DOI QR코드

DOI QR Code

Activity of Allyl Isothiocyanate and Its Synergy with Fluconazole against Candida albicans Biofilms

  • Received : 2016.07.29
  • Accepted : 2017.01.31
  • Published : 2017.04.28

Abstract

Candidiasis involving the biofilms of Candida albicans is a threat to immunocompromised patients. Candida biofilms are intrinsically resistant to the antifungal drugs and hence novel treatment strategies are desired. The study intended to evaluate the anti-Candida activity of allyl isothiocyanate (AITC) alone and with fluconazole (FLC), particularly against the biofilms. Results revealed the concentration-dependent activity of AITC against the planktonic growth and virulence factors of C. albicans. Significant (p <0.05) inhibition of the biofilms was evident at ${\leq}1mg/ml$ concentrations of AITC. Notably, a combination of 0.004 mg/ml of FLC and 0.125 mg/ml of AITC prevented the biofilm formation. Similarly, the preformed biofilms were significantly (p <0.05) inhibited by the AITC-FLC combination. The fractional inhibitory concentration indices ranging from 0.132 to 0.312 indicated the synergistic activity of AITC and FLC against the biofilm formation and the preformed biofilms. No hemolytic activity at the biofilm inhibitory concentrations of AITC and the AITC-FLC combination suggested the absence of cytotoxic effects. The recognizable synergy between AITC and FLC offers a potential therapeutic strategy against biofilm-associated Candida infections.

Keywords

References

  1. Ganguly S, Mitchell AP. 2011. Mucosal biofilms of Candida albicans. Curr. Opin. Microbiol. 14: 380-385. https://doi.org/10.1016/j.mib.2011.06.001
  2. Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6: 979-986. https://doi.org/10.1111/j.1567-1364.2006.00117.x
  3. Desai JV, Mitchell AP, Andes DR. 2014. Fungal biofilms, drug resistance, and recurrent infection. Cold Spring Harb. Perspect. Med. 1: 10.
  4. Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17: 255-267. https://doi.org/10.1128/CMR.17.2.255-267.2004
  5. Crump JA, Collignon PJ. 2000. Intravascular catheterassociated infections. Eur. J. Clin. Microbiol. Infect. Dis. 19: 1-8. https://doi.org/10.1007/s100960050001
  6. Mukherjee PK, Chandra J. 2004. Candida biofilm resistance. Drug Res. Updates 7: 301-309. https://doi.org/10.1016/j.drup.2004.09.002
  7. Fanning S, Mitchell AP. 2012. Fungal biofilms. PLoS Pathog. 8: e1002585. https://doi.org/10.1371/journal.ppat.1002585
  8. Srinivasan A, Lopez-Ribot JL, Ramasubramanian AK. 2014. Overcoming antifungal resistance. Drug Disc. Today Technol. 11: 65-71. https://doi.org/10.1016/j.ddtec.2014.02.005
  9. Ramage G, Robertson SN, Williams C. 2014. Strength in numbers: antifungal strategies against fungal biofilms. Int. J. Antimicrob. Agents 43: 114-120. https://doi.org/10.1016/j.ijantimicag.2013.10.023
  10. Cowan MM. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12: 564-582.
  11. Cragg GM, Newman DJ. 2013. Natural products: a continuing source of novel drug leads. Biochim. Biophys. Acta 1830: 3670-3695. https://doi.org/10.1016/j.bbagen.2013.02.008
  12. Lee HS, Kim Y. 2016. Antifungal activity of Salvia miltiorrhiza against Candida albicans is associated with the alteration of membrane permeability and $(1,3)-{\beta}-{\small{D}}$-glucan synthase activity. J. Microbiol. Biotechnol. 26: 610-617. https://doi.org/10.4014/jmb.1511.11009
  13. Raut JS, Karuppayil SM. 2016. Phytochemicals as inhibitors of Candida biofilm. Curr. Pharm. Des. 22: 4111-4134. https://doi.org/10.2174/1381612822666160601104721
  14. Wagner H, Ulrich-Merzenich G. 2009. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine 16: 97-110. https://doi.org/10.1016/j.phymed.2008.12.018
  15. Betts JW, Wareham DW, Haswell SJ, Kelly SM. 2013. Antifungal synergy of theaflavin and epicatechin combinations against Candida albicans. J. Microbiol. Biotechnol. 23: 1322-1326. https://doi.org/10.4014/jmb.1303.03010
  16. Doke SK, Raut JS, Dhawale SC, Karuppayil SM. 2014. Sensitization of Candida albicans biofilms to fluconazole by terpenoids of plant origin. J. Gen. Appl. Microbiol. 60: 163-168. https://doi.org/10.2323/jgam.60.163
  17. Wilson AE, Bergaentzle M, Bindler F, Marchioni E, Lintz A, Ennahar S. 2013. In vitro efficacies of various isothiocyanates from cruciferous vegetables as antimicrobial agents against foodborne pathogens and spoilage bacteria. Food Control 30: 318-324. https://doi.org/10.1016/j.foodcont.2012.07.031
  18. Wu X, Zhou QH, Xu K. 2009. Are isothiocyanates potential anti-cancer drugs? Acta Pharmacol. Sin. 30: 501-512. https://doi.org/10.1038/aps.2009.50
  19. Davaatseren M, Hwang JT, Park JH, Kim MS, Wang S, Sung MJ. 2014. Allyl isothiocyanate ameliorates angiogenesis and inflammation in dextran sulfate sodium-induced acute colitis. PLoS One 9: e102975. https://doi.org/10.1371/journal.pone.0102975
  20. Rhee MS, Lee SY, Dougherty RH, Kang DH. 2003. Antimicrobial effects of mustard flour and acetic acid against Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 69: 2959-2963. https://doi.org/10.1128/AEM.69.5.2959-2963.2003
  21. Shin IS, Masuda H, Naohide K. 2004. Bactericidal activity of wasabi (Wasabia japonica) against Helicobacter pylori. Int. J. Food Microbiol. 94: 255-261. https://doi.org/10.1016/S0168-1605(03)00297-6
  22. Depree JA, Howard TM, Savage GP. 1998. Flavour and pharmaceutical properties of the volatile sulphur compounds of wasabi (Wasabia japonica). Food Res. Int. 31: 329-337. https://doi.org/10.1016/S0963-9969(98)00105-7
  23. Harvey SG, Hannahan HN, Sams CE. 2002. Indian mustard and allyl isothiocyanate inhibit Sclerotium rolfsii. J. Am. Soc. Hort. Sci. 127: 27-31.
  24. Isshiki K, Tokuoka K, Mori R, Chiba S. 1992. Preliminary examination of allyl isothiocyanate vapor for food preservation. Biosci. Biotechnol. Biochem. 56: 1476-1477. https://doi.org/10.1271/bbb.56.1476
  25. Nowicki D, Rodzik O, Herman-Antosiewicz A, Szalewska-Palasz A. 2016. Isothiocyanates as effective agents against enterohemorrhagic Escherichia coli: insight to the mode of action. Sci. Rep. 6: 22263. https://doi.org/10.1038/srep22263
  26. Abreu AC, Borges A, Mergulhao F, Simoes M. 2014. Use of phenyl isothiocyanate for biofilm prevention and control. Int. Biodeterior. Biodegrad. 86: 34-41. https://doi.org/10.1016/j.ibiod.2013.03.024
  27. Borges A, Simoes LC, Saavedra MJ, Simoes M. 2014. The action of selected isothiocyanates on bacterial biofilm prevention and control. Int. Biodeterior. Biodegrad. 86: 25-33. https://doi.org/10.1016/j.ibiod.2013.01.015
  28. Clinical and Laboratory Standards Institute (CLSI). 2002. Reference method for broth dilution antifungal susceptibility testing of yeast. Approved Standard, M27-A2, 2nd Ed. Clinical and Laboratory Standards Institute, Wayne, PA. USA.
  29. Raut JS, Shinde RB, Chauhan NM, Karuppayil SM. 2014. Phenylpropanoids of plant origin as inhibitors of biofilm formation by Candida albicans. J. Microbiol. Biotechnol. 24: 1216-1225. https://doi.org/10.4014/jmb.1402.02056
  30. Raut JS, Shinde RB, Chauhan NM, Karuppayil SM. 2013. Terpenoids of plant origin inhibit morphogenesis, adhesion, and biofilm formation by Candida albicans. Biofouling 29: 87-96. https://doi.org/10.1080/08927014.2012.749398
  31. Liu W, Li LP, Zhang JD, Li Q, Shen H, Chene SM, et al. Synergistic antifungal effect of glabridin and fluconazole. PLoS One 9: e103442. https://doi.org/10.1371/journal.pone.0103442
  32. Shinde RB, Raut JS, Chauhan NM, Karuppayil SM. 2013. Chloroquine sensitizes biofilms of Candida albicans to antifungal azoles. Braz. J. Infect. Dis. 17: 395-400. https://doi.org/10.1016/j.bjid.2012.11.002
  33. Ahmad A, Khan A, Manzoor N, Khan LA. 2010. Evolution of ergosterol biosynthesis inhibitors as fungicidal against Candida. Microb. Pathog. 48: 35-41. https://doi.org/10.1016/j.micpath.2009.10.001
  34. Park HW, Choi KD, Shin IS. 2013. Antimicrobial activity of isothiocyanates (ITCs) extracted from horseradish (Armoracia rusticana) root against oral microorganisms. Biocontrol. Sci. 18: 163-168. https://doi.org/10.4265/bio.18.163
  35. Guiamet PS, Gomez de Saravia SG. 2005. Laboratory studies of biocorrosion control using traditional and environmentally friendly biocides: an overview. Lat. Am. Appl. Res. 35: 295-300.
  36. Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012: 528521.
  37. Verstrepen KJ, Klis FM. 2006. Flocculation, adhesion and biofilm formation in yeasts. Mol. Microbiol. 60: 5-15. https://doi.org/10.1111/j.1365-2958.2006.05072.x
  38. Vila T, Romo JA, Pierce CG, McHardy SF, Saville SP, Lopez-Ribot JL. 2016. Targeting Candida albicans filamentation for antifungal drug development. Virulence 2016: DOI: 10.1080/21505594.2016.1197444.
  39. Nickerson KW, Atkin AL, Hornby JM. 2006. Quorum sensing in dimorphic fungi: farnesol and beyond. Appl. Environ. Microbiol. 72: 3805-3813. https://doi.org/10.1128/AEM.02765-05
  40. Cui J, Ren B, Tong Y, Dai H, Zhang L. 2015. Synergistic combinations of antifungals and anti-virulence agents to fight against Candida albicans. Virulence 6: 362-371. https://doi.org/10.1080/21505594.2015.1039885
  41. Turgis M, Han J, Caillet S, Lacroix M. 2009. Antimicrobial activity of mustard essential oil against Escherichia coli O157:H7 and Salmonella typhi. Food Control 20: 1073-1079. https://doi.org/10.1016/j.foodcont.2009.02.001
  42. Raut JS, Karuppayil SM. 2014. A status review on the medicinal properties of essential oils. Ind. Crops Prod. 62: 250-264. https://doi.org/10.1016/j.indcrop.2014.05.055
  43. Xiao D, Srivastava SK, Lew KL, Zeng Y, Hershberger P, Johnson CS, et al. 2003. Allyl isothiocyanate, a constituent of cruciferous vegetables, inhibits proliferation of human prostate cancer cells by causing G2/M arrest and inducing apoptosis. Carcinogenesis 24: 891-897. https://doi.org/10.1093/carcin/bgg023
  44. National Toxicology Program (NTP). 1982. Carcinogenesis bioassay of allyl isothiocyanate (CAS No. 57-06-7) in F344/N Rats and B6C3F1 mice (Gavage study). Natl. Toxicol. Prog. Tech. Rep. Ser. 234: 1-142.
  45. Zhang Y. 2010. Allyl isothiocyanate as a cancer chemopreventive phytochemical. Mol. Nutr. Food Res. 54: 127-135. https://doi.org/10.1002/mnfr.200900323

Cited by

  1. Biofabricated Silver Nanoparticles Synergistically Activate Amphotericin B Against Mature Biofilm Forms of Candida Albicans vol.4, pp.None, 2017, https://doi.org/10.2174/1875933501704010001
  2. Cell Surface Hydrophobicity as a Virulence Factor in Candida albicans vol.14, pp.4, 2017, https://doi.org/10.13005/bbra/2598
  3. The antifungal agent of silver nanoparticles activated by diode laser as light source to reduce C. albicans biofilms: an in vitro study vol.34, pp.5, 2019, https://doi.org/10.1007/s10103-018-2677-4
  4. Anti-biofilm activity of a semi-synthetic molecule obtained from resveratrol against Candida albicans biofilm vol.58, pp.4, 2020, https://doi.org/10.1093/mmy/myz087
  5. The effect of benzyl isothiocyanate on Candida albicans growth, cell size, morphogenesis, and ultrastructure vol.36, pp.10, 2017, https://doi.org/10.1007/s11274-020-02929-9
  6. Effects of Glucosinolate-Derived Isothiocyanates on Fungi: A Comprehensive Review on Direct Effects, Mechanisms, Structure-Activity Relationship Data and Possible Agricultural Applications vol.7, pp.7, 2017, https://doi.org/10.3390/jof7070539
  7. Interactions between Brassica Biofumigants and Soil Microbiota: Causes and Impacts vol.69, pp.39, 2017, https://doi.org/10.1021/acs.jafc.1c03776