Therapeutic Effect of Propolis against Biofilm Gene Expression in Candida albicans

Authors

  • Mouna Akeel Hamed Al-Oebady Biology Department, College of Science, Al-Muthanna University, Iraq.

DOI:

https://doi.org/10.35516/jjps.v18i1.3130

Keywords:

Expression, Ece1, Sap5, Als3, genes

Abstract

The sticky substance called propolis is made from plants and is produced by honeybees. It has been used as a folk remedy since ancient times, and it has numerous pharmaceutical benefits, such as antibacterial and antifungal. The objective of this work was to determine the impact of propolis on the expression of three genes (Ece1, Sap5, and Als3) known to be implicated in the development of C.albicans biofilms and define the minimum inhibitory concentration of propolis required for this purpose. The XTT test was used to assess the anti-biofilm activity of propolis in order to ascertain the formation of biofilm on 100 C. albicans isolates from stool samples and calculate the minimum inhibitory concentration of propolis that inhibits the biofilm of C. albicans during 24 and 48 h. Finally, the impact of propolis on the expression of the Ece1, Sap5, and Als3 genes in C. albicans was examined using a real-time polymerase chain reaction and compared with the results that appeared in the gene expression of the biofilm C. albicans untreated propolis during 24 and 48 h, and it was considered a control. Through comparison, biofilm formation was found to decrease as propolis concentration and time increased. Accordingly, the MIC of propolis was 40% w/v, and its minimum fungicidal concentration (MFC) was 50% (w/v) in biofilm-forming C .albicans. Additionally, gene expression level analysis revealed a decrease in Ece1, Sap5, and Als3 expression levels with propolis treatment during 24 and 48h.

References

Ayuningtyas NF., Mahdani FY., Pasaribu TAS., Chalim M., Ayna VK., Santosh AB., Santacroce L. and Surboyo MD. Role of Candida albicans in Oral Carcinogenesis. Pathophysiology. 2022;29:650–62. DOI: https://doi.org/10.3390/pathophysiology29040051

Umami A., Paulik E., Molnar R. and Murti B. The relationship between genital hygiene behaviors and genital infections among women: A systematic review. Jurnal Ners. 2022; 17:89–101. DOI: https://doi.org/10.20473/jn.v17i1.34402

Wall G., Montelongo-Jauregui D., Vidal Bonifacio B., Lopez-Ribot JL. and Uppuluri P. Candida albicans biofilm growth and dispersal: contributions to pathogenesis. Curr Opin Microbiol. 2019; 52-16. DOI: https://doi.org/10.1016/j.mib.2019.04.001

Ridwan RD., Diyatri I., Juliastuti WS., Waskita FA., Ananda GC. and Juliana NV. The Ability of Hylocereus Polyrhizus for Gram Positive Bacteria and Candida Albicans. Biochem Cell Arch. 2020; 20:4839–44.

Masfufatun M., Raharjo LH., Wiradinata H.,Tania PO., Ni'matuzahroh NM. and Baktir A .2021. New phenomena for clinicians, model of Candida albicans mobilization before and after biofilm formation in the intestinal mucosa of Wistar rats (Rattus norvegicus). Int J One Health. 2021; 7:165–70. DOI: https://doi.org/10.14202/IJOH.2021.165-170

Anggraini W., Purwanto DA., Kusumawati I., Isnaeni. and Suryanto. Influence of the Environment on Biofilm Formation Candida albicans of Vulvovaginal Candidiasis Isolate Patient. Pharmacognosy J. 2023; 15:216–22. DOI: https://doi.org/10.5530/pj.2023.15.32

Masfufatun M., Purbowati R., Arum NA., Yasinta MS., Sumarsih S. and Baktir A. An intestinal Candida albicans model for monomicrobial and polymicrobial biofilms and effects of hydrolases and the Bgl2 ligand.Vet World. 2022; 15:1134–40. DOI: https://doi.org/10.14202/vetworld.2022.1134-1140

Asih DW., Widodo ADW., Setiabudi RJ., Tyasningsih W. and Wahyunitisari MR. Biofilm formation by the interaction of fungi (Candida tropicalis) with various bacteria. J Adv Biotechnol Exper Therapeut. 2023; 6:84–93. DOI: https://doi.org/10.5455/jabet.2023.d108

Capoci IR., Bonfim-Mendonça PD., Arita GS, Pereira RR., Consolaro ME., Bruschi ML., Negri M. and Svidzinski TI. Propolis is an efficient fungicide and inhibitor of biofilm production by vaginal Candida albicans. Evidence‐Based Complementary and Alternative Medicine. 2015; 1:287-693. DOI: https://doi.org/10.1155/2015/287693

Abd Rashid N., Mohammed SNF., Syed Abd Halim SA., Ghafar NA. and Abdul Jalil NA. Therapeutic Potential of Honey and Propolis on Ocular Disease. Pharmaceuticals. 2022; 15:1419. DOI: https://doi.org/10.3390/ph15111419

Okińczyc P., Paluch E., Franiczek R., Widelski J., Wojtanowski KK., Mroczek T. and Sroka Z. Antimicrobial activity of Apis mellifera L. and Trigona sp. propolis from Nepal and its phytochemical analysis. Biomedicine & Pharmacotherapy. 2020; 129:110-435. DOI: https://doi.org/10.1016/j.biopha.2020.110435

Hadi Wiyono., Handoko E., Noorhamdani. and Prawiro SR. Effect of Ethanolic Extract Propolis Trigona spp. Malang Indonesia on Isolate Staphylococcus aureus Biofilm Architecture from Chronic Rhinosinusitis A Confocal Laser Scanning Microscopic Study. Int J Pharm Sci & Res. 2019; 10:2711-17.

Garcia M C., Lee J T., Ramsook C B., Alsteens D., Dufrêne Y F. and Lipke P N. A role for amyloid in cell aggregation and biofilm formation. PLoS One. 2011; 6:17-32. DOI: https://doi.org/10.1371/journal.pone.0017632

Sardi J C., Scorzoni L., Bernardi T., Fusco-Almeida A M. and Mendes G M J. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. Journal of Medical Microbiology. 2013; 62:10-24. DOI: https://doi.org/10.1099/jmm.0.045054-0

Carvalho-Pereira J., Vaz C., Carneiro C., Pais C. and Sampaio P. Genetic Variability of Candida albicans Sap8 Propeptide in Isolates from Different Types of Infection. Hindawi Publishing Corporation BioMed Research Internationa0l. 2015; 8:148-343. DOI: https://doi.org/10.1155/2015/148343

Li F and Palecek S P. Distinct domains of the Candida albicans adhesin Eap1p mediate cellcell and cell-substrate interactions. Microbiology. 2008; 154:1193–203. DOI: https://doi.org/10.1099/mic.0.2007/013789-0

Mohammed NA., Ajah HA. and Abdulbaqi NT. Determination the Gene Expression Levels of adhesins and Extracellular Enzymes Genes in Candida albicans biofilm producer by Quantitative Real Time PCR Technique (qRT-PCR). Indian Journal of Forensic Medicine & Toxicology. 2021; 2:1517-1527. DOI: https://doi.org/10.37506/ijfmt.v15i2.14553

Garbe E., Thielemann N., Hohner S., Kumar A., Vylkova S., Kurzai O. and Martinb R. Functional analysis of the Candida albicans ECE1 Promoter. Microbiology spectrum. 2023; 1-11. DOI: https://doi.org/10.1128/spectrum.00253-23

ABBAS., Hayder M., HASAN., Marwa A., ALI. and Sinor D. Effect of Bee Venom on MRSA Isolated from Patient's Wounds at Tikrit Teaching Hospital. Indian Journal of Public Health Research & Development. 2019; 10:1-10.‏ DOI: https://doi.org/10.5958/0976-5506.2019.02945.0

Agarwal V., Lal P. and Pruthi V. Effect of plant oils on Candida albicans. J Microbiol Immunol Infect. 2010; 43:447-451. DOI: https://doi.org/10.1016/S1684-1182(10)60069-2

Lal P., Sharma D., Pruthi P. and Pruthi V. Exopolysaccharide analysis of biofilm-forming Candida albicans. J Applied Microbiol. 2010; 109:128-136. DOI: https://doi.org/10.1111/j.1365-2672.2009.04634.x

Roehm N., Rogers G., Hatfield S. and Glasebrook AL. An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J Immunol Methods. 1991; 142:257-265. DOI: https://doi.org/10.1016/0022-1759(91)90114-U

Uppuluri P., Dinakaran H., Thomas DP., Chaturvedi AK. and Lopez-Ri-bot JL. Characteristics of Candida albicans biofilms grown in a synthetic urine medium. J Clin Microbiol. 2009; 47:4078-83. DOI: https://doi.org/10.1128/JCM.01377-09

Nailis H., Kucharíková S., Ricicová M., Van Dijck P., Deforce D., Nelis H. and Coenye T. Real-time PCR expression profiling of genes encod-ing potential virulence factors in Candida albicans biofilms: iden-tification of model-dependent and -independent gene expression. BMC Microbiol. 2010; 10:1-11. DOI: https://doi.org/10.1186/1471-2180-10-114

Chen L., Mehta A., Berenbaum M., Zangerl AR. and Engeseth NJ. Honeys from different floral sources as inhibitors of enzymatic browning in fruit and vegetable homogenates. J Agric Food Chem. 2000; 48:4997-5000. DOI: https://doi.org/10.1021/jf000373j

Mundo M. and Padilla-Zakour O. Growth inhibition of foodborne patho- gens and food spoilage organisms by select raw honeys. Int J Food Microbiol. 2004; 9:1-8. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.03.025

Al-Waili NS., Salom K., Butler G. and Al Ghamdi AA. Honey and microbial infections: a review supporting the use of honey for microbial control. J Med Food. 2011; 10:1079-1096. DOI: https://doi.org/10.1089/jmf.2010.0161

Biswal B., Zakaria A. and Ahmad N. Topical application of honey in the management of radiation mucositis: a preliminary study. Support Care Cancer. 2003; 11:242-248. DOI: https://doi.org/10.1007/s00520-003-0443-y

English H., Pack A. and Molan P. The effects of manuka honey on plaque and gingivitis: a pilot study. J Int Acad Periodontol. 2004; 6:63-67.

Motallebnejad M., Akram S., Moghadamnia A., Moulana Z and Omidi S. The effect of topical application of pure honey on radiation-induced mucositis: a randomized clinical trial. J Contemp Dent Pract. 2008; 9:40-47. DOI: https://doi.org/10.5005/jcdp-9-3-40

Bouchelaghem S. Propolis characterization and antimicrobial activities against Staphylococcus aureus and Candida albicans: A review. Saudi journal of biological sciences. 2022; 1:1936-46. DOI: https://doi.org/10.1016/j.sjbs.2021.11.063

Béji-Srairi R., Younes I., Snoussi M., Yahyaoui K., Borchard G., Ksouri R., Frachet V. and Wided MK. Ethanolic extract of Tunisian propolis: chemical composition, antioxidant, antimicrobial and antiproliferative properties. Journal of Apicultural Research. 2020; 59:917–927. DOI: https://doi.org/10.1080/00218839.2020.1732572

Mutlu Sariguzel F., Berk E., Koc A.N., Sav H. and Demir G. Antifungal activity of propolis against yeasts isolated from blood culture: In vitro evaluation. Journal of Clinical Laboratory Analysis. 2016; 30:513–516. DOI: https://doi.org/10.1002/jcla.21889

Cooper R, Lindsay E. and Molan P. Testing the susceptibility to manuka honey of streptococci isolated from wound swabs. J Apiprod Apimed Sci. 2011; 3:117-122. DOI: https://doi.org/10.3896/IBRA.4.03.3.02

Maddocks S., Lopez M., Rowlands R. and Cooper RA. Manuka honey inhibits the development of Streptococcus pyogenes biofilms and causes reduced expression of two fibronectin binding proteins. Microbiology. 2012; 158:781-790. DOI: https://doi.org/10.1099/mic.0.053959-0

Bueno-Silva B., Marsola A., Ikegaki M., Alencar SM. and Rosalen PL. The effect of seasons on Brazilian red propolis and its botanical source: chemical composition and antibacterial activity. Natural Product Research. 2017; 31:1318–1324. DOI: https://doi.org/10.1080/14786419.2016.1239088

Toreti VC., Sato HH., Pastore GM. and Park YK. Recent progress of propolis for Its biological and chemical compositions and its botanical origin. EvidenceBased Complementary and Alternative Medicine. 2013; 1–13. DOI: https://doi.org/10.1155/2013/697390

Dezmirean DS., Pasca C., Moise A.R. and Bobis O. Plant Sources Responsible for the Chemical Composition and Main Bioactive Properties of Poplar-Type Propolis. Plants. 2021; 10-22. DOI: https://doi.org/10.3390/plants10010022

Regueira MS., Tintino SR., da Silva ARP., Costa MdS., Boligon AA., Matias EFF., de Queiroz Balbino V., Menezes IRA. and Melo Coutinho HD. Seasonal variation of Brazilian red propolis: Antibacterial activity, synergistic effect and phytochemical screening. Food and Chemical Toxicology. 2017; 107:572–580. DOI: https://doi.org/10.1016/j.fct.2017.03.052

Anjum SI., Ullah A., Khan KA., Attaullah M., Khan H., Ali H., Bashir MA., Tahir M., Ansari MJ., Ghramh HA., Adgaba N. and Dash CK. Composition and functional properties of propolis (bee glue): A review. Saudi Journal of Biological. 2019; 26:1695–1703. DOI: https://doi.org/10.1016/j.sjbs.2018.08.013

El-Guendouz S., Aazza S., Lyoussi B., Bankova V., Popova M., Neto L., Faleiro ML. and Miguel M da G. Moroccan Propolis: A natural antioxidant, antibacterial, and antibiofilm against Staphylococcus aureus with no induction of resistance after continuous exposure. Evidence-Based Complementary and Alternative Medicine. 2018; 1–19. DOI: https://doi.org/10.1155/2018/9759240

Ezzat SM., Khattaby AM., Abdelmageed S. and Abd Elaal MA. Cytotoxicity, antioxidant, anti-inflammatory activity, and GC-MS analysis of Egyptian propolis. Comp Clin Pathol. 2019; 28:1589–1598. DOI: https://doi.org/10.1007/s00580-019-02971-6

Piccinelli AL., Mencherini T., Celano R., Mouhoubi Z., Tamendjari A., Aquino R.P. and Rastrelli L. Chemical composition and antioxidant activity of Algerian propolis. J. Agric. Food Chem. 2013; 61:5080–5088. DOI: https://doi.org/10.1021/jf400779w

Staab JF., Bradway SD., Fidel PL. and Sundstrom P. Adhesive and mammalian transglutaminase substrate properties of Candida albi-cans Hwp1. Science.1999; 283:1535-8. DOI: https://doi.org/10.1126/science.283.5407.1535

Hoyer LL. The ALS gene family of Candida albicans. Trends Mi-crobiol. 2001; 9:176-80. DOI: https://doi.org/10.1016/S0966-842X(01)01984-9

Birse CE., Irwin MY., Fonzi WA. and Sypherd PS. Cloning and charac-terization of ECE1, a gene expressed in association with cell elon-gation of the dimorphic pathogen Candida albicans. Infect Immun. 1993; 61:3648-55. DOI: https://doi.org/10.1128/iai.61.9.3648-3655.1993

Naglik JR., Challacombe SJ. and Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev. 2003; 67:400-28. DOI: https://doi.org/10.1128/MMBR.67.3.400-428.2003

Majhol RH., Al-Rashedi NAM. and Al-Oebady MAH. Bacterial activity on hyphal formation of Candida albicans. J PHARM NEGATIVE RESULTS. 2022; 13:552-555. DOI: https://doi.org/10.47750/pnr.2022.13.03.083

Aslani P., Roudbar S. and Roudbary M. Novel formulated zinc oxide nanoparticles reduce Hwp1 Gene expression involved in biofilm formation in Candida albicans with minimum cytotoxicity effect on human cells. Jundishapur J Microbiol. 2018; 11:79-562. DOI: https://doi.org/10.5812/jjm.79562

AlHoly., Taif., and Walid Khaddam. Extracellular Synthesis of Magnesium Oxide at Nano and Bulk Scale: Antifungal Effect Against Candida albicans, Aspergillus niger. Jordan Journal of Pharmaceutical Sciences. 2023; 16.4.

Khajeh E., Hosseini SJ., Rajabibazl M., Roudbary M., Rafiei S., Aslani P. and Farahnejad Z. Antifungal effect of Echinophora platyloba on expression of CDR1 and CDR2 genes in fluconazole-resistant Candida albicans. Br J Biomed Sci. 2016; 73:44–8. DOI: https://doi.org/10.1080/09674845.2016.1155269

Baghini GS., Sepahi AA., Tabatabaei RR. and Tahvildari K. The combined effects of ethanolic extract of Artemisia aucheri and Artemisia oliveriana on biofilm genes expression of methicillin resistant Staphylococcus aureus. Iran J Microbiol. 2018; 10:417–23.

Teggar., Naoual., et al. Chemical composition and biological evaluation of Algerian propolis from six different regions. Jordan Journal of Pharmaceutical Sciences. 2023: 184-197. DOI: https://doi.org/10.35516/jjps.v16i2.1319

Tyagi SP., Sinha DJ., Garg P., Singh UP., Mishra CC. and Nagpal R. Comparison of antimicrobial efficacy of propolis, Morinda citrifolia, Azadirachta indica (Neem) and 5% sodium hypochlorite on Candida albicans biofilm formed on tooth substrate: An in-vitro study. Journal of conservative dentistry. 2013; 16:6- 532. DOI: https://doi.org/10.4103/0972-0707.120973

Majiene D., Macioniene I., Kursvietiene L., Bernatoniene J., Davalgiene J., Lazauskas R. and Savickas A. The effect of propolis on microbial vitality and oxygen consumption. Journal of Medicinal Plants Research. 2010; 4:954-958.

Mohammed., Ghada Abdulmunim. Studying the Anti Candidal-Activity of Different Herbal Oils Incorporated into Tissue Conditioner:(A Comparative study). Jordan Journal of Pharmaceutical Sciences .2023; 16: 871-879. DOI: https://doi.org/10.35516/jjps.v16i4.2086

MAH Al-Oebady., AAA Dakl., HM Nahab. Influence of Staphylococcus Aureus on the Oral Candida Albicans. Journal of Global Pharma Technology. 2019; 11: 288-293.

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Published

2025-03-25

How to Cite

Al-Oebady, M. A. H. (2025). Therapeutic Effect of Propolis against Biofilm Gene Expression in Candida albicans. Jordan Journal of Pharmaceutical Sciences, 18(1), 292–304. https://doi.org/10.35516/jjps.v18i1.3130

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