Araştırma Makalesi
BibTex RIS Kaynak Göster

Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B

Yıl 2024, Cilt: 54 Sayı: 2, 189 - 194, 26.08.2024
https://doi.org/10.26650/IstanbulJPharm.2024.1417841

Öz

Background and Aims: Quorum sensing is a mechanism of cell-to-cell communication for controlling virulence and the biofilm formation of microorganisms. Due to this new treatment requiring approaches for biofilm-related infections, this study aims to examine the biofilm formation properties of both Candida albicans and non-albicans (NAC) strains and to compare the effects of the quorum-sensing molecules (QSMs) farnesol and tyrosol with the widely used antifungal agent amphotericin B with regard to biofilm attachment and biofilm formation.

Methods: Biofilm formation of 57 nonrepeat clinical isolates of Candida spp. (36 C. albicans and 21 NAC) was assessed through the crystal violet technique. Farnesol (300 μM), tyrosol (80 μM), and amphotericin B (4 μg/ml) were evaluated against biofilm attachment and biofilm formation (plates incubated 2, 4, 6 and 24 h).

Results: All isolates displayed biofilm-forming capabilities. C. albicans demonstrated mostly weak biofilm formation (42.2%), whereas the NAC species showed strong biofilm formation (52.38%). Depending on the stage at which they were added, farnesol and tyrosol significantly inhibited the biofilm formation of C. albicans and NAC species, especially at 6 h, which is the early stage of biofilm development. Unfortunately, QSM activity decreased at 24 h. In addition, amphotericin B showed a stronger inhibitory effect than the QSMs at all time points studied, with up to 60% inhibition being observed.

Conclusion: QSMs can significantly inhibit biofilm development in both C. albicans and NAC species depending on the stage when they are added, especially in the early stages of biofilm formation.

Proje Numarası

This work was supported by the Research Fund of Istanbul University [project number 34926].

Kaynakça

  • Albuquerque, P., & Casadevall, A. (2012). Quorum sens-ing in fungi-a review. Medical Mycology, 50(4), 337-345. doi:10.3109/13693786.2011.652201 google scholar
  • Alem, M. A., Oteef, M. D., Flowers, T. H., & Douglas, L. J. (2006). Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryotic Cell, 5(10), 1770-1779. https://doi.org/10.1128/EC.00219-06 google scholar
  • Atiencia-Carrera, M. B., Cabezas-Mera, F. S., Tejera, E., & Machado, A. (2022). Prevalence of biofilms in Candida spp. blood-stream infections: A meta-analysis. PLoS One, 17(2), e0263522. https://doi.org/10.1371/journal.pone.0263522 google scholar
  • Atriwal, T., Azeem, K., Husain, F. M., Hussain, A., Khan, M. N., Alajmi, M. F., & Abid, M. (2021). Mechanistic un-derstanding of Candida albicans biofilm formation and ap-proaches for its inhibition. Frontiers in Microbiology, 12, 638609. https://doi.org/10.3389/fmicb.2021.638609 google scholar
  • Bozkurt-Guzel, C., Hacioglu, M., & Savage, P. B. (2018). Investigation of the in vitro antifungal and antibiofilm activities of ceragenins CSA-8, CSA-13, CSA-44, CSA-131, and CSA-138 against Candida species. Diagnos-tic Microbiology and Infectious Disease, 91(4), 324-330. https://doi.org/10.1016/j.diagmicrobio.2018.03.014 google scholar
  • Brackman, G., & Coenye, T. (2015). Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design, 21(1), 5-11. https://doi.org/10.2174/1381612820666140905114627 google scholar
  • Cavalheiro, M., & Teixeira, M. C. (2018). Candida biofilms: threats, challenges, and promising strategies. Frontiers in Medicine, 5, 28. https://doi.org/10.3389/fmed.2018.00028 google scholar
  • Chin, V. K., Lee, T. Y., Rusliza, B., & Chong, P. P. (2016). Dissecting Candida albicans infection from the perspective of C. albicans virulence and omics approaches on host-pathogen interaction: a review. International Journal of Molecular Sciences, 17(10), 1643. https://doi.org/10.3390/ijms17101643 google scholar
  • Cordeiro, R. D. A., Teixeira, C. E., Brilhante, R. S., Castelo-Branco, D. S., Alencar, L. P., de Oliveira, J. S., ... & Rocha, google scholar
  • M. F. (2015). Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their suscep-tibility to antifungals. FEMS Yeast Research, 15(4), fov012. https://doi.org/10.1093/femsyr/fov012 google scholar
  • De Sordi, L., & Mühlschlegel, F. A. (2009). Quorum sensing and fun-gal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Research, 9(7), 990-999. https://doi.org/10.1111/j.1567-1364.2009.00573.x google scholar
  • Djordjevic, D., Wiedmann, M., & McLandsborough, L. A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6), 2950-2958. doi:10.1128/AEM.68.6.2950-2958.2002 google scholar
  • Fourie, R., & Pohl, C. H. (2019). Beyond antagonism: the interaction between Candida species and Pseudomonas aeruginosa. Journal of Fungi, 5(2), 34. https://doi.org/10.3390/jof5020034 google scholar
  • Hacioglu, M., Tan, A. S. B., Dosler, S., Inan, N., & Otuk, G. (2018). In vitro activities of antifungals alone and in combination with tigecycline against Candida albicans biofilms. PeerJ, 6, e5263. https://doi.org/10.7717/peerj.5263 google scholar
  • Hacioglu, M., Guzel, C. B., Savage, P. B., & Tan, A. S. B. (2019a). Antifungal susceptibilities, in vitro production of virulence fac-tors and activities of ceragenins against Candida spp. isolated from vulvovaginal candidiasis. Medical Mycology, 57(3), 291299. https://doi.org/10.1093/mmy/myy023 google scholar
  • Hacioglu, M., Haciosmanoglu, E., Birteksoz-Tan, A. S., Bozkurt-Guzel, C., & Savage, P. B. (2019b). Effects of ceragenins and conventional antimicrobials on Candida albicans and Staphylococcus aureus mono and multispecies biofilms. Di-agnostic Microbiology and Infectious Disease, 95(3), 114863. https://doi.org/10.1016/j.diagmicrobio.2019.06.014 google scholar
  • Hamill, R. J. (2013). Amphotericin B formulations: a compar-ative review of efficacy and toxicity. Drugs, 73, 919-934. https://doi.org/10.1007/s40265- 013-0069-4 google scholar
  • Katragkou, A., McCarthy, M., Alexander, E. L., Antachopou-los, C., Meletiadis, J., Jabra-Rizk, M. A., ... & Walsh, T. J. (2015). In vitro interactions between farnesol and flucona-zole, amphotericin B or micafungin against Candida albicans biofilms. Journal of Antimicrobial Chemotherapy, 70(2), 470-478. https://doi.org/10.1093/jac/dku374 google scholar
  • Malinovskâ, Z., Conkovâ, E., & Vâczi, P. (2023). Biofilm Formation in medically important Candida species. Journal of Fungi, 9(10), 955. https://doi.org/10.3390/jof9100955 google scholar
  • Nami, S., Aghebati-Maleki, A., Morovati, H., & Aghebati-Maleki, L. (2019). Current antifungal drugs and immunotherapeu-tic approaches as promising strategies to treatment of fun-gal diseases. Biomedicine & Pharmacotherapy, 110, 857-868. https://doi.org/10.1016/j.biopha.2018.12.009 google scholar
  • Oyardi, O., Hacioglu, M., Yilmaz, F.N., Inan, N., & Birteksoz Tan, A.S. (2023). Antibiotic susceptibility and biofilm for-mation of multi-drug resistant Gram-negative bacteria. Istan-bul Journal of Pharmacy, 53(1), 45-50. doi: 10.26650/Istan-bulJPharm.2023.1156339 google scholar
  • Ramage, G., Vande Walle, K., Wickes, B. L., & Lopez-Ribot, J. L. (2001). Standardized method for in vitro an-tifungal susceptibility testing of Candida albicans biofilms. Antimicrobial Agents and Chemotherapy, 45(9), 2475-2479. https://doi.org/10.1128/aac.45.9.2475-2479.2001 google scholar
  • Rodrigues, C. F., & Cernakova, L. (2020). Farnesol and ty-rosol: secondary metabolites with a crucial quorum-sensing role in Candida biofilm development. Genes, 11(4), 444. https://doi.org/10.3390/genes11040444 google scholar
  • Sebaa, S., Boucherit-Otmani, Z., & Courtois, P. (2019). Effects of tyrosol and farnesol on Candida albicans biofilm. Molecular Medicine Reports, 19(4), 3201-3209. https://doi.org/10.3892/mmr.2019.9981 google scholar
  • Shanmughapriya, S., Sornakumari, H., Lency, A., Kavitha, S., & Natarajaseenivasan, K. (2014). Synergistic effect of amphotericin B and tyrosol on biofilm formed by Candida krusei and Can-dida tropicalis from intrauterine device users. Medical Mycology, 52(8), 853-861. https://doi.org/10.1093/mmy/myu046 google scholar
  • Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2012). Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and an-tifungal resistance. FEMS Microbiology Reviews, 36(2), 288-305. https://doi.org/10.1111/j.1574-6976.2011.00278.x google scholar
  • Tian, X., Ding, H., Ke, W., & Wang, L. (2021). Quorum sensing in fungal species. Annual Review of Microbiology, 75, 449-469. https://doi.org/10.1146/annurev-micro-060321-045510 google scholar
  • Tobudic, S., Kratzer, C., Lassnigg, A., & Presterl, E. (2012). Antifungal susceptibility of Candida albicans in biofilms. Mycoses, 55(3), 199-204. https://doi.org/10.1111/j.1439-0507.2011.02076.x google scholar
  • Touil, H. F. Z., Boucherit-Otmani, Z., & Boucherit, K. (2018). In vitro activity of antifungal combinations against planktonic and sessile cells of Candida albicans isolated from medical devices in an intensive care department. Journal de Mycologie Medicale, 28(3), 414-418. https://doi.org/10.1016/j.mycmed.2018.06.008 google scholar
  • Weber, K., Sohr, R., Schulz, B., Fleischhacker, M., & Ruhnke, M. (2008). Secretion of E, E-farnesol and biofilm formation in eight different Candida species. Antimicrobial Agents and Chemother-apy, 52(5), 1859-1861. https://doi.org/10.1128/AAC.01646-07 google scholar
  • Yapıcı, M., Gürsu, B. Y., & Dağ, İ. (2021). In vitro antibiofilm efficacy of farnesol against Candida species. International Microbiology, 24(2), 251-262. https://doi.org/10.1007/s10123-021-00162-4 google scholar
Yıl 2024, Cilt: 54 Sayı: 2, 189 - 194, 26.08.2024
https://doi.org/10.26650/IstanbulJPharm.2024.1417841

Öz

Proje Numarası

This work was supported by the Research Fund of Istanbul University [project number 34926].

Kaynakça

  • Albuquerque, P., & Casadevall, A. (2012). Quorum sens-ing in fungi-a review. Medical Mycology, 50(4), 337-345. doi:10.3109/13693786.2011.652201 google scholar
  • Alem, M. A., Oteef, M. D., Flowers, T. H., & Douglas, L. J. (2006). Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryotic Cell, 5(10), 1770-1779. https://doi.org/10.1128/EC.00219-06 google scholar
  • Atiencia-Carrera, M. B., Cabezas-Mera, F. S., Tejera, E., & Machado, A. (2022). Prevalence of biofilms in Candida spp. blood-stream infections: A meta-analysis. PLoS One, 17(2), e0263522. https://doi.org/10.1371/journal.pone.0263522 google scholar
  • Atriwal, T., Azeem, K., Husain, F. M., Hussain, A., Khan, M. N., Alajmi, M. F., & Abid, M. (2021). Mechanistic un-derstanding of Candida albicans biofilm formation and ap-proaches for its inhibition. Frontiers in Microbiology, 12, 638609. https://doi.org/10.3389/fmicb.2021.638609 google scholar
  • Bozkurt-Guzel, C., Hacioglu, M., & Savage, P. B. (2018). Investigation of the in vitro antifungal and antibiofilm activities of ceragenins CSA-8, CSA-13, CSA-44, CSA-131, and CSA-138 against Candida species. Diagnos-tic Microbiology and Infectious Disease, 91(4), 324-330. https://doi.org/10.1016/j.diagmicrobio.2018.03.014 google scholar
  • Brackman, G., & Coenye, T. (2015). Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design, 21(1), 5-11. https://doi.org/10.2174/1381612820666140905114627 google scholar
  • Cavalheiro, M., & Teixeira, M. C. (2018). Candida biofilms: threats, challenges, and promising strategies. Frontiers in Medicine, 5, 28. https://doi.org/10.3389/fmed.2018.00028 google scholar
  • Chin, V. K., Lee, T. Y., Rusliza, B., & Chong, P. P. (2016). Dissecting Candida albicans infection from the perspective of C. albicans virulence and omics approaches on host-pathogen interaction: a review. International Journal of Molecular Sciences, 17(10), 1643. https://doi.org/10.3390/ijms17101643 google scholar
  • Cordeiro, R. D. A., Teixeira, C. E., Brilhante, R. S., Castelo-Branco, D. S., Alencar, L. P., de Oliveira, J. S., ... & Rocha, google scholar
  • M. F. (2015). Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their suscep-tibility to antifungals. FEMS Yeast Research, 15(4), fov012. https://doi.org/10.1093/femsyr/fov012 google scholar
  • De Sordi, L., & Mühlschlegel, F. A. (2009). Quorum sensing and fun-gal-bacterial interactions in Candida albicans: a communicative network regulating microbial coexistence and virulence. FEMS Yeast Research, 9(7), 990-999. https://doi.org/10.1111/j.1567-1364.2009.00573.x google scholar
  • Djordjevic, D., Wiedmann, M., & McLandsborough, L. A. (2002). Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology, 68(6), 2950-2958. doi:10.1128/AEM.68.6.2950-2958.2002 google scholar
  • Fourie, R., & Pohl, C. H. (2019). Beyond antagonism: the interaction between Candida species and Pseudomonas aeruginosa. Journal of Fungi, 5(2), 34. https://doi.org/10.3390/jof5020034 google scholar
  • Hacioglu, M., Tan, A. S. B., Dosler, S., Inan, N., & Otuk, G. (2018). In vitro activities of antifungals alone and in combination with tigecycline against Candida albicans biofilms. PeerJ, 6, e5263. https://doi.org/10.7717/peerj.5263 google scholar
  • Hacioglu, M., Guzel, C. B., Savage, P. B., & Tan, A. S. B. (2019a). Antifungal susceptibilities, in vitro production of virulence fac-tors and activities of ceragenins against Candida spp. isolated from vulvovaginal candidiasis. Medical Mycology, 57(3), 291299. https://doi.org/10.1093/mmy/myy023 google scholar
  • Hacioglu, M., Haciosmanoglu, E., Birteksoz-Tan, A. S., Bozkurt-Guzel, C., & Savage, P. B. (2019b). Effects of ceragenins and conventional antimicrobials on Candida albicans and Staphylococcus aureus mono and multispecies biofilms. Di-agnostic Microbiology and Infectious Disease, 95(3), 114863. https://doi.org/10.1016/j.diagmicrobio.2019.06.014 google scholar
  • Hamill, R. J. (2013). Amphotericin B formulations: a compar-ative review of efficacy and toxicity. Drugs, 73, 919-934. https://doi.org/10.1007/s40265- 013-0069-4 google scholar
  • Katragkou, A., McCarthy, M., Alexander, E. L., Antachopou-los, C., Meletiadis, J., Jabra-Rizk, M. A., ... & Walsh, T. J. (2015). In vitro interactions between farnesol and flucona-zole, amphotericin B or micafungin against Candida albicans biofilms. Journal of Antimicrobial Chemotherapy, 70(2), 470-478. https://doi.org/10.1093/jac/dku374 google scholar
  • Malinovskâ, Z., Conkovâ, E., & Vâczi, P. (2023). Biofilm Formation in medically important Candida species. Journal of Fungi, 9(10), 955. https://doi.org/10.3390/jof9100955 google scholar
  • Nami, S., Aghebati-Maleki, A., Morovati, H., & Aghebati-Maleki, L. (2019). Current antifungal drugs and immunotherapeu-tic approaches as promising strategies to treatment of fun-gal diseases. Biomedicine & Pharmacotherapy, 110, 857-868. https://doi.org/10.1016/j.biopha.2018.12.009 google scholar
  • Oyardi, O., Hacioglu, M., Yilmaz, F.N., Inan, N., & Birteksoz Tan, A.S. (2023). Antibiotic susceptibility and biofilm for-mation of multi-drug resistant Gram-negative bacteria. Istan-bul Journal of Pharmacy, 53(1), 45-50. doi: 10.26650/Istan-bulJPharm.2023.1156339 google scholar
  • Ramage, G., Vande Walle, K., Wickes, B. L., & Lopez-Ribot, J. L. (2001). Standardized method for in vitro an-tifungal susceptibility testing of Candida albicans biofilms. Antimicrobial Agents and Chemotherapy, 45(9), 2475-2479. https://doi.org/10.1128/aac.45.9.2475-2479.2001 google scholar
  • Rodrigues, C. F., & Cernakova, L. (2020). Farnesol and ty-rosol: secondary metabolites with a crucial quorum-sensing role in Candida biofilm development. Genes, 11(4), 444. https://doi.org/10.3390/genes11040444 google scholar
  • Sebaa, S., Boucherit-Otmani, Z., & Courtois, P. (2019). Effects of tyrosol and farnesol on Candida albicans biofilm. Molecular Medicine Reports, 19(4), 3201-3209. https://doi.org/10.3892/mmr.2019.9981 google scholar
  • Shanmughapriya, S., Sornakumari, H., Lency, A., Kavitha, S., & Natarajaseenivasan, K. (2014). Synergistic effect of amphotericin B and tyrosol on biofilm formed by Candida krusei and Can-dida tropicalis from intrauterine device users. Medical Mycology, 52(8), 853-861. https://doi.org/10.1093/mmy/myu046 google scholar
  • Silva, S., Negri, M., Henriques, M., Oliveira, R., Williams, D. W., & Azeredo, J. (2012). Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and an-tifungal resistance. FEMS Microbiology Reviews, 36(2), 288-305. https://doi.org/10.1111/j.1574-6976.2011.00278.x google scholar
  • Tian, X., Ding, H., Ke, W., & Wang, L. (2021). Quorum sensing in fungal species. Annual Review of Microbiology, 75, 449-469. https://doi.org/10.1146/annurev-micro-060321-045510 google scholar
  • Tobudic, S., Kratzer, C., Lassnigg, A., & Presterl, E. (2012). Antifungal susceptibility of Candida albicans in biofilms. Mycoses, 55(3), 199-204. https://doi.org/10.1111/j.1439-0507.2011.02076.x google scholar
  • Touil, H. F. Z., Boucherit-Otmani, Z., & Boucherit, K. (2018). In vitro activity of antifungal combinations against planktonic and sessile cells of Candida albicans isolated from medical devices in an intensive care department. Journal de Mycologie Medicale, 28(3), 414-418. https://doi.org/10.1016/j.mycmed.2018.06.008 google scholar
  • Weber, K., Sohr, R., Schulz, B., Fleischhacker, M., & Ruhnke, M. (2008). Secretion of E, E-farnesol and biofilm formation in eight different Candida species. Antimicrobial Agents and Chemother-apy, 52(5), 1859-1861. https://doi.org/10.1128/AAC.01646-07 google scholar
  • Yapıcı, M., Gürsu, B. Y., & Dağ, İ. (2021). In vitro antibiofilm efficacy of farnesol against Candida species. International Microbiology, 24(2), 251-262. https://doi.org/10.1007/s10123-021-00162-4 google scholar
Toplam 31 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Farmasotik Mikrobiyoloji
Bölüm Original Article
Yazarlar

Müzeyyen Aydın 0000-0002-8082-9470

Mayram Hacıoğlu 0000-0003-0823-631X

Neşe İnan 0000-0002-1559-6244

Proje Numarası This work was supported by the Research Fund of Istanbul University [project number 34926].
Yayımlanma Tarihi 26 Ağustos 2024
Gönderilme Tarihi 12 Ocak 2024
Kabul Tarihi 26 Mart 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 54 Sayı: 2

Kaynak Göster

APA Aydın, M., Hacıoğlu, M., & İnan, N. (2024). Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B. İstanbul Journal of Pharmacy, 54(2), 189-194. https://doi.org/10.26650/IstanbulJPharm.2024.1417841
AMA Aydın M, Hacıoğlu M, İnan N. Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B. iujp. Ağustos 2024;54(2):189-194. doi:10.26650/IstanbulJPharm.2024.1417841
Chicago Aydın, Müzeyyen, Mayram Hacıoğlu, ve Neşe İnan. “Comparison of the Inhibition of Candida Spp. Biofilm Formation by Quorum-Sensing Molecules, Farnesol and Tyrosol With Amphotericin B”. İstanbul Journal of Pharmacy 54, sy. 2 (Ağustos 2024): 189-94. https://doi.org/10.26650/IstanbulJPharm.2024.1417841.
EndNote Aydın M, Hacıoğlu M, İnan N (01 Ağustos 2024) Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B. İstanbul Journal of Pharmacy 54 2 189–194.
IEEE M. Aydın, M. Hacıoğlu, ve N. İnan, “Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B”, iujp, c. 54, sy. 2, ss. 189–194, 2024, doi: 10.26650/IstanbulJPharm.2024.1417841.
ISNAD Aydın, Müzeyyen vd. “Comparison of the Inhibition of Candida Spp. Biofilm Formation by Quorum-Sensing Molecules, Farnesol and Tyrosol With Amphotericin B”. İstanbul Journal of Pharmacy 54/2 (Ağustos 2024), 189-194. https://doi.org/10.26650/IstanbulJPharm.2024.1417841.
JAMA Aydın M, Hacıoğlu M, İnan N. Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B. iujp. 2024;54:189–194.
MLA Aydın, Müzeyyen vd. “Comparison of the Inhibition of Candida Spp. Biofilm Formation by Quorum-Sensing Molecules, Farnesol and Tyrosol With Amphotericin B”. İstanbul Journal of Pharmacy, c. 54, sy. 2, 2024, ss. 189-94, doi:10.26650/IstanbulJPharm.2024.1417841.
Vancouver Aydın M, Hacıoğlu M, İnan N. Comparison of the inhibition of Candida spp. biofilm formation by quorum-sensing molecules, farnesol and tyrosol with amphotericin B. iujp. 2024;54(2):189-94.