203
Views
2
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Synergy and Mechanism of Leflunomide Plus Fluconazole Against Resistant Candida albicans: An in vitro Study

, , , , &
Pages 4147-4158 | Received 20 Apr 2023, Accepted 10 Jun 2023, Published online: 27 Jun 2023

References

  • Gow NAR, Yadav B. Microbe profile: Candida albicans: a shape-changing, opportunistic pathogenic fungus of humans. Microbiology. 2017;163:1145–1147. doi:10.1099/mic.0.000499
  • Robbins N, Caplan T, Cowen LE. Molecular evolution of antifungal drug resistance. Annu Rev Microbiol. 2017;71(1):753–775. doi:10.1146/annurev-micro-030117-020345
  • Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20(1):133–163. doi:10.1128/CMR.00029-06
  • Naveen KV, Saravanakumar K, Sathiyaseelan A, et al. Human fungal infection, immune response, and clinical challenge-a perspective during COVID-19 pandemic. Appl Biochem Biotechnol. 2022;194(9):4244–4257. doi:10.1007/s12010-022-03979-5
  • Chavda VP, Mishra T, Kamaraj S, et al. Post-COVID-19 fungal infection in the aged population. Vaccines. 2023:11. doi:10.3390/vaccines11030555
  • Hoenigl M, Seidel D, Sprute R, et al. COVID-19-associated fungal infections. Nat Microbiol. 2022;7(8):1127–1140. doi:10.1038/s41564-022-01172-2
  • World Health Organization. WHO Fungal Priority Pathogens List to Guide Research, Development and Public Health Action. World Health Organization; 2022.
  • Liu S, Yue L, Gu W, et al. Synergistic effect of fluconazole and calcium channel blockers against resistant Candida albicans. PLoS One. 2016;11(3):e0150859. doi:10.1371/journal.pone.0150859
  • Gao Y, Zhang C, Lu C, et al. Synergistic effect of doxycycline and fluconazole against Candida albicans biofilms and the impact of calcium channel blockers. FEMS Yeast Res. 2013;13(5):453–462. doi:10.1111/1567-1364.12048
  • Sun S, Li Y, Guo Q, et al. In vitro interactions between tacrolimus and azoles against Candida albicans determined by different methods. Antimicrob Agents Chemother. 2008;52(2):409–417. doi:10.1128/AAC.01070-07
  • Wibawa T, Baly I, Daeli PR, et al. Cyclosporine A decreases the fluconazole minimum inhibitory concentration of Candida albicans clinical isolates but not biofilm formation and cell growth. Trop Biomed. 2015;32:176–182.
  • Zhang M, Qi C, Zha Y, et al. Leflunomide versus cyclophosphamide in the induction treatment of proliferative lupus nephritis in Chinese patients: a randomized trial. Clin Rheumatol. 2019;38(3):859–867. doi:10.1007/s10067-018-4348-z
  • Zhang C, Chu M. Leflunomide: a promising drug with good antitumor potential. Biochem Biophys Res Commun. 2018;496(2):726–730. doi:10.1016/j.bbrc.2018.01.107
  • Li Y, Sun S, Guo Q, et al. In vitro interaction between azoles and cyclosporin A against clinical isolates of Candida albicans determined by the chequerboard method and time-kill curves. J Antimicrob Chemother. 2008;61(3):577–585. doi:10.1093/jac/dkm493
  • Li X, Yu C, Huang X, et al. Synergistic effects and mechanisms of budesonide in combination with fluconazole against resistant Candida albicans. PLoS One. 2016;11(12):e0168936. doi:10.1371/journal.pone.0168936
  • Rex JH, Alexander BD, Andes D, et al. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard—Third Edition. Vol. 28. CLSI; 2008.
  • Savage KA, Parquet MC, Allan DS, et al. Iron restriction to clinical isolates of Candida albicans by the novel chelator DIBI inhibits growth and increases sensitivity to azoles in vitro and in vivo in a murine model of experimental vaginitis. Antimicrob Agents Chemother. 2018;62. doi:10.1128/AAC.02576-17
  • Odds FC. Synergy, antagonism, and what the chequerboard puts between them. J Antimicrob Chemother. 2003;52(1):1. doi:10.1093/jac/dkg301
  • Chen X, Shi Y, Li Y, et al. Antifungal effects and potential mechanisms of lonidamine in combination with fluconazole against Candida albicans. Expert Rev Anti Infect Ther. 2021;19(1):109–115. doi:10.1080/14787210.2020.1811684
  • Chang W, Li Y, Zhang L, et al. Retigeric acid B attenuates the virulence of Candida albicans via inhibiting adenylyl cyclase activity targeted by enhanced farnesol production. PLoS One. 2012;7(7):e41624. doi:10.1371/journal.pone.0041624
  • Wang T, Flint S, Palmer J. Magnesium and calcium ions: roles in bacterial cell attachment and biofilm structure maturation. Biofouling. 2019;35(9):959–974. doi:10.1080/08927014.2019.1674811
  • Weissman L, Garty J, Hochman A. Rehydration of the Lichen Ramalina lacera results in production of reactive oxygen species and nitric oxide and a decrease in antioxidants. Appl Environ Microbiol. 2005;71(4):2121–2129. doi:10.1128/AEM.71.4.2121-2129.2005
  • Li Y, Jiao P, Li Y, et al. The synergistic antifungal effect and potential mechanism of D-penicillamine combined with fluconazole against Candida albicans. Front Microbiol. 2019;10:2853. doi:10.3389/fmicb.2019.02853
  • Zhang M, Yan H, Lu M, et al. Antifungal activity of ribavirin used alone or in combination with fluconazole against Candida albicans is mediated by reduced virulence. Int J Antimicrob Agents. 2020;55(1):105804. doi:10.1016/j.ijantimicag.2019.09.008
  • Li X, Sun S. Targeting the fungal calcium-calcineurin signaling network in overcoming drug resistance. Future Med Chem. 2016;8:1379–1381. doi:10.4155/fmc-2016-0094
  • Tian J, Lu Z, Wang Y, et al. Nerol triggers mitochondrial dysfunction and disruption via elevation of Ca(2+) and ROS in Candida albicans. Int J Biochem Cell Biol. 2017;85:114–122. doi:10.1016/j.biocel.2017.02.006
  • Spengler G, Gajdacs M, Donadu MG, et al. Evaluation of the antimicrobial and antivirulent potential of essential oils isolated from Juniperus oxycedrus L. ssp. macrocarpa aerial parts. Microorganisms. 2022;10(4):758. doi:10.3390/microorganisms10040758
  • Hamdy R, Fayed B, Hamoda AM, et al. Essential oil-based design and development of novel anti-Candida azoles formulation. Molecules. 2020;25(6):1463. doi:10.3390/molecules25061463
  • Cid-Chevecich C, Muller-Sepulveda A, Jara JA, et al. Origanum vulgare L. essential oil inhibits virulence patterns of Candida spp. and potentiates the effects of fluconazole and nystatin in vitro. BMC Complement Med Ther. 2022;22(1):39. doi:10.1186/s12906-022-03518-z
  • Lohse MB, Gulati M, Johnson AD, et al. Development and regulation of single- and multi-species Candida albicans biofilms. Nat Rev Microbiol. 2018;16(1):19–31. doi:10.1038/nrmicro.2017.107
  • Desai JV, Mitchell AP, Ghannoum M, Parsek M, Whiteley M, Mukherjee P. Candida albicans biofilm development and its genetic control. Microbiol Spectr. 2015;3(3). doi:10.1128/microbiolspec.MB-0005-2014
  • Oppenheimer-Shaanan Y, Steinberg N, Kolodkin-Gal I. Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol. 2013;21(11):594–601. doi:10.1016/j.tim.2013.08.005
  • Gow NA, van de Veerdonk FL, Brown AJ, et al. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol. 2011;10:112–122. doi:10.1038/nrmicro2711
  • Meng L, Zhao H, Zhao S, et al. Inhibition of yeast-to-hypha transition and virulence of Candida albicans by 2-alkylaminoquinoline derivatives. Antimicrob Agents Chemother. 2019;63(4). doi:10.1128/AAC.01891-18
  • Maesaki S, Marichal P, Vanden Bossche H, et al. Rhodamine 6G efflux for the detection of CDR1-overexpressing azole-resistant Candida albicans strains. J Antimicrob Chemother. 1999;44(1):27–31. doi:10.1093/jac/44.1.27
  • Wu XZ, Cheng AX, Sun LM, et al. Plagiochin E, an antifungal bis(bibenzyl), exerts its antifungal activity through mitochondrial dysfunction-induced reactive oxygen species accumulation in Candida albicans. Biochim Biophys Acta. 2009;1790:770–777. doi:10.1016/j.bbagen.2009.05.002
  • Hwang IS, Lee J, Jin HG, et al. Amentoflavone stimulates mitochondrial dysfunction and induces apoptotic cell death in Candida albicans. Mycopathologia. 2012;173:207–218. doi:10.1007/s11046-011-9503-x
  • Frohlich KU, Fussi H, Ruckenstuhl C. Yeast apoptosis--from genes to pathways. Semin Cancer Biol. 2007;17:112–121. doi:10.1016/j.semcancer.2006.11.006
  • Tian H, Qu S, Wang Y, et al. Calcium and oxidative stress mediate perillaldehyde-induced apoptosis in Candida albicans. Appl Microbiol Biotechnol. 2017;101(8):3335–3345. doi:10.1007/s00253-017-8146-3
  • Hwang JH, Hwang IS, Liu QH, et al. (+)-Medioresinol leads to intracellular ROS accumulation and mitochondria-mediated apoptotic cell death in Candida albicans. Biochimie. 2012;94:1784–1793. doi:10.1016/j.biochi.2012.04.010
  • Chen Y, Zeng H, Tian J, et al. Dill (Anethum graveolens L.) seed essential oil induces Candida albicans apoptosis in a metacaspase-dependent manner. Fungal Biol. 2014;118(4):394–401. doi:10.1016/j.funbio.2014.02.004
  • Peng L, Yu Q, Zhu H, et al. The V-ATPase regulates localization of the TRP Ca(2+) channel Yvc1 in response to oxidative stress in Candida albicans. Int J Med Microbiol. 2020;310:151466. doi:10.1016/j.ijmm.2020.151466
  • Sharma M, Manoharlal R, Puri N, et al. Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. Biosci Rep. 2010;30(6):391–404. doi:10.1042/BSR20090151
  • Bi S, Lv QZ, Wang TT, et al. SDH2 is involved in proper hypha formation and virulence in Candida albicans. Future Microbiol. 2018;13:1141–1156. doi:10.2217/fmb-2018-0033
  • Pasrija R, Krishnamurthy S, Prasad T, et al. Squalene epoxidase encoded by ERG1 affects morphogenesis and drug susceptibilities of Candida albicans. J Antimicrob Chemother. 2005;55(6):905–913. doi:10.1093/jac/dki112