Efficacy of the quorum sensing inhibitor FS10 alone and in combination with tigecycline in an animal model of staphylococcal infected wound

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Simonetti, Oriana ^a   Cirioni, Oscar ^a   Cacciatore, Ivana ^b   Baldassarre, Leonardo ^b   Orlando, Fiorenza ^c   Pierpaoli, Elisa ^c   Lucarini, Guendalina ^a   Orsetti, Elena ^a   Provinciali, Mauro ^c   Fornasari, Erika ^b   Di Stefano, Antonio ^b   Giacometti, Andrea ^a   Offidani, Annamaria ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c INRCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; COLLAGEN; FS 10; MELITTIN; TIGECYCLINE; UNCLASSIFIED DRUG; MINOCYCLINE; OLIGOPEPTIDE; RNAIII INHIBITING PEPTIDE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIUM CULTURE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG DETERMINATION; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; DRUG SAFETY; DRUG SCREENING; EPITHELIZATION; FOAM DRESSING; GROWTH INHIBITION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; MALE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MONOTHERAPY; MOUSE; NONHUMAN; QUORUM SENSING; STAPHYLOCOCCUS INFECTION; WOUND HEALING; WOUND INFECTION; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HUMAN; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCAL INFECTIONS;

ANIMALS; ANTI-BACTERIAL AGENTS; DISEASE MODELS, ANIMAL; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MINOCYCLINE; OLIGOPEPTIDES; QUORUM SENSING; STAPHYLOCOCCAL INFECTIONS; WOUND INFECTION;

EID: 84973325034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151956     Document Type: Article

References (36)

1. Deurenberg RH, Stobberingh EE. The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus. Curr Mol Med. 2009; 9(2):100-15. PMID: 19275621
2. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002; 15(2):167-93. PMID: 11932229
3. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001; 14: 358 (9276):135-8. PMID: 11463434
4. De la Fuente-Núñez C, Reffuveille F. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opinion Microbiol. 2014; 96-104.
5. Krucke GW, Grimes DE, Grimes RM, Dang TD. Antibiotic resistance in staphylococcus aureus-containing cutaneous abscesses of patients with HIV. Am J Emerg Med. 2009; 27: 344-347. doi: 10.1016/j.ajem.2008.03.046 PMID: 19328381
6. Hancock RE, Sahl HG. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol. 2006; 24(12):1551-1557. PMID: 17160061
7. Vaara M. New approaches in peptide antibiotics. Curr Opin Pharmacol. 2009; 9(5):571-6. doi: 10.1016/j.coph.2009.08.002 PMID: 19734091
8. Cirioni O, Wu G, Li L, Orlando F, Silvestri C, Ghiselli R et al. S-thanatin enhances the efficacy of tigecycline in an experimental rat model of polymicrobial peritonitis. Peptides. 2010; 31(7):1231-6. doi: 10.1016/j.peptides.2010.03.034 PMID: 20381561
9. Simonetti O, Arzeni D, Ganzetti G, Silvestri C, Cirioni O, Gabrielli E et al. In vitro activity of the lipopeptide derivative (Pal-Lys-Lys-NH), alone and in combination with antifungal agents, against clinical isolates of dermatophytes. Br J Dermatol. 2009; 161(2):249-52. doi: 10.1111/j.1365-2133.2009.09166.x PMID: 19438437
10. Simonetti O, Cirioni O, Ghiselli R, Goteri G, Orlando F, Monfregola L et al. Antimicrobial properties of distinctin in an experimental model of MRSA-infected wounds. Eur J ClinMicrobiol Infect Dis. 2012; 31 (11):3047-55.
11. Simonetti O, Cirioni O, Ghiselli R, Orlando F, Silvestri C, Mazzocato S et al. In vitro activity and in vivo animal model efficacy of IB-367 alone and in combination with imipenem and colistin against Gram-negative bacteria. Peptides. 2014; 55:17-22. doi: 10.1016/j.peptides.2014.01.029 PMID: 24531033
12. Simonetti O, Cirioni O, Goteri G, Ghiselli R, Kamysz W, Kamysz E et al. Temporin A is effective in MRSA-infected wounds through bactericidal activity and acceleration of wound repair in amurine model. Peptides. 2008; 29(4):520-8. doi: 10.1016/j.peptides.2007.12.011 PMID: 18255189
13. Simonetti O, Ganzetti G, Arzeni D, Campanati A, Marconi B, Silvestri C et al. In vitro activity of Tachyplesin III alone and in combination with terbinafine against clinical isolates of dermatophytes. Peptides. 2009; 30(10):1794-7. doi: 10.1016/j.peptides.2009.06.033 PMID: 19591887
14. Balaban N, Cirioni O, Giacometti A, Ghiselli R, Braunstein JB, Silvestri C et al. Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother. 2007; 51(6):2226-9. PMID: 17371825
15. Cirioni O, Giacometti A, Ghiselli R, Dell'Acqua G, Gov Y, Kamysz W. Prophylactic efficacy of topical temporin A and RNAIII-inhibiting peptide in a subcutaneous rat Pouch model of graft infection attributable to staphylococci with intermediate resistance to glycopeptides.Circulation. 2003; 108(6):767-71. PMID: 12885754
16. Cirioni O, Giacometti A, Ghiselli R, Dell'Acqua G, Orlando F, Mocchegiani F et al. RNAIII-inhibiting peptide significantly reduces bacterial load and enhances the effect of antibiotics in the treatment of central venous catheter-associated Staphylococcus aureus infections. J Infect Dis. 2006; 193(2):180-6. PMID: 16362881
17. Cirioni O, Ghiselli R, Minardi D, Orlando F, Mocchegiani F, Silvestri C et al. RNAIII-inhibiting peptide affects biofilm formation in a rat model of staphylococcal ureteral stent infection. Antimicrob Agents Chemother. 2007; 51(12):4518-20. PMID: 17875996
18. Simonetti O, Cirioni O, Ghiselli R, Goteri G, Scalise A, Orlando F et al. RNAIII-inhibiting peptide enhances healing of wounds infected with methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2008; 52(6):2205-11. doi: 10.1128/AAC.01340-07 PMID: 18391046
19. Baldassarre L, Fornasari E, Cornacchia C, Cirioni O, Silvestri C, Castelli P et al. Discovery of novel RIP derivatives by alanine scanning for the treatment of S. aureus infections. Med Chem Comm. 2013; 4(7):1114-1117.
20. Cirioni O, Mocchegiani F, Cacciatore I, Vecchiet J, Silvestri C, Baldassarre L et al. Quorum sensing inhibitor FS3-coated vascular graft enhances daptomycin efficacy in a rat model of staphylococcal infection. Peptides. 2013; 40:77-81. doi: 10.1016/j.peptides.2012.12.002 PMID: 23262356
21. Simonetti O, Cirioni O, Mocchegiani F, Cacciatore I, Silvestri C, Baldassarre L et al. The efficacy of the quorum sensing inhibitor FS8 and tigecycline in preventing prosthesis biofilm in an animal model of staphylococcal infection. Int J Molec Sci. 2013; 14 (8):16321-16332.
22. González JE, Keshavan ND. Messing with bacterial quorum sensing. Microbiol Mol Biol Revi. 2006; 70 (4): 859-875.
23. Peterson LR. A review of tigecycline - the first glycylcycline. Int J Antimicrob Agents 2008; 32:S215-22. doi: 10.1016/S0924-8579(09)70005-6 PMID: 19134522
24. Silvestri C, Cirioni O, Arzeni D, Ghiselli R, Simonetti O, Orlando F et al. In vitro activity and in vivo efficacy of tigecycline alone and in combination with daptomycin and rifampin against Gram-positive cocci isolated from surgical wound infection. Eur J Clin Microbiol Infect Dis. 2012; 31(8):1759-64. doi: 10.1007/s10096-011-1498-1 PMID: 22160846
25. Simonetti O, Cirioni O, Lucarini G, Orlando F, Ghiselli R, Silvestri C et al. Tigecycline accelerates staphylococcal-infected burn wound healing through matrix metalloproteinase-9 modulation. J Antimicrob Chemother 2012; 67(1):191-201. doi: 10.1093/jac/dkr440 PMID: 22065244
26. Dinar S. A new material for the standard burn model: adhesive. Plas Reconstr Surg. 2006; 117:717-8.
27. Clinical and Laboratory Standards Institute (CLSI). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard M7-A6. Ninth ed. Villanova, PA. 2012.
28. Kugelberg E, Norström T, Petersen TK, Duvold T, Andersson DI, Hughes D. Establishment of a superficial skin infection model in mice by using Staphylococcus aureus and Streptococcus pyogenes. Antimicrob Agents Chemother 2005; 49(8):3435-41. PMID: 16048958
29. Bowler PG, Welsby S, Towers V, Booth R, Hogarth A, Rowlands V et al. Multidrug-resistant organisms, wounds and topical antimicrobial protection. Int Wound J 2012; 9(4):387-96. doi: 10.1111/j.1742-481X.2012.00991.x PMID: 22640181
30. McCarthy H, Rudkin JK, Black NS, Gallagher L, O'Neill E, O'Gara JP. Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol 2015; 28; 5:1-9. doi: 10.3389/fcimb.2015.00001 PMID: 25674541
31. Wolcott RD, Rhoads DD, Bennett ME, Wolcott BM, Gogokhia L, Costerton JW et al. Chronic wounds and the medical biofilm paradigm. J Wound Care 2010; 19(2):45-6, 48-50. PMID: 20216488
32. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. Inflammation and Host Response to Injury, Large Scale Collaborative Research Program. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A 2013; 26; 110(9):3507-12. doi: 10.1073/pnas.1222878110 PMID: 23401516
33. Webb DR. Animal models of human disease: inflammation. Biochem Pharmacol 2014; 87(1):121-30. doi: 10.1016/j.bcp.2013.06.014 PMID: 23811309
34. Osuchowski MF, Remick DG, Lederer JA, Lang CH, Aasen AO, Aibiki M. Abandon the mouse research ship? Not just yet! Shock. 2014; 41(6):463-75. doi: 10.1097/SHK.0000000000000153 PMID: 24569509
35. Lowery CA, Salzameda NT, Sawada D, Kaufmann GF, Janda KD. Medicinal chemistry as a conduit for the modulation of Quorum sensing. Journal of Medicinal Chemistry 2010; 53 (21):7467-7489. doi: 10.1021/jm901742e PMID: 20669927
36. Simonetti O, Lucarini G, Cirioni O, Zizzi A, Orlando F, Provinciali M et al. Delayed wound healing in aged skin rat models after thermal injury is associated with an increased MMP-9, K6 and CD44 expression. Burns 2013; 39(4):776-87. doi: 10.1016/j.burns.2012.09.013 PMID: 23084631