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Antifungal activity of magnoflorine against Candida strains

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Abstract

Candida albicans is a major invasive pathogen, and the development of strains resistant to conventional antifungal agents has been reported in recent years. We evaluated the antifungal activity of 44 compounds against Candida strains. Magnoflorine showed the highest growth inhibitory activity of the tested Candida strains, with a minimum inhibitory concentration (MIC) of 50 μg/mL based on microdilution antifungal susceptibility testing. Disk diffusion assay confirmed the antifungal activity of magnoflorine and revealed that this activity was stable over 3 days compared to those of berberine and cinnamaldehyde. Cytotoxicity testing showed that magnoflorine could potentially be used in a clinical setting because it didn’t have any toxicity to HaCaT cells even in 200 μg/mL of treatment. Magnoflorine at 50 μg/mL inhibited 55.91 ± 7.17% of alpha-glucosidase activity which is required for normal cell wall composition and virulence of Candida albicans. Magnoflorine also reduced the formation of C. albicans’ biofilm. Combined treatment with magnoflorine and miconazole decreased the amount of miconazole required to kill various Candida albicans. Therefore, magnoflorine is a good candidate lead compound for novel antifungal agents.

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References

  • Alastruey-Izquierdo A, Melhem MS, Bonfietti LX, Rodriguez-Tudela JL (2015) Susceptibility test for fungi: clinical and laboratorial correlations in medical mycology. Rev Inst Med Trop Sao Paulo 57:57–64

    Article  CAS  Google Scholar 

  • Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6:71–79

    Article  Google Scholar 

  • Bates S, Hughes HB, Munro CA, Thomas WP, MacCallum DM, Bertram G, Atrih A, Ferguson MA, Brown AJ, Odds FC, Gow NA (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281:90–98

    Article  CAS  Google Scholar 

  • Bischoff H (1995) The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin Invest Med 18:303–311

    CAS  PubMed  Google Scholar 

  • Bramono K, Tsuboi R, Ogawa H (1995) A carbohydrate-degrading enzyme from Candida albicans: correlation between a-glucosidase activity and fungal growth. Mycose 38:349–353

    Article  CAS  Google Scholar 

  • CCLS document M27-A3 (2008) National Committee for Clinical Laboratory Standards, reference method for broth dilution antifungal susceptibility testing of yeasts. Pennsylvania, USA

  • Chandra J, Long L, Isham N, Mukherjee PK, DiSciullo G, Appelt K, Ghannoum MA (2018) In vitro and in vivo activity of a novel catheter lock solution against bacterial and fungal biofilms. Antimicrob Agents Chemother 4:AAC.00722 – 18

  • Chen JH, Du ZZ, Shen YM, Yang YP (2009) Aporphine alkaloids from Clematis parviloba and their antifungal activity. Arch Pharm Res 32:3–5

    Article  CAS  Google Scholar 

  • Cornely OA, Lass-Florl C, Lagrou K, Valentina AA (2017) Improving outcome of fungal diseases—guiding experts and patients towards excellence. Mycoses 60:420–425

    Article  Google Scholar 

  • Dhale RP, Ghorpade MV, Dharmadhikari CA (2014) Comparison of various methods used to detect biofilm production of Candida species. J Clin Diagn Res 8:DC18–DC20

    PubMed  PubMed Central  Google Scholar 

  • Drogari-Apiranthitou M, Mantopoulou FD, Skiada A, Kanioura L, Grammatikou M, Vrioni G, Mitroussia-Ziouva A, Tsakris A, Petrikkos G (2012) In vitro antifungal susceptibility of filamentous fungi causing rare infections: synergy testing of amphotericin B, posaconazole and anidulafungin in pairs. J Antimicrob Chemother 67:1937–1940

    Article  CAS  Google Scholar 

  • EUCAST (2017) Antimicrobial susceptibility testing EUCAST disk diffusion method. ESCMID Manual v 6:0

  • Haque F, Alfatah M, Ganesan K, Bhattacharyya MS (2016) Inhibitory effect of sophorolipid on Candida albicans biofilm formation and hyphal growth. Sci Rep 6:23575

    Article  CAS  Google Scholar 

  • Hisatomi E, Matsui M, Kubota K, Kobayashi A (2000) Antioxidative activity in the pericarp and seed of Japanese pepper (Xanthoxylum piperitum DC). J Agric Food Chem 48:4924–4928

    Article  CAS  Google Scholar 

  • Klis FM, Groot PD, Hellungwerf K (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39:1–8

    Article  CAS  Google Scholar 

  • Küpeli E, Koşar M, Yeşilada E, Hüsnü K, Başer C (2002) A comparative study on the anti-inflammatory, antinociceptive and antipyretic effects of isoquinoline alkaloids from the roots of Turkish Berberis species. Life Sci 72:645–657

    Article  Google Scholar 

  • Li C, Wang M-H (2014) Potential biological activities of magnoflorine: a compound from Aristolochia debilis Sieb. et Zucc. Korean J Plant Resour 27:223–228

    Article  Google Scholar 

  • Lozano-Chiu M, Nelson PW, Paetznick VL, Rex JH (1999) Disk diffusion method for determining susceptibilities of Candida spp. to MK-0991. J Clin Microbiol 37:1625–1627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mumma JO, Chhay JS, Ross KL, Eaton JS, Newell-Litwa KA, Fridovich-Keil JL (2008) Distinct roles of galactose-1P in galactose-mediated growth arrest of yeast deficient in galactose-1P uridylyltransferase (GALT) and UDP-galactose 4′-epimerase (GALE). Mol Genet Metab 93:160–171

    Article  CAS  Google Scholar 

  • Ngan LTM, Moon JK, Shibamoto T, Ahn YJ (2012) Growth-inhibiting, bactericidal, and urease inhibitory effects of Paeonia lactiflora root constituents and related compounds on antibiotic-susceptible and -resistant strains of Helicobacter pylori. J Agric Food Chem 60:9062–9073

    Article  CAS  Google Scholar 

  • Nikolić M, Vasić S, Đurđević J, Stefanović O, Čomić L (2014) Antibacterial and anti-biofilm activity of ginger (Zingiber officinale (Roscoe)) ethanolic extract. Kragujevac J Sci 36:129–136

    Article  Google Scholar 

  • Ora-Montes HM, Bates S, Netea MG et al (2007) Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal host-fungus interaction. Eukaryot Cell 6:2184–2193

    Article  Google Scholar 

  • Pal M (2017) Morbidity and mortality due to fungal infections. J Appl Microbiol Biochem 1:1–3

    Google Scholar 

  • Patel MB, Mishra SM (2012) Magnoflorine from Tinospora cordifolia stem inhibits α-glucosidase and is antiglycemic in rats. J Funct Foods 4:79–86

    Article  CAS  Google Scholar 

  • Pootong A, Norrapong B, Cowawintaweewat S (2017) Antifungal activity of cinnamaldehyde against Candida albicans. Southeast Asian J Trop Med 48:150–158

    Google Scholar 

  • Sato T, Kishi M, Suda M et al (2017) Prevalence of Candida albicans and non-albicans on the tongue dorsa of elderly people living in a post-disaster area: a cross-sectional survey. BMC Oral Health 17:51

    Article  Google Scholar 

  • Shai LJ, Masoko P, Mokgotho MP, Magano SR, Mogale AM, Boaduo N, Eloff JN (2010) Yeast alpha glucosidase inhibitory and antioxidant activities of six medicinal plants collected in Phalaborwa, South Africa. S Afr J Bot 76:465–470

    Article  Google Scholar 

  • Shao J, Shi G, Wang TM, Wu DQ, Wang CZ (2016) Antiproliferation of berberine in combination with fluconazole from the perspectives of reactive oxygen species, ergosterol and drug efflux in a fluconazole-resistant Candida tropicalis isolate. Front Microbiol 7:15–16

    Article  Google Scholar 

  • Shin YK, Kim KY (2016) Macelignan inhibits bee pathogenic fungi Ascophaera apis growth through HOG1 pathway. Braz J Med Biol Res 49:5313

    Article  Google Scholar 

  • Shin JH, Kee SJ, Shin MG, Kim SH, Shin DH, Lee SK, Suh SP, Ryang DW (2002) Biofilm production by isolates of Candida species recovered from nonneutropenic patients: comparison of bloodstream isolates with isolates from other sources. J Clin Microbiol 30:1244–1248

    Article  Google Scholar 

  • Siddiqua S, Anusha BA, Ashwini LS, Negi PS (2015) Antibacterial activity of cinnamaldehyde and clove oil: effect on selected foodborne pathogens in model food systems and watermelon juice. J Food Sci Technol 52:5834–5841

    Article  CAS  Google Scholar 

  • Singh S, Srivastava R, Choudhary S (2010) Antifungal and HPLC analysis of the crude extracts of Acorus calamus, Tinospora cordifolia and Celestrus paniculatus. Int J Agric Technol 6:149–158

    Google Scholar 

  • Taff HT, Nett JE, Andes DR (2012) Comparative analysis of Candida biofilm quantitation assays. Med Mycol 50:214–218

    Article  Google Scholar 

  • Tavares LdC, Zanon G, Weber AD et al (2014) Structure-activity relationship of benzophenanthridine alkaloids from Zanthoxylum rhoifolium having antimicrobial activity. PLoS ONE 9:97000

    Article  Google Scholar 

  • Whaley SG, Berkow EL, Rybak JM, Nishimoto AT, Barker KS, Rogers PD (2016) Azole antifungal resistance in Candida albicans and emerging non-albicans Candida species. Front Microbiol 7:02173

    Google Scholar 

  • Zida A, Bamba S, Yacouba A, Ouedraogo-Traore R, Guiguemdé RT (2017) Anti-Candida albicans natural products, sources of new antifungal drugs: a review. J Mycol Med 27:01–19

    Article  CAS  Google Scholar 

  • Zorić N, Kosalec I, Tomić S, Bobnjarić I, Jug M, Vlainić T, Vlainić J (2017) Membrane of Candida albicans as a target of berberine. BMC Complement Altern Med 17:268

    Article  Google Scholar 

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Acknowledgements

This research was supported by the Basic Science Research Program through grants from the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2015R1D1A1A01061225) and IPET (116094-03-1-SB010).

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Author notes

  1. Jaegoo Kim and Thinh Ha Quang Bao have contributed equally as first authors.

Authors and Affiliations

  1. Graduate School of Biotechnology, Kyung Hee University, Yongin-si, Gyeonggi-do, Republic of Korea

    Jaegoo Kim, Thinh Ha Quang Bao & Ki-Young Kim

  2. Department of Internal Medicine, Seoul National University Bundang Hospital, 172 Dolma-ro, Bundang-gu, Gyeonggi-do, Republic of Korea

    Yu-Kyong Shin

  3. Department of Genetic Engineering College of Life Science and Graduate School of Biotechnology, Kyung Hee University, 1732, Deogyeong-daero, Giheung-gu, Yongin-si, Gyeonggi-do, Republic of Korea

    Ki-Young Kim

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  1. Jaegoo Kim
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  2. Thinh Ha Quang Bao
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Correspondence to Ki-Young Kim.

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Kim, J., Ha Quang Bao, T., Shin, YK. et al. Antifungal activity of magnoflorine against Candida strains. World J Microbiol Biotechnol 34, 167 (2018). https://doi.org/10.1007/s11274-018-2549-x

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  • DOI: https://doi.org/10.1007/s11274-018-2549-x

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