Comparative exoprotein profiling of different staphylococcus epidermidis strains reveals potential link between nonclassical protein export and virulence

Journal of Proteome Research

Volumn 13, Issue 7, 2014, Pages 3249-3261

  Siljamäki, Pia ^a   Varmanen, Pekka ^a   Kankainen, Matti ^c   Sukura, Antti ^b   Savijoki, Kirsi ^a   Nyman, Tuula A ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c CSC Scientific Computing Ltd   (Finland)

Author keywords

adaptation; exoproteome; GeLC MS MS; membrane vesicles; moonlighting proteins; nonclassical secretion; Staphylococcus epidermidis; virulence

Indexed keywords

ABC TRANSPORTER; ADHESIN; ALP PROTEIN; BACTERIAL PROTEIN; BETA LACTAMASE; CELL SURFACE PROTEIN; CYTOPLASM PROTEIN; EXOPROTEOME; FIBRONECTIN BINDING PROTEIN; FMHA PROTEIN; FTSH PROTEIN; HEMAGGLUTININ; HMRA PROTEIN; ISAB PROTEIN; LIPOPROTEIN; LYTH PROTEIN; MREC PROTEIN; PROTEOME; PSM ALPHA; SES1 PROTEIN; SESE PROTEIN; SESG PROTEIN; SESH PROTEIN; UNCLASSIFIED DRUG; UREASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; EXOPROTEOME PROFILING; MEMBRANE VESICLE; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; SECRETORY PATHWAY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; SUPERNATANT; TANDEM MASS SPECTROMETRY; ANIMAL; COMPARATIVE STUDY; HUMAN; METABOLISM; PATHOGENICITY; SECRETION (PROCESS); VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BETA-LACTAMASES; HUMANS; STAPHYLOCOCCUS EPIDERMIDIS; UREASE; VIRULENCE;

EID: 84903702098     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500075j     Document Type: Article

References (79)

1. Otto, M. Molecular basis of Staphylococcus epidermidis infections Semin. Immunopathol. 2012, 2, 201-214
2. Sugimoto, S.; Iwamoto, T.; Takada, K.; Okuda, K. I.; Tajima, A.; Iwase, T.; Mizunoe, Y. Staphylococcus epidermidis Esp degrades specific proteins associated with Staphylococcus aureus biofilm formation and host-pathogen interaction J. Bacteriol. 2013, 8, 1645-1655
3. Al-Mahrous, M. M.; Jack, R. W.; Sandiford, S. K.; Tagg, J. R.; Beatson, S. A.; Upton, M. Identification of a haemolysin-like peptide with antibacterial activity using the draft genome sequence of Staphylococcus epidermidis strain A487 FEMS Immunol. Med. Microbiol. 2011, 3, 273-282
4. Schoenfelder, S. M.; Lange, C.; Eckart, M.; Hennig, S.; Kozytska, S.; Ziebuhr, W. Success through diversity-How Staphylococcus epidermidis establishes as a nosocomial pathogen Int. J. Med. Microbiol. 2010, 6, 380-386
5. Zhang, Y. Q.; Ren, S. X.; Li, H. L.; Wang, Y. X.; Fu, G.; Yang, J.; Qin, Z. Q.; Miao, Y. G.; Wang, W. Y.; Chen, R. S.; Shen, Y.; Chen, Z.; Yuan, Z. H.; Zhao, G. P.; Qu, D.; Danchin, A.; Wen, Y. M. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228) Mol. Microbiol. 2003, 6, 1577-1593
6. Gill, S. R.; Fouts, D. E.; Archer, G. L.; Mongodin, E. F.; Deboy, R. T.; Ravel, J.; Paulsen, I. T.; Kolonay, J. F.; Brinkac, L.; Beanan, M.; Dodson, R. J.; Daugherty, S. C.; Madupu, R.; Angiuoli, S. V.; Durkin, A. S.; Haft, D. H.; Vamathevan, J.; Khouri, H.; Utterback, T.; Lee, C.; Dimitrov, G.; Jiang, L.; Qin, H.; Weidman, J.; Tran, K.; Kang, K.; Hance, I. R.; Nelson, K. E.; Fraser, C. M. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain J. Bacteriol. 2005, 7, 2426-2438
7. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 5418, 1318-1322
8. Pyörälä, S.; Taponen, S. Coagulase-negative staphylococci-emerging mastitis pathogens Vet. Microbiol. 2009, 1-2, 3-8
9. Thorberg, B. M.; Danielsson-Tham, M. L.; Emanuelson, U.; Persson Waller, K. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci J. Dairy Sci. 2009, 10, 4962-4970
10. Fitzgerald, J. R. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat Trends Microbiol. 2012, 4, 192-198
11. Piessens, V.; Van Coillie, E.; Verbist, B.; Supre, K.; Braem, G.; Van Nuffel, A.; De Vuyst, L.; Heyndrickx, M.; De Vliegher, S. Distribution of coagulase-negative Staphylococcus species from milk and environment of dairy cows differs between herds J. Dairy Sci. 2011, 6, 2933-2944
12. Thorberg, B. M.; Kuhn, I.; Aarestrup, F. M.; Brandstrom, B.; Jonsson, P.; Danielsson-Tham, M. L. Pheno- and genotyping of Staphylococcus epidermidis isolated from bovine milk and human skin Vet. Microbiol. 2006, 1-3, 163-172
13. Jaglic, Z.; Michu, E.; Holasova, M.; Vlkova, H.; Babak, V.; Kolar, M.; Bardon, J.; Schlegelova, J. Epidemiology and characterization of Staphylococcus epidermidis isolates from humans, raw bovine milk and a dairy plant Epidemiol. Infect. 2010, 5, 772-782
14. Sawant, A. A.; Gillespie, B. E.; Oliver, S. P. Antimicrobial susceptibility of coagulase-negative Staphylococcus species isolated from bovine milk Vet. Microbiol. 2009, 1-2, 73-81
15. Becher, D.; Hempel, K.; Sievers, S.; Zuhlke, D.; Pane-Farre, J.; Otto, A.; Fuchs, S.; Albrecht, D.; Bernhardt, J.; Engelmann, S.; Volker, U.; van Dijl, J. M.; Hecker, M. A proteomic view of an important human pathogen-towards the quantification of the entire Staphylococcus aureus proteome PLoS One 2009, 12, e8176
16. Hempel, K.; Herbst, F. A.; Moche, M.; Hecker, M.; Becher, D. Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions J. Proteome Res. 2011, 4, 1657-1666
17. Muthukrishnan, G.; Quinn, G. A.; Lamers, R. P.; Diaz, C.; Cole, A. L.; Chen, S.; Cole, A. M. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage J. Proteome Res. 2011, 4, 2064-2078
18. Pocsfalvi, G.; Cacace, G.; Cuccurullo, M.; Serluca, G.; Sorrentino, A.; Schlosser, G.; Blaiotta, G.; Malorni, A. Proteomic analysis of exoproteins expressed by enterotoxigenic Staphylococcus aureus strains Proteomics 2008, 12, 2462-2476
19. Ravipaty, S.; Reilly, J. P. Comprehensive characterization of methicillin-resistant Staphylococcus aureus subsp. aureus COL secretome by two-dimensional liquid chromatography and mass spectrometry Mol. Cell. Proteomics 2010, 9, 1898-1919
20. Resch, A.; Leicht, S.; Saric, M.; Pasztor, L.; Jakob, A.; Gotz, F.; Nordheim, A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling Proteomics 2006, 6, 1867-1877
21. Schallenberger, M. A.; Niessen, S.; Shao, C.; Fowler, B. J.; Romesberg, F. E. Type I signal peptidase and protein secretion in S. aureus J. Bacteriol. 2012, 10, 2677-2686
22. Sibbald, M. J.; Ziebandt, A. K.; Engelmann, S.; Hecker, M.; de Jong, A.; Harmsen, H. J.; Raangs, G. C.; Stokroos, I.; Arends, J. P.; Dubois, J. Y.; van Dijl, J. M. Mapping the pathways to staphylococcal pathogenesis by comparative secretomics Microbiol. Mol. Biol. Rev. 2006, 3, 755-788
23. Wolf, C.; Kusch, H.; Monecke, S.; Albrecht, D.; Holtfreter, S.; von Eiff, C.; Petzl, W.; Rainard, P.; Broker, B. M.; Engelmann, S. Genomic and proteomic characterization of Staphylococcus aureus mastitis isolates of bovine origin Proteomics 2011, 12, 2491-2502
24. Ziebandt, A. K.; Kusch, H.; Degner, M.; Jaglitz, S.; Sibbald, M. J.; Arends, J. P.; Chlebowicz, M. A.; Albrecht, D.; Pantucek, R.; Doskar, J.; Ziebuhr, W.; Broker, B. M.; Hecker, M.; van Dijl, J. M.; Engelmann, S. Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation Proteomics 2010, 8, 1634-1644
25. Yang, X. M.; Li, N.; Chen, J. M.; Ou, Y. Z.; Jin, H.; Lu, H. J.; Zhu, Y. L.; Qin, Z. Q.; Qu, D.; Yang, P. Y. Comparative proteomic analysis between the invasive and commensal strains of Staphylococcus epidermidis FEMS Microbiol. Lett. 2006, 1, 32-40
26. Batzilla, C. F.; Rachid, S.; Engelmann, S.; Hecker, M.; Hacker, J.; Ziebuhr, W. Impact of the accessory gene regulatory system (Agr) on extracellular proteins, codY expression and amino acid metabolism in Staphylococcus epidermidis Proteomics 2006, 12, 3602-3613
27. Savijoki, K.; Lietzen, N.; Kankainen, M.; Alatossava, T.; Koskenniemi, K.; Varmanen, P.; Nyman, T. A. Comparative proteome cataloging of Lactobacillus rhamnosus strains GG and Lc705 J. Proteome Res. 2011, 8, 3460-3473
28. Wolff, S.; Hahne, H.; Hecker, M.; Becher, D. Complementary analysis of the vegetative membrane proteome of the human pathogen Staphylococcus aureus Mol. Cell. Proteomics 2008, 8, 1460-1468
29. Hempel, K.; Pane-Farre, J.; Otto, A.; Sievers, S.; Hecker, M.; Becher, D. Quantitative cell surface proteome profiling for SigB-dependent protein expression in the human pathogen Staphylococcus aureus via biotinylation approach J. Proteome Res. 2010, 3, 1579-1590
30. Beganovic, J.; Guillot, A.; van de Guchte, M.; Jouan, A.; Gitton, C.; Loux, V.; Roy, K.; Huet, S.; Monod, H.; Monnet, V. Characterization of the insoluble proteome of Lactococcus lactis by SDS-PAGE LC-MS/MS leads to the identification of new markers of adaptation of the bacteria to the mouse digestive tract J. Proteome Res. 2010, 2, 677-688
31. Fang, Y.; Robinson, D. P.; Foster, L. J. Quantitative analysis of proteome coverage and recovery rates for upstream fractionation methods in proteomics J. Proteome Res. 2010, 4, 1902-1912
32. Taponen, S.; Koort, J.; Björkroth, J.; Saloniemi, H.; Pyörälä, S. Bovine intramammary infections caused by coagulase-negative staphylococci may persist throughout lactation according to amplified fragment length polymorphism-based analysis J. Dairy Sci. 2007, 7, 3301-3307
33. Simojoki, H.; Salomäki, T.; Taponen, S.; Iivanainen, A.; Pyörälä, S. Innate immune response in experimentally induced bovine intramammary infection with Staphylococcus simulans and S. epidermidis Vet. Res. 2011, 1, 49
34. Fischetti, V. A.; Novick, R. P.; Ferretti, J. J.; Portnoy, D. A.; Rood, J. I. Gram-Positive Pathogens; ASM Press: Washington, DC, 2000; pp 1-849.
35. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 5259, 680-685
36. Steinberg, T. H.; Jones, L. J.; Haugland, R. P.; Singer, V. L. SYPRO orange and SYPRO red protein gel stains: one-step fluorescent staining of denaturing gels for detection of nanogram levels of protein Anal. Biochem. 1996, 2, 223-237
37. Lietzen, N.; Natri, L.; Nevalainen, O. S.; Salmi, J.; Nyman, T. A. Compid: a new software tool to integrate and compare MS/MS based protein identification results from Mascot and Paragon J. Proteome Res. 2010, 12, 6795-6800
38. Vizcaino, J. A.; Cote, R. G.; Csordas, A.; Dianes, J. A.; Fabregat, A.; Foster, J. M.; Griss, J.; Alpi, E.; Birim, M.; Contell, J.; OKelly, G.; Schoenegger, A.; Ovelleiro, D.; Perez-Riverol, Y.; Reisinger, F.; Rios, D.; Wang, R.; Hermjakob, H. The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013 Nucleic Acids Res. 2013, D1063-D1069
39. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 3, 207-214
40. Sutcliffe, I. C.; Russell, R. R. Lipoproteins of gram-positive bacteria J. Bacteriol. 1995, 5, 1123-1128
41. Matsushima, N.; Miyashita, H.; Mikami, T.; Kuroki, Y. A nested leucine rich repeat (LRR) domain: the precursor of LRRs is a ten or eleven residue motif BMC Microbiol. 2010, 235, 235-1-235-10
42. Scott, J. R.; Barnett, T. C. Surface proteins of Gram-positive bacteria and how they get there Annu. Rev. Microbiol. 2006, 60, 397-423
43. Heilmann, C.; Hartleib, J.; Hussain, M. S.; Peters, G. The multifunctional Staphylococcus aureus autolysin Aaa mediates adherence to immobilized fibrinogen and fibronectin Infect. Immun. 2005, 8, 4793-4802
44. Desvaux, M.; Dumas, E.; Chafsey, I.; Hebraud, M. Protein cell surface display in Gram-positive bacteria: from single protein to macromolecular protein structure FEMS Microbiol. Lett. 2006, 1, 1-15
45. Mazmanian, S. K.; Ton-That, H.; Su, K.; Schneewind, O. An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis Proc. Natl. Acad. Sci. U.S.A. 2002, 4, 2293-2298
46. Scott, J. R.; Zahner, D. Pili with strong attachments: Gram-positive bacteria do it differently Mol. Microbiol. 2006, 2, 320-330
47. Altschul, S. F.; Wootton, J. C.; Gertz, E. M.; Agarwala, R.; Morgulis, A.; Schaffer, A. A.; Yu, Y. K. Protein database searches using compositionally adjusted substitution matrices FEBS J. 2005, 20, 5101-5109
48. Li, L.; Stoeckert, C. J., Jr.; Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes Genome Res. 2003, 9, 2178-2189
49. Niskanen, S.; Östergård, P. R. J. Cliquer Users Guide: Version 1.0, T48 ed.; Helsinki University of Technology: Helsinki, Finland, 2003; pp 1-22.
50. OCallaghan, C.; Morris, A. Inhibition of beta-lactamases by beta-lactam antibiotics Antimicrob. Agents Chemother. 1972, 6, 442-448
51. Christensen, W. B. Urea decomposition as a means of differentiating Proteus and Paracolon cultures from each other and from Salmonella and Shigella types J. Bacteriol. 1946, 4, 461-466
52. Kainulainen, V.; Korhonen, T. Dancing to another tune-Adhesive moonlighting proteins in bacteria Biology 2014, 3, 178-204
53. DebRoy, S.; Dao, J.; Söderberg, M.; Rossier, O.; Cianciotto, N. P. Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung Proc. Natl. Acad. Sci. U.S. A. 2006, 50, 19146-19151
54. Kiran, M. D.; Akiyoshi, D. E.; Giacometti, A.; Cirioni, O.; Scalise, G.; Balaban, N. OpuC-an ABC transporter that is associated with Staphylococcus aureus pathogenesis Int. J. Artif. Organs 2009, 9, 600-610
55. Burne, R. A.; Chen, Y. Y. Bacterial ureases in infectious diseases Microbes Infect. 2000, 5, 533-542
56. Wang, H.; Chang-Wong, T.; Tang, H. Y.; Speicher, D. W. Comparison of extensive protein fractionation and repetitive LC-MS/MS analyses on depth of analysis for complex proteomes J. Proteome Res. 2010, 2, 1032-1040
57. Lee, E. Y.; Choi, D. Y.; Kim, D. K.; Kim, J. W.; Park, J. O.; Kim, S.; Kim, S. H.; Desiderio, D. M.; Kim, Y. K.; Kim, K. P.; Gho, Y. S. Gram-positive bacteria produce membrane vesicles: proteomics-based characterization of Staphylococcus aureus -derived membrane vesicles Proteomics 2009, 24, 5425-5436
58. Gurung, M.; Moon, D. C.; Choi, C. W.; Lee, J. H.; Bae, Y. C.; Kim, J.; Lee, Y. C.; Seol, S. Y.; Cho, D. T.; Kim, S. I.; Lee, J. C. Staphylococcus aureus produces membrane-derived vesicles that induce host cell death PLoS One 2011, 11, e27958
59. Siljamäki, P.; Varmanen, P.; Kankainen, M.; Pyörälä, S.; Iivanainen, A.; Auvinen, P.; Paulin, L.; Laine, P. K.; Taponen, S.; Simojoki, H.; Sukura, A.; Nyman, T. A.; Savijoki, K. Global proteome profiling of bovine and human Staphylococcus epidermidis strains to search for factors contributing to host-specificity and adaptation. Proteomics, in revision.
60. Wang, G.; Xia, Y.; Cui, J.; Gu, Z.; Song, Y.; Chen, Y. Q.; Chen, H.; Zhang, H.; Chen, W. The roles of moonlighting proteins in bacteria Curr. Issues Mol. Biol. 2013, 2, 15-22
61. Hurmalainen, V.; Edelman, S.; Antikainen, J.; Baumann, M.; Lähteenmäki, K.; Korhonen, T. K. Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen Microbiology 2007, Pt 4, 1112-1122
62. Antikainen, J.; Kuparinen, V.; Lähteenmäki, K.; Korhonen, T. K. pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids J. Bacteriol. 2007, 12, 4539-4543
63. Kainulainen, V.; Loimaranta, V.; Pekkala, A.; Edelman, S.; Antikainen, J.; Kylväjä, R.; Laaksonen, M.; Laakkonen, L.; Finne, J.; Korhonen, T. K. Glutamine synthetase and glucose-6-phosphate isomerase are adhesive moonlighting proteins of Lactobacillus crispatus released by epithelial cathelicidin LL-37 J. Bacteriol. 2012, 10, 2509-2519
64. Biswas, S.; Biswas, I. Role of HtrA in surface protein expression and biofilm formation by Streptococcus mutans Infect. Immun. 2005, 10, 6923-6934
65. Egea, L.; Aguilera, L.; Gimenez, R.; Sorolla, M. A.; Aguilar, J.; Badia, J.; Baldoma, L. Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen Int. J. Biochem. Cell Biol. 2007, 6, 1190-1203
66. Yang, C. K.; Ewis, H. E.; Zhang, X.; Lu, C. D.; Hu, H. J.; Pan, Y.; Abdelal, A. T.; Tai, P. C. Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis J. Bacteriol. 2011, 20, 5607-5615
67. Tjalsma, H.; Lambooy, L.; Hermans, P. W.; Swinkels, D. W. Shedding & shaving: disclosure of proteomic expressions on a bacterial face Proteomics 2008, 7, 1415-1428
68. Planchon, S.; Chambon, C.; Desvaux, M.; Chafsey, I.; Leroy, S.; Talon, R.; Hebraud, M. Proteomic analysis of cell envelope from Staphylococcus xylosus C2a, a coagulase-negative Staphylococcus J. Proteome Res. 2007, 9, 3566-3580
69. Severin, A.; Nickbarg, E.; Wooters, J.; Quazi, S. A.; Matsuka, Y. V.; Murphy, E.; Moutsatsos, I. K.; Zagursky, R. J.; Olmsted, S. B. Proteomic analysis and identification of Streptococcus pyogenes surface-associated proteins J. Bacteriol. 2007, 5, 1514-1522
70. Ruiz, L.; Coute, Y.; Sanchez, B.; de los Reyes-Gavilan, C. G.; Sanchez, J. C.; Margolles, A. The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment Microbiology 2009, Pt 3, 957-967
71. Sinha, S.; Kosalai, K.; Arora, S.; Namane, A.; Sharma, P.; Gaikwad, A. N.; Brodin, P.; Cole, S. T. Immunogenic membrane-associated proteins of Mycobacterium tuberculosis revealed by proteomics Microbiology 2005, Pt 7, 2411-2419
72. Geng, H.; Zhu, L.; Yuan, Y.; Zhang, W.; Li, W.; Wang, J.; Zheng, Y.; Wei, K.; Cao, W.; Wang, H.; Jiang, Y. Identification and characterization of novel immunogenic proteins of Streptococcus suis serotype 2 J. Proteome Res. 2008, 9, 4132-4142
73. Nho, S. W.; Hikima, J.; Cha, I. S.; Park, S. B.; Jang, H. B.; del Castillo, C. S.; Kondo, H.; Hirono, I.; Aoki, T.; Jung, T. S. Complete genome sequence and immunoproteomic analyses of the bacterial fish pathogen Streptococcus parauberis J. Bacteriol. 2011, 13, 3356-3366
74. MacDonald, I. A.; Kuehn, M. J. Offense and defense: microbial membrane vesicles play both ways Res. Microbiol. 2012, 9-10, 607-618
75. Thay, B.; Wai, S. N.; Oscarsson, J. Staphylococcus aureus alpha-toxin-dependent induction of host cell death by membrane-derived vesicles PLoS One 2013, 1, e54661
76. Kulp, A.; Kuehn, M. J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles Annu. Rev. Microbiol. 2010, 64, 163-184
77. Macdonald, I. A.; Kuehn, M. J. Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa J. Bacteriol. 2013, 13, 2971-2981
78. Lee, J.; Lee, E. Y.; Kim, S. H.; Kim, D. K.; Park, K. S.; Kim, K. P.; Kim, Y. K.; Roh, T. Y.; Gho, Y. S. Staphylococcus aureus extracellular vesicles carry biologically active beta-lactamase Antimicrob. Agents Chemother. 2013, 6, 2589-2595
79. Krishnappa, L.; Dreisbach, A.; Otto, A.; Goosens, V. J.; Cranenburgh, R. M.; Harwood, C. R.; Becher, D.; van Dijl, J. M. Extracytoplasmic proteases determining the cleavage and release of secreted proteins, lipoproteins, and membrane proteins in Bacillus subtilis J. Proteome Res. 2013, 9, 4101-4110