T. F., Randolph M.. 1978; Carriage of Neisseria meningitidis and Neisseria lactamica in infants and children. J Infect Dis137:112–121
    [Google Scholar]
  13. Gorringe A. R.. 2005; Can Neisseria lactamica antigens provide an effective vaccine to prevent meningococcal disease?. Expert Rev Vaccines4:373–379
    [Google Scholar]
  14. Gray S. J., Trotter C. L., Ramsay M. E., Guiver M., Fox A. J., Borrow R., Mallard R. H., Kaczmarski E. B.. 2006; Epidemiology of meningococcal disease in England and Wales 1993/94 to 2003/04: contribution and experiences of the Meningococcal Reference Unit. J Med Microbiol55:887–896
    [Google Scholar]
  15. Griffiss J. M., Brandt B., Jarvis G. A.. 1987; Natural immunity to Neisseria meningitidis . In Evolution of Meningococcal Disease vol. II pp99–119 Edited by Vedros N. A. Boca Raton, FL: CRC Press;
    [Google Scholar]
  16. Griffiss J. M., Yamasaki R., Estabrook M., Kim J. J.. 1991; Meningococcal molecular mimicry and the search for an ideal vaccine. Trans R Soc Trop Med Hyg85:Suppl 132–36
    [Google Scholar]
  17. Guibourdenche M., Popoff M. Y., Riou J. Y.. 1986; Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and “ Neisseria polysaccharea ”. Ann Inst Pasteur Microbiol137B:177–185
    [Google Scholar]
  18. Jelfs J., Munro R., Wedege E., Caugant D. A.. 2000; Sequence variation in the porA gene of a clone of Neisseria meningitidis during epidemic spread. Clin Diagn Lab Immunol7:390–395
    [Google Scholar]
  19. Jolley K. A., Chan M. S., Maiden M. C.. 2004; mlstdbNet – distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics5:86
    [Google Scholar]
  20. Kim J. J., Mandrell R. E., Griffiss J. M.. 1989; Neisseria lactamica and Neisseria meningitidis share lipooligosaccharide epitopes but lack common capsular and class 1, 2, and 3 protein epitopes. Infect Immun57:602–608
    [Google Scholar]
  21. Kimura M.. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol16:111–120
    [Google Scholar]
  22. Kraulis P. J.. 1991; MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr24:946–950
    [Google Scholar]
  23. Kumar S., Tamura K., Jakobsen I. B., Nei M.. 2001; mega2: Molecular Evolutionary Genetics Analysis software. Bioinformatics17:1244–1245
    [Google Scholar]
  24. Li Y., Zhang Q., Winterbotham M., Mowe E., Gorringe A., Tang C. M.. 2006; Immunization with live Neisseria lactamica protects mice against meningococcal challenge and can elicit serum bactericidal antibodies. Infect Immun74:6348–6355
    [Google Scholar]
  25. Linz B., Schenker M., Zhu P., Achtman M.. 2000; Frequent interspecific genetic exchange between commensal neisseriae and Neisseria meningitidis . Mol Microbiol36:1049–1058
    [Google Scholar]
  26. Maiden M. C. J., Suker J., McKenna A. J., Bygraves J. A., Feavers I. M.. 1991; Comparison of the class 1 outer membrane proteins of eight serological reference strains of Neisseria meningitidis . Mol Microbiol5:727–736
    [Google Scholar]
  27. Majewski J.. 2001; Sexual isolation in bacteria. FEMS Microbiol Lett199:161–169
    [Google Scholar]
  28. Oliver K. J., Reddin K. M., Bracegirdle P., Hudson M. J., Borrow R., Feavers I. M., Robinson A., Cartwright K., Gorringe A. R.. 2002; Neisseria lactamica protects against experimental meningococcal infection. Infect Immun70:3621–3626
    [Google Scholar]
  29. Rudel T., Schmid A., Benz R., Kolb H. A., Lang F., Meyer T. F.. 1996; Modulation of Neisseria porin (PorB) by cytosolic ATP/GTP of target cells: parallels between pathogen accommodation and mitochondrial endosymbiosis. Cell85:391–402
    [Google Scholar]
  30. Russell J. E., Jolley K. A., Feavers I. M., Maiden M. C., Suker J.. 2004; PorA variable regions of Neisseria meningitidis . Emerg Infect Dis10:674–678
    [Google Scholar]
  31. Sali A., Potterton L., Yuan F., van Vlijmen H., Karplus M.. 1995; Evaluation of comparative protein modeling by MODELLER. Proteins23:318–326
    [Google Scholar]
  32. Schifman R. B., Ryan K. J.. 1983; Neisseria lactamica septicemia in an immunocompromised patient. J Clin Microbiol17:934–935
    [Google Scholar]
  33. Schirmer T.. 1998; General and specific porins from bacterial outer membranes. J Struct Biol121:101–109
    [Google Scholar]
  34. Schneider S., Roessli D., Excoffier L.. 2000; Arlequin version 2.000: a software for population genetic data analysis Geneva: University of Geneva;
    [Google Scholar]
  35. Staden R.. 1996; The Staden sequence analysis package. Mol Biotechnol5:233–241
    [Google Scholar]
  36. Suker J.. 1997; Variation of meningococcal porin antigens PhD thesis Department of Biochemistry, Royal Free Hospital School of Medicine, University of London;
    [Google Scholar]
  37. Swofford D.. 1998; paup*: Phylogenetic analysis using parsimony (and other methods Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  38. Tang C., Moxon R., Levine M. M.. 1999; For discussion: live attenuated vaccines for group B meningococcus. Vaccine17:114–117
    [Google Scholar]
  39. Troncoso G., Sanchez S., Moreda M., Criado M. T., Ferreiros C. M.. 2000; Antigenic cross-reactivity between outer membrane proteins of Neisseria meningitidis and commensal Neisseria species. FEMS Immunol Med Microbiol27:103–109
    [Google Scholar]
  40. Troncoso G., Sanchez S., Criado M. T., Ferreiros C. M.. 2002; Analysis of Neisseria lactamica antigens putatively implicated in acquisition of natural immunity to Neisseria meningitidis . FEMS Immunol Med Microbiol34:9–15
    [Google Scholar]
  41. Urwin R., Holmes E. C., Fox A. J., Derrick J. P., Maiden M. C.. 2002; Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. Mol Biol Evol19:1686–1694
    [Google Scholar]
  42. van der Ley P., Heckels J. E., Virji M., Hoogerhout P., Poolman J. T.. 1991; Topology of outer membrane porins in pathogenic Neisseria species. Infect Immun59:2963–2971
    [Google Scholar]
  43. van der Ley P., van der Biezen J., Poolman J. T.. 1995; Construction of Neisseria meningitidis strains carrying multiple chromosomal copies of the porA gene for use in the production of a multivalent outer membrane vesicle vaccine. Vaccine13:401–407
    [Google Scholar]
  44. Ward M. J., Lambden P. R., Heckels J. E.. 1992; Sequence analysis and relationships between meningococcal class 3 serotype proteins and other porins of pathogenic and non- pathogenic Neisseria species. FEMS Microbiol Lett94:283–290
    [Google Scholar]
  45. Wilson H. D., Overman T. L.. 1976; Septicemia due to Neisseria lactamica . J Clin Microbiol4:214–215
    [Google Scholar]
  46. Womble D. D.. 2000; GCG: the Wisconsin Package of sequence analysis programs. Methods Mol Biol132:3–22
    [Google Scholar]
  47. Yang Z.. 1997; PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci13:555–556
    [Google Scholar]
  48. Zeth K., Diederichs K., Welte W., Engelhardt H.. 2000; Crystal structure of Omp32, the anion-selective porin from Comamonas acidovorans , in complex with a periplasmic peptide at 2. Å resolution. Structure8:981–992
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/015479-0
Loading
/content/journal/micro/10.1099/mic.0.2007/015479-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error