Proteomic and genomic analysis of methicillin-resistant staphylococcus aureus (MRSA) exposed to manuka honey in vitro demonstrated down-regulation of virulence markers

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 3, 2014, Pages 603-615

  Jenkins, Rowena ^a   Burton, Neil ^a   Cooper, Rose ^a  

^a CARDIFF METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

2D DIGE; Biofilms; Microarrays; Quorum sensing; Wounds

Indexed keywords

PROTEOME; VIRULENCE FACTOR;

BIOSYNTHESIS; CHEMISTRY; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HONEY; MASS SPECTROMETRY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; REAL TIME POLYMERASE CHAIN REACTION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

DOWN-REGULATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HONEY; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PROTEOME; REAL-TIME POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE FACTORS;

EID: 84894041802     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkt430     Document Type: Article

References (55)

1. Fischbach MA, Walsh CT. Antibiotics for emerging pathogens. Science 2009; 325: 1089-93.
2. Mahady GB. Medicinal plants for the prevention and treatment of bacterial infections. Curr Pharm Des 2005; 11: 2405-27.
3. Cooper RA, Molan PC, Harding KG. The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds. J Appl Microbiol 2002; 93: 857-63.
4. Cooper RA, Halas E, Molan PC. The efficacy of manuka honey in inhibiting strains of Pseudomonas aeruginosa frominfected burns. J Burns Care Rehab 2002; 23: 366-70.
5. Blair SE, Cockcetin NN, Harry EJ et al. The unusual antibacterial activity of medical-grade Leptospermum honey: antibacterial spectrum, resistance and transcriptome analysis. Eur J Clin Microbiol Infect Dis 2009; 10: 1199-208.
6. Maddocks SE, Salinas Lopez M, Rowlands R et al. Manuka honey inhibits the development of biofilms of Streptococcus pyogenes and causes reduced expression of two fibronectin binding proteins. Microbiol 2012; 158: 781-90.
7. Majtan J, Majtanova L, Bohora J et al. Honeydew honey as a potent antibacterial agent in eradication of multi-drug resistant Stenotrophomonas maltophila isolates from cancer patients. Phytother Res 2011; 25: 584-7.
8. Kwakman PHS, te Velde AA, de Boer L et al. Two major medicinal honeys have different mechanisms of bactericidal activity. PLoS One 2011; 6: e17709.
9. Mavric E, Wittmann S, Barth G et al. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of manuka (Leptospermum scoparium) honeys from New Zealand. Mol Nutr Food Res 2008; 52: 483-9.
10. Adams CJ, Boult CH, Deadman BJ et al. Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydr Res 2008; 343: 651-9.
11. Kato Y, Umeda N, Maeda A et al. Identification of a novel glycoside, leptosin, as a chemical marker of manuka honey. J Agric Food Chem 2012; 60: 3418-23.
12. Henriques A, Jenkins RE, Burton NF et al. The intracellular effects of manuka honey on Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 2010; 29: 45-50.
13. Jenkins RE, Burton N, Cooper RA. Manuka honey inhibits cell division in methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 2011; 66: 2536-42.
14. Jenkins RE, Burton NF, Cooper RA. The effect of manuka honey on the expression of universal stress protein A in methicillin-resistant Staphylococcus aureus. Int J Antimicrob Agents 2011; 37: 373-6.
15. Packer JM, Irish J, Herbert BR et al. Specific non-peroxide antibacterial effect of manuka honey on the Staphylococcus aureus proteome. Int J Antimicrob Agents 2012; 40: 43-50.
16. James G, Swogger E,Wolcott R et al. Biofilms in chronic wounds.Wound Rep Regen 2008; 16: 37-44.
17. Bernhardt J, Büttner K, Scharf C et al. Dual channel imaging of two-dimensional electropherograms in Bacillus subtilis. Electrophoresis 1999; 20: 2225-40.
18. Kohler C, von Eiff C, Peters G et al. Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J Bacteriol 2003; 185: 6928-37.
19. Shevchenko A, Wilm M, Vorm O et al. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 1996; 68: 850-8.
20. Medzidhradszky KF, Campbell JM, Baldwin MA et al. The characteristics of peptide collision-induced dissociation using a high performance MALDI-TOF/TOF tandem mass spectrometer. Anal Chem 2000; 72: 552-8.
21. Bienvenut WV, Deon C, Pasguarello C et al. Matrix-assisted laser desorption/ionization-tandem mass spectrometry with high resolution and sensitivity for identification and characterization of proteins. Proteomics 2002; 2: 868-76.
22. Perkins DN, Pappin DJ, Creasy DM et al. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999; 20: 3551-67.
23. Purves J, Cockayne A, Moody PC et al. Comparison of the regulation, metabolic functions, and roles in virulence of the glyceraldehyde-3-phosphate dehydrogenase homologues gapA and gapB in Staphylococcus aureus. Infect Immun 2010; 78: 5223-32.
24. Jarraud S, Mougel C, Thioulouse J et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002; 70: 631-41.
25. Manna AC, Ingavale SS, MaloneyMet al. Identification of sarV (SA2062), anewtranscriptional regulator, is repressedbySarAandMgrA(SA0641)and involved in the regulation of autolysis in Staphylococcus aureus. J Bacteriol 20045; 186: 5267-80.
26. Groicher KH, Firek BA, FujimotoDBet al. The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 2000; 182: 1794-801.
27. Sotto A, Lina G, Richard J-L et al. Virulence potential of Staphylococcus aureus strains isolated from diabetic foot ulcers. Diabetes Care 2008; 31: 2318-24.
28. Booth MC, Cheung AL, Hatter KL et al. Staphylococcal accessory regulator (sar) in conjunction with agr contributes to Staphylococcus aureus virulence in endophthalmitis. Infect Immun 1997; 65: 1150-6.
29. Chan F, Foster SJ. The role of SarA in virulence determinant production and environmental signal transduction in Staphylococcus aureus. J Bacteriol 1998; 180: 6232-41.
30. Peng HL, Novick RP, Kreiswirth B et al. Cloning, characterisation, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 1998; 170: 4365-72.
31. Novick RP, Ross HF, Projan S et al. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO 1993; 12: 3967-75.
32. Haslinger-Loffler B, Khal BC, Grundmeier M et al. Multiple virulence factors are required for Staphylococcus aureus-induced apoptosis in endothelial cells. Cell Microbiol 2005; 7: 1087-97.
33. Truchado P, López-Gálvez F, Gil MI et al. Quorum sensing inhibitory and antimicrobial activities of honeys and the relationship with individual phenolics. Food Chem 2009; 115: 1337-44.
34. Truchado P, Gil-Izquierdo A, Tomás-Barbéran F et al. Inhibition by chestnut honey of N-acetyl-l-homoserine lactones and biofilm formation in Erwinia carotovora, Yersinia enterocolitica, and Aeromonas hydrophila. J Agric Food Chem 2009; 57: 11186-93.
35. Wang R, Starkey M, Hazan R et al. Honey's ability to counter bacterial infections arises from both bactericidal compounds and QS inhibition. Front Microbiol 2012; 3: 144.
36. Alandejani T, Marsan JG, Ferris W et al. Effectiveness of honey on Staphylococccus aureus and Pseudomonas aeruginosa biofilms. Otolaryngol Head Neck Surg 2009; 139: 107-11.
37. Merckoll P, Jonassen Tø, Vad ME et al. Bacteria, biofilm and honey: a study of the effects of honey on 'planktonic' and biofilm-embedded chronic wound bacteria. Scand J Infect Dis 2009; 41: 341-7.
38. Caiazza NC, O'Toole GA. Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J Bacteriol 2003; 185: 3214-7.
39. Goekre C, Fluckiger U, Steinhuber A et al. Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infections resolved by quantitative transcript analysis. Mol Microbiol 2001; 40: 1439-47.
40. Harraghy N, Kormanec J,Wolz C et al. sae is essential for expression of the staphylococcal adhesions Eap and Emp. Microbiology 2005; 151: 1789-800.
41. Johnson M, Cockayne A, Morrissey JA. Iron-regulated biofilm formation in Staphylococcus aureus Newman requires ica and the secreted protein Emp. Infect Immun 2008; 76: 1756-65.
42. Bjarnsholt T, Kirketerp-Møller K, Jensen PØ et al. Why chronic wounds will not heal: a novel hypothesis.Wound Rep Regen 2008; 16: 2-10.
43. Modun B, Williams P. The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. InfectImmun1999; 67: 1086-92.
44. Piriz DS, Kayser FH, Berger-Bachi B. Impact of sar and agr on methicillin resistance in Staphylococcus aureus. FEMS Microbiol Lett 1996; 141: 255-60.
45. Jenkins RE, Cooper RA. Synergy between oxacillin and manuka honey sensitizes methicillin-resistant Staphylococcus aureus to oxacillin. J Antimicrob Chemother 2012; 67: 1405-7.
46. BrunskillEW, de Jonge BLM, BaylesKW. The Staphylococcus aureus scdA gene: a novel locus that affects cell division and morphogenesis. Microbiology 1997; 143: 2877-82.
47. Rice KC, Firek BA, Nelson JB et al. The Staphylococcal aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J Bacteriol 2003; 185: 2635-43.
48. Rice KC, Nelson JB, Patton TG et al. Acetic acid induces expression of the Staphylococcal aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 2005; 187: 813-21.
49. Cordwell SJ, Larsen MR, Cole RT et al. Comparative proteomics of Staphylococcus aureus and the response of methicillin-resistant and methicillin-sensitive strains to Triton X-100. Microbiology 2002; 148: 2765-81.
50. Jolly L, Pompeo F, van Heijenoort J et al. Autophosphorylation of phosphoglucosamine mutase from Escherichia coli. J Bacteriol 2000; 182: 1280-5.
51. Michel A, Agerer F, Hauck CR et al. Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J Bacteriol 2006; 188: 5783-96.
52. Chatterjee IP, Becker M, GrundmeierMet al. Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J Bacteriol 2005; 187: 4488-96.
53. Frees D, Chastanet A, Qazi S et al. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol 2004; 54: 1445-62.
54. Sadykov MR, BaylesKW. The control of death and lysis in staphylococcal biofilms: a coordination of physiological signals. Curr Opin Microbiol 2012; 15: 211-5.
55. Brunskill EW, Bayles KW. Identification of LytSR-regulated genes from Staphylococcus aureus. J Bacteriol 1996; 178: 5810-2.