N-Butylphthalide Potentiates the Effect of Fluconazole Against Drug-Resistant Candida glabrata and Candida tropicalis. Evidence for Its Mechanism of Action

References

• Lakoh S, Kamudumuli PS, Penney ROS, et al. Diagnostic capacity for invasive fungal infections in advanced HIV disease in Africa: a continent-wide survey. Lancet Infect Dis. 2023;23(5):598–608.
   PubMed Web of Science ®Google Scholar
• Lawrence DS, Muthoga C, Meya DB, et al. Cost-effectiveness of single, high-dose, liposomal amphotericin regimen for HIV-associated cryptococcal meningitis in five countries in sub-Saharan Africa: an economic analysis of the AMBITION-cm trial. Lancet Glob Health. 2022;10(12):e1845–e1854.
   PubMed Web of Science ®Google Scholar
• The Lancet Global Health. Moving mycoses up the global agenda. Lancet Glob Health. 2022;10(12):e1688.
   PubMed Web of Science ®Google Scholar
• Vento S, Cainelli F. Infections in patients with cancer undergoing chemotherapy: aetiology, prevention, and treatment. Lancet Oncol. 2003;4(10):595–604.
   PubMed Web of Science ®Google Scholar
• Denning DW. Calling upon all public health mycologists: to accompany the country burden papers from 14 countries. Eur J Clin Microbiol Infect Dis. 2017;36(6):923–924.
   PubMedGoogle Scholar
• Pappas PG, Kauffman CA, Andes DR, et al. Clinical Practice Guideline for the Management of Candidiasis: 2016 Update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;62(4):e1–e50.
   PubMed Web of Science ®Google Scholar
• Ryan P, Motherway C, Powell J, et al. Candidaemia in an Irish intensive care unit setting between 2004 and 2018 reflects increased incidence of Candida glabrata. J Hosp Infect. 2019;102(3):347–350.
   PubMed Web of Science ®Google Scholar
• Megri Y, Arastehfar A, Boekhout T, et al. Candida tropicalis is the most prevalent yeast species causing candidemia in Algeria: the urgent need for antifungal stewardship and infection control measures. Antimicrob Resist Infect Control. 2020;9(1):50.
   PubMed Web of Science ®Google Scholar
• Cangui-Panchi SP, Ñacato-Toapanta AL, Enríquez-Martínez LJ, et al. Battle royale: immune response on biofilms - host-pathogen interactions. Curr Res Immunol. 2023;4:100057.
   PubMedGoogle Scholar
• Atiencia-Carrera MB, Cabezas-Mera FS, Tejera E, et al. Prevalence of biofilms in Candida spp. bloodstream infections: a meta-analysis. PLoS One. 2022;17(2):e0263522.
   PubMed Web of Science ®Google Scholar
• Atiencia-Carrera MB, Cabezas-Mera FS, Vizuete K, et al. Evaluation of the biofilm life cycle between Candida albicans and Candida tropicalis. Front Cell Infect Microbiol. 2022;12:953168.
   PubMed Web of Science ®Google Scholar
• McCarty TP, White CM, Pappas PG. Candidemia and Invasive Candidiasis. Infect Dis Clin North Am. 2021;35(2):389–413.
   PubMed Web of Science ®Google Scholar
• Xiao M, Chen SC, Kong F, et al. Distribution and Antifungal Susceptibility of Candida Species Causing Candidemia in China: an Update From the CHIF-NET Study. J Infect Dis. 2020;221(Suppl 2):S139.
   PubMedGoogle Scholar
• Falces-Romero I, Romero-Gómez MP, Moreno-Ramos F, et al. Epidemiology of bloodstream Candida species in a Spanish tertiary care hospital as a guide for implementation of T2MR (T2CANDIDA®) for rapid diagnosis of candidemia. Med Mycol. 2021;59(4):350–354.
   PubMed Web of Science ®Google Scholar
• Wang Y, Fan X, Wang H, et al. Continual Decline in Azole Susceptibility Rates in Candida tropicalis Over a 9-Year Period in China. Front Microbiol. 2021;12:702839.
   PubMed Web of Science ®Google Scholar
• Alobaid K, Ahmad S, Asadzadeh M, et al. Epidemiology of Candidemia in Kuwait: a Nationwide, Population-Based Study. J Fungi. 2021;7(8):673.
   Web of Science ®Google Scholar
• Lee Y, Puumala E, Robbins N, Cowen LE. Antifungal Drug Resistance: molecular Mechanisms in Candida albicans and Beyond. Chem Rev. 2021;121(6):3390–3411.
   PubMed Web of Science ®Google Scholar
• Hassan Y, Chew SY, Than LTL. Candida glabrata: pathogenicity and Resistance Mechanisms for Adaptation and Survival. J Fungi. 2021;7(8):667.
   Web of Science ®Google Scholar
• Fan X, Xiao M, Zhang D, et al. Molecular mechanisms of azole resistance in Candida tropicalis isolates causing invasive candidiasis in China. Clin Microbiol Infect. 2019;25(7):885–891.
   PubMed Web of Science ®Google Scholar
• Sharifzadeh A, Khosravi AR, Shokri H, Tari PS. Synergistic anticandidal activity of menthol in combination with itraconazole and nystatin against clinical Candida glabrata and Candida krusei isolates. Microb Pathog. 2017;107:390–396.
   PubMed Web of Science ®Google Scholar
• Machado GD RM, Pippi B, Dalla Lana DF, et al. Reversal of fluconazole resistance induced by a synergistic effect with Acca sellowiana in Candida glabrata strains. Pharm Biol. 2016;54(11):2410–2419.
   PubMed Web of Science ®Google Scholar
• Sharifzadeh A, Shokri H, Abbaszadeh S. Interaction of carvacroland voriconazole against drug - resistant Candida strains isolated from patients with candidiasis. J Mycol Med. 2019;29(1):44–48.
   PubMed Web of Science ®Google Scholar
• Giap TH, Dung NA, Thoa HT, et al. Phthalides and Other Metabolites from Roots of Ligusticum wallichii. Chem Nat Compd. 2018;54:34–37.
   Web of Science ®Google Scholar
• Wei W, XiuWen W, XiuWei Y. Novel phthalide derivatives from the rhizomes of Ligusticum chuanxiong and their inhibitory effect against lipopolysaccharide-induced nitric oxide production in RAW 264.7 macrophage cells. RSC Adv. 2016;6(66):61037–61046.
   Web of Science ®Google Scholar
• Zhang LB, Lv JL, Liu JW. Phthalide Derivatives with Anticoagulation Activities from Angelica sinensis. J Nat Prod. 2016;79(7):1857–1861.
   PubMed Web of Science ®Google Scholar
• Clinical and Laboratory Standards Institute. M27 Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. 4th ed. 2017.
   Google Scholar
• Odds FC. Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother. 2003;52(1):1.
   PubMed Web of Science ®Google Scholar
• Adeniji OO, Nontongana N, Okoh JC, et al. The Potential of Antibiotics and Nanomaterial Combinations as Therapeutic Strategies in the Management of Multidrug-Resistant Infections: a Review. Int J Mol Sci. 2022;23(23):15038.
   PubMed Web of Science ®Google Scholar
• Shrestha SK, Fosso MY, Garneau-Tsodikova S. A combination approach to treating fungal infections. Sci Rep. 2015;5:17070.
   PubMed Web of Science ®Google Scholar
• Li H, Zhang C, Chen Z, et al. A promising approach of overcoming the intrinsic resistance of Candida krusei to fluconazole (FLC) --combining tacrolimus with FLC. FEMS Yeast Res. 2014;14(5):808–811.
   PubMed Web of Science ®Google Scholar
• Liang RM, Yong XL, Jiang YP, et al. 2-amino-nonyl-6-methoxyl-tetralin muriate activity against Candida albicans augments endogenous reactive oxygen species production --a microarray analysis study. FEBS J. 2011;278(7):1075–1085.
   PubMed Web of Science ®Google Scholar
• Kadenbach B. Complex IV - The regulatory center of mitochondrial oxidative phosphorylation. Mitochondrion. 2021;58:296–302.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):56.
   Web of Science ®Google Scholar
• Gong Y, Liu W, Huang X, et al. Antifungal Activity and Potential Mechanism of N-Butylphthalide Alone and in Combination With Fluconazole Against Candida albicans. Front Microbiol. 2019;10:1461.
   PubMed Web of Science ®Google Scholar
• Zheng S, Chang W, Zhang M, et al. Chiloscyphenol A derived from Chinese liverworts exerts fungicidal action by eliciting both mitochondrial dysfunction and plasma membrane destruction. Sci Rep. 2018;8(1):326.
   PubMedGoogle Scholar
• Zhang T, Chen W. The Candida albicans Inhibitory Activity of the Extract from Papaya (Carica papaya L.) Seed Relates to Mitochondria Dysfunction. Int J Mol Sci. 2017;18(9):1858.
   PubMed Web of Science ®Google Scholar
• Yang S, Lian G. ROS and diseases: role in metabolism and energy supply. Mol Cell Biochem. 2020;467(1–2).
   Web of Science ®Google Scholar
• Dryden M. Reactive oxygen species: a novel antimicrobial. Int J Antimicrob Agents. 2018;51(3):299–303.
   PubMed Web of Science ®Google Scholar
• Herb M, Schramm M. Functions of ROS in Macrophages and Antimicrobial Immunity. Antioxidants. 2021;10(2):313.
   Web of Science ®Google Scholar
• Zhao RZ, Jiang S, Zhang L, Yu ZB. Mitochondrial electron transport chain, ROS generation and uncoupling (Review). Int J Mol Med. 2019;44(1):3–15.
   PubMed Web of Science ®Google Scholar
• Wang Y, Gulis G, Buckner S, et al. The MAP kinase Pmk1 and protein kinase A are required for rotenone resistance in the fission yeast, Schizosaccharomyces pombe. Biochem Biophys Res Commun. 2010;399(2):123–128.
   PubMed Web of Science ®Google Scholar
• Musatov A, Robinson NC. Susceptibility of mitochondrial electron-transport complexes to oxidative damage. Focus on cytochrome c oxidase. Free Radic Res. 2012;46(11):1313–1326.
   PubMed Web of Science ®Google Scholar
• Fiori A, Perez-Martinez X, Fox TD. Overexpression of the COX2 translational activator, Pet111p, prevents translation of COX1 mRNA and cytochrome c oxidase assembly in mitochondria of Saccharomyces cerevisiae. Mol Microbiol. 2005;56(6):1689–1704.
   PubMed Web of Science ®Google Scholar
• García-Villegas R, Camacho-Villasana Y, Shingú-Vázquez MÁ, et al. The Cox1 C-terminal domain is a central regulator of cytochrome c oxidase biogenesis in yeast mitochondria. J Biol Chem. 2017;292(26):10912–10925.
   PubMed Web of Science ®Google Scholar
• Silva S, Negri M, Henriques M, et al. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev. 2012;36(2):288–305.
   PubMed Web of Science ®Google Scholar
• Esfahani A, Omran AN, Salehi Z, et al. Molecular epidemiology, antifungal susceptibility, and ERG11 gene mutation of Candida species isolated from vulvovaginal candidiasis: comparison between recurrent and non-recurrent infections. Microb Pathog. 2022;170:105696.
   PubMed Web of Science ®Google Scholar
• Rocha DAS, Lfr S, Pinto ACC, et al. Characterisation of an ABC transporter of a resistant Candida glabrata clinical isolate. Mem Inst Oswaldo Cruz. 2018;113(4):e170484.
   PubMed Web of Science ®Google Scholar
• Gohar AA, Badali H, Shokohi T, Nabili M, Amirrajab N, Moazeni M. Expression Patterns of ABC Transporter Genes in Fluconazole-Resistant Candida glabrata. Mycopathologia. 2017;182(3–4).
   PubMed Web of Science ®Google Scholar
• Whaley SG, Zhang Q, Caudle KE, et al. Relative Contribution of the ABC Transporters Cdr1, Pdh1, and Snq2 to Azole Resistance in Candida glabrata. Antimicrob Agents Chemother. 2018;62(10):e01070–18.
   PubMed Web of Science ®Google Scholar
• Berkow EL, Lockhart SR. Fluconazole resistance in Candida species: a current perspective. Infect Drug Resist. 2017;10:237–245.
   PubMed Web of Science ®Google Scholar
• Taudorf EH, Jemec GBE, Hay RJ, et al. Cutaneous candidiasis - an evidence-based review of topical and systemic treatments to inform clinical practice. J Eur Acad Dermatol Venereol. 2019;33(10):1863–1873.
   PubMed Web of Science ®Google Scholar
• Shields BE, Rosenbach M, Brown-Joel Z, et al. Angioinvasive fungal infections impacting the skin: background, epidemiology, and clinical presentation. J Am Acad Dermatol. 2019;80(4):869–880.e5.
   PubMed Web of Science ®Google Scholar
• Wang BN, Wu CB, Chen ZM, et al. DL-3-n-butylphthalide ameliorates diabetes-associated cognitive decline by enhancing PI3K/Akt signaling and suppressing oxidative stress. Acta Pharmacol Sin. 2021;42(3):347–360.
   PubMed Web of Science ®Google Scholar
• Li M, Meng N, Guo X, et al. Dl-3-n-Butylphthalide Promotes Remyelination and Suppresses Inflammation by Regulating AMPK/SIRT1 and STAT3/NF-κB Signaling in Chronic Cerebral Hypoperfusion. Front Aging Neurosci. 2020;12:137.
   PubMed Web of Science ®Google Scholar
• Yang Z, Luo G, Ying Y, et al. Novel 2,6-disubstituted benzofuran-3-one analogues improve cerebral ischemia/reperfusion injury via neuroprotective and antioxidative effects. Bioorg Chem. 2023;3(132):106346.
   Google Scholar
• Brock M. Fungal metabolism in host niches. Curr Opin Microbiol. 2009;12(4):371–376.
   PubMed Web of Science ®Google Scholar
• Helmerhorst EJ, Stan M, Murphy MP, et al. The concomitant expression and availability of conventional and alternative, cyanide-insensitive, respiratory pathways in Candida albicans. Mitochondrion. 2005;5(3):200–211.
   PubMed Web of Science ®Google Scholar