Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae

Journal of Proteomics

Volumn 106, Issue , 2014, Pages 46-60

  Olaya Abril, Alfonso ^a,b   Prados Rosales, Rafael ^c   McConnell, Michael J ^b,d   Martín Peña, Reyes ^b,d   González Reyes, José Antonio ^a   Jiménez Munguía, Irene ^a,b   Gómez Gascón, Lidia ^a,b   Fernández, Javier ^a   Luque García, José L ^e   García Lidón, Carlos ^e   Estévez, Héctor ^e   Pachón, Jerónimo ^b,d   Obando, Ignacio ^f   Casadevall, Arturo ^c   Pirofski, Liise anne ^c   Rodríguez Ortega, Manuel J ^a,b  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d CSIC   (Spain)

^e UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^f HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

Extracellular vesicles; Membrane vesicles; Pneumococcus; Proteomics; Surface proteins; Vaccine

Indexed keywords

LIPOPROTEIN; MEMBRANE PROTEIN; PNEUMOCOCCUS VACCINE; SHORT CHAIN FATTY ACID; VIRULENCE FACTOR; ANTIINFECTIVE AGENT; FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CASE REPORT; CELL MEMBRANE; CELL VACUOLE; CHEMICAL ANALYSIS; CHILD; CONTROLLED STUDY; CYTOLYSIS; FATTY ACID ANALYSIS; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PNEUMOCOCCAL INFECTION; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEOMICS; SERUM; STREPTOCOCCUS PNEUMONIAE; ANIMAL; ANTIBIOTIC RESISTANCE; BAGG ALBINO MOUSE; BIOLOGY; BLOOD; CHEMISTRY; CHROMATOGRAPHY; FLOW CYTOMETRY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; METABOLISM; PNEUMOCOCCAL INFECTIONS; PROTEIN DATABASE; TANDEM MASS SPECTROMETRY;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL MEMBRANE; CHILD, PRESCHOOL; CHROMATOGRAPHY; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; DRUG RESISTANCE, BACTERIAL; FATTY ACIDS; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MICE; MICE, INBRED BALB C; PNEUMOCOCCAL INFECTIONS; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STREPTOCOCCUS PNEUMONIAE; TANDEM MASS SPECTROMETRY;

EID: 84899887850     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.04.023     Document Type: Article

References (57)

1. Amano A., Takeuchi H., Furuta N. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect 2010, 12:791-798.
2. Macdonald I.A., Kuehn M.J. Offense and defense: microbial membrane vesicles play both ways. Res Microbiol 2012, 163:607-618.
3. Wai S.N., Lindmark B., Soderblom T., Takade A., Westermark M., Oscarsson J., et al. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 2003, 115:25-35.
4. Mashburn L.M., Whiteley M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 2005, 437:422-425.
5. Deatherage B.L., Lara J.C., Bergsbaken T., Rassoulian Barrett S.L., Lara S., Cookson B.T. Biogenesis of bacterial membrane vesicles. Mol Microbiol 2009, 72:1395-1407.
6. Ebersold H.R., Cordier J.L., Luthy P. Bacterial mesosomes: method dependent artifacts. Arch Microbiol 1981, 130:19-22.
7. Silva M.T., Sousa J.C., Polonia J.J., Macedo M.A., Parente A.M. Bacterial mesosomes. Real structures or artifacts?. Biochim Biophys Acta 1976, 443:92-105.
8. Albuquerque P.C., Nakayasu E.S., Rodrigues M.L., Frases S., Casadevall A., Zancope-Oliveira R.M., et al. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 2008, 10:1695-1710.
9. Oliveira D.L., Nakayasu E.S., Joffe L.S., Guimaraes A.J., Sobreira T.J., Nosanchuk J.D., et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One 2010, 5:e11113.
10. Rodrigues M.L., Nakayasu E.S., Oliveira D.L., Nimrichter L., Nosanchuk J.D., Almeida I.C., et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 2008, 7:58-67.
11. Vallejo M.C., Nakayasu E.S., Matsuo A.L., Sobreira T.J., Longo L.V., Ganiko L., et al. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteome Res 2012, 11:1676-1685.
12. Lee E.Y., Choi D.Y., Kim D.K., Kim J.W., Park J.O., Kim S., et al. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9:5425-5436.
13. Prados-Rosales R., Baena A., Martinez L.R., Luque-Garcia J., Kalscheuer R., Veeraraghavan U., et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest 2011, 121:1471-1483.
14. Rivera J., Cordero R.J., Nakouzi A.S., Frases S., Nicola A., Casadevall A. Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 2010, 107:19002-19007.
15. Gurung M., Moon D.C., Choi C.W., Lee J.H., Bae Y.C., Kim J., et al. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death. PLoS One 2011, 6:e27958.
16. Thay B., Wai S.N., Oscarsson J. Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles. PLoS One 2013, 8:e54661.
17. Blasi F., Mantero M., Santus P., Tarsia P. Understanding the burden of pneumococcal disease in adults. Clin Microbiol Infect 2012, 18(Suppl. 5):7-14.
18. Kyaw M.H., Lynfield R., Schaffner W., Craig A.S., Hadler J., Reingold A., et al. Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med 2006, 354:1455-1463.
19. Pilishvili T., Lexau C., Farley M.M., Hadler J., Harrison L.H., Bennett N.M., et al. Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 2010, 201:32-41.
20. Weinberger D.M., Malley R., Lipsitch M. Serotype replacement in disease after pneumococcal vaccination. Lancet 2011, 378:1962-1973.
21. Assaad U., El-Masri I., Porhomayon J., El-Solh A.A. Pneumonia immunization in older adults: review of vaccine effectiveness and strategies. Clin Interv Aging 2012, 7:453-461.
22. Olaya-Abril A., Jimenez-Munguia I., Gomez-Gascon L., Obando I., Rodriguez-Ortega M.J. Identification of potential new protein vaccine candidates through pan-surfomic analysis of pneumococcal clinical isolates from adults. PLoS One 2013, 8:e70365.
23. Olaya-Abril A., Gomez-Gascon L., Jimenez-Munguia I., Obando I., Rodriguez-Ortega M.J. Another turn of the screw in shaving Gram-positive bacteria: optimization of proteomics surface protein identification in Streptococcus pneumoniae. J Proteomics 2012, 75:3733-3746.
24. Hoskins J., Alborn W.E., Arnold J., Blaszczak L.C., Burgett S., DeHoff B.S., et al. Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 2001, 183:5709-5717.
25. Hakenbeck R., Martin C., Morelli G. Streptococcus pneumoniae proteins released into medium upon inhibition of cell wall biosynthesis. J Bacteriol 1983, 155:1372-1381.
26. Tomasz A., Jamieson J.D., Ottolenghi E. The fine structure of Diplococcus pneumoniae. J Cell Biol 1964, 22:453-467.
27. McBroom A.J., Kuehn M.J. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 2007, 63:545-558.
28. Witwer K.W., Buzas E.I., Bemis L.T., Bora A., Lasser C., Lotvall J., et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013, 2.
29. Rodrigues M.L., Franzen A.J., Nimrichter L., Miranda K. Vesicular mechanisms of traffic of fungal molecules to the extracellular space. Curr Opin Microbiol 2013, 16:414-420.
30. Rabilloud T. Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 2009, 30(Suppl. 1):S174-S180.
31. Rabilloud T., Chevallet M., Luche S., Lelong C. Two-dimensional gel electrophoresis in proteomics: past, present and future. J Proteomics 2010, 73:2064-2077.
32. Mercier R., Dominguez-Cuevas P., Errington J. Crucial role for membrane fluidity in proliferation of primitive cells. Cell Rep 2012, 1:417-423.
33. Bomberger J.M., Maceachran D.P., Coutermarsh B.A., Ye S., O'Toole G.A., Stanton B.A. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 2009, 5:e1000382.
34. Mitchell A.M., Mitchell T.J. Streptococcus pneumoniae: virulence factors and variation. Clin Microbiol Infect 2010, 16:411-418.
35. Martner A., Dahlgren C., Paton J.C., Wold A.E. Pneumolysin released during Streptococcus pneumoniae autolysis is a potent activator of intracellular oxygen radical production in neutrophils. Infect Immun 2008, 76:4079-4087.
36. Martner A., Skovbjerg S., Paton J.C., Wold A.E. Streptococcus pneumoniae autolysis prevents phagocytosis and production of phagocyte-activating cytokines. Infect Immun 2009, 77:3826-3837.
37. Claverys J.P., Havarstein L.S. Cannibalism and fratricide: mechanisms and raisons d'etre. Nat Rev Microbiol 2007, 5:219-229.
38. Price K.E., Greene N.G., Camilli A. Export requirements of pneumolysin in Streptococcus pneumoniae. J Bacteriol 2012, 194:3651-3660.
39. Bergmann S., Rohde M., Chhatwal G.S., Hammerschmidt S. Alpha-enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol 2001, 40:1273-1287.
40. Bergmann S., Rohde M., Hammerschmidt S. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect Immun 2004, 72:2416-2419.
41. Dallo S.F., Kannan T.R., Blaylock M.W., Baseman J.B. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol Microbiol 2002, 46:1041-1051.
42. Feng Y., Pan X., Sun W., Wang C., Zhang H., Li X., et al. Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface. J Infect Dis 2009, 200:1583-1592.
43. Henningham A., Chiarot E., Gillen C.M., Cole J.N., Rohde M., Fulde M., et al. Conserved anchorless surface proteins as group A streptococcal vaccine candidates. J Mol Med (Berl) 2012, 90:1197-1207.
44. Jin H., Agarwal S., Pancholi V. Surface export of GAPDH/SDH, a glycolytic enzyme, is essential for Streptococcus pyogenes virulence. MBio 2011, 2:e00068-11.
45. Kolberg J., Hammerschmidt S., Frank R., Jonak J., Sanderova H., Aase A. The surface-associated elongation factor Tu is concealed for antibody binding on viable pneumococci and meningococci. FEMS Immunol Med Microbiol 2008, 53:222-230.
46. Nieves W., Heang J., Asakrah S., Honer zu Bentrup K., Roy C.J., Morici L.A. Immunospecific responses to bacterial elongation factor Tu during Burkholderia infection and immunization. PLoS One 2010, 5:e14361.
47. Oliveira S.C., Splitter G.A. Immunization of mice with recombinant L7/L12 ribosomal protein confers protection against Brucella abortus infection. Vaccine 1996, 14:959-962.
48. Zhang A., Chen B., Mu X., Li R., Zheng P., Zhao Y., et al. Identification and characterization of a novel protective antigen, enolase of Streptococcus suis serotype 2. Vaccine 2009, 27:1348-1353.
49. Olaya-Abril A., Jimenez-Munguia I., Gomez-Gascon L., Rodriguez-Ortega M.J. Surfomics: shaving live organisms for a fast proteomic identification of surface proteins. J Proteomics 2014, 97:164-176.
50. Sumby P., Barbian K.D., Gardner D.J., Whitney A.R., Welty D.M., Long R.D., et al. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci U S A 2005, 102:1679-1684.
51. Holmlund E., Quiambao B., Ollgren J., Jaakkola T., Neyt C., Poolman J., et al. Antibodies to pneumococcal proteins PhtD, CbpA, and LytC in Filipino pregnant women and their infants in relation to pneumococcal carriage. Clin Vaccine Immunol 2009, 16:916-923.
52. Ramos-Sevillano E., Moscoso M., Garcia P., Garcia E., Yuste J. Nasopharyngeal colonization and invasive disease are enhanced by the cell wall hydrolases LytB and LytC of Streptococcus pneumoniae. PLoS One 2011, 6:e23626.
53. Sakai F., Talekar S.J., Klugman K.P., Vidal J.E. For the investigators G. Expression of virulence-related genes in the nasopharynx of healthy children. PLoS One 2013, 8:e67147.
54. Gomez-Gascon L., Luque I., Olaya-Abril A., Jimenez-Munguia I., Orbegozo-Medina R.A., Peralbo E., et al. Exploring the pan-surfome of Streptococcus suis: looking for common protein antigens. J Proteomics 2012, 75:5654-5666.
55. Rodriguez-Ortega M.J., Norais N., Bensi G., Liberatori S., Capo S., Mora M., et al. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 2006, 24:191-197.
56. Sanz J.C., Cercenado E., Marin M., Ramos B., Ardanuy C., Rodriguez-Avial I., et al. Multidrug-resistant pneumococci (serotype 8) causing invasive disease in HIV+patients. Clin Microbiol Infect 2011, 17:1094-1098.
57. Vanderkooi O.G., Church D.L., MacDonald J., Zucol F., Kellner J.D. Community-based outbreaks in vulnerable populations of invasive infections caused by Streptococcus pneumoniae serotypes 5 and 8 in Calgary, Canada. PLoS One 2011, 6:e28547.