1887

Journal of Medical Microbiology logo

Volume 67, Issue 4

1,4-Naphthoquinone derivatives potently suppress growth, inhibit formation of hyphae and show no toxicity toward zebrafish embryos Free

Abstract

In this study, we applied various assays to find new activities of 1,4-naphthoquinone derivatives for potential anti- applications.

These assays determined (a) the antimicrobial effect on growth/cell multiplication in fungal cultures, (b) the effect on formation of hyphae and biofilm, (c) the influence on cell membrane integrity, (d) the effect on cell morphology using atomic force microscopy, and (e) toxicity against zebrafish embryos. We have demonstrated the activity of these compounds against different species and clinical isolates of .

1,4-Naphthoquinones significantly affected fungal strains at 8–250 mg l of MIC. Interestingly, at concentrations below MICs, the chemicals showed effectiveness in inhibition of hyphal formation and cell aggregation in . Of note, atomic force microscopy (AFM) analysis revealed an influence of the compounds on cell morphological properties. However, at low concentrations (0.8–31.2 mg l), it did not exert any evident toxic effects on zebrafish embryos.

Our research has evidenced the effectiveness of 1,4-naphthoquinones as potential anti- agents.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): atomic force microscopy , biofilm , Candida albicans , hyphae , Naphthoquinones and zebrafish
© 2018 The Authors
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000700
2018-04-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/67/4/598.html?itemId=/content/journal/jmm/10.1099/jmm.0.000700&mimeType=html&fmt=ahah

References

  1. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 2007; 20:133–163 [View Article][PubMed]
     [Google Scholar]
  2. Yang YL. Virulence factors of Candida species. J Microbiol Immunol Infect 2003; 36:223–228[PubMed]
     [Google Scholar]
  3. Ortega M, Marco F, Soriano A, Almela M, Martínez JA et al. Candida species bloodstream infection: epidemiology and outcome in a single institution from 1991 to 2008. J Hosp Infect 2011; 77:157–161 [View Article][PubMed]
     [Google Scholar]
  4. Ellepola AN, Samaranayake LP. Oral candidal infections and antimycotics. Crit Rev Oral Biol Med 2000; 11:172–198 [View Article][PubMed]
     [Google Scholar]
  5. Sykes LM, Sukha A. Potential risk of serious oral infections in the diabetic patient: a clinical report. J Prosthet Dent 2001; 86:569–573 [View Article][PubMed]
     [Google Scholar]
  6. Jautová J, Baloghová J, Dorko E, Pilipcinec E, Svický E et al. Cutaneous candidosis in immunosuppressed patients. Folia Microbiol 2001; 46:359–360 [View Article][PubMed]
     [Google Scholar]
  7. Fidel PL. Candida-host interactions in HIV disease: relationships in oropharyngeal candidiasis. Adv Dent Res 2006; 19:80–84 [View Article][PubMed]
     [Google Scholar]
  8. Hasan F, Xess I, Wang X, Jain N, Fries BC. Biofilm formation in clinical Candida isolates and its association with virulence. Microbes Infect 2009; 11:753–761 [View Article][PubMed]
     [Google Scholar]
  9. Magaldi S, Mata S, Hartung C, Verde G, Deibis L et al. In vitro susceptibility of 137 Candida sp. isolates from HIV positive patients to several antifungal drugs. Mycopathologia 2001; 149:63–68 [View Article][PubMed]
     [Google Scholar]
  10. Nett JE, Sanchez H, Cain MT, Ross KM, Andes DR. Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot Cell 2011; 10:1660–1669 [View Article][PubMed]
     [Google Scholar]
  11. Kumagai Y, Shinkai Y, Miura T, Cho AK. The chemical biology of naphthoquinones and its environmental implications. Annu Rev Pharmacol Toxicol 2012; 52:221–247 [View Article][PubMed]
     [Google Scholar]
  12. Sharma A, Santos IO, Gaur P, Ferreira VF, Garcia CR et al. Addition of thiols to o-quinone methide: new 2-hydroxy-3-phenylsulfanylmethyl[1,4]naphthoquinones and their activity against the human malaria parasite Plasmodium falciparum (3D7). Eur J Med Chem 2013; 59:48–53 [View Article][PubMed]
     [Google Scholar]
  13. Nasiri HR, Madej MG, Panisch R, Lafontaine M, Bats JW et al. Design, synthesis, and biological testing of novel naphthoquinones as substrate-based inhibitors of the quinol/fumarate reductase from Wolinella succinogenes. J Med Chem 2013; 56:9530–9541 [View Article][PubMed]
     [Google Scholar]
  14. Sritrairat N, Nukul N, Inthasame P, Sansuk A, Prasirt J et al. Antifungal activity of lawsone methyl ether in comparison with chlorhexidine. J Oral Pathol Med 2011; 40:90–96 [View Article][PubMed]
     [Google Scholar]
  15. Nittayananta W, Pangsomboon K, Panichayupakaranant P, Chanowanna N, Chelae S et al. Effects of lawsone methyl ether mouthwash on oral Candida in HIV-infected subjects and subjects with denture stomatitis. J Oral Pathol Med 2013; 42:698–704 [View Article][PubMed]
     [Google Scholar]
  16. Ibis C, Tuyun AF, Bahar H, Ayla SS, Stasevych MV et al. Nucleophilic substitution reactions of 1,4-naphthoquinone and biologic properties of novel S-, S,S-, N-, and N,S-substituted 1,4-naphthoquinone derivatives. Medicinal Chemistry Research 2014; 23:2140–2149 [View Article]
     [Google Scholar]
  17. Mahapatra A, Tshikalange TE, Meyer JJM, Lall N. Synthesis and HIV-1 reverse transcriptase inhibition activity of 1,4-naphthoquinone derivatives. Chem Nat Compd 2012; 47:883–887 [View Article]
     [Google Scholar]
  18. Kapadia GJ, Rao GS, Sridhar R, Ichiishi E, Takasaki M et al. Chemoprevention of skin cancer: effect of Lawsonia inermis L. (Henna) leaf powder and its pigment artifact, lawsone in the Epstein- Barr virus early antigen activation assay and in two-stage mouse skin carcinogenesis models. Anticancer Agents Med Chem 2013; 13:1500–1507 [View Article][PubMed]
     [Google Scholar]
  19. Pérez-Sacau E, Díaz-Peñate RG, Estévez-Braun A, Ravelo AG, García-Castellano JM et al. Synthesis and pharmacophore modeling of naphthoquinone derivatives with cytotoxic activity in human promyelocytic leukemia HL-60 cell line. J Med Chem 2007; 50:696–706 [View Article][PubMed]
     [Google Scholar]
  20. Jiménez-Alonso S, Orellana HC, Estévez-Braun A, Ravelo AG, Pérez-Sacau E et al. Design and synthesis of a novel series of pyranonaphthoquinones as topoisomerase II catalytic inhibitors. J Med Chem 2008; 51:6761–6772 [View Article][PubMed]
     [Google Scholar]
  21. Klaus V, Hartmann T, Gambini J, Graf P, Stahl W et al. 1,4-Naphthoquinones as inducers of oxidative damage and stress signaling in HaCaT human keratinocytes. Arch Biochem Biophys 2010; 496:93–100 [View Article][PubMed]
     [Google Scholar]
  22. Bhasin D, Chettiar SN, Etter JP, Mok M, Li PK. Anticancer activity and SAR studies of substituted 1,4-naphthoquinones. Bioorg Med Chem 2013; 21:4662–4669 [View Article][PubMed]
     [Google Scholar]
  23. Oramas-Royo S, Torrejón C, Cuadrado I, Hernández-Molina R, Hortelano S et al. Synthesis and cytotoxic activity of metallic complexes of lawsone. Bioorg Med Chem 2013; 21:2471–2477 [View Article][PubMed]
     [Google Scholar]
  24. Schuck DC, Ferreira SB, Cruz LN, da Rocha DR, Moraes MS et al. Biological evaluation of hydroxynaphthoquinones as anti-malarials. Malar J 2013; 12:234 [View Article][PubMed]
     [Google Scholar]
  25. García-Barrantes PM, Lamoureux GV, Pérez AL, García-Sánchez RN, Martínez AR et al. Synthesis and biological evaluation of novel ferrocene-naphthoquinones as antiplasmodial agents. Eur J Med Chem 2013; 70:548–557 [View Article][PubMed]
     [Google Scholar]
  26. Janeczko M, Demchuk OM, Strzelecka D, Kubiński K, Masłyk M. New family of antimicrobial agents derived from 1,4-naphthoquinone. Eur J Med Chem 2016; 124:1019–1025 [View Article][PubMed]
     [Google Scholar]
  27. Myszka H, Sokołowska P, Cieślińska A, Nowacki A, Jaśkiewicz M et al. Diosgenyl 2-amino-2-deoxy-β-D-galactopyranoside: synthesis, derivatives and antimicrobial activity. Beilstein J Org Chem 2017; 13:2310–2315 [View Article][PubMed]
     [Google Scholar]
  28. Walczewska A, Grzywacz D, Bednarczyk D, Dawgul M, Nowacki A et al. N-Alkyl derivatives of diosgenyl 2-amino-2-deoxy-β-D-glucopyranoside; synthesis and antimicrobial activity. Beilstein J Org Chem 2015; 11:869–874 [View Article][PubMed]
     [Google Scholar]
  29. Masłyk M, Janeczko M, Martyna A, Kubiński K. CX-4945: the protein kinase CK2 inhibitor and anti-cancer drug shows anti-fungal activity. Mol Cell Biochem 2017; 435: [View Article][PubMed]
     [Google Scholar]
  30. Moreira CS, Silva AC, Novais JS, Sá Figueiredo AM, Ferreira VF et al. Searching for a potential antibacterial lead structure against bacterial biofilms among new naphthoquinone compounds. J Appl Microbiol 2017; 122:651–662 [View Article][PubMed]
     [Google Scholar]
  31. Ramage G, Saville SP, Wickes BL, López-Ribot JL. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 2002; 68:5459–5463 [View Article][PubMed]
     [Google Scholar]
  32. Lee HS, Kim Y. Antifungal Activity of Salvia miltiorrhiza Against Candida albicans Is Associated with the Alteration of Membrane Permeability and (1,3)-β-D-Glucan Synthase Activity. J Microbiol Biotechnol 2016; 26:610–617 [View Article][PubMed]
     [Google Scholar]
  33. Khan MS, Ahmad I, Cameotra SS. Phenyl aldehyde and propanoids exert multiple sites of action towards cell membrane and cell wall targeting ergosterol in Candida albicans. AMB Express 2013; 3:54 [View Article][PubMed]
     [Google Scholar]
  34. Yang X, Summerhurst DK, Koval SF, Ficker C, Smith ML et al. Isolation of an antimicrobial compound from Impatiens balsamina L. using bioassay-guided fractionation. Phytother Res 2001; 15:676–680 [View Article][PubMed]
     [Google Scholar]
  35. Sasaki K, Abe H, Yoshizaki F. In vitro antifungal activity of naphthoquinone derivatives. Biol Pharm Bull 2002; 25:669–670 [View Article][PubMed]
     [Google Scholar]
  36. de Paiva SR, Figueiredo MR, Aragão TV, Kaplan MA. Antimicrobial activity in vitro of plumbagin isolated from Plumbago species. Mem Inst Oswaldo Cruz 2003; 98:959–961 [View Article][PubMed]
     [Google Scholar]
  37. Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol 2013; 62:10–24 [View Article][PubMed]
     [Google Scholar]
  38. Abd E-BRM, El Ela D, Gfm G. N-acetylcysteine Inhibits and Eradicates Candida albicans Biofilms. Am J Infect Dis Microbiol 2014; 2:122–130
     [Google Scholar]
  39. Wang S, Beechem JM, Gratton E, Glaser M. Orientational distribution of 1,6-diphenyl-1,3,5-hexatriene in phospholipid vesicles as determined by global analysis of frequency domain fluorimetry data. Biochemistry 1991; 30:5565–5572 [View Article][PubMed]
     [Google Scholar]
  40. Halder S, Yadav KK, Sarkar R, Mukherjee S, Saha P et al. Alteration of Zeta potential and membrane permeability in bacteria: a study with cationic agents. Springerplus 2015; 4:672 [View Article][PubMed]
     [Google Scholar]
  41. Prasad R, Shah AH, Rawal MK. Antifungals: Mechanism of Action and Drug Resistance. Adv Exp Med Biol 2016; 892:327–349 [View Article][PubMed]
     [Google Scholar]
  42. Mu X, Chai T, Wang K, Zhu L, Huang Y et al. The developmental effect of difenoconazole on zebrafish embryos: A mechanism research. Environ Pollut 2016; 212:18–26 [View Article][PubMed]
     [Google Scholar]
  43. Mu X, Pang S, Sun X, Gao J, Chen J et al. Evaluation of acute and developmental effects of difenoconazole via multiple stage zebrafish assays. Environ Pollut 2013; 175:147–157 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000700
Loading
1,4-Naphthoquinone derivatives potently suppress Candida albicans growth, inhibit formation of hyphae and show no toxicity toward zebrafish embryos
J. Med. Microbiol. 67, 598 (2018); https://doi.org/10.1099/jmm.0.000700
/content/journal/jmm/10.1099/jmm.0.000700
/content/journal/jmm/10.1099/jmm.0.000700
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error