659
Views
0
CrossRef citations to date
0
Altmetric
Research article

Sub-lethal concentrations of chlorhexidine inhibit Candida albicans growth by disrupting ROS and metal ion homeostasis

, , , &
Article: 2278937 | Received 27 Oct 2022, Accepted 31 Oct 2023, Published online: 09 Nov 2023

References

  • Calderone RA. Candida and candidiasis. Washington DC: ASM Press; 2002.
  • Alnuaimi AD, Wiesenfeld D, O’Brien-Simpson NM, et al. Oral Candida colonization in oral cancer patients and its relationship with traditional risk factors of oral cancer: a matched case-control study. Oral Oncol. 2015;51(2):139–10. doi: 10.1016/j.oraloncology.2014.11.008
  • Brailsford SR, Shah B, Simons D, et al. The predominant aciduric microflora of root-caries lesions. J Dent Res. 2001;80:1828–1833.
  • Canabarro A, Valle C, Farias MR, et al. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013;48(4):428–432. doi: 10.1111/jre.12022
  • Xiao J, Huang X, Alkhers N, et al. Candida albicans and early childhood caries: a systematic review and meta-analysis. Caries Res. 2018;52(1–2):102–112. doi: 10.1159/000481833
  • Yoo YJ, Kim AR, Perinpanayagam H, et al. Candida albicans virulence factors and pathogenicity for endodontic infections. Microorganisms. 2020;8(9):1300. doi: 10.3390/microorganisms8091300
  • Löe H, Schiott CR. The effect of mouthrinses and topical application of chlorhexidine on the development of dental plaque and gingivitis in man. J Periodontal Res. 1970;5:79–83.
  • Bobichon H, Bouchet P. Action of chlorhexidine on budding Candida albicans: scanning and transmission electron microscopic study. Mycopathologia. 1987;100(1):27–35. doi: 10.1007/BF00769565
  • McCourtie J, MacFarlane TW, Samaranayake LP. A comparison of the effects of chlorhexidine gluconate, amphotericin B and nystatin on the adherence of Candida species to denture acrylic. J Antimicrob Chemother. 1986;17(5):575–583. doi: 10.1093/jac/17.5.575
  • Lan CY, Rodarte G, Murillo LA, et al. Regulatory networks affected by iron availability in Candida albicans. Mol Microbiol. 2004;53(5):1451–1469. doi: 10.1111/j.1365-2958.2004.04214.x
  • Li Y, Sun L, Lu C, et al. Promising antifungal targets against Candida albicans based on ion homeostasis. Front Cell Infect Microbiol. 2018;8:286. doi: 10.3389/fcimb.2018.00286
  • Łoboda D, Rowińska-Żyrek M. Zinc binding sites in Pra1, a zincophore from Candida albicans. Dalton Trans. 2017;46:13695–13703. doi: 10.1039/c7dt01675a
  • Yu Q, Wang F, Zhao Q, et al. A novel role of the vacuolar calcium channel Yvc1 in stress response, morphogenesis and pathogenicity of Candida albicans. Int J Med Microbiol. 2014;304(3–4):339–350. doi: 10.1016/j.ijmm.2013.11.022
  • Yun J, Lee DG. Role of potassium channels in chlorogenic acid-induced apoptotic volume decrease and cell cycle arrest in Candida albicans. Biochim Biophys Acta Gen Subj. 2017;1861(3):585–592. doi: 10.1016/j.bbagen.2016.12.026
  • Chen C, Pande K, French SD, et al. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe. 2011;10(2):118–135. doi: 10.1016/j.chom.2011.07.005
  • Gerwien F, Skrahina V, Kasper L, et al. Metals in fungal virulence. FEMS Microbiol Rev. 2018;42(1):fux050. doi: 10.1093/femsre/fux050
  • Touati D. Iron and oxidative stress in bacteria. Arch Biochem Biophys. 2000;373(1):1–6. doi: 10.1006/abbi.1999.1518
  • Nobile CJ, Mitchell AP. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol. 2005;15(12):1150–1155. doi: 10.1016/j.cub.2005.05.047
  • Du H, Guan G, Xie J, et al. The transcription factor Flo8 mediates CO2 sensing in the human fungal pathogen Candida albicans ? Mol Biol Cell. 2012;23(14):2692–2701. doi: 10.1091/mbc.e12-02-0094
  • Homann OR, Dea J, Noble SM, et al. A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 2009;5(12):e1000783. doi: 10.1371/journal.pgen.1000783
  • Park YN, Morschhauser J. Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot Cell. 2005;4(8):1328–1342. doi: 10.1128/EC.4.8.1328-1342.2005
  • Reuss O, Vik A, Kolter R, et al. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene. 2004;341:119–127. doi: 10.1016/j.gene.2004.06.021
  • Clinical and Laboratory Standard Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. CLSI document M27-A3. 3rd ed. Vol 28, no. 14. Wayne, PA: Clinical and Laboratory Standards Institute;2008. p. 1–25.
  • Gulati M, Lohse MB, Ennis CL, et al. In vitro culturing and screening of Candida albicans biofilms. CP Microbiol. 2018;50(1):e60. doi: 10.1002/cpmc.60
  • Wang X, Bing J, Zheng Q, et al. The first isolate of Candida auris in China: clinical and biological aspects. Emerg Microbes Infect. 2018;7:93. doi: 10.1038/s41426-018-0095-0
  • Stewart LJ, Ong CY, Zhang MM, et al. Role of Glutathione in buffering excess intracellular copper in Streptococcus pyogenes. MBio. 2020;11(6):e02804–20. doi: 10.1128/mBio.02804-20
  • Szpunar J. Advances in analytical methodology for bioinorganic speciation analysis: metallomics, metalloproteomics and heteroatom-tagged proteomics and metabolomics. Analyst. 2005;130(4):442–465. doi: 10.1039/b418265k
  • Emilson CG. Susceptibility of various microorganisms to chlorhexidine. Scandinavian J Dental Res. 1977;85:255–265.
  • Mohammadi Z, Abbott PV. The properties and applications of chlorhexidine in endodontics. Int Endodontic J. 2009;42(4):288–302. doi: 10.1111/j.1365-2591.2008.01540.x
  • Cheung HY, Wong MM, Cheung SH, et al. Differential actions of chlorhexidine on the cell wall of Bacillus subtilis and Escherichia coli. PLoS One. 2012;7(5):e36659. doi: 10.1371/journal.pone.0036659
  • Kuyyakanond T, Quesnel LB. The mechanism of action of chlorhexidine. FEMS Microbiol Lett. 1992;100(1–3):211–215. doi: 10.1111/j.1574-6968.1992.tb05705.x
  • Maki DG, Stolz SM, Wheeler S, et al. Prevention of central venous catheter-related bloodstream infection by use of an antiseptic-impregnated catheter: a randomized, controlled trial. Ann Intern Med. 1997;127(4):257–266. doi: 10.7326/0003-4819-127-4-199708150-00001
  • Puig-Silla M, Montiel-Company JM, Almerich-Silla JM. Use of chlorhexidine varnishes in preventing and treating periodontal disease. A review of the literature. Med Oral Patol Oral Cir Bucal. 2008;13(4):E257–60.
  • Denton GW. 1991. Chlorhexidine. In: disinfection, sterilization and preservation. Block SS. Editor 4th Philadelphia: Lea & Febiger; pp. 274–289
  • Gelinas P, Goulet J. Neutralization of the activity of eight disinfectants by organic matter. J Appl Bacteriol. 1983;54(2):243–247. doi: 10.1111/j.1365-2672.1983.tb02613.x
  • Basrani B, Santos JM, Tjäderhane L, et al. Substantive antimicrobial activity in chlorhexidine-treated human root dentin. Oral Surg, Oral Med Oral Pathol Oral Radiol Endod. 2002;94(2):240–245. doi: 10.1067/moe.2002.124002
  • Carrilho MR, Carvalho RM, Sousa EN, et al. Substantivity of chlorhexidine to human dentin. Dental Materials. 2010;26(8):779–785. doi: 10.1016/j.dental.2010.04.002
  • Franco CF, Pataro AL, Souza E, et al. In vitro effects of a chlorhexidine controlled delivery system. Artif Organs. 2003;27(5):486–491. doi: 10.1046/j.1525-1594.2003.07245.x
  • Baca P, Junco P, Arias-Moliz MT, et al. Residual and antimicrobial activity of final irrigation protocols on Enterococcus faecalis biofilm in dentin. J Endod. 2011;37(3):363–366. doi: 10.1016/j.joen.2010.11.036
  • Rosenthal S, Spangberg L, Safavi K. Chlorhexidine substantivity in root canal dentin. Oral Surg, Oral Med Oral Pathol Oral Radiol Endod. 2004;98(4):488–492. doi: 10.1016/j.tripleo.2003.07.005
  • Jomova K, Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology. 2011;283(2–3):65–87. doi: 10.1016/j.tox.2011.03.001
  • Pereira C, Silva RD, Saraiva L, et al. Mitochondria-dependent apoptosis in yeast. Biochim Biophys Acta. 2008;1783(7):1286–1302. doi: 10.1016/j.bbamcr.2008.03.010
  • Perrone GG, Tan SX, Dawes IW. Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta, Mol Cell Res. 2008;1783(7):1354–1368. doi: 10.1016/j.bbamcr.2008.01.023
  • Jungmann J, Reins HA, Lee J, et al. Mac1, a nuclear regulatory protein related to Cu-dependent transcription factors is involved in Cu/Fe utilization and stress resistance in yeast. EMBO J. 1993;12(13):5051–5056. doi: 10.1002/j.1460-2075.1993.tb06198.x
  • Khemiri I, Tebbji F, Sellam A. Transcriptome analysis uncovers a link between copper metabolism, and both fungal fitness and antifungal sensitivity in the opportunistic yeast Candida albicans. Front Microbiol. 2020;11:935. doi: 10.3389/fmicb.2020.00935
  • Culbertson EM, Bruno VM, Cormack BP, et al. Expanded role of the Cu-sensing transcription factor Mac1p in Candida albicans. Mol Microbiol. 2020;114(6):1006–1018. doi: 10.1111/mmi.14591
  • Li CX, Gleason JE, Zhang SX, et al. Candida albicans adapts to host copper during infection by swapping metal cofactors for superoxide dismutase. Proc Natl Acad Sci USA. 2015;112(38):E5336–E5342. doi: 10.1073/pnas.1513447112
  • Mamouei Z, Zeng G, Wang YM, et al. Candida albicans possess a highly versatile and dynamic high-affinity iron transport system important for its commensal-pathogenic lifestyle. Mol Microbiol. 2017;106(6):986–998. doi: 10.1111/mmi.13864
  • Ramanan N, Wang Y. A high-affinity iron permease essential for Candida albicans virulence. Science. 2000;288(5468):1062–1064. doi: 10.1126/science.288.5468.1062
  • Hsu PC, Yang CY, Lan CY. Candida albicans Hap43 is a repressor induced under low-iron conditions and is essential for iron-responsive transcriptional regulation and virulence. Eukaryotic Cell. 2011;10(2):207–225. doi: 10.1128/EC.00158-10
  • Marvin ME, Mason RP, Cashmore AM. The CaCTR1 gene is required for high-affinity iron uptake and is transcriptionally controlled by a copper-sensing transactivator encoded by CaMAC1. Microbiol. 2004;150(7):2197–2208. doi: 10.1099/mic.0.27004-0
  • Nam E, Han J, Suh JM, et al. Link of impaired metal ion homeostasis to mitochondrial dysfunction in neurons. Curr Opin Chem Biol. 2018;43:8–14. doi: 10.1016/j.cbpa.2017.09.009