Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Opposite Effects of Vitamin C and Vitamin E on the Antifungal Activity of Honokiol

  • Sun, Lingmei (Department of Pharmacology, Medical School of Southeast University) ;
  • Ye, Xiaolong (Department of Endocrinology, The Second Affiliated Hospital of Nanjing Medical University, Nanjing Medical University) ;
  • Ding, Dafa (Department of Endocrinology, The Second Affiliated Hospital of Nanjing Medical University, Nanjing Medical University) ;
  • Kai, Liao (Department of Pathology and Pathophysiology, Medical School of Southeast University)
  • Received : 2019.01.07
  • Accepted : 2019.03.02
  • Published : 2019.04.28
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Abstract

The aim of the present study was to evaluate the effects of two well-known natural antioxidants, vitamin C (VC) and vitamin E (VE), on the antifungal activity of honokiol against Candida albicans. The broth microdilution method was employed to test the antifungal activities of honokiol with or without antioxidants in the medium against C. albicans strain. Intracellular reactive oxygen species and lipid peroxidation were determined by fluorescence staining assay. Mitochondrial dysfunction was assessed by detecting the mitochondrial DNA and the mitochondrial membrane potential. We observed that VC could significantly potentiate the antifungal activities of honokiol while VE reduced the effectiveness of honokiol against C. albicans. In addition, VC accelerated honokiol-induced mitochondrial dysfunction and inhibited glycolysis leading to a decrease in cellular ATP. However, VE could protect against mitochondrial membrane lipid peroxidation and rescue mitochondrial function after honokiol treatment. Our research provides new insight into the understanding of the action mechanism of honokiol and VC combination against C. albicans.

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References

  1. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. 2007. Mitochondria, oxidative stress and cell death. Apoptosis 12: 913-922. https://doi.org/10.1007/s10495-007-0756-2
  2. Villanueva C, Kross RD. 2012. Antioxidant-induced stress. Int. J. Mol. Sci. 13: 2091-2109. https://doi.org/10.3390/ijms13022091
  3. Ayer A, Gourlay CW, Dawes IW. 2014. Cellular redox homeostasis, reactive oxygen species and replicative ageing in Saccharomyces cerevisiae. FEMS Yeast Res. 14: 60-72. https://doi.org/10.1111/1567-1364.12114
  4. Traber MG, Stevens JF. 2011. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic. Biol. Med. 51: 1000-1013. https://doi.org/10.1016/j.freeradbiomed.2011.05.017
  5. Buettner GR. 1986. Ascorbate autoxidation in the presence of iron and copper chelates. Free Radic. Res. Commun. 1: 349-353. https://doi.org/10.3109/10715768609051638
  6. De Francesco EM, Bonuccelli G, Maggiolini M, Sotgia F, Lisanti MP. 2017. Vitamin C and doxycycline: a synthetic lethal combination therapy targeting metabolic flexibility in cancer stem cells (CSCs). Oncotarget 8: 67269-67286. https://doi.org/10.18632/oncotarget.18428
  7. Amorati R, Zotova J, Baschieri A, Valgimigli L. 2015. Antioxidant activity of magnolol and honokiol: kinetic and mechanistic investigations of their reaction with peroxyl radicals. J. Org. Chem. 80: 10651-10659. https://doi.org/10.1021/acs.joc.5b01772
  8. Liao K, Sun L. 2018. The Roles of Hsp90-calcineurin pathway in the antifungal activity of honokiol. J. Microbiol. Biotechnol. 28: 1086-1093. https://doi.org/10.4014/jmb.1801.01024
  9. Sun LM, Liao K. 2018. Saccharomyces cerevisiae Hog1 MAP kinase pathway is activated in response to honokiol exposure. J. Appl. Microbiol. 124: 754-763. https://doi.org/10.1111/jam.13649
  10. Sun L, Liao K, Hang C, Wang D. 2017. Honokiol induces reactive oxygen species-mediated apoptosis in Candida albicans through mitochondrial dysfunction. PLoS One 12: e172228.
  11. Sun L, Liao K, Wang D. 2017. Honokiol induces superoxide production by targeting mitochondrial respiratory chain complex I in Candida albicans. PLoS One 12: e184003.
  12. Sun L, Liao K, Wang D. 2015. Effects of magnolol and honokiol on adhesion, yeast-hyphal transition, and formation of biofilm by Candida albicans. PLoS One 10: e117695.
  13. Clinical and Laboratory Standards Institute (CLSI). 2008. M27-A3, Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts: Approved Standard, 3rd ed. Wayne, PA: Clinical and Laboratory Standards Institute.
  14. Klepser ME, Wolfe EJ, Jones RN, Nightingale CH, Pfaller MA. 1997. Antifungal pharmacodynamic characteristics of fluconazole and amphotericin B tested against Candida albicans. Antimicrob. Agents Chemother. 41: 1392-1395. https://doi.org/10.1128/AAC.41.6.1392
  15. Takahashi M, Shibata M, Niki E. 2001. Estimation of lipid peroxidation of live cells using a fluorescent probe, diphenyl-1-pyrenylphosphine. Free Radic. Biol. Med. 31: 164-174. https://doi.org/10.1016/S0891-5849(01)00575-5
  16. Cossarizza A, Salvioli S. 2001. Flow cytometric analysis of mitochondrial membrane potential using JC-1. Curr. Protoc. Cytom. Chapter 9: unit 9-14.
  17. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, et al. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA 88: 3671-3675. https://doi.org/10.1073/pnas.88.9.3671
  18. Sun L, Zhao Y, Yuan H, Li X, Cheng A, Lou H. 2011. Solamargine, a steroidal alkaloid glycoside, induces oncosis in human K562 leukemia and squamous cell carcinoma KB cells. Cancer Chemother. Pharmacol. 67: 813-821. https://doi.org/10.1007/s00280-010-1387-9
  19. Chang W, Zhang M, Li Y, Lou H. 2015. Flow cytometry-based method to detect persisters in Candida albicans. Antimicrob. Agents Chemother. 59: 5044-5048. https://doi.org/10.1128/AAC.00255-15
  20. Morita M, Naito Y, Yoshikawa T, Niki E. 2016. Plasma lipid oxidation induced by peroxynitrite, hypochlorite, lipoxygenase and peroxyl radicals and its inhibition by antioxidants as assessed by diphenyl-1-pyrenylphosphine. Redox Biol. 8: 127-135. https://doi.org/10.1016/j.redox.2016.01.005
  21. Dellinger M, Geze M. 2001. Detection of mitochondrial DNA in living animal cells with fluorescence microscopy. J. Microsc. 204: 196-202. https://doi.org/10.1046/j.1365-2818.2001.00954.x
  22. Yun J, Mullarky E, Lu C, Bosch KN, Kavalier A, Rivera K, et al. 2015. Vitamin C selectively kills KRAS and BRAF mutant colorectal cancer cells by targeting GAPDH. Science 350: 1391-1396. https://doi.org/10.1126/science.aaa5004
  23. Pelicano H, Martin DS, Xu RH, Huang P. 2006. Glycolysis inhibition for anticancer treatment. Oncogene 25: 4633-4646. https://doi.org/10.1038/sj.onc.1209597
  24. Wisplinghoff H, Seifert H, Wenzel RP, Edmond MB. 2003. Current trends in the epidemiology of nosocomial bloodstream infections in patients with hematological malignancies and solid neoplasms in hospitals in the United States. Clin. Infect. Dis. 36: 1103-1110. https://doi.org/10.1086/374339
  25. Bondaryk M, Kurzatkowski W, Staniszewska M. 2013. Antifungal agents commonly used in the superficial and mucosal candidiasis treatment: mode of action and resistance development. Postepy Dermatol. Alergol. 30: 293-301.
  26. Teodoro GR, Ellepola K, Seneviratne CJ, Koga-Ito CY. 2015. Potential use of phenolic acids as anti-Candida agents: a review. Front Microbiol. 6: 1420. https://doi.org/10.3389/fmicb.2015.01420
  27. Sun L, Hang C, Liao K. 2018. Synergistic effect of caffeic acid phenethyl ester with caspofungin against Candida albicans is mediated by disrupting iron homeostasis. Food Chem. Toxicol. 116: 51-58. https://doi.org/10.1016/j.fct.2018.04.014
  28. Sun L, Liao K, Hang C. 2018. Caffeic acid phenethyl ester synergistically enhances the antifungal activity of fluconazole against resistant Candida albicans. Phytomedicine 40: 55-58. https://doi.org/10.1016/j.phymed.2017.12.033
  29. Labriola D, Livingston R. 1999. Possible interactions between dietary antioxidants and chemotherapy. Oncology (Williston Park) 13: 1003-1008,
  30. Belhachemi MH, Boucherit K, Boucherit-Otmani Z, Belmir S, Benbekhti Z. 2014. Effects of ascorbic acid and alphatocopherol on the therapeutic index of amphotericin B. J. Mycol. Med. 24: e137-e142. https://doi.org/10.1016/j.mycmed.2014.04.003
  31. Yin H, Xu L, Porter NA. 2011. Free radical lipid peroxidation: mechanisms and analysis. Chem. Rev. 111: 5944-5972. https://doi.org/10.1021/cr200084z
  32. Zhu X, Zou S, Li Y, Liang Y. 2017. Transcriptomic analysis of Saccharomyces cerevisiae upon honokiol treatment. Res. Microbiol. 168: 626-635. https://doi.org/10.1016/j.resmic.2017.04.007
  33. Stohs SJ, Bagchi D. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18: 321-336. https://doi.org/10.1016/0891-5849(94)00159-H
  34. Carr A, Frei B. 1999. Does vitamin C act as a pro-oxidant under physiological conditions? FASEB J. 13: 1007-1024. https://doi.org/10.1096/fasebj.13.9.1007
  35. Clement MV, Ramalingam J, Long LH, Halliwell B. 2001. The in vitro cytotoxicity of ascorbate depends on the culture medium used to perform the assay and involves hydrogen peroxide. Antioxid. Redox Signal. 3: 157-163. https://doi.org/10.1089/152308601750100687
  36. Halliwell B. 2013. The antioxidant paradox: less paradoxical now? Br. J. Clin. Pharmacol. 75: 637-644. https://doi.org/10.1111/j.1365-2125.2012.04272.x
  37. Gohil K, Packer L, de Lumen B, Brooks GA, Terblanche SE. 1986. Vitamin E deficiency and vitamin C supplements: exercise and mitochondrial oxidation. J. Appl. Physiol. 60: 1986-1991. https://doi.org/10.1152/jappl.1986.60.6.1986
  38. Bonuccelli G, De Francesco EM, de Boer R, Tanowitz HB, Lisanti MP. 2017. NADH autofluorescence, a new metabolic biomarker for cancer stem cells: Identification of vitamin C and CAPE as natural products targeting "stemness". Oncotarget 8: 20667-20678. https://doi.org/10.18632/oncotarget.15400

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