Proteomic analysis of Staphylococcus aureus biofilms grown in vitro on mechanical heart valve leaflets

Journal of Biomedical Materials Research - Part A

Volumn 88, Issue 4, 2009, Pages 1069-1078

  Bénard, Laetitia ^a,b   Litzler, Pierre Yves ^a   Cosette, Pascal ^b   Lemeland, Jean François ^a,b   Jouenne, Thierry ^b   Junter, Guy Alain ^b  

^a HÔPITAL CHARLES NICOLLE   (France)

^b UNIVERSITÉ DE ROUEN   (France)

Author keywords

Bacterial adhesion; Immobilized cells; Prosthetic materials; Proteome; Two dimensional electrophoresis

Indexed keywords

BACTERIAL ADHESION; IMMOBILIZED CELLS; PROSTHETIC MATERIALS; PROTEOME; TWO-DIMENSIONAL ELECTROPHORESIS;

ADHESION; BACTERIOLOGY; BIOFILMS; CELL CULTURE; CELL IMMOBILIZATION; CELL PROLIFERATION; CYTOLOGY; ELECTROCHEMISTRY; ELECTROPHORESIS; HEART VALVE PROSTHESES; OPTICAL PROJECTORS; POPULATION STATISTICS; PRINCIPAL COMPONENT ANALYSIS; PROSTHETICS; PROTEINS; SURFACE PROPERTIES; TWO DIMENSIONAL; VALVES (MECHANICAL);

BIOFILTERS;

PROTEIN; TRYPSIN;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BIOFILM; DEVICE INFECTION; ELECTROPHORESIS; HEART VALVE PROSTHESIS; MASS SPECTROMETRY; MEMBRANE LEAFLET; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY;

BACTERIAL PROTEINS; BIOFILMS; HEART VALVE PROSTHESIS; HEART VALVES; HUMANS; PROSTHESIS-RELATED INFECTIONS; PROTEOME; STAPHYLOCOCCUS AUREUS;

EID: 60349099322     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.31941     Document Type: Article

References (64)

1. Darouiche RO. Treatment of infections associated with surgical implants. New Eng J Med 2004;350:1422-1429.
2. Arvay A, Lengyel M. Incidence and risk factors of prosthetic valve endocarditis. Eur J Cardio-Thorac Surg 1988;2:340-346.
3. Vongpatanasin W, Hillis LD, Lange RA. Prosthetic heart valves. New Eng J Med 1996;335:407-416.
4. Rubin JR, Yao JST, Thompson RG, Bergan JJ. Management of infection of major amputation stumps after failed femorodistal grafts. Surgery 1985;98:810-815.
5. Mertens RA, O'Hara PJ, Hertzer NR, Krajewski LP, Beven EG. Surgical management of infrainguinal arterial prosthetic graft infections: Review of a thirty-five-year experience. J Vasc Surg 1995;21:782-791.
6. Huebner J, Goldmann DA. Coagulase-negative staphylococci: Role as pathogens. Annu Rev Med 1999;50:223-236.
7. Dahn MS. What's new in vascular infections? Curr Surg 1999;56:335-340.
8. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 1999;67:5427-5433.
9. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol 1995;49:711-775.
10. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: A common cause of persistent infections. Science 1999;284:1318-1322.
11. Mah T-FC, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001;9:34-39.
12. Davies D. Understanding biofilm resistance to antimicrobial agents. Nature Rev 2003;2:114-122.
13. Beloin C, Ghigo J-M. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 2005;13:16-19.
14. Junter GA, Jouenne T. Immobilized viable microbial cells: From the process to the proteome or the cart before the horse. Biotechnol Adv 2004;22:633-658.
15. Dykes GA, Sampathkumar B, Korber DR. Planktonic or biofilm growth affects survival, hydrophobicity and protein expression patterns of a pathogenic Campylobacter jejuni strain. Int J Food Microbiol 2003;89:1-10.
16. Oosthuizen MC, Steyn B, Theron J, Cosette P, Lindsay D, Van Holy A, Brözel VS. Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl Environ Microbiol 2002;68:2770-2780.
17. Sauer K, Camper AK, Erlich GA, Costerton JW, Davies DG. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 2002;184:1140-1154.
18. Steyn B, Oosthuizen MC, MacDonald R, Theron J, Brözel VS. The use of glass wool as an attachment surface for studying phenotypic changes in Pseudomonas aeruginosa biofilms by two-dimensional gel electrophoresis. Proteomics 2001;1:871-879.
19. Svensäter G, Welin J, Wilkins JC, Beighton D, Hamilton IR. Protein expression by planktonic and biofilm cells of Streptococcus mutans. FEMS Microbiol Lett 2001;205:139-146.
20. Trémoulet F, Duché O, Namane A, Martinie B, Labadie JC. A proteomic study of Escherichia coli O157:H7 NCTC 12900 cultivated in biofilm or in planktonic growth mode. FEMS Microbiol Lett 2002;215:7-14.
21. Hecker M, Engelmann S, Cordwell SJ. Proteomics of Staphylococcus aureus: Current state and future challenges. J Chromatogr 2003;787:179-195.
22. Resch A, Leicht S, Saric M, Pásztor L, Jakob A, Götz F, Nordheim A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with franscriptome profiling. Proteomics 2006;6:1867-1877 (additional material available on the WWW under http://www.wiley-vch.de/contents/jc-120/2006/pro0531-.pdf).
23. Strathmann M, Wingender J. Use of an oxonol dye in combination with confocal laser scanning microscopy to monitor damage to Staphylococcus aureus cells during colonisation of silver-coated vascular grafts. Int J Antimicrob Agents 2004;24:234-240.
24. Van de Belt H, Neut D, Schenk W, Van Horn JR, Van der Mei HC, Busscher HJ. Staphylococcus aureus biofilm formation on different gentamicin-loaded polymethylmethacrylate bone cements. Biomaterials 2001;22:1607-1611.
25. Wang J, Huang N, Pan CJ, Kwok SCH, Yang P, Leng YX, Chen JY, Sun H, Wan GJ, Liu ZY, Chu PK. Bacterial repellence from polyethylene terephthalate surface modified by acetylene plasma immersion ion implantation deposition. Surf Coating Technol 2004;186:299-304.
26. Buczynski BW, Kory MM, Steiner RP, Kittinger TA, Ramsier RD. Bacterial adhesion to zirconium surfaces. Colloid Surf B-Biointerfaces 2003;30:167-175.
27. Harris LG, Tosatti S, Wieland M, Textor M, Richards RG. Staphylococcus aureus adhesion to titanium oxide surfaces coated with non-functionalized and peptide-functionalized poly(L-lysine)-grafted-poly(ethylene glycol) copolymers. Biomaterials 2004;25:4135-4148.
28. Vilain S, Cosette P, Hubert M, Lange C, Junter GA, Jouenne T. Proteomic analysis of agar gel-entrapped Pseudomonas aeruginosa. Proteomics 2004;4:1996-2004.
29. Vilain S, Cosette P, Zimmerlin I, Dupont J-P, Junter GA, Jouenne T. The biofilm proteome: Homogeneity or versatility? J Proteome Res 2004;3:132-136.
30. Rosenberg M, Gutnick D, Rosenberg E. Adherence of bacteria to hydrocarbons: A simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 1980;9:29-33.
31. Gibbons RJ, Etherden I. Comparative hydrophobicities of oral bacteria and their adherence to salivary pellicles. Infect Immun 1983;41:1190-1196.
32. Coquet L, Cosette P, Junter GA, Beucher E, Saiter JM, Jouenne T. Adhesion of Yersinia ruckeri to fish farm materials: Influence of cell and material surface properties. Colloid Surf B-Biointerfaces 2002;26:373-378.
33. Rabilloud T, Charmont S. Detection of proteins on two-dimensional electrophoresis gels. In: Rabilloud T, editor. Proteome Research: Two-Dimensional Gel Electrophoresis and Identification Methods. Berlin, Heidelberg: Springer-Verlag; 2000, Chapter 5, p 107-126.
34. Mamo W, Rozgonyi F, Brown A, Hjertén S, Wadström T. Cell surface hydrophobicity and charge of Staphylococcus aureus and coagulase-negative staphylococci from bovine mastitis. J Appl Bacteriol 1987;62:241-249.
35. Reifsteck F, Wee S, Wilkinson BJ. Hydrophobicity-hydrophilicity of staphylococci. J Med Microbiol 1987;24:65-73.
36. Van der Mei HC, Bos R, Busscher HJ. A reference guide to microbial cell surface hydrophobicity based on contact angles. Colloid Surf B-Biointerfaces 1998;11:213-221.
37. Okpalugo TIT, Ogwu AA, Maguire PD, McLaughlin JAD. Platelet adhesion on silicon modified hydrogenated amorphous carbon films. Biomaterials 2004;25:239-245.
38. Goodman SL, Tweden KS, Albrecht RM. Platelet interaction with pyrolytic carbon heart-valve leaflets. J Biomed Mater Res 1996;32:249-258.
39. Bradshaw DJ, Marsh PD, Schilling KM, Cummings D. A modified chemostat system to study the ecology of oral biofilms. J Appl Bacteriol 1996;80:124-130.
40. Francolini I, Donelli D, Stoodley P. Polymer designs to control biofilm growth on medical devices. Rev Environ Sci Bio/Technol 2003;2:307-319.
41. Rasmussen K, Østgaard K. Adhesion of the marine bacterium Pseudomonas sp. NCIMB 2021 to different hydrogel surfaces. Water Res 2003;37:519-524.
42. Nyvad B, Kilian M. Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res 1987;95:369-380.
43. Bos R, van der Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions - Its mechanisms and methods for study. FEMS Microbiol Rev 1999;23:179-229.
44. Bos R, van der Mei HC, Gold J, Busscher HJ. Retention of bacteria on a substratum surface with micro-patterned hydrophobicity. FEMS Microbiol Lett 2000;189:311-315.
45. Carlén A, Nikdel K, Wennerberg A, Holmberg K, Olsson J. Surface characteristics and in vitro biofilm formation on glass ionomer and composite resin. Biomaterials 2001;22:481-487.
46. Bruinsma GM, Rustema-Abbing M, de Vries J, Busscher HJ, van der Linden ML, Hooymans JMM, van der Mei HC. Multiple surface properties of worn RGP lenses and adhesion of Pseudomonas aeruginosa. Biomaterials 2003;24:1663-1670.
47. Li B, Logan BE. Bacterial adhesion to glass and metal-oxide surfaces. Colloid Surf B: Biointerf 2004;36:81-90.
48. Litzler PY, Bénard L, Barbier-Frébourg N, Vilain S, Jouenne T, Beucher E, Bunel C, Lemeland JF, Bessou JP. Biofilm formation on pyrolytic carbon heart valves: influence of surface free energy, roughness and bacterial species. J Thor Cardiovascul Surg 2007;134:1025-1032.
49. Luppens SBI, ten Cate JM. Effect of biofilm model, mode of growth, and strain on Streptococcus mutans protein expression as determined by two-dimensional difference gel electrophoresis. J Proteome Res 2005;4:232-237.
50. Schembri MA, Kjærgaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol 2003;48:253-267.
51. Cordwell SJ, Larsen MR, Cole RT, Walsh BJ. Comparative proteomics of Staphylococcus aureus and the response of methicillin-resistant and methicillin-sensitive strains to Triton X-100. Microbiology 2002;148:2765-2781.
52. Goldstein J, Pollitt NS, Inouye M. Major cold shock protein of Escherichia coli. Proc Natl Acad Sci USA 1990;87:283-287.
53. Ramos JL, Gallegos M-T, Marqués S, Ramos-González; M-I, Espinosa-Urgel M, Segura A. Responses of Gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 2001;4:166-171.
54. Kohler C, Wolff S, Albrecht D, Fuchs S, Becher D, Büttner K, Engelmann S, Hecker M. Proteome analyses of Staphylococcus aureus in growing and non-growing cells: A physiological approach. Int J Med Microbiol 2005;295:547-565.
55. Yoon SS, Hennigan RF, Hilliard GM, Ochsner UA, Parvatiyar K, Kamani MC, Allen HL, DeKievit TR, Gardner PR, Schwab U, Rowe JJ, Iglewski BH, McDermott TR, Mason RP, Wozniak DJ, Hancock REW, Parsek MR, Noah TL, Boucher RC, Hassett DJ. Pseudomonas aeruginosa anaerobic respiration in biofilms: Relationships to cystic fibrosis pathogenesis. Dev Cell 2002;3:593-603.
56. Clements MO, Foster SJ. Stress resistance in Staphylococcus aureus. Trends Microbiol 1999;7:458-462.
57. Clements JM, Beckett RP, Brown A, Catlin G, Lobell M, Palan S, Thomas W, Whittaker M, Wood S, Salama S, Baker PJ, Rodgers HF, Barynin V, Rice DW, Hunter MG. Antibiotic activity and characterization of BB-3497, a novel peptide deformylase inhibitor. Antimicrob Agents Chemother 2001;45:563-570.
58. Yuan Z, Trias J, White RJ. Deformylase as a novel antibacterial target. Drug Discov Today 2001;6:954-961.
59. Garcia-Lara J, Masalha M, Foster SJ. Staphylococcus aureus: The search for novel targets. Drug Discov Today 2005;10:643-651.
60. Hanson RS, Hanson TE. Methanotrophic bacteria. Microbiol Rev 1996;60:439-471.
61. Orita I, Yurimoto H, Hirai R, Kawarabayasi Y, Sakai Y, Kato N. The Archaeon Pyrococcus horikoshii possesses a bifunctional enzyme for formaldehyde fixation via the ribulose monophosphate pathway. J Bacteriol 2005;187:3636-3642.
62. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2004;2:95-108.
63. Scherl A, François P, Bento M, Deshusses JM, Charbonnier Y, Converset V, Huyghe A, Walter N, Hoogland C, Appel RD, Sanchez J-C, Zimmermann-Ivol CG, Corthals GL, Hochstrasser DF, Schrenzel J. Correlation of proteomic and transcriptomic profiles of Staphylococcus aureus during the post-exponential phase of growth. J Microbiol Meth 2005;60:247-257 (supplemental Table 2 in the online version at doi: 10.1016/j.mimet. 2004.09.017).
64. Luppens SB, ten Cate JM. Effect of biofilm model, mode of growth, and strain on Streptococcus mutans protein expression as determined by two-dimensional difference gel electrophoresis. J Proteome Res 2005;4:232-237.