In vitro synergism between berberine and miconazole against planktonic and biofilm Candida cultures

Archives of Oral Biology

Volumn 56, Issue 6, 2011, Pages 565-572

  Wei, Guo Xian ^a   Xu, Xin ^a   Wu, Christine D ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Antimycotics; Candida biofilm; Combination therapy; Hydrastis canadensis; Natural oral antifungal

Indexed keywords

ANTIFUNGAL AGENT; BERBERINE; MICONAZOLE;

ARTICLE; BIOFILM; CANDIDA; CANDIDIASIS; DRUG EFFECT; DRUG POTENTIATION; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY;

ANTIFUNGAL AGENTS; BERBERINE; BIOFILMS; CANDIDA; CANDIDIASIS; DRUG SYNERGISM; MICONAZOLE; MICROBIAL SENSITIVITY TESTS;

CANDIDA; CANDIDA ALBICANS; CANDIDA GLABRATA; CANDIDA PARAPSILOSIS; CANDIDA TROPICALIS; HYDRASTIS; HYDRASTIS CANADENSIS; ISSATCHENKIA ORIENTALIS; KLUYVEROMYCES MARXIANUS;

EID: 79956196073     PISSN: 00039969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.archoralbio.2010.11.021     Document Type: Article

References (56)

1. M.A. Pfaller, and D.J. Diekema Epidemiology of invasive candidiasis: a persistent public health problem Clin Microbiol Rev 20 2007 133 163 (Pubitemid 46167771)
2. L.P. Samaranayake, W. Keung Leung, and L. Jin Oral mucosal fungal infections Periodontology 2000 49 2009 39 59
3. A.N. Ellepola, and L.P. Samaranayake Oral candidal infections and antimycotics Crit Rev Oral Biol Med 11 2000 172 198 (Pubitemid 30481379)
4. M.M. Coogan, P.L. Fidel Jr., M.C. Komesu, N. Maeda, and L.P. Samaranayake (B1) Candida and mycotic infections Adv Dent Res 19 2006 130 138
5. A.G. Luque, M.S. Biasoli, M.E. Tosello, A. Binolfi, S. Lupo, and H.M. Magaro Oral yeast carriage in HIV-infected and non-infected populations in Rosario, Argentina Mycoses 52 2009 53 59
6. J.J. Weems Jr. Candida parapsilosis: epidemiology, pathogenicity, clinical manifestations, and antimicrobial susceptibility Clin Infect Dis 14 1992 756 766
7. C.A. Kumamoto, and M.D. Vinces Alternative Candida albicans lifestyles: growth on surfaces Annu Rev Microbiol 59 2005 113 133 (Pubitemid 41507426)
8. A.L. Mavor, S. Thewes, and B. Hube Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes Curr Drug Targets 6 2005 863 874 (Pubitemid 41672448)
9. P.K. Mukherjee, G. Zhou, R. Munyon, and M.A. Ghannoum Candida biofilm: a well-designed protected environment Med Mycol 43 2005 191 208 (Pubitemid 40867493)
10. L.J. Douglas Candida biofilms and their role in infection Trends Microbiol 11 2003 30 36 (Pubitemid 36084353)
11. E.M. Kojic, and R.O. Darouiche Candida infections of medical devices Clin Microbiol Rev 17 2004 255 267 (Pubitemid 38534029)
12. A.Y. Zhang, W.L. Camp, and B.E. Elewski Advances in topical and systemic antifungals Dermatol Clin 25 2007 165 183 (Pubitemid 46550722)
13. V. Joly, J. Bolard, and P. Yeni In vitro models for studying toxicity of antifungal agents Antimicrob Agents Chemother 36 1992 1799 1804
14. B.D. Alexander, and J.R. Perfect Antifungal resistance trends towards the year 2000. Implications for therapy and new approaches Drugs 54 1997 657 678 (Pubitemid 27480239)
15. L. Angiolella, A.R. Stringaro, F. De Bernardis, B. Posteraro, M. Bonito, and L. Toccacieli Increase of virulence and its phenotypic traits in drug-resistant strains of Candida albicans Antimicrob Agents Chemother 52 2008 927 936 (Pubitemid 351358372)
16. T.C. Birdsall, and G.S. Kelly Berberine: therapeutic potential of an alkaloid found in several medicinal plants Alternative Med Rev 2 1997 94 103 (Pubitemid 127735667)
17. A.R. Ball, G. Casadei, S. Samosorn, J.B. Bremner, F.M. Ausubel, and T.I. Moy Conjugating berberine to a multidrug efflux pump inhibitor creates an effective antimicrobial ACS Chem Biol 1 2006 594 600
18. J. Coulburn, Y.-W. Chin, H. Parekh, S. Yildiz, R. Beavers, and A.D. Kinghorn Oral Antimicrobial Compounds from Hydrastis canadensis L. (Goldenseal) Leaves J Dent Res 86 Suppl. A 2007 2156
19. B.Y. Hwang, S.K. Roberts, L.R. Chadwick, C.D. Wu, and A.D. Kinghorn Antimicrobial constituents from goldenseal (the Rhizomes of Hydrastis canadensis) against selected oral pathogens Planta Med 69 2003 623 627 (Pubitemid 37041057)
20. H. Quan, Y.Y. Cao, Z. Xu, J.X. Zhao, P.H. Gao, and X.F. Qin Potent in vitro synergism of fluconazole and berberine chloride against clinical isolates of Candida albicans resistant to fluconazole Antimicrob Agents Chemother 50 2006 1096 1099 (Pubitemid 43327820)
21. K. Nakamoto, M. Tamamoto, and T. Hamada In vitro study on the effects of trial denture cleansers with berberine hydrochloride J Prosthet Dent 73 1995 530 533
22. J.P. Hu, N. Takahashi, and T. Yamada Coptidis rhizoma inhibits growth and proteases of oral bacteria Oral Dis 6 2000 297 302
23. L.R. Chadwick, C.D. Wu, and A.D. Kinghorn Isolation of alkaloids from goldenseal (Hydrastis canadensis rhizomes) using pH-zone refining countercurrent chromatography J Liquid Chromatogr Relat Technol 24 2001 2445 2453 (Pubitemid 32937348)
24. L. Iauk, R. Costanzo, F. Caccamo, A. Rapisarda, R. Musumeci, and I. Milazzo Activity of Berberis aetnensis root extracts on Candida strains Fitoterapia 78 2007 159 161 (Pubitemid 46188501)
25. K. Iwasa, M. Kamigauchi, M. Sugiura, and H. Nanba Antimicrobial activity of some 13-alkyl substituted protoberberinium salts Planta Med 63 1997 196 198 (Pubitemid 27287056)
26. R.S. Iwazaki, E.H. Endo, T. Ueda-Nakamura, C.V. Nakamura, L.B. Garcia, and B.P. Filho In vitro antifungal activity of the berberine and its synergism with fluconazole Antonie Van Leeuwenhoek 97 2010 201 205
27. Y. Han, and J.H. Lee Berberine synergy with amphotericin B against disseminated candidiasis in mice Biol Pharm Bull 28 2005 541 544 (Pubitemid 40879986)
28. National Committee for Clinical Laboratory Standards Reference method for broth dilution antifungal susceptibility testing of yeast: approved standard. NCCLS document M27-A 1997 National Committee for Clinical Laboratory Standards Wayne, PA
29. G.X. Wei, and L.A. Bobek In vitro synergic antifungal effect of MUC7 12-mer with histatin-5 12-mer or miconazole J Antimicrob Chemother 53 2004 750 758 (Pubitemid 38660274)
30. K.P. Leung, T.D. Crowe, J.J. Abercrombie, C.M. Molina, C.J. Bradshaw, and C.L. Jensen Control of oral biofilm formation by an antimicrobial decapeptide J Dent Res 84 2005 1172 1177 (Pubitemid 43827787)
31. J. Pratten, A.W. Smith, and M. Wilson Response of single species biofilms and microcosm dental plaques to pulsing with chlorhexidine J Antimicrob Chemother 42 1998 453 459 (Pubitemid 28473004)
32. C. Dawes Salivary flow patterns and the health of hard and soft oral tissues J Am Dent Assoc 139 Suppl. 2008 18S 24S
33. D.P. Bakker, A. van der Plaats, G.J. Verkerke, H.J. Busscher, and H.C. van der Mei Comparison of velocity profiles for different flow chamber designs used in studies of microbial adhesion to surfaces Appl Environ Microbiol 69 2003 6280 6287 (Pubitemid 37280356)
34. C.G. Pierce, P. Uppuluri, A.R. Tristan, F.L. Wormley Jr., E. Mowat, and G. Ramage A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing Nat Protoc 3 2008 1494 1500
35. J.W. Costerton, P.S. Stewart, and E.P. Greenberg Bacterial biofilms: a common cause of persistent infections Science 284 1999 1318 1322 (Pubitemid 29289651)
36. R.M. Donlan, and J.W. Costerton Biofilms: survival mechanisms of clinically relevant microorganisms Clin Microbiol Rev 15 2002 167 193 (Pubitemid 34303762)
37. D.P. Kontoyiannis, and R.E. Lewis Antifungal drug resistance of pathogenic fungi Lancet 359 2002 1135 1144 (Pubitemid 34270742)
38. M.R. Capoor, D. Nair, M. Deb, P.K. Verma, L. Srivastava, and P. Aggarwal Emergence of non-albicans Candida species and antifungal resistance in a tertiary care hospital Jpn J Infect Dis 58 2005 344 348 (Pubitemid 43078730)
39. B. Collin, C.J. Clancy, and M.H. Nguyen Antifungal resistance in non-albicans Candida species Drug Resist Updat 2 1999 9 14 (Pubitemid 29217089)
40. P. Stoodley, K. Sauer, D.G. Davies, and J.W. Costerton Biofilms as complex differentiated communities Annu Rev Microbiol 56 2002 187 209 (Pubitemid 35217453)
41. G. Ramage, S.P. Saville, D.P. Thomas, and J.L. Lopez-Ribot Candida biofilms: an update Eukaryot Cell 4 2005 633 638 (Pubitemid 40600417)
42. P. Stoodley, Z. Lewandowski, J.D. Boyle, and H.M. Lappin-Scott Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology Biotechnol Bioeng 65 1999 83 92 (Pubitemid 29406774)
43. B. Purevdorj-Gage, M.E. Orr, P. Stoodley, K.B. Sheehan, and L.E. Hyman The role of FLO11 in Saccharomyces cerevisiae biofilm development in a laboratory based flow-cell system FEMS Yeast Res 7 2007 372 379 (Pubitemid 46555510)
44. G. Ramage, B.L. Wickes, and J.L. Lopez-Ribot A seed and feed model for the formation of Candida albicans biofilms under flow conditions using an improved modified Robbins device Rev Iberoam Micol 25 2008 37 40 (Pubitemid 351518327)
45. J. Chandra, D.M. Kuhn, P.K. Mukherjee, L.L. Hoyer, T. McCormick, and M.A. Ghannoum Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance J Bacteriol 183 2001 5385 5394 (Pubitemid 32802612)
46. L.A. Murillo, G. Newport, C.Y. Lan, S. Habelitz, J. Dungan, and N.M. Agabian Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans Eukaryot Cell 4 2005 1562 1573 (Pubitemid 41339111)
47. M.W. Davidson, I. Lopp, S. Alexander, and W.D. Wilson The interaction of plant alkaloids with DNA. II. Berberinium chloride Nucleic Acids Res 4 1977 2697 2712 (Pubitemid 8158857)
48. K.Y. Kim, Y.K. Shin, J.C. Park, J.H. Kim, H. Yang, and D.M. Han Molecular cloning and biochemical characterization of Candida albicans acyl-CoA:sterol acyltransferase, a potential target of antifungal agents Biochem Biophys Res Commun 319 2004 911 919 (Pubitemid 38739407)
49. K.S. Park, K.C. Kang, J.H. Kim, D.J. Adams, T.N. Johng, and Y.K. Paik Differential inhibitory effects of protoberberines on sterol and chitin biosyntheses in Candida albicans J Antimicrob Chemother 43 1999 667 674 (Pubitemid 29231692)
50. K.S. Park, K.C. Kang, K.Y. Kim, P.Y. Jeong, J.H. Kim, and D.J. Adams HWY-289, a novel semi-synthetic protoberberine derivative with multiple target sites in Candida albicans J Antimicrob Chemother 47 2001 513 519 (Pubitemid 32447636)
51. Y. Xu, Y. Wang, L. Yan, R.M. Liang, B.D. Dai, and R.J. Tang Proteomic analysis reveals a synergistic mechanism of fluconazole and berberine against fluconazole-resistant Candida albicans: endogenous ROS augmentation J Proteome Res 8 2009 5296 5304
52. S. De Nollin, and M. Borgers Scanning electron microscopy of Candida albicans after in vitro treatment with miconazole Antimicrob Agents Chemother 7 1975 704 711
53. E.M. Bailey, D.J. Krakovsky, and M.J. Rybak The triazole antifungal agents: a review of itraconazole and fluconazole Pharmacotherapy 10 1990 146 153 (Pubitemid 20149608)
54. C.A. Lyman, and T.J. Walsh Systemically administered antifungal agents. A review of their clinical pharmacology and therapeutic applications Drugs 44 1992 9 35
55. K. Thevissen, K.R. Ayscough, A.M. Aerts, W. Du, K. De Brucker, and E.M. Meert Miconazole induces changes in actin cytoskeleton prior to reactive oxygen species induction in yeast J Biol Chem 282 2007 21592 21597 (Pubitemid 47195737)
56. D. Kobayashi, K. Kondo, N. Uehara, S. Otokozawa, N. Tsuji, and A. Yagihashi Endogenous reactive oxygen species is an important mediator of miconazole antifungal effect Antimicrob Agents Chemother 46 2002 3113 3117