Comparative proteomic analysis of biofilm and planktonic cells of Neisseria meningitidis

Proteomics

Volumn 10, Issue 24, 2010, Pages 4512-4521

  Van Alen, Tessa ^a   Claus, Heike ^a   Zahedi, René P ^b,c   Groh, Janos ^a   Blazyca, Heinrich ^a   Lappann, Martin ^a   Sickmann, Albert ^b,c,d   Vogel, Ulrich ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Biofilms; Microbiology; MntC protein; Neisseria meningitidis; Oxidative stress

Indexed keywords

ALCOHOL DEHYDROGENASE; BETA PHOSPHOGLUCOMUTASE; BINDING PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; FTSZ PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP); ISOMERASE; MNTC PROTEIN; REACTIVE OXYGEN METABOLITE; SODC PROTEIN; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE A; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BIOFILM; CELL GROWTH; CELL METABOLISM; IN VITRO STUDY; NEISSERIA MENINGITIDIS; NONHUMAN; PLANKTON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REGULATORY MECHANISM;

NEISSERIA MENINGITIDIS;

EID: 78650037810     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000267     Document Type: Article

References (50)

1. Cartwright, K. A., Stuart, J. M., Jones, D. M., Noah, N. D., The Stonehouse survey: nasopharyngeal carriage of Meningococci and Neisseria lactamica. Epidemiol. Infect. 1987, 99, 591-601.
2. Goldschneider, I., Gotschlich, E. C., Artenstein, M. S., Human immunity to the meningococcus. II. Development of natural immunity. J. Exp. Med. 1969, 129, 1327-1348.
3. Claus, H., Maiden, M. C., Maag, R., Frosch, M., et al., Many carried Meningococci lack the genes required for capsule synthesis and transport. Microbiology 2002, 148, 1813-1819.
4. Sim, R. J., Harrison, M. M., Moxon, E. R., Tang, C. M., Underestimation of meningococci in tonsillar tissue by nasopharyngeal swabbing. Lancet 2000, 356, 1653-1654.
5. Yi, K., Rasmussen, A. W., Gudlavalleti, S. K., Stephens, D. S., et al., Biofilm formation by Neisseria meningitidis. Infect. Immun. 2004, 72, 6132-6138.
6. O'Dwyer, C. A., Li, M. S., Langford, P. R., Kroll, J. S., Meningococcal biofilm growth on an abiotic surface - a model for epithelial colonization? Microbiology 2009, 155, 1940-1952.
7. Lappann, M., Haagensen, J. A., Claus, H., Vogel, U., et al., Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system. Mol. Microbiol. 2006, 62, 1292-1309.
8. Lappann, M., Claus, H., van Alen, T., Harmsen, M. et al., A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol. Microbiol. 2010, 75, 1355-1371.
9. Neil, R. B., Shao, J. Q., Apicella, M. A., Biofilm formation on human airway epithelia by encapsulated Neisseria meningitidis serogroup B. Microbes Infect. 2009, 11, 281-287.
10. Neil, R. B., Apicella, M. A., Role of HrpA in biofilm formation of Neisseria meningitidis and regulation of the hrpBAS transcripts. Infect. Immun. 2009, 77, 2285-2293.
11. Falsetta, M. L., Bair, T. B., Ku, S. C., Vanden Hoven, R. N. et al., Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms. Infect. Immun. 2009, 77, 3522-3532.
12. Bernardini, G., Renzone, G., Comanducci, M., Mini, R. et al., Proteome analysis of Neisseria meningitidis serogroup A. Proteomics 2004, 4, 2893-2926.
13. Mignogna, G., Giorgi, A., Stefanelli, P., Neri, A. et al., Inventory of the proteins in Neisseria meningitidis serogroup B strain MC58. J. Proteome Res. 2005, 4, 1361-1370.
14. Mendum, T. A., Newcombe, J., McNeilly, C. L., McFadden, J., Towards the immunoproteome of Neisseria meningitidis. PLoS One 2009, 4, e5940.
15. Williams, J. N., Skipp, P. J., O'Connor, C. D., Christodoulides, M., et al., Immunoproteomic analysis of the development of natural immunity in subjects colonized by Neisseria meningitidis reveals potential vaccine candidates. Infect. Immun. 2009, 77, 5080-5089.
16. Dunn, K. L., Virji, M., Moxon, E. R., Investigations into the molecular basis of meningococcal toxicity for human endothelial and epithelial cells: the synergistic effect of LPS and pili. Microb. Pathog. 1995, 18, 81-96.
17. Archibald, F. S., DeVoe, I. W., Iron in Neisseria meningitidis: minimum requirements, effects of limitation, and characteristics of uptake. J. Bacteriol. 1978, 136, 35-48.
18. Reinders, J., Wagner, K., Zahedi, R. P., Stojanovski, D. et al., Profiling phosphoproteins of yeast mitochondria reveals a role of phosphorylation in assembly of the ATP synthase. Mol. Cell. Proteomics 2007, 6, 1896-1906.
19. Ishihama, Y., Oda, Y., Tabata, T., Sato, T. et al., Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 2005, 4, 1265-1272.
20. Tseng, H. J., Srikhanta, Y., McEwan, A. G., Jennings, M. P., Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol. Microbiol. 2001, 40, 1175-1186.
21. Seib, K. L., Tseng, H. J., McEwan, A. G., Apicella, M. A., et al., Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J. Infect. Dis. 2004, 190, 136-147.
22. Wilks, K. E., Dunn, K. L., Farrant, J. L., Reddin, K. M. et al., Periplasmic superoxide dismutase in meningococcal pathogenicity. Infect. Immun. 1998, 66, 213-217.
23. Gelfand, D. H., Steinberg, R. A., Escherichia coli mutants deficient in the aspartate and aromatic amino acid aminotransferases. J. Bacteriol. 1977, 130, 429-440.
24. Jantama, K., Zhang, X., Moore, J. C., Shanmugam, K. T. et al., Eliminating side products and increasing succinate yields in engineered strains of Escherichia coli C. Biotechnol. Bioeng. 2008, 101, 881-893.
25. Grifantini, R., Bartolini, E., Muzzi, A., Draghi, M. et al., Gene expression profile in Neisseria meningitidis and Neisseria lactamica upon host-cell contact: from basic research to vaccine development. Ann. NY Acad. Sci. 2002, 975, 202-216.
26. Rose, I. A., Grunberg-Manago, M., Korey, S. R., Ochoa, S., Enzymatic phosphorylation of acetate. J. Biol. Chem. 1954, 211, 737-756.
27. Oyedotun, K. S., Lemire, B. D., The quaternary structure of the Saccharomyces cerevisiae succinate dehydrogenase. Homology modeling, cofactor docking, and molecular dynamics simulation studies. J. Biol. Chem. 2004, 279, 9424-9431.
28. Ren, J., Sainsbury, S., Combs, S. E., Capper, R. G. et al., The structure and transcriptional analysis of a global regulator from Neisseria meningitidis. J. Biol. Chem. 2007, 282, 14655-14664.
29. Claus, H., Maiden, M. C., Wilson, D. J., McCarthy, N. D. et al., Genetic analysis of Meningococci carried by children and young adults. J. Infect. Dis. 2005, 191, 1263-1271.
30. Mikkelsen, H., Duck, Z., Lilley, K. S., Welch, M., Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J. Bacteriol. 2007, 189, 2411-2416.
31. Archibald, F. S., Duong, M. N., Superoxide dismutase and oxygen toxicity defenses in the genus Neisseria. Infect. Immun. 1986, 51, 631-641.
32. Tettelin, H., Saunders, N. J., Heidelberg, J., Jeffries, A. C. et al., Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 2000, 287, 1809-1815.
33. Nigaud, Y., Cosette, P., Collet, A., Song, P. C. et al., Biofilm-induced modifications in the proteome of Pseudomonas aeruginosa planktonic cells. Biochim. Biophys. Acta 2010, 1804, 957-966.
34. Murphy, T. F., Kirkham, C., Sethi, S., Lesse, A. J., Expression of a peroxiredoxin-glutaredoxin by Haemophilus influenzae in biofilms and during human respiratory tract infection. FEMS Immunol. Med. Microbiol. 2005, 44, 81-89.
35. Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., et al., Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 2002, 184, 1140-1154.
36. Sampathkumar, B., Napper, S., Carrillo, C. D., Willson, P. et al., Transcriptional and translational expression patterns associated with immobilized growth of Campylobacter jejuni. Microbiology 2006, 152, 567-577.
37. Martinez-Gomariz, M., Perumal, P., Mekala, S., Nombela, C. et al., Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans. Proteomics 2009, 9, 2230-2252.
38. Tremoulet, F., Duche, O., Namane, A., Martinie, B., et al., Comparison of protein patterns of Listeria monocytogenes grown in biofilm or in planktonic mode by proteomic analysis. FEMS Microbiol. Lett. 2002, 210, 25-31.
39. Ram, R. J., Verberkmoes, N. C., Thelen, M. P., Tyson, G. W. et al., Community proteomics of a natural microbial biofilm. Science 2005, 308, 1915-1920.
40. Resch, A., Rosenstein, R., Nerz, C., Gotz, F., Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 2005, 71, 2663-2676.
41. Resch, A., Leicht, S., Saric, M., Pasztor, L. et al., Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 2006, 6, 1867-1877.
42. Lim, K. H., Jones, C. E., vanden Hoven, R. N., Edwards, J. L. et al., Metal binding specificity of the MntABC permease of Neisseria gonorrhoeae and its influence on bacterial growth and interaction with cervical epithelial cells. Infect. Immun. 2008, 76, 3569-3576.
43. Wu, H., Soler-Garcia, A. A., Jerse, A. E., A strain-specific catalase mutation and mutation of the metal-binding transporter gene mntC attenuate Neisseria gonorrhoeae in vivo but not by increasing susceptibility to oxidative killing by phagocytes. Infect. Immun. 2009, 77, 1091-1102.
44. Ang, C. S., Veith, P. D., Dashper, S. G., Reynolds, E. C., Application of 16O/18O reverse proteolytic labeling to determine the effect of biofilm culture on the cell envelope proteome of Porphyromonas gingivalis W50. Proteomics 2008, 8, 1645-1660.
45. Planchon, S., Desvaux, M., Chafsey, I., Chambon, C. et al., Comparative subproteome analyses of planktonic and sessile Staphylococcus xylosus C2a: new insight in cell physiology of a coagulase-negative Staphylococcus in biofilm. J. Proteome Res. 2009, 8, 1797-1809.
46. Peng, L., Shimizu, K., Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement. Appl. Microbiol. Biotechnol. 2003, 61, 163-178.
47. Bartolini, E., Frigimelica, E., Giovinazzi, S., Galli, G. et al., Role of FNR and FNR-regulated, sugar fermentation genes in Neisseria meningitidis infection. Mol. Microbiol. 2006, 60, 963-972.
48. Weiss, D. S., Bacterial cell division and the septal ring. Mol. Microbiol. 2004, 54, 588-597.
49. Ramirez-Arcos, S., Salimnia, H., Bergevin, I., Paradis, M., et al., Expression of Neisseria gonorrhoeae cell division genes ftsZ, ftsE and minD is influenced by environmental conditions. Res. Microbiol. 2001, 152, 781-791.
50. Kawarai, T., Furukawa, S., Narisawa, N., Hagiwara, C. et al., Biofilm formation by Escherichia coli in hypertonic sucrose media. J. Biosci. Bioeng. 2009, 107, 630-635.