Assessment of in vivo antimicrobial activity of the carbene silver(I) acetate derivative SBC3 using Galleria mellonella larvae

BioMetals

Volumn 27, Issue 4, 2014, Pages 745-752

  Browne, Niall ^a   Hackenberg, Frauke ^b   Streciwilk, Wojciech ^b   Tacke, Matthias ^b   Kavanagh, Kevin ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Antimicrobial drug; Candida albicans; Carbene silver complex; Galleria mellonella; In vivo toxicity; Staphylococcus aureus

Indexed keywords

1,3-DIBENZYL-4,5-DIPHENYL-IMIDAZOL-2-YLIDENE SILVER(I) ACETATE; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; IMIDAZOLINE DERIVATIVE; INSECT PROTEIN; ORGANOMETALLIC COMPOUND;

ANIMAL; CANDIDA ALBICANS; DRUG EFFECTS; HUMORAL IMMUNITY; IMMUNOLOGY; LARVA; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOTH; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; IMIDAZOLINES; IMMUNITY, HUMORAL; INSECT PROTEINS; LARVA; MICROBIAL SENSITIVITY TESTS; MOTHS; ORGANOMETALLIC COMPOUNDS; STAPHYLOCOCCUS AUREUS;

EID: 84905079847     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-014-9766-z     Document Type: Article

References (40)

1. Adams AP, Santschi EM, Mellencamp MA (1999) Antibacterial properties of a silver chloride-coated nylon wound dressing. Vet Surg 28:219-225 (Pubitemid 129742502)
2. Atiyeh BS, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33:139-148 (Pubitemid 46188672)
3. Beresford P, Basinski-Gray JM, Chiu JKC, Chadwick JS, Aston WP (1997). Characterisation of hemolytic and cytotoxic gallysins: A relationship with arylophorins. Dev Comp Immunol 21:253-266. (Pubitemid 27329115)
4. Bergin D, Murphy L, Keenan J, Clynes M, Kavanagh K (2006) Pre-exposure to yeast protects larvae of Galleria mellonella from a subsequent lethal infection by Candida albicans and is mediated by the increased expression of antimicrobial peptides. Microbe Infect 8:2105-2112 (Pubitemid 44311574)
5. Boman HG, Hultmark D (1987) Cell-free immunity in insects. Ann Rev Microbiol 41:103-126
6. Brennan M, Thomas DY, Whiteway M, Kavanagh K (2002) Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol 34:153-157
7. Browne N, Heelan M, Kavanagh K (2013) An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4:1-7
8. Castellano JJ, Shafii SM, Ko F, Donate G, Wright TE, Mannari RJ, Payne WG, Smith DJ, Robson MC (2007) Comparative evaluation of silver-containing antimicrobial dressings and drugs. Int Wound J 4:114-122
9. Cotter G, Doyle S, Kavanagh K (2000) Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Microbiol 27:163-169 (Pubitemid 30047095)
10. Desbois AP, Coote PJ (2012) Utility of greater wax moth larva (Galleria mellonella) for evaluating the toxicity and efficacy of new antimicrobial agents. Adv Appl Microbiol 78:25-53
11. Fuchs B, Mylonakis E (2006) Using non-mammalian host to study fungal virulence and host defense. Curr Opin Microbiol 9:346-351 (Pubitemid 44108716)
12. Gupta L, Noh JY, Jo YH, Oh SH, Kumar S, Noh MY, Lee YS, Cha SJ, Seo SJ, Kim I, Han YS, Barillas-Mury C (2010) Apolipophorin-III mediates anti-plasmodial epithelial responses in Anopheles gambiae (G3) mosquitoes. PLoS ONE 5:e15410
13. Hackenberg F, Tacke M (2014) Benzyl-substituted metallocarbene antibiotics and anticancer drugs. Dalton transactions. (in print). http://dx.doi.org/10.1039/C4DT00624K
14. Hamamoto H, Kurokawa K, Kaito C, Kamura K, Manitra Razanajatovo I, Kusuhara H, Santa T, Sekimizu K (2004) Quantitative evaluation of the therapeutic effects of antibiotics using silkworms infected with human pathogenic microorganisms. Antimicrob Agents Chemother 48:774-779 (Pubitemid 38280323)
15. Hindi KM, Siciliano TJ, Durmus S, Panzner MJ, Medvetz DA, Reddy DV, Hogue LA, Hovis CE, Hilliard JK, Mallet RJ, Tessier CA, Cannon CL, Youngs WJ (2008) Synthesis, stability, and antimicrobial studies of electronically tuned silver acetate N-heterocyclic carbenes. JMed Chem 51:1577-1583 (Pubitemid 351438841)
16. Hornsey M, Wareham DW (2011) In vivo efficacy of glycopeptide-colistin combination therapies in a Galleria mellonella model of Acinetobacter baumannii infection. Antimicrob Agents Chemother 55:3534-3537
17. Jander G, Rahme L, Ausbel F (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182:3843-3845 (Pubitemid 30413039)
18. Kascatan-Nebioglu A, Melaiye A, Hindi K, Durmus S, Panzner MJ, Hogue LA, Mallett RJ, Hovis CE, Coughenour M, Crosby SD, Milsted A, Ely DL, Tessier CA, Cannon CL, Youngs WJ (2006) Synthesis from caffeine of a mixed N-heterocyclic carbene-silver acetate complex active against resistant respiratory pathogens. J Med Chem 49:6811-6818 (Pubitemid 44749748)
19. Kavanagh K, Fallon J (2010) Galleria mellonella larvae as models for studying fungal virulence. Fungal Biol Rev 24:79-83
20. Kavanagh K, Reeves EP (2004) Exploiting the potential of Insects for in vivo pathogenicity testing of Microbial pathogens. FEMS Microbiol Rev 28:101-112 (Pubitemid 38224509)
21. Kelly J, Kavanagh K (2011) Caspofungin primes the immune response of the larvae of Galleria mellonella and induces a non-specific antimicrobial response. J Med Microbiol 60:189-196
22. Lahm A, Paradisi A, Green DR, Melino G (2003) Death fold domain interaction in apoptosis. Cell Death Differ 10:10-12 (Pubitemid 36511826)
23. Lavine MD, Strand MR (2002) Insect haemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295-1309
24. Lionakis MS, Kontoyiannis DP (2005) Fruit flies as a mini-host model for studying drug activity and virulence in Aspergillus. Med Mycol 43:111-114
25. Lionakis MS, Lewis RE, May GS, Wiederhold NP, Albert ND, Halder G, Kontoyiannis DP (2005) Toll-deficient Drosophila flies as a fast, high-throughput model for the study of antifungal drug efficacy against invasive aspergillosis and Aspergillus virulence. J Infect Dis 191:1188-1195 (Pubitemid 40404379)
26. Maple PAC, Hamilton-Miller JMT, Brumfitt W (1989) Worldwide antibiotic resistance in methicillin-resistant Staphylococcus aureus. Lancet 333:537-540 (Pubitemid 19075214)
27. Mijnendonckx K, Leys N, Mahillon J, Silver S, Van Houdt R (2013) Antimicrobial silver: uses, toxicity and potential for resistance. Biometals 26:609-621
28. Mowlds P, Coates C, Renwick J, Kavanagh K (2010) Dose-dependent cellular and humoral responses in Galleria mellonella larvae following β-Glucan inoculation. Microb Infect 12:146-153
29. Oehninger L, Rubbiani R, Ott I (2013) N-Heterocyclic carbene metal complexes in medicinal chemistry. Dalton Trans 42:3269-3284
30. Park HJ, Kim JY, Kim J, Lee JH, Hahn JS, Gu MB, Yoon J (2009) Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res 43:1027-1032
31. Patil S, Tacke M (2011) NHC-Silver(I) Acetates as bioorganometallic anticancer and antibacterial drugs. In: Melník M, Segá P, Tatarko M (eds) Insights into coordination, bioinorganic and applied inorganic chemistry. Press of Slovak University of Technology, Bratislava, pp 555-566
32. Patil S, Deally A, Gleeson B, Müller-Bunz H, Paradisi F, Tacke M (2011) Novel benzyl-substituted N-heterocyclic carbene-silver acetate complexes: synthesis, cytotoxicity and antibacterial studies. Metallomics 3:74-88
33. Percival SL, Bowler PG, Russell D (2005) Bacterial resistance to silver in wound care. J Hosp Infect 60:1-7 (Pubitemid 40485843)
34. Rex JH (2014) ND4BB: addressing the antimicrobial resistance crisis. Nature Rev Microbiol 12:231-232
35. Rowan R, Moran C, McCann M, Kavanagh K (2009) Use of Galleria mellonella larvae to evaluate the in vivo anti-fungal activity of [Ag2(mal)(phen)3]. Biometals 22:461-467
36. Rowan R, McCann M, Kavanagh K (2010) Analysis of the response of Candida albicans cells to Silver (I). Med Mycol 48:498-505
37. Sharkey MA, O'Gara JP, Gordon SV, Hackenberg F, Healy C, Paradisi F, Patil S, Schaible B, Tacke M (2012) Investigations into the antibacterial activity of the silver-based antibiotic drug candidate SBC3. Antibiotics 1:25-28
38. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856-2860
39. Taylor JL, Radic Z (1994) The cholinesterases: from genes to proteins. Annu Rev Pharmacol Toxicol 34:281-320
40. Vogt RG, Riddiford LM, Prestwich GD (1985) Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea Polyphemus. Proc Natl Acad Sci USA 82:8827-8831 (Pubitemid 16101138)