Synergy between novel antimicrobials and conventional antibiotics or bacteriocins

• Autorzy: Wolska K.I. , Grzes K. , Kurek A.
• Języki publikacji: EN

Abstrakty

EN

Due to the alarming spread of resistance to classic antimicrobial agents, innovative therapeutic methods to combat antibiotic-resistant bacterial pathogens are urgently required. This minireview examines the enhancement of antibiotic efficacy by their combination with new antimicrobials, such as plant-derived compounds, metal ions and nanoparticles and bacteriophage lytic enzymes. The mechanisms of the observed synergy are also described. The promising results of basic research indicate that in future, combined therapy may be applied in human and veterinary medicine, agriculture and the food industry to combat bacterial pathogens.

Słowa kluczowe

EN

synergy; antimicrobial antibiotic; conventional antibiotic; bacteriocin; antibiotic; bacteriophage; nanoparticle; plant compound; bacterial pathogen

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2012
• Tom: 61
• Numer: 2
• Opis fizyczny: p.95-104,ref.

Twórcy

autor

Wolska K.I.

• Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland

autor

Grzes K.

autor

Kurek A.

Bibliografia

• Ahmad I. and F. Aqil. 2007. In vitro efficacy of bioactive extracts of 15 medicinal plants against ES beta L-producing multidrug resistant enteric bacteria. Microbiol. Res. 162: 264–275.
• Aiyegoro O.A., A.J. Afolayan and A.I. Okoh. 2010. Interactions of antibiotics and extracts of Helichrysum pedunculatum against bacteria implicated in wound infections. Folia Microbiol. 55: 176–180.
• Aqil F., M.S. Khan, M. Owais and I. Ahmad. 2005. Effect of certain bioactive plant extracts on clinical isolates of beta-lactamase producing methicillin resistant Staphylococcus aureus. J. Basic Microbiol. 45: 106–114.
• Ammons M.C., L.S. Ward and G.A. James. 2011. Anti-biofilm efficacy of a lactoferrin/xylitol wound hydrogel used in combination with silver wound dressings. Int. Wound J. 8: 268–273.
• Bapela N.B., N. Lall, P.B. Fourie, S.G. Franzblau and C.E.J. Van Rensburg. 2006. Activity of 7-methyljuglone in combination with antituberculous drugs against Mycobacterium tuberculosis. Phyto-medicine 13: 630–635.
• Becker S.C., J. Foster-Frey and D.M. Donovan. 2008. The phage K lytic enzyme LysK and lysostaphin act synergistically to kill MRSA. FEMS Microbiol. Lett. 287: 185–191.
• Birla S.S., V.V. Tiwari, A.K. Gade, A.P. Ingle, A.P. Yadav and M.K. Rai. 2009. Fabrication of silver nanoparticles by Phoma glomerata and its combined e%ect agaist Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Lett. Appl. Microbiol. 48: 173–179.
• Brehm-Stecher B.F. and E.A. Johnson. 2003. Sensitization of Staphy lococcus aureus and Escherichia coli to antibiotics by the sesquiterpenoids nerolidol, farnesol, bisabolol and apritone. Antimicrob. Agents Chemother. 47: 3357–3360.
• Burygin G.L., B.N. Khlebtsov, A.N. Shantrokha, L.A. Dykman, V.A. Bogatyrev and N.G. Khlebtsov. 2009. On the enhanced antibacterial activity of antibiotics mixed with gold nanoparticles. Nanoscale Res. Lett. 4: 794–801.
• Chibani-Chennoufi S., J. Sidoti, A. Bruttin, E. Kutter, S. Sarker and H. Brusow. 2004. In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob. Agents Chemother. 48: 2558–2569.
• Chopra I. 2007. The increasing use of silver-based products as antimicrobial agents: a useful development or a case for concern? J. Antimicrobial. Chem. 59: 587–590.
• Chung P.Y., P. Navaratnam and L.Y. Chung. 2011. Synergistic antimicrobial activity between pentacyclic triterpenoids and antibiotics against Staphylococcus aureus strains. Ann. Clin. Microbiol. Animicrob. 10: 25–30.
• Chusri S., I. Villanueva, S.P. Voravuthikunchai and J. Davies. 2009. Enhancing antibiotic activity: a strategy to control Acineto-bacter infections. J. Antimicrob. Chemother. 64: 1203–1211.
• Coleman K. 2011. Diazabicyclooctanes (DBOs): a potent new class of a non-β-lactam-lactamase inhibitors. Curr. Opin. Microbiol. 14: 550–555.
• Cushnie T.P. and A.J. Lamb. 2011. Recent advances in understanding the antibacterial properties of flavonoids. Int. J. Antimicrob. Agents 38: 99–107.
• Dajcs J.J., E.B. Hume, J.M. Moreau, A.R. Caballero, B.M. Cannon and R.J. O’Callaghan. 2000. Lysostaphin treatment of methicillin-resistant Staphylococcus aureus keratitis in the rabbit (1). Am. J.Ophtalmol. 130: 544.
• Daniel A., C. Euler, M. Collin, P. Chahales, K.J. Gorelick and V.A. Fischetti. 2010. Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylo-coccus aureus. Antimicrob. Agents Chemother. 54: 1603–1612.
• Defoirdt T., P. Sorgeloos and P. Bossier. 2011. Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr. Opin. Microbiol. 14: 251–258.
• Djurkovic S., J.M. Loeffer and V.A. Fischetti. 2005. Synergistic killing of Streptococcus pneumoniae with the bacteriophage lytic enzyme Cpl-1 and penicillin or gentamicin depends on the level of penicillin resistance. Antimicrob Agents Chemother. 49: 1225–1228.
• Durán N., P.D. Marcato, R. De Conti, O.L. Alves, F.T.M. Costa and M. Brocchi. 2010. Potential use of silver nanoparticles on pathogenic bacteria, their toxicity and possible mechanisms of action. J. Braz. Chem. Soc. 21: 949–959.
• EUCAST, 2000. Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. http://www. escmid.org/Files/E_def_1_2_03_2000.pdf
• Ettayebi K., J. El Yamani and B. Rossi-Hassani. 2000. Synergistic effect of nisin and thymol on antimicrobial activities in Listeria monocytogenes and Bacillus subtilis. FEMS Microbiol. Lett. 183: 191–195.
• Eumkeb G., S. Sakdarat and S. Siriwong. 2010. Reversing β-lactam antibiotic resistance against Staphylococcus aureus with galangin from Alpinia officinarum Hance and synergism with ceftazidime. Phytomedicine 18: 40–45.
• Falagas M.E. and S.K. Kasiakou. 2005. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin. Infect. Dis. 40: 1333–1341.
• Fayaz A.M., K. Balaji, M. Girilal, R. Yadav, P.T. Kalaichelvan and R. Venketesan. 2010. Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. Nanomedicine 6: 103–109.
• Fernebro J. 2011. Fighting bacterial infections – Future treatment options. Drug Resist. Updat. 14: 125–139.
• Fiamegos Y.C., P.L. Kastritis, V. Exarchou, H. Han, A.M. Bonvin, J. Vervoort, K. Lewis, M.R. Hamblin and G.P. Tegos. 2011. Antimicrobial and e\ux pump inhibitory activity of caffeoylquinic acids from Artemisia absinthium against Gram-positive pathogenic bacteria. PLoS ONE 6: e18127.
• Fischbach M. 2011. Combination therapies for combating antibacterial resistance. Curr. Opin. Microbiol. 14: 519–523.
• Fujita M., S. Shiota, T. Kuroda, T. Hatano, T. Yoshida, T. Mizushima and T. Tsuchiya. 2005. Remarkable synergies between baicalein and tetracycline and baicalein and β-lactam against methicillinesistant Staphylococcus aureus. Microbiol. Immunol. 49: 391–396.
• García P., B. Martínez, L. Rodríguez and A. Rodríguez. 2010. Synergy between the phage endolysin LysH5 and nisin to kill Staphylococcus aureus in pasteurized milk. Int. J. Food Microbiol. 141: 151–155.
• Garo E., G.R. Eldridge, M.G. Goering, E. DeLancey Pulcini, M.A. Hamilton, J.W. Costerton and G.A. James. 2007. Asiatic acid and corosolic acid enhance the susceptibility of Pseudomonas aeruginosa biofilms to tobramycin. Antimicrob. Agents Chemother. 51: 1813–1817.
• Garvey M.I., M.M. Rahman, S. Gibbons and L.J. Piddock. 2011. Medical plant extracts with e\ux inhibitory activity against Gramnegative bacteria. Int. J. Antimicrob. Agents 37: 145–151.
• Ge F., F. Zeng, S. Liu, N. Guo, H. Ye, Y. Song, J. Fan, X. Wu, X. Wang, X. Deng, Q. Jin and L. Yu. 2010. In vitro synergistic interactions of oleanolic acid in combination with isoniazid, rifampicin or ethambutanol against Mycobacterium tuberculosis. J. Med. Microbiol. 59: 567–572.
• Gibbons S. and E.E. Udo. 2000. !e effect of reserpine, a modulator of multidrug pumps, on the in vitro activity of tetracycline against clinical isolates of methicillin resistant Staphylococcus aureus (MRSA) possessing the tet(k) determinant. Phytother. Res. 14: 139–140.
• Ginsberg A.M. and M. Spigelman. 2007. Challenges in tuberculosis drug research and development. Nat. Med. 13: 290–294.
• Gould S.W., M.D. Fielder, A.F. Kelly and D.P. Naughton. 2009a. Anti-microbial activities of pomegranate rind extracts: enhancement by cupric sulphate against clinical isolates of S. aureus, MRSA and PVL positive CA-MSSA. BMC Complement. Altern. Med. 9: 23
• Gould S.W., M.D. Fielder, A.F. Kelly, W. El Sankary and D.P. Naughton. 2009 b. Antimicrobial pomegranate rind extracts: enhancement by Cu(II) and vitamin C combinations against clinical isolates of Pseudomonas aeruginosa. Br. J. Biomed. Sci. 66: 129–132.
• Górski A., A. Miedzobrodzki, J. Weber-Dabrowska, M. Łobocka, W. Fortuna, S. Letkiewicz, M. Zimecki and G. Filby. 2009. Bacteriophage therapy for the treatment of infections. Curr. Opin. Investig. Drugs 10: 766–774.
• Grande M.J., R.L. López, H. Abriouel, E. Valdivia, N. Ben Omar, M. Maqueda, M. Martinez-Canamero and A. Gálvez. 2007. Treatment of vegetable sauce with enterocin AS-48 alone or in combination with phenolic compounds to inhibit proliferation of Staphylococcus aureus. J. Food Prot. 70: 405–411.
• Grandgirard D., J.M. Loeffer, V.A. Fischetti and S.I. Lieb. 2008. Phage lytic enzyme CpL-1 for antibacterial therapy in experimental pneumococcal meningitis. J. Infect. Dis. 197: 1519–1522.
• Grudniak A.M., A. Kurek, J. Szarlak and K.I. Wolska. 2011. Oleanolic and ursolic acids influence the expression of the cysteine regulon and the stress response in Escherichia coli. Curr. Microbiol. 62: 1331–1336.
• Gu H., P.L. Ho, E. Tong, L. Wang and B. Xu. 2003. Presenting vancomycin on nanoparticles to enhance antimicrobial activities. Nano Lett. 3: 1261–1263.
• Hamill T.M., B.F. Gilmore, D.S. Jones and S.P. Gorman. 2007. Strategies for the development of the urinary catheters. Expert Rev. Med. Devices 4: 215–225.
• Hardes J., C. von Eiff, A. Streitbuerger, M. Balke, T. Budny, M.P. Henrichs, G. Hauschild and H. Ahrens. 2010. Reduction of periprosthetic infection with silver-coated megaprostheses in patients with bone sarcoma. J. Surg. Oncol. 101: 389–395.
• Hemaiswarya S., A.K. Kruthiventi and M. Doble. 2008. Synergism between natural products and antibiotics against infectious diseases. Phytomedicine 15: 639–652.
• Horiuchi K., S. Shiota, T. Kuroda, T. Hatano, T. Yoshida and T. Tsuchiya. 2007. Potentiation of antimicrobial activity of aminoglycosides by carnosol from Salvia officinalis. Biol. Pharm. Bull. 30: 287–290.
• Hu Z.-Q., W.-H. Zhao, Y. Hara and T. Shimamura. 2001. Epigallocatechin gallate synergy with ampicillin/sulbactam against 28 clinical isolates of methicillin-resistant Staphylococcus aureus J. Antimicrob. Chemother. 48: 361–364.
• Im A.R., L. Han, E.R. Kim, Y.S. Kim and Y. Park. 2011. Enhanced antibacterial activities of Leonuri Herba extracts containing silver nanoparticles. Phytother. Res. Doi: 10.1002/ptr.3683.
• Kaneko M., N. Togashi, H. Hamashima, M. Hirohara and Y. Inoue. 2011. Effect of farnesol on mevalonate pathway of Staphylococcus aureus. J. Antibiot. 64: 547–549.
• Kondo K., Y. Takaishi, H. Shibata and T. Higuti. 2006. ILSMRs (intensifier of beta-lactam-susceptibility in methicillin-resistant Staphylococcus aureus) from Tara [Caesalpinia spinosa (Molina) Kuntze]. Phytomedicine 13: 209–212.
• Kozai K., J. Suzuki, M. Okada and N. Nagasaka. 1999. Effect of oleanolic acid-cyclodextrin inclusion compounds on dental carries by in vitro experiment in rat-carries model. Microbios 97: 179–188.
• Kurek A., A.M., Grudniak, M. Szwed, A. Klicka, Ł. Samluk and K.I. Wolska. 2010. Oleanolic acid and ursolic acid affect peptidoglycan metabolism in Listeria monocytogenes. Anton. Leuven. Int. J. Mol. Biol. 97: 61–68.
• Kurek A., A.M. Grudniak, A. Kraczkiewicz-Dowjat and K.I. Wolska. 2011. New antibacterial therapeutics and strategies. Pol. J. Microbiol. 60: 3–12.
• Kurek A., P. Nadkowska, S. Pliszka and K.I. Wolska. 2012. Modulation of antibiotic resistance in bacterial pathogens by oleanolic acid and ursolic acid. Phytomedicine, doi: 10.1016/j. phymed. 2011.12.009.
• Kuroda M., S. Nagasaki and T. Ohta. 2007. Sesquiterpene farnesol inhibits recycling of the C55 lipid carrier of the murein monomer precursor contributing to increased susceptibility to β-lactams in methicillin-resistant Staphylococcus aureus. J. Antimicrob. Chemother. 59: 425–432.
• Li Y., P. Leung, Q.W. Song and E. Newton. 2006. Antimicrobial effect of surgical masks coated with nanoparticles. J. Hosp. Infect. 62: 58–63.
• Lim Y.H., I.H. Kim and J.J. Seo. 2007. In vitro activity of kaempferol isolated from Impatiens balsamina alone and in combination with erythromycin and clindamycin against Propionnibacterium acnes. J. Microbiol. 45: 473–477.
• Lin J.J., W.C. Lin, R.X. Dong and S.H. Hsu. 2012. The cellular responses and antibacterial activities of silver nanoparticles stabilized by different polymers. Nanotechnology 23: 065102.
• Liu C.S., T.M. Cham, C.H. Yang, H.W. Chang, C.H. Chen and L.Y. Chuang. 2007. Antibacterial properties of Chinese herbal medicines against nosocomical antibiotic resistant strains of Psuedomonas aeruginosa in Taiwan. Am. J. Chin. Med. 35: 1047–1060.
• Liu M.H., N. Otsuka, K. Noyori, S. Shiota, W. Ogawa, T. Kuroda, T. Hatano and T. Tsuchiya. 2009. Synergistic effect of kaempferol glycosides purified from Laurus nobilis and $uoroquinolones on methicillin-resistant Staphylococcus aureus. Biol. Pharm. Bull. 32: 489–492.
• Loeffer J.M. and V.A. Fischetti. 2003. Synergistic lethal effect of a combination of phage lytic enzymes with different activities on penicillin-sensitive and -resistant Streptococcus pneumoniae strains. Antimicrob. Agents Chemother. 47: 375–377.
• Lok C.M., C.M. Ho, R. Chen, Q.Y. He, W-Y. Yu, H. Sun, P.K. Tam, J.F. Chiu and C.M. Che. 2006. Proteomic analysis of the mode of antibacterial action of silver nanoparticles. J. Prot. Res. 5: 916–924.
• López R. and E. García. 2004. Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes and bacteriophage. FEMS Microbiol. Rev. 28: 553–580.
• Lorenzi V., A. Muselli, A.F. Bernardini, L. Berti, J.M. Pages, L. Amaral and J.M. Bolla. 2009. Geraniol restores antibiotic activities against multidrug-resistant isolates from gram-negative species. Antimicrob. Agents Chemother. 53: 2209–2211.
• Martínez B., J.M. Obeso, A. Rodríguez and P. García. 2008. Nisinbacteriophage crossresistance in Staphylococcus aureus. Int. J. Food Microbiol. 122: 253–258.
• Michalet S., G. Cartier, B. David, A.M. Mariotte, M.G. Dijoux-Franca, G.W. Kaatz, M. Stavri and S. Gibbons. 2007. N-caffeoylphenalkylamide derivatives as bacterial e\ux pump inhibitors. Bioorg. Med. Chem. Lett. 17: 1755–1758.
• Modak S. and C.L. Fox Jr. 1985. Synergistic action of silver sulfadiazine and sodium piperacillin on resistant Pseudomonas aeruginosa in vitro and in experimental burn wound infections. J. Trauma. 25: 27–31.
• Monteiro D.R., L.F. Gorup, A.S. Takamiya, A.C. Ruvollo-Filho, E.R. de Camargo and D.B. Barbosa. 2009. The growing importance of materials that prevent microbial adhesion; antimicrobial effect of metal devices containing silver. Int. J. Antimicrob. Agents 34: 103–110.
• Mulyaningsih S., F. Sporer, S. Zimmermann, J. Reichling and M. Wink. 2010. Synergistic properties of the terpenoids aromadendrene and 1,8-cineole from the essential oil of Eucalyptus globulus against antibiotic-susceptible and antibiotic-resistant pathogens. Phytomedicine 17: 1061–1066.
• Nascimento A.M., M.G. Brandao, G.B. Oliveira, I.C. Fortes and E. Chartone-Souza. 2007. Synergistic bactericidal activity of Eremanthus erythropappus oil or β-bisabolene with ampicillin against Staphylococcus aureus. Anton. Loeven. Int J. Mol. Biol. 92: 95–100.
• Nascimento J.G., M.D. Guerreiro-Pereira, S.F. Costa, C. Sao-José and M.A. Santos. 2008. Nisin-triggered activity of Lys44, the secreted endolysin from Oenococcus oeni phage fOg44. J. Bacteriol. 190: 457–461.
• Natarajan P., S. Katta, I. Andrei, V. Babu Rao Ambati, M. Leonida, G.J. Haas. 2008. Positive antibacterial co-action between hop (Humulus lupulus) constituents and selected antibiotics. Phytomedicine 15: 194–201.
• Neal A.I. 2008. What can be inferred from bacterium – nanoparticle interactions about the potential consequences of environmental exposure to nanoparticles? Exotoxicobiology 7: 362–371.
• Nelson D., L. Loomis and V.A. Fischetti. 2001. Prevention and elimination of upper respiratory colonization of mice by group A streptococci by using a bacteriophage lytic enzyme. Proc. Natl. Acad. Sci. U.S.A. 98: 4107–4112.
• Obeso J.M., B. Martínez, A. Rodríguez and P. García. 2008. Lytic activity of the recombinant staphylococcal bacteriophage phiH5 endolysin active against Staphylococcus aureus in milk. Int. J. Food Microbiol. 128: 212–218.
• O’Flaherty S., A. Coffey, W. Meaney, G.F. Fitzgerald and R.P. Ross. 2005. The recombinant phage lysin LysK has a broad spectrum of lytic activity against clinically relevant staphylococci, including methicillin-resistant Staphylococcus aureus. J. Bacteriol. 187: 7161–7164.
• Ohnishi Y., J. Ishikawa, H. Hara, H. Suzuki, M. Ikenoya, H. Ikeda, A. Yamashita, M. Hattori and S. Horinouchi. 2008. Genome sequence of the streptomycin-producing microorganism Strepto-myces griseus IFO 13350. J. Bacteriol. 190: 4050–4060.
• Parson J.B. and C.O. Rock. 2011. Is bacterial fatty acid synthesis a valid target for antibacterial drug discovery? Curr. Opin. Microbiol. 14: 544–549.
• Patil S.S., R.S. Dhumal, M.V. Varghese, A.R. Paradkar and P.K. Khanna. 2009. Synthesis and antibacterial studies of chloramphenicol loaded nano-silver against Salmonella typhi. Synth. React. Inorg. Met-Org. Nano-Met. Chem. 39: 65–72.
• Pissuwan D., C.H. Cortie, S.M. Valenzuela and M.B. Cortie. 2010. Functionalised gold nanoparticles for controlling patogenic bacteria. Trends Biotechnol. 28: 207–213.
• Plaper A., M. Golob, I. Hafner, M. Oblak, T. Solmajer and R. Jerala. 2003. Characterization of quercetin binding site on DNA gyrase. Biochem. Biophys. Res. Commun. 306: 530–536.
• Potara M., E. Jakab, A. Damert, O. Popescu, V. Canpean and S. Astilean. 2011. Synergistic antibacterial activity of chitosansilver nanocomposites on Staphylococcus aureus. Nanotechnology 22: 135101.
• Rai M., A. Yadav and A. Gade. 2009. Silver nanoparticles as a new generation of antimicrobials. Biotech. Adv. 27: 76–83.
• Rashel M., J. Uchiyama, T. Ujihara, Y. Uehara, S. Kuramoto, S. Sugihara, K. Yagyu, A. Muraoka, M. Sugai, K. Hiramatsu, K. Honke and S. Matsuzaki. 2007. Efficient elimination of multidrug- resistant Staphylococcus aureus by cloned lysine derived from bacteriophage phi MR11. J. Infect. Dis. 196: 1237–1247.
• Ren D., R. Zuo, A.F. Gonzalez Barrios, L.A. Bedzyk, G.R. Eldridge, M.E. Pasmore and T.K. Wood. 2005. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl. Environ. Microbiol. 71: 4022–4034.
• Riley M.A. and J.E. Wertz. 2002. Bacteriocins: evolutions, ecology, and application. Annu Rev. Microbiol. 56: 117–137.
• Rivardo F., M.G. Martinotti, R.J. Turner and H. Ceri. 2010. The activity of silver against Escherichia coli biofilm is increased by a lipopeptide biosurfactant. Can. J. Microbiol. 56: 272–278.
• Rodríguez-Cerrato V., P. García, G. del Prado, E. García, M. Garcia, L. Huelves, C. Ponte, R. López and F. Soriano. 2007. In vitro interactions of LytA, the major pneumococcal autolysin, with two bacteriophage lytic enzymes (Clp-1 and Pal), cefotaxime and moxifloxacin against antibiotic-susceptible and -resistant Streptococcus pneumoniae strains. J. Antimicrob. Chemother. 60: 1159–1162.
• Rosemary M.J., I. McLaren, T. Pradeep. 2006. Investigations of the antibacterial properties of ciprofloxacin SiO2. Langmuir. 22: 10125–10129.
• Ruden S., K. Hilpert, M. Berditsch, P. Wadhwani and A.S. Ulrich. 2009. Synergistic interaction between silver nanoparticles and membrane-permeabilizing antimicrobial peptides. Antimicrob. Agents Chemother. 53: 3538–3540.
• Schindler M. and M.J. Osborn. 1979. Interaction of divalent cations and polymyxin B with lipopolysaccharide. Biochemistry 18: 4425–4430.
• Shahverdi A.R., A. Fakhimi, H.R. Shahverdi and S. Minaian. 2007. Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine 3: 168–171.
• Singh M., S. Singh, S. Prasada and I.S. Gambhir. 2008. Nanotechnology in medicine and antibacterial effect of silver nanoparticles. Digest J. Nanomat. Biostruct. 3: 115–122.
• Sivarooban T., N.S. Hettiarachchy and M.G. Johnson. 2008. Transmission electron microscopy study of Listeria monocytogenes treated with nisin in combination with either grape seed or green tea seed. J. Food Prot. 71: 2105–2109.
• Srivastava A., M. Talaue, S. Liu, D. Degen, R.Y. Ebright, E. Sineva, A. Chakraborty, S.Y. Druzhinin, S. Chatterjee, J. Mukhopadhyay, J.W. Ebright, A. Zozula, J. Shen, S. Sengupta, R.R. Niedfeldt, C. Xin, T. Kaneko, H. Irschik, R. Jansen, S. Donadio, N. Connell and R.H. Ebright 2011. New target for inhibition of bacterial RNA polymerase: ”swith region”. Curr. Opin. Microbiol. 14: 532–543.
• Stavri M., L.J. Piddock and S. Gibbons. 2007. Bacterial efflux pump inhibitors from natural sources. J. Antimicrob. Chemother. 59: 1247–1260.
• Sultana N., M.S. Arayne and R. Sabri. 2005. Erytromycin synergism with essential and trace elements. Pak. J. Pharm. Sci. 18: 35–39.
• Theuretzbacher U. 2011. Resistance drives antibacterial drug development. Curr. Opin. Pharmacol. 11: 433–438.
• Tom R.T., V. Suryanarayanan, P.G. Reddy, S. Baskaran and T. Pradeep. 2004. Ciprofloxacin-protected gold nanoparticles. Lang-muir. 20: 1909–1914.
• Tsuchiya H. and M. Iinuma. 2000. Reduction of membrane fluidity by antibacterial sophoraflavanone G isolated from Sophora exigua. Phytomedicine 7: 161–165.
• Tu D., G. Blaha, P.B. Moore and T.A. Steitz. 2005. Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation of resistance. Cell 121: 257–270.
• Vitiello M., M. Galdiero, E. Finamore, S. Galdiero and M. Galdiero. 2012. NF-κB as a potential therapeutic target in microbial diseases. Mol. Biosyst. 8: 1108–1120.
• Wagner H. and G. Ulrich-Merzenich. 2009. Synergy research: approaching a new generation of phytopharmaceuticals. Phyto-medicine 2–3: 97–110.
• Walencka E., S. Rózalska, H. Wysokinska, M. Rózalski, L. Kuzma and B. Rózalska. 2007. Salvipisone and aethopinone from Salvia sclarea hairy roots modulate staphylococcal antibiotic resistance and express anti-biofilm activity. Planta Med. 73: 545–551.
• Wolska K.I., A.M. Grudniak, B. Fiecek, A. Kraczkiewicz-Dowjat, A. Kurek. 2010. Antibacterial activity of oleanolic and ursolic acids and their derivatives. Centr. Eur. J. Biol. 5: 543–553.
• Wormser G.P., G.T. Keusch and R.C. Heel. 1982. Co-trimoxazole (trimethoprim-sulfamethoxazole): an updated review of its antibacterial activity and clinical efficacy. Drugs 24: 459–518.
• Yam Y.S., J.M.T. Hamilton-Miller and S. Shah. 1998. !e effect of a component of tea (Camellia sinensis) on methicillin resistance, PBP2’ synthesis, and β-lactamase production in Staphylococcus aureus. J. Antimicrob. Chemother. 42: 211–216.
• Yoong P., R. Schuch, D. Nelson and V.A. Fischetti. 2006. PlyPH, a bacteriolytic enzyme with a broad pH range of activity and lytic action against Bacillus anthracis. J. Bacteriol. 188: 2711–2714.
• Zhao W.-H., Z.Q. Hu, S. Okuba, Y. Hara and T. Shimamaura. 2001. Mechanism of synergy between epigallocatechin gallate and β-lactams against methicillin-resistant Staphylococcus aureus. Anti-microb. Agents Chemother. 45: 1737–1742.
• Zhao W.-H., Z.-. Hu, Y. Hara, T. Shimamura. 2002. Inhibition of penicillinase by epigallocatechin gallate resulting in restoration of antibacterial activity of penicillin against penicillinase producing Staphylococcus aureus. Antimicrob. Agents Chemother. 36: 2266–2268.