DOI QR코드

DOI QR Code

Synergistic Antifungal Activity of Phellodendri Cortex and Magnoliae Cortex against Candida albicans

  • NA, Hyunjeong (Department of Forest Products and Biotechnology, College of Science and Technology, Kookmin University) ;
  • KIM, Tae-Jong (Department of Forest Products and Biotechnology, College of Science and Technology, Kookmin University)
  • 투고 : 2021.11.19
  • 심사 : 2021.12.28
  • 발행 : 2022.01.25

초록

Many studies on plant extracts have been reported for the treatment of candidiasis caused by Candida albicans, a representative fungal infection. This study demonstrates the synergistic antifungal activity of the combination of Phellodendri Cortex and Magnoliae Cortex, previously reported to have antifungal efficacy. Considering the antifungal efficacy and the separation of the active constituents, berberine and magnolol, hot water extraction and carbon dioxide supercritical extraction were selected for Phellodendri Cortex and Magnoliae Cortex, respectively. A combination of 0.55 g/L hot water extract of Phellodendri Cortex and 0.59 g/L carbon dioxide supercritical extract of Magnoliae Cortex showed synergistic antifungal activity. The synergistic antifungal activity of 160 μM berberine and 100 μM magnolol, which are representative antifungal compounds of Phellodendri Cortex and Magnoliae Cortex, respectively, contributes to the synergistic antifungal effect of their extracts. The additive decrease in cellular ergosterol level and the increased antifungal efficacy by extracellular ergosterol suggest that disruption of the biological function of ergosterol in the cell membrane is not responsible for the synergistic antifungal activity of berberine and magnolol. Synergistic cellular release of chromosomal DNA upon mixing berberine and magnolol indicates that disruption of the cellular structure is responsible for the synergistic antifungal effect of berberine and magnolol.

키워드

과제정보

This study was carried out with the support of "R&D Program for Forest Science Technology" (Project No. 2019150B10-2123-0301) provided by Korea Forest Service (Korea Forestry Promotion Institute).

참고문헌

  1. Adfa, M., Romayasa, A., Kusnanda, A.J., Avidlyandi, A., Yudha, S.S., Banon, C., Gustian, I. 2020. Chemical components, antitermite and antifungal activities of Cinnamomum parthenoxylon wood vinegar. Journal of the Korean Wood Science and Technology 48(1): 107-116. https://doi.org/10.5658/WOOD.2020.48.1.107
  2. Akroum, S. 2017. Antifungal activity of acetone extracts from Punica granatum L., Quercus suber L. and Vicia faba L. Journal de Mycologie Medicale 27(1): 83-89. https://doi.org/10.1016/j.mycmed.2016.10.004
  3. Arthington-Skaggs, B.A., Jradi, H., Desai, T., Morrison, C.J. 1999. Quantitation of ergosterol content: Novel method for determination of fluconazole susceptibility of Candida albicans. Journal of Clinical Microbiology 37(10): 3332-3337. https://doi.org/10.1128/JCM.37.10.3332-3337.1999
  4. Baddley, J.W., Poppas, P.G. 2005. Antifungal combination therapy: Clinical potential. Drugs 65(11): 1461-1480. https://doi.org/10.2165/00003495-200565110-00002
  5. Behbehani, J., Shreaz, S., Irshad, M., Karched, M. 2017. The natural compound magnolol affects growth, biofilm formation, and ultrastructure of oral Candida isolates. Microbial Pathogenesis 113: 209-217. https://doi.org/10.1016/j.micpath.2017.10.040
  6. Bennis, S., Chami, F., Chami, N., Bouchikhi, T., Remmal, A. 2004. Surface alteration of Saccharomyces cerevisiae induced by thymol and eugenol. Letters in Applied Microbiology 38(6): 454-458. https://doi.org/10.1111/j.1472-765X.2004.01511.x
  7. Bernardes, I., Felipe Rodrigues, M.P., Bacelli, G.K., Munin, E., Alves, L.P., Costa, M.S. 2012. Aloe vera extract reduces both growth and germ tube formation by Candida albicans. Mycoses 55(3): 257-261. https://doi.org/10.1111/j.1439-0507.2011.02079.x
  8. Bona, E., Cantamessa, S., Pavan, M., Novello, G., Massa, N., Rocchetti, A., Berta, G., Gamalero, E. 2016. Sensitivity of Candida albicans to essential oils: Are they an alternative to antifungal agents? Journal of Applied Microbiology 121(6): 1530-1545. https://doi.org/10.1111/jam.13282
  9. Brown, G.D., Denning, D.W., Gow, N.A.R., Levitz, S.M., Netea, M.G., White, T.C. 2012. Hidden killers: Human fungal infections. Science Translational Medicine 4(165): 165rv13. https://doi.org/10.1126/scitranslmed.3004404
  10. Campos, R.S., Silva, C.R., Neto, J.B.A., Sampaio, L.S., Nascimento, F.B.S.A., Moraes, M.O., Cavalcanti, B.C., Magalhaes, H.F., Gomes, A.O.C.V., Lobo, M.D.P., Junior, H.V.N. 2018. Antifungal activity of palmatine against strains of Candida spp. resistant to azoles in planktonic cells and biofilm. International Journal of Current Microbiology and Applied Sciences 7(2): 3657-3669.
  11. Cernakova, M., Kos?alova, D. 2002. Antimicrobial activity of berberine: A constituent of Mahonia aquifolium. Folia Microbiologica 47(4): 375-378. https://doi.org/10.1007/BF02818693
  12. Chan, C.O., Chu, C.C., Mok, D.K.W., Chau, F.T. 2007. Analysis of berberine and total alkaloid content in cortex phellodendri by near infrared spectroscopy (NIRS) compared with high-performance liquid chromatography coupled with ultra-visible spectrometric detection. Analytica Chimica Acta 592(2): 121-131. https://doi.org/10.1016/j.aca.2007.04.016
  13. Chan, L.W., Cheah, E.L.C., Saw, C.L.L., Weng, W., Heng, P.W.S. 2008. Antimicrobial and antioxidant activities of Cortex Magnoliae Officinalis and some other medicinal plants commonly used in South-East Asia. Chinese Medicine 3(1): 15. https://doi.org/10.1186/1749-8546-3-15
  14. Chen, G., Xu, X., Zhu, Y., Zhang, L., Yang, P. 2006. Determination of honokiol and magnolol in Cortex Magnoliae Officinalis by capillary electrophoresis with electrochemical detection. Journal of Pharmaceutical and Biomedical Analysis 41(4): 1479-1484. https://doi.org/10.1016/j.jpba.2006.04.001
  15. Chen, Y., Zeng, H., Tian, J., Ban, X., Ma, B., Wang, Y. 2013. Antifungal mechanism of essential oil from Anethum graveolens seeds against Candida albicans. Journal of Medical Microbiology 62(8): 1175-1183. https://doi.org/10.1099/jmm.0.055467-0
  16. Chen, Y.H., Lu, M.H., Guo, D.S., Zhai, Y.Y., Miao, D., Yue, J.Y., Yuan, C.H., Zhao, M.M., An, D.R. 2019. Antifungal effect of magnolol and honokiol from Magnolia officinalis on Alternaria alternata causing tobacco brown spot. Molecules 24(11): 2140. https://doi.org/10.3390/molecules24112140
  17. Cheng, Y.C., Hueng, D.Y., Huang, H.Y., Chen, J.Y., Chen, Y. 2016. Magnolol and honokiol exert a synergistic anti-tumor effect through autophagy and apoptosis in human glioblastomas. Oncotarget 7(20): 29116-29130. https://doi.org/10.18632/oncotarget.8674
  18. Cuenca-Estrella, M., Gomez-Lopez, A., Mellado, E., Garcia-Effron, G., Rodriguez-Tudela, J.L. 2004. In vitro activities of ravuconazole and four other antifungal agents against fluconazole-resistant or-susceptible clinical yeast isolates. Antimicrobial Agents and Chemotherapy 48(8): 3107-3111. https://doi.org/10.1128/AAC.48.8.3107-3111.2004
  19. D'Auria, F.D., Tecca, M., Strippoli, V., Salvatore, G., Battinelli, L., Mazzanti, G. 2005. Antifungal activity of Lavandula angustifolia essential oil against Candida albicans yeast and mycelial form. Medical Mycology 43(5): 391-396. https://doi.org/10.1080/13693780400004810
  20. Dartevelle, P., Ehlinger, C., Zaet, A., Boehler, C., Rabineau, M., Westermann, B., Strub, J.M., Cianferani, S., Haikel, Y., Metz-Boutigue, M.H., Marban, C. 2018. D-Cateslytin: A new antifungal agent for the treatment of oral Candida albicans associated infections. Scientific Reports 8(1): 9235. https://doi.org/10.1038/s41598-018-27417-x
  21. de Oliveira Santos, G.C., Vasconcelos, C.C., Lopes, A.J.O., de Sousa Cartagenes, M.S., Filho, A.K.D.B., do Nascimento, F.R.F., Ramos, R.M., Pires, E.R.R.B., de Andrade, M.S., Rocha, F.M.G., de Andrade Monteiro, C. 2018. Candida infections and therapeutic strategies: Mechanisms of action for traditional and alternative agents. Frontiers in Microbiology 9: 1351. https://doi.org/10.3389/fmicb.2018.01351
  22. do Nascimento Dias, J., de Souza Silva, C., de Araujo, A.R., Souza, J.M.T., de Holanda Veloso Junior, P.H., Cabral, W.F., da Gloria da Silva, M., Eaton, P., de Souza de Almeida Leite, J.R., Nicola, A.M., Albuquerque, P., Silva-Pereira, I. 2020. Mechanisms of action of antimicrobial peptides ToAP2 and NDBP-5.7 against Candida albicans planktonic and biofilm cells. Scientific Reports 10(1): 10327. https://doi.org/10.1038/s41598-020-67041-2
  23. Eksi, F., Gayyurhan, E.D., Balci, I. 2013. In vitro susceptibility of Candida species to four antifungal agents assessed by the reference broth microdilution method. The Scientific World Journal 2013: 236903. https://doi.org/10.1155/2013/236903
  24. Enoch, D.A., Ludlam, H.A., Brown, N.M. 2006. Invasive fungal infections: A review of epidemiology and management options. Journal of Medical Microbiology 55(7): 809-818. https://doi.org/10.1099/jmm.0.46548-0
  25. Escalante, A., Gattuso, M., Perez, P., Zacchino, S. 2008. Evidence for the mechanism of action of the antifungal phytolaccoside B isolated from Phytolacca tetramera Hauman. Journal of Natural Products 71(10): 1720-1725. https://doi.org/10.1021/np070660i
  26. Espinel-Ingroff, A., Pfaller, M.A., Bustamante, B., Canton, E., Fothergill, A., Fuller, J., Gonzalez, G.M., Lass-Florl, C., Lockhart, S.R., Martin-Mazuelos, E., Meis, J.F., Melhem, M.S.C., Ostrosky-Zeichner, L., Pelaez, T., Szeszs, M.W., St-Germain, G., Bonfietti, L.X., Guarro, J., Turnidge, J. 2014. Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole. Antimicrobial Agents and Chemotherapy 58(4): 2006-2012. https://doi.org/10.1128/AAC.02615-13
  27. Freile M.L., Giannini, F., Pucci, G., Sturniolo, A., Rodero, L., Pucci, O., Balzareti, V., Enriz, R.D. 2003. Antimicrobial activity of aqueous extracts and of berberine isolated from Berberis heterophylla. Fitoterapia 74(7-8): 702-705. https://doi.org/10.1016/S0367-326X(03)00156-4
  28. Fujii, A., Okuyama, T., Wakame, K., Okumura, T., Ikeya, Y., Nishizawa, M. 2017. Identification of anti-inflammatory constituents in Phellodendri Cortex and Coptidis Rhizoma by monitoring the suppression of nitric oxide production. Journal of Natural Medicines 71(4): 745-756. https://doi.org/10.1007/s11418-017-1107-4
  29. Goncalves, M.J., Piras, A., Porcedda, S., Marongiu, B., Falconieri, D., Cavaleiro, C., Rescigno, A., Rosa, A., Salgueiro, L. 2015. Antifungal activity of extracts from Cynomorium coccineum growing wild in Sardinia island (Italy). Natural Product Research 29(23): 2247-2250. https://doi.org/10.1080/14786419.2014.1000892
  30. Gonzalez, G.M., Robledo, E., Garza-Gonzalez, E., Elizondo, M., Gonzalez, J.G. 2009. Efficacy of albaconazole against Candida albicans in a vaginitis model. Antimicrobial Agents and Chemotherapy 53(10): 4540-4541. https://doi.org/10.1128/AAC.00565-09
  31. Ham, Y., An, J.E., Lee, S.M., Chung, S.H., Kim, S.H., Park, M.J. 2021. Isolation and identification of fungi associated with decay of Quercus mongolica. Journal of the Korean Wood Science and Technology 49(3): 234-253. https://doi.org/10.5658/WOOD.2021.49.3.234
  32. Hammer, K.A., Carson, C.F., Riley, T.V. 2004. Antifungal effects of Melaleuca alternifolia (tea tree) oil and its components on Candida albicans, Candida glabrata and Saccharomyces cerevisiae. Journal of Antimicrobial Chemotherapy 53(6): 1081-1085. https://doi.org/10.1093/jac/dkh243
  33. Hassan, H.A., Genaidy, M.M., Kamel, M.S., Abdelwahab, S.F. 2020. Synergistic antifungal activity of mixtures of clove, cumin and caraway essential oils and their major active components. Journal of Herbal Medicine 24: 100399. https://doi.org/10.1016/j.hermed.2020.100399
  34. Hidayat, A., Turjaman, M., Faulina, S.A., Ridwan, F., Najmulah, A.A., Irawadi, T.T., Iswanto, A.H. 2019. Antioxidant and antifungal activity of endophytic fungi associated with agarwood trees. Journal of the Korean Wood Science and Technology 47(4): 459-471. https://doi.org/10.5658/WOOD.2019.47.4.459
  35. Irfan, M., Alam, S., Manzoor, N., Abid, M. 2017. Effect of quinoline based 1,2,3-triazole and its structural analogues on growth and virulence attributes of Candida albicans. PLOS ONE 12(4): e0175710. https://doi.org/10.1371/journal.pone.0175710
  36. Jiang, Y., Vaysse, J., Gilard, V., Balayssac, S., Dejean, S., Malet-Martino, M., David, B., Fiorini, C., Barbin, Y. 2012. Quality assessment of commercial Magnoliae Officinalis Cortex by 1H-NMR-based metabolomics and HPLC methods. Phytochemical Analysis 23(4): 387-395. https://doi.org/10.1002/pca.1369
  37. Jung, H.C. 2019. Enhancement of laccase production from wood-rotting fungus by co-culture with Trichoderma longibrachiatum. Journal of the Korean Wood Science and Technology 47(2): 210-220. https://doi.org/10.5658/WOOD.2019.47.2.210
  38. Khan, M.S.A., Ahmad, I., Cameotra, S.S. 2013. Phenyl aldehyde and propanoids exert multiple sites of action towards cell membrane and cell wall targeting ergosterol in Candida albicans. AMB Express 3(1): 54. https://doi.org/10.1186/2191-0855-3-54
  39. Kim, J., Bao, T.H.Q., Shin, Y.K., Kim, K.Y. 2018. Antifungal activity of magnoflorine against Candida strains. World Journal of Microbiology and Biotechnology 34(11): 167. https://doi.org/10.1007/s11274-018-2549-x
  40. Kim, J.H., Weeratunga, P., Kim, M.S., Nikapitiya, C., Lee, B.H., Uddin, M.B., Kim, T.H., Yoon, J.E., Park, C., Ma, J.Y., Kim, H., Lee, J.S. 2016. Inhibitory effects of an aqueous extract from Cortex Phellodendri on the growth and replication of broad-spectrum of viruses in vitro and in vivo. BMC Complementary and Alternative Medicine 16(1): 265. https://doi.org/10.1186/s12906-016-1206-x
  41. Kim, K.S., Kim, H.C. 2004. Analytical method for the determination of standard compounds in oriental medicine materials listed in the Korean Pharmacopoeia (KPVIII). The Korean Society of Crop Science 49(spc1): 117-145.
  42. Kumar, A., Ekavali, Chopra, K., Mukherjee, M., Pottabathini, R., Dhull, D.K. 2015. Current knowledge and pharmacological profile of berberine: An update. European Journal of Pharmacology 761: 288-297. https://doi.org/10.1016/j.ejphar.2015.05.068
  43. Kuo, C.L., Chi, C.W., Liu, T.Y. 2004. The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Letters 203(2): 127-137. https://doi.org/10.1016/j.canlet.2003.09.002
  44. Landers, D.V., Wiesenfeld, H.C., Heine, R.P., Krohn, M.A., Hillier, S.L. 2004. Predictive value of the clinical diagnosis of lower genital tract infection in women. American Journal of Obstetrics and Gynecology 190(4): 1004-1008. https://doi.org/10.1016/j.ajog.2004.02.015
  45. Lee, H.S., Kim, Y. 2016. Antifungal activity of Salvia miltiorrhiza against Candida albicans is associated with the alteration of membrane permeability and (1,3)-β-D-glucan synthase activity. Journal of Microbiology and Biotechnology 26(3): 610-617. https://doi.org/10.4014/jmb.1511.11009
  46. Lee, S.Y., Lee, D.S., Cho, S.M., Kim, J.C., Park, M.J., Choi, I.G. 2021. Antioxidant properties of 7 domestic essential oils and identification of physiologically active components of essential oils against Candida albicans. Journal of the Korean Wood Science and Technology 49(1): 23-43. https://doi.org/10.5658/WOOD.2021.49.1.23
  47. Leite, M.C.A., Bezerra, A.P.B., de Sousa, J.P., Guerra, F.Q.S., Lima, E.O. 2014a. Evaluation of antifungal activity and mechanism of action of citral against Candida albicans. Evidence-Based Complementary and Alternative Medicine 2014: 378280. https://doi.org/10.1155/2014/378280
  48. Leite, M.C.A., de Brito Bezerra, A.P., de Sousa, J.P., de Oliveira Lima, E. 2014b. Investigating the antifungal activity and mechanism(s) of geraniol against Candida albicans strains. Medical Mycology 53(3): 275-284. https://doi.org/10.1093/mmy/myu078
  49. Lemar, K.M., Passa, O., Aon, M.A., Cortassa, S., Muller, C.T., Plummer, S., O'Rourke, B., Lloyd, D. 2005. Allyl alcohol and garlic (Allium sativum) extract produce oxidative stress in Candida albicans. Microbiology 151(10): 3257-3265. https://doi.org/10.1099/mic.0.28095-0
  50. Li, Y., Jiao, P., Li, Y., Gong, Y., Chen, X., Sun, S. 2019. The synergistic antifungal effect and potential mechanism of D-penicillamine combined with fluconazole against Candida albicans. Frontiers in Microbiology 10: 2853. https://doi.org/10.3389/fmicb.2019.02853
  51. Lum, K.Y., Tay, S.T., Le, C.F., Lee, V.S., Sabri, N.H., Velayuthan, R.D., Hassan, H., Sekaran, S.D. 2015. Activity of novel synthetic peptides against Candida albicans. Scientific Reports 5(1): 9657. https://doi.org/10.1038/srep09657
  52. Luo, H., Wu, H., Yu, X., Zhang, X., Lu, Y., Fan, J., Tang, L., Wang, Z. 2019. A review of the phytochemistry and pharmacological activities of Magnoliae Officinalis Cortex. Journal of Ethnopharmacology 236: 412-442. https://doi.org/10.1016/j.jep.2019.02.041
  53. Masomi, F., Hassanshahian, M. 2016. Antimicrobial activity of five medicinal plants on Candida albicans. The Iranian Journal of Toxicology 10(6): 39-43.
  54. Min, B.S., Bang, K.H., Lee, J.S., Bae, G.H. 1996. Screening of the antifungal activity from natural products against Candida albicans and Penicillium avellaneum. Yakhak Hoeji 40(5): 582-590.
  55. Miron, D., Battisti, F., Silva, F.K., Lana, A.D., Pippi, B., Casanova, B., Gnoatto, S., Fuentefria, A., Mayorga, P., Schapoval, E.E.S. 2014. Antifungal activity and mechanism of action of monoterpenes against dermatophytes and yeasts. Revista Brasileira de Farmacognosia 24(6): 660-667. https://doi.org/10.1016/j.bjp.2014.10.014
  56. Ng, K.P., Kuan, C.S., Kaur, H., Na, S.L., Atiya, N., Velayuthan, R.D. 2015. Candida species epidemiology 2000-2013: A laboratory-based report. Tropical Medicine & International Health 20(11): 1447-1453. https://doi.org/10.1111/tmi.12577
  57. Ni, H., Cai, X., Qiu, X., Liu, L., Ma, X., Wan, L., Ye, H., Chen, L. 2020. Biphenyl-type neolignans from stem bark of Magnolia officinalis with potential anti-tumor activity. Fitoterapia 147: 104769. https://doi.org/10.1016/j.fitote.2020.104769
  58. Oufensou, S., Scherm, B., Pani, G., Balmas, V., Fabbri, D., Dettori, M.A., Carta, P., Malbran, I., Migheli, Q., Delogu, G. 2019. Honokiol, magnolol and its monoacetyl derivative show strong anti-fungal effect on Fusarium isolates of clinical relevance. PLOS ONE 14(9): e0221249. https://doi.org/10.1371/journal.pone.0221249
  59. Park, J., Lee, J., Jung, E., Park, Y., Kim, K., Park, B., Jung, K., Park, E., Kim, J., Park, D. 2004a. In vitro antibacterial and anti-inflammatory effects of honokiol and magnolol against Propionibacterium sp. European Journal of Pharmacology 496(1-3): 189-195. https://doi.org/10.1016/j.ejphar.2004.05.047
  60. Park, K.S., Kang, H.I., Lee, J.W., Paik, Y.K. 2004b. Anti-Candida activity of YH-1715R, a new triazole derivative. Journal of Microbiology and Biotechnology 14(4): 693-697.
  61. Park, K.S., Kang, K.C., Kim, J.H., Adams, D.J., Johng, T.N., Paik, Y.K. 1999. Differential inhibitory effects of protoberberines on sterol and chitin biosyntheses in Candida albicans. Journal of Antimicrobial Chemotherapy 43(5): 667-674. https://doi.org/10.1093/jac/43.5.667
  62. Parray, H.A., Lone, J., Park, J.P., Choi, J.W., Yun, J.W. 2018. Magnolol promotes thermogenesis and attenuates oxidative stress in 3T3-L1 adipocytes. Nutrition 50: 82-90. https://doi.org/10.1016/j.nut.2018.01.017
  63. Patel, M., Coogan, M.M. 2008. Antifungal activity of the plant Dodonaea viscosa var. angustifolia on Candida albicans from HIV-infected patients. Journal of Ethnopharmacology 118(1): 173-176. https://doi.org/10.1016/j.jep.2008.03.009
  64. Pfaller, M., Chaturvedi, V., Espinel-Ingroff, A., Ghannoum, M.A., Gosey, L.L., Odds, F.C. 2008a. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard-second edition. CLSI document M27-A2. The Clinical and Laboratory Standards Institute: Malvern, PA, USA.
  65. Pfaller, M.A., Diekema, D.J. 2007. Epidemiology of invasive candidiasis: A persistent public health problem. Clinical Microbiology Reviews 20(1): 133-163. https://doi.org/10.1128/CMR.00029-06
  66. Pfaller, M.A., Diekema, D.J., Ostrosky-Zeichner, L., Rex, J.H., Alexander, B.D., Andes, D., Brown, S.D., Chaturvedi, V., Ghannoum, M.A., Knapp, C.C., Sheehan, D.J., Walsh, T.J. 2008b. Correlation of MIC with outcome for Candida species tested against caspofungin, anidulafungin, and micafungin: Analysis and proposal for interpretive MIC breakpoints. Journal of Clinical Microbiology 46(8): 2620-2629. https://doi.org/10.1128/JCM.00566-08
  67. Pristov, K.E., Ghannoum, M.A. 2019. Resistance of Candida to azoles and echinocandins worldwide. Clinical Microbiology and Infection 25(7): 792-798. https://doi.org/10.1016/j.cmi.2019.03.028
  68. Rajkowska, K., Nowak, A., Kunicka-Styczynska, A., Siadura, A. 2016. Biological effects of various chemically characterized essential oils: Investigation of the mode of action against Candida albicans and HeLa cells. RSC Advances 6(99): 97199-97207. https://doi.org/10.1039/c6ra21108a
  69. Ramamourthy, G., Park, J., Seo, C., Vogel, H.J., Park, Y. 2020. Antifungal and antibiofilm activities and the mechanism of action of repeating lysine-tryptophan peptides against Candida albicans. Microorganisms 8(5): 758. https://doi.org/10.3390/microorganisms8050758
  70. Rex, J.H., Rinaldi, M.G., Pfaller, M.A. 1995. Resistance of Candida species to fluconazole. Antimicrobial Agents and Chemotherapy 39(1): 1-8. https://doi.org/10.1128/AAC.39.1.1
  71. Richter, S.S., Galask, R.P., Messer, S.A., Hollis, R.J., Diekema, D.J., Pfaller, M.A. 2005. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. Journal of Clinical Microbiology 43(5): 2155-2162. https://doi.org/10.1128/JCM.43.5.2155-2162.2005
  72. Ryuk, J.A., Zheng, M.S., Lee, M.Y., Seo, C.S., Li, Y., Lee, S.H., Moon, D.C., Lee, H.W., Lee, J.H., Park, J.Y., Son, J.K., Ko, B.S. 2012. Discrimination of Phellodendron amurense and P. chinense based on DNA analysis and the simultaneous analysis of alkaloids. Archives of Pharmacal Research 35(6): 1045-1054. https://doi.org/10.1007/s12272-012-0612-y
  73. Saag, M.S., Dismukes, W.E. 1988. Azole antifungal agents: Emphasis on new triazoles. Antimicrobial Agents and Chemotherapy 32(1): 1-8. https://doi.org/10.1128/AAC.32.1.1
  74. Saito, J., Fukushima, H., Nagase, H. 2009. Anti-clastogenic effect of magnolol-containing Hange-koboku-to, Dai-joki-to, Goshaku-san, and Magnoliae Cortex on benzo(a)pyrene-induced clastogenicity in mice. Biological and Pharmaceutical Bulletin 32(7): 1209-1214. https://doi.org/10.1248/bpb.32.1209
  75. Sandven, P. 2000. Epidemiology of candidemia. Revista Iberoamericana de Micologia 17(3): 73-81.
  76. Sanglard, D., Coste, A.T. 2016. Activity of isavuconazole and other azoles against Candida clinical isolates and yeast model systems with known azole resistance mechanisms. Antimicrobial Agents and Chemotherapy 60(1): 229-238. https://doi.org/10.1128/AAC.02157-15
  77. Serra, E., Hidalgo-Bastida, L.A., Verran, J., Williams, D., Malic, S. 2018. Antifungal activity of commercial essential oils and biocides against Candida albicans. Pathogens 7(1): 15. https://doi.org/10.3390/pathogens7010015
  78. Shai, L.J., McGaw, L.J., Masoko, P., Eloff, J.N. 2008. Antifungal and antibacterial activity of seven traditionally used South African plant species active against Candida albicans. South African Journal of Botany 74(4): 677-684. https://doi.org/10.1016/j.sajb.2008.04.003
  79. Sharon, V., Fazel, N. 2010. Oral candidiasis and angular cheilitis. Dermatologic Therapy 23(3): 230-242. https://doi.org/10.1111/j.1529-8019.2010.01320.x
  80. Shen, P., Zhang, Z., He, Y., Gu, C., Zhu, K., Li, S., Li, Y., Lu, X., Liu, J., Zhang, N., Cao, Y. 2018. Magnolol treatment attenuates dextran sulphate sodium-induced murine experimental colitis by regulating inflammation and mucosal damage. Life Sciences 196: 69-76. https://doi.org/10.1016/j.lfs.2018.01.016
  81. Soliman, S.S.M., Semreen, M.H., El-Keblawy, A.A., Abdullah, A., Uppuluri, P., Ibrahim, A.S. 2017. Assessment of herbal drugs for promising anti-Candida activity. BMC Complementary Medicine and Therapies 17(1): 257. https://doi.org/10.1186/s12906-017-1760-x
  82. Soll, D.R., Galask, R., Schmid, J., Hanna, C., Mac, K., Morrow, B. 1991. Genetic dissimilarity of commensal strains of Candida spp. carried in different anatomical locations of the same healthy women. Journal of Clinical Microbiology 29(8): 1702-1710. https://doi.org/10.1128/jcm.29.8.1702-1710.1991
  83. Sun, L., Liao, K., Wang, D. 2015a. Effects of magnolol and honokiol on adhesion, yeast-hyphal transition, and formation of biofilm by Candida albicans. PLOS ONE 10(2): e0117695. https://doi.org/10.1371/journal.pone.0117695
  84. Sun, L., Sun, S., Cheng, A., Wu, X., Zhang, Y., Lou, H. 2009. In vitro activities of retigeric acid B alone and in combination with azole antifungal agents against Candida albicans. Antimicrobial Agents and Chemotherapy 53(4): 1586-1591. https://doi.org/10.1128/AAC.00940-08
  85. Sun, L.M., Liao, K., Liang, S., Yu, P.H., Wang, D.Y. 2015b. Synergistic activity of magnolol with azoles and its possible antifungal mechanism against Candida albicans. Journal of Applied Microbiology 118(4): 826-838. https://doi.org/10.1111/jam.12737
  86. Sun, Y., Lenon, G.B., Yang, A.W.H. 2019. Phellodendri Cortex: A phytochemical, pharmacological, and pharmacokinetic review. Evidence-Based Complementary and Alternative Medicine 2019: 7621929. https://doi.org/10.1155/2019/7621929
  87. Suprapti, S., Djarwanto, D., Listya Mustika, D. 2020. Determining the wood (Parashorea spp.) decaying and metal corroding abilities of eight fungi. Journal of the Korean Wood Science and Technology 48(1): 50-60. https://doi.org/10.5658/WOOD.2020.48.1.50
  88. Tampieri, M.P., Galuppi, R., Macchioni, F., Carelle, M.S., Falcioni, L., Cioni, P.L., Morelli, I. 2005. The inhibition of Candida albicans by selected essential oils and their major components. Mycopathologia 159(3): 339-345. https://doi.org/10.1007/s11046-003-4790-5
  89. Taylor, M., Raja, A. 2021. Oral Candidiasis. In: StatPearls. StatPearls Publishing: Treasure Island, FL, USA.
  90. Tian, X., Xu, Z., Hu, P., Yu, Y., Li, Z., Ma, Y., Chen, M., Sun, Z., Liu, F., Li, J., Huang, C. 2020. Determination of the antidiabetic chemical basis of Phellodendri Chinensis Cortex by integrating hepatic disposition in vivo and hepatic gluconeogenese inhibition in vitro. Journal of Ethnopharmacology 263: 113215. https://doi.org/10.1016/j.jep.2020.113215
  91. Tsai, T.H., Chen, C.F. 1992. Identification and determination of honokiol and magnolol from Magnolia officinalis by high-performance liquid chromatography with phtodiode-array UV detection. Journal of Chromatography A 598(1): 143-146. https://doi.org/10.1016/0021-9673(92)85125-D
  92. Vincent-Ballereau, F.N., Patey, O.N., Lafaix, C. 1991. Fluconazole: Review and situation among antifungal drugs in the treatment of opportunistic mycoses of human immuno-deficiency virus infections. Pharmaceutisch Weekblad 13(2): 45-57. https://doi.org/10.1007/BF01974981
  93. Violante, I.M.P., Hamerski, L., Garcez, W.S., Batista, A.L., Chang, M.R., Pott, V.J., Garcez, F.R. 2012. Antimicrobial activity of some medicinal plants from the cerrado of the central-western region of Brazil. Brazilian Journal of Microbiology 43(4): 1302-1308. https://doi.org/10.1590/S1517-83822012000400009
  94. Wang, K., Dang, W., Xie, J., Zhu, R., Sun, M., Jia, F., Zhao, Y., An, X., Qiu, S., Li, X., Ma, Z., Yan, W., Wang, R. 2015. Antimicrobial peptide protonectin disturbs the membrane integrity and induces ROS production in yeast cells. Biochimica et Biophysica Acta (BBA) - Biomembranes 1848(10 Pt A): 2365-2373. https://doi.org/10.1016/j.bbamem.2015.07.008
  95. Whaley, S.G., Berkow, E.L., Rybak, J.M., Nishimoto, A.T., Barker, K.S., Rogers, P.D. 2017. Azole antifungal resistance in Candida albicans and emerging non-albicansCandida species. Frontiers in Microbiology 7: 2173. https://doi.org/10.3389/fmicb.2016.02173
  96. Xian, Y.F., Lin, Z.X., Ip, S.P., Su, Z.R., Chen, J.N., Lai, X.P. 2013. Comparison the neuropreotective effect of Cortex Phellodendri chinensis and Cortex Phellodendri amurensis against beta-amyloid-induced neurotoxicity in PC12 cells. Phytomedicine 20(2): 187-193. https://doi.org/10.1016/j.phymed.2012.09.028
  97. Xie, Y., Liu, X., Zhou, P. 2020. In vitro antifungal effects of berberine against Candida spp. in planktonic and biofilm conditions. Drug Design, Development and Therapy 14: 87-101. https://doi.org/10.2147/dddt.s230857
  98. Xu, B., Yan, Y., Huang, J., Yin, B., Pan, Y., Ma, L. 2020. Cortex Phellodendri extract's anti-diarrhea effect in mice related to its modification of gut microbiota. Biomedicine and Pharmacotherapy 123: 109720. https://doi.org/10.1016/j.biopha.2019.109720
  99. Yamamoto, T., Umegawa, Y., Tsuchikawa, H., Hanashima, S., Matsumori, N., Funahashi, K., Seo, S., Shinoda, W., Murata, M. 2019. The amphotericin B-ergosterol complex spans a lipid bilayer as a single-length assembly. Biochemistry 58(51): 5188-5196. https://doi.org/10.1021/acs.biochem.9b00835
  100. Yapar, N. 2014. Epidemiology and risk factors for invasive candidiasis. Therapeutics and Clinical Risk Management 10: 95-105. https://doi.org/10.2147/TCRM.S40160
  101. Yoon, J., Kim, T.J. 2021. Synergistic antifungal activity of Magnoliae Cortex and Syzyii Flos against Candida albicans. Journal of the Korean Wood Science and Technology 49(2): 142-153. https://doi.org/10.5658/WOOD.2021.49.2.142
  102. Yun, J., Shin, H.C., Hwang, W.J., Yoon, S.M., Kim, Y.S. 2021. Identification of sapstain fungi on weathered wooden surfaces of buildings at Jangheung and Jeju island. Journal of the Korean Wood Science and Technology 49(6): 591-601. https://doi.org/10.5658/WOOD.2021.49.6.591
  103. Zazharskyi, V.V., Davydenko, P.O., Kulishenko, O.M., Borovik, I.V., Zazharska, N.M., Brygadyrenko, V.V. 2020. Antibacterial and fungicidal activities of ethanol extracts of 38 species of plants. Biosystems Diversity 28(3): 281-289. https://doi.org/10.15421/012037
  104. Zhao, Y., Yan, D., Wang, J., Zhang, P., Xiao, X. 2010. Anti-fungal effect of berberine on Candida albicans by microcalorimetry with correspondence analysis. Journal of Thermal Analysis and Calorimetry 102(1): 49-55. https://doi.org/10.1007/s10973-009-0565-7
  105. Zhou, P., Fu, J., Hua, H., Liu, X. 2017. In vitro inhibitory activities of magnolol against Candida spp. Drug Design, Development and Therapy 11: 2653-2661. https://doi.org/10.2147/DDDT.S146529
  106. Zhu, S., Dou, S., Liu, X., Liu, R., Zhang, W, Huang, H., Zhang, Y., Hu, Y., Wang, S. 2011. Qualitative and quantitative analysis of alkaloids in Cortex Phellodendri by HPLC-ESI-MS/MS and HPLC-DAD. Chemical Research in Chinese Universities 27(1): 38-44.
  107. Zida, A., Bamba, S., Yacouba, A., Ouedraogo-Traore, R., Guiguemde, R.T. 2017. Anti-Candida albicans natural products, sources of new antifungal drugs: A review. Journal de Mycologie Medicale 27(1): 1-19. https://doi.org/10.1016/j.mycmed.2016.10.002
  108. Zoric, N., Kosalec, I., Tomic, S., Bobnjaric, I., Jug, M., Vlainic, T., Vlainic, J. 2017. Membrane of Candida albicans as a target of berberine. BMC Complementary Medicine and Alternative Medicin 17(1): 268. https://doi.org/10.1186/s12906-017-1773-5