Proteomics of Staphylococcus aureus biofilm matrix in a rat model of orthopedic implant-associated infection

PLoS ONE

Volumn 12, Issue 11, 2017, Pages

  Lei, Mei G ^a   Gupta, Ravi Kr ^a   Lee, Chia Y ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; LEUKOCIDIN; MATRIX PROTEIN; BACTERIAL PROTEIN; CARRIER PROTEIN; EBH PROTEIN, STAPHYLOCOCCUS AUREUS; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHROPLASTY; ARTICLE; BACTERIAL COUNT; BACTERIAL LOAD; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BIOFILM; BONE TISSUE; COLONY FORMING UNIT; DEVICE INFECTION; IMMUNOHISTOCHEMISTRY; INFECTION; MOUSE; NONHUMAN; OSTEOMYELITIS; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN SECRETION; PROTEOMICS; SALMONELLA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; DISEASE MODEL; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES; RAT;

ANIMALS; ARTHROPLASTY; BACTERIAL PROTEINS; BIOFILMS; CARRIER PROTEINS; DISEASE MODELS, ANIMAL; LEUKOCIDINS; MEMBRANE PROTEINS; PROTEOMICS; RATS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 85033784741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0187981     Document Type: Article

References (53)

1. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Ann Rev Microbiol. 1995; 49: 711–745.
2. Otto M. Staphylococcal biofilms. Curr Top Microbiol Immunol. 2008; 322: 207–228. PMID: 18453278
3. O’Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000; 54: 49–79. https://doi.org/10.1146/annurev.micro.54.1.49 PMID: 11018124
4. Götz F. Staphylococcus and biofilms. Mol Microbiol. 2002; 43: 1367–1378. PMID: 11952892
5. Bayles KW. The biological role of death and lysis in biofilm development. Nat Rev Microbiol. 2007; 5: 721–726. https://doi.org/10.1038/nrmicro1743 PMID: 17694072
6. Paharik AE, Horswill AR. The staphylococcal biofilm: adhesins, regulation, and host response. Microbiol spectr. 2016; 4(2).
7. Speziale P, Pietrocola G, Foster TJ, Geoghegan JA. Protein-based biofilm matrices in staphylococci. Front Cell Infect Microbiol. 2014; 4: 171. https://doi.org/10.3389/fcimb.2014.00171 PMID: 25540773
8. Brady RA, Leid JG, Camper AK, Costerton JW, Shirtliff ME. Identification of Staphylococcus aureus proteins recognized by the antibody-mediated immune response to a biofilm infection. Infect Immun. 2006; 74: 3415–3426. https://doi.org/10.1128/IAI.00392-06 PMID: 16714572
9. Bernthal NM, Stavrakis AI, Billi F, Cho JS, Kremen TJ, Simon SI, et al. A mouse model of post-arthroplasty Staphylococcus aureus joint infection to evaluate in vivo the efficacy of antimicrobial implant coatings. PloS one. 2010; 5: e12580. https://doi.org/10.1371/journal.pone.0012580 PMID: 20830204
10. Pribaz JR, Bernthal NM, Billi F, Cho JS, Ramos RI, Guo Y, et al. Mouse model of chronic post-arthroplasty infection: Noninvasive in vivo bioluminescence imaging to monitor bacterial burden for long-term study. J Orthop Res. 2012; 30: 335–340. https://doi.org/10.1002/jor.21519 PMID: 21837686
11. Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, Smeltzer MS. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun. 1995; 63: 3373–3380. PMID: 7642265
12. Sugai M, Akiyama T, Komatsuzawa H, Miyake Y, Suginaka H. Characterization of sodium dodecyl sulfate-stable Staphylococcus aureus bacteriolytic enzymes by polyacrylamide gel electrophoresis. J Bacteriol. 1990; 172: 6494–6498. PMID: 2228971
13. Schneewind O, Model P, Fischetti VA. Sorting of protein A to the staphylococcal cell wall. Cell. 1992; 70: 267–281. PMID: 1638631
14. Sassi M, Sharma D, Brinsmade SR, Felden B, Augagneur Y. Genome sequence of the clinical isolate Staphylococcus aureus subsp. aureus strain UAMS-1. Genome Announc. 2015; 3: e01584–14. https://doi.org/10.1128/genomeA.01584-14 PMID: 25676774
15. Clarke SR, Harris LG, Richards RG, Foster SJ. Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect Immun. 2002; 70: 6680–6687. https://doi.org/10.1128/IAI.70.12.6680-6687.2002 PMID: 12438342
16. Cheng AG, Missiakas D, Schneewind O. The giant protein Ebh is a determinant of Staphylococcus aureus cell size and complement resistance. J Bacteriol. 2014; 196: 971–981. https://doi.org/10.1128/JB.01366-13 PMID: 24363342
17. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, Jelenska J, et al. Passage of heme-iron across the envelope of Staphylococcus aureus. Science. 2003; 299: 906–909. https://doi.org/10.1126/science.1081147 PMID: 12574635
18. Uziel O, Borovok I, Schreiber R, Cohen G, Aharonowitz Y. Transcriptional regulation of the Staphylococcus aureus thioredoxin and thioredoxin reductase genes in response to oxygen and disulfide stress. J Bacteriol. 2004; 186: 326–334. https://doi.org/10.1128/JB.186.2.326-334.2004 PMID: 14702300
19. Nyström T, Neidhardt FC. Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol Microbiol. 1994; 11: 537–544. PMID: 8152377
20. Kvint K, Nachin L, Diez A, Nyström T. The bacterial universal stress protein: function and regulation. Curr Opin Microbiol. 2003; 6: 140–145. PMID: 12732303
21. Liu WT, Karavolos MH, Bulmer DM, Allaoui A, Hormaeche RD, Lee JJ, et al. Role of the universal stress protein UspA of Salmonella in growth arrest, stress and virulence. Microbial pathogenesis. 2007; 42: 2–10. https://doi.org/10.1016/j.micpath.2006.09.002 PMID: 17081727
22. Henderson B, Martin A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun. 2011; 79: 3476–3491. https://doi.org/10.1128/IAI.00179-11 PMID: 21646455
23. Wang W, Jeffery CJ. An analysis of surface proteomics results reveals novel candidates for intracellular/surface moonlighting proteins in bacteria. Mol Biosyst. 2016; 12: 1420–1431. https://doi.org/10.1039/c5mb00550g PMID: 26938107
24. Foulston L, Elsholz AK, DeFrancesco AS, Losick R. The extracellular matrix of Staphylococcus aureus biofilms comprises cytoplasmic proteins that associate with the cell surface in response to decreasing pH. mBio. 2014; 5: e01667–14. https://doi.org/10.1128/mBio.01667-14 PMID: 25182325
25. Alonzo F, Torres VJ. The bicomponent pore-forming leucocidins of Staphylococcus aureus. Microbiol Mol Biol Rev. 2014; 78: 199–230. https://doi.org/10.1128/MMBR.00055-13 PMID: 24847020
26. Roche FM, Massey R, Peacock SJ, Day NP, Visai L, Speziale P, et al. Characterization of novel LPXTG-containing proteins of Staphylococcus aureus identified from genome sequences. Microbiol. 2003; 149: 643–654.
27. Yamada S, Sugai M, Komatsuzawa H, Nakashima S, Oshida T, Matsumoto A, et al. An autolysin ring associated with cell separation of Staphylococcus aureus. J Bacteriol. 1996; 178: 1565–1571. PMID: 8626282
28. Malachowa N, Kohler PL, Schlievert PM, Chuang ON, Dunny GM, Kobayashi SD, et al. Characterization of a Staphylococcus aureus surface virulence factor that promotes resistance to oxidative killing and infectious endocarditis. Infect Immun. 2011; 79: 342–352. https://doi.org/10.1128/IAI.00736-10 PMID: 20937760
29. Sheldon JR, Heinrichs DE. The iron-regulated staphylococcal lipoproteins. Front Cell Infect Microbiol. 2012; 2: 24–36.
30. Houston P, Rowe SE, Pozzi C, Waters EM, O’Gara JP. Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun. 2011; 79: 1153–1165. https://doi.org/10.1128/IAI.00364-10 PMID: 21189325
31. Bose JL, Lehman MK, Fey PD, Bayles KW. Contribution of the Staphylococcus aureus Atl AM and GL murein hydrolase activities in cell division, autolysis, and biofilm formation. PloS one. 2012; 7: e42244. https://doi.org/10.1371/journal.pone.0042244 PMID: 22860095
32. Junecko JM, Zielinska AK, Mrak LN, Ryan DC, Graham JW, Smeltzer MS, et al. Transcribing virulene in Staphylococcus aureus. World J Clin Infect Dis. 2012; 2: 63–76.
33. Lu J, Holmgren A. The thioredoxin antioxidant system. Free Radical Biol Med. 2014; 66: 75–87.
34. Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol. 2007; 5: 264–277. https://doi.org/10.1038/nrmicro1620 PMID: 17363965
35. Fournier B, Philpott DJ. Recognition of Staphylococcus aureus by the innate immune system. Clin Microbiol Rev. 2005; 18: 521–540. https://doi.org/10.1128/CMR.18.3.521-540.2005 PMID: 16020688
36. Schröder NW, Morath S, Alexander C, Hamann L, Hartung T, Zähringer U, et al. Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem. 2003; 278: 15587–15594. https://doi.org/10.1074/jbc.M212829200 PMID: 12594207
37. Bannerman DD, Paape MJ, Lee JW, Zhao X, Hope JC, Rainard P. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin Diagn Lab Immunol. 2004; 11: 463–472. https://doi.org/10.1128/CDLI.11.3.463-472.2004 PMID: 15138171
38. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010; 8: 623–633. https://doi.org/10.1038/nrmicro2415 PMID: 20676145
39. Zarnowski R, Sanchez H, Andes DR. Large-scale production and isolation of Candida biofilm extracellular matrix. Nat Protoc. 2016; 11: 2320–2327. https://doi.org/10.1038/nprot.2016.132 PMID: 27809313
40. Cassat JE, Dunman PM, McAleese F, Murphy E, Projan SJ, Smeltzer MS. Comparative genomics of Staphylococcus aureus musculoskeletal isolates. J Bacteriol. 2005; 187: 576–592. https://doi.org/10.1128/JB.187.2.576-592.2005 PMID: 15629929
41. Spaan AN, Reyes-Robles T, Badiou C, Cochet S, Boguslawski KM, Yoong P, et al. Staphylococcus aureus targets the Duffy Antigen Receptor for Chemokines (DARC) to lyse erythrocytes. Cell Host Microbe. 2015; 18: 363–370. https://doi.org/10.1016/j.chom.2015.08.001 PMID: 26320997
42. Scherr TD, Hanke ML, Huang O, James DB, Horswill AR, Bayles KW, et al. Staphylococcus aureus biofilms induce macrophage dysfunction through leukocidin AB and alpha-toxin. mBio. 2015; 6: e01021–15. https://doi.org/10.1128/mBio.01021-15 PMID: 26307164
43. Den Reijer PM, Haisma EM, Lemmens-den Toom NA, Willemse J, Koning RA, Demmers JA, et al. Detection of alpha-toxin and other virulence factors in biofilms of Staphylococcus aureus on polystyrene and a human epidermal model. PloS one. 2016; 11: e0145722. https://doi.org/10.1371/journal.pone.0145722 PMID: 26741798
44. Enany S, Yoshida Y, Magdeldin S, Bo X, Zhang Y, Enany M, et al. Two dimensional electrophoresis of the exo-proteome produced from community acquired methicillin resistant Staphylococcus aureus belonging to clonal complex 80. Microbiol Res. 2013; 168: 504–511. https://doi.org/10.1016/j.micres.2013.03.004 PMID: 23566758
45. Glowalla E, Tosetti B, Krönke M, Krut O. Proteomics-based identification of anchorless cell wall proteins as vaccine candidates against Staphylococcus aureus. Infect Immun. 2009; 77: 2719–2729. https://doi.org/10.1128/IAI.00617-08 PMID: 19364833
46. Muthukrishnan G, Quinn GA, Lamers RP, Diaz C, Cole AL, Chen S, et al. Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J Proteome Res. 2011; 10: 2064–2078. https://doi.org/10.1021/pr200029r PMID: 21338050
47. Gil C, Solano C, Burgui S, Latasa C, García B, Toledo-Arana A, et al. Biofilm matrix exoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infect Immun. 2014; 82: 1017–1029. https://doi.org/10.1128/IAI.01419-13 PMID: 24343648
48. Pasztor L, Ziebandt AK, Nega M, Schlag M, Haase S, Franz-Wachtel M, et al. Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J Biol Chem. 2010; 285: 36794–36803. https://doi.org/10.1074/jbc.M110.167312 PMID: 20847047
49. Yang CK, Ewis HE, Zhang X, Lu CD, Hu HJ, Pan Y, et al. Nonclassical protein secretion by Bacillus subtilis in the stationary phase is not due to cell lysis. J Bacteriol. 2011; 193: 5607–5615. https://doi.org/10.1128/JB.05897-11 PMID: 21856851
50. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick RP. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl Environ Microbiol. 2004; 70: 6076–6085. https://doi.org/10.1128/AEM.70.10.6076-6085.2004 PMID: 15466553
51. Bose JL, Fey PD, Bayles KW. Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus. Appl Environ Microbiol. 2013; 79: 2218–2224. https://doi.org/10.1128/AEM.00136-13 PMID: 23354696
52. Nesvizhskii AI, Keller A, Kolker E, Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem. 2003; 75: 4646–4658. PMID: 14632076
53. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protoc. 2009; 4: 44–57.