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Amoebicidal and Cytotoxic Activity of Propolis collected from Different Regions in Turkey on Acanthamoeba castellanii Trophozoites

Year 2023, Volume: 9 Issue: 2, 312 - 324, 31.05.2023
https://doi.org/10.19127/mbsjohs.1253511

Abstract

Objective: The present study aimed to investigate the amoebicidal effects of propolis collected from different regions in Turkey on Acanthamoeba trophozoites.

Method: The propolis was collected from different geographic sites (Van, Erzurum, Gümüşhane, Ordu, Rize, and Muğla) in Turkey. Different concentrations of propolis ethanolic extract (in quantities from 1, 2, 3, 4, 5, 6, 7, and 8 mg/mL) and the same volume of trophozoites in 100 μl culture were blended for the identification of the amoebicidal efficiency of propolis.

Results: The growth of trophozoites stopped in Turkish propolis extracts with 50% inhibitory concentrations (IC50)/48h for 5 mg/mL extract solution. Propolis showed more potent inhibitory effects on Acanthamoeba trophozoites at concentrations of 7, 6, 5, 4, and 3 mg/mL for 72 h. Propolis extract substantially inhibited human bronchial epithelial cells, especially at higher concentrations (7, 8, and 16 mg/mL).
Propolis can kill Acanthamoeba trophozoites at a concentration (of 3-6 mg/mL) but is safe for human bronchial epithelial cells at the same concentrations after 72 h treatment, this paves the way for propolis to be an alternative source of therapeutic drugs in the treatment of Acanthamoeba spp.

Conclusion: Acanthamoeba infection still cannot be treated with drugs. In this study, propolis collected from different regions of Turkey showed amoebic and cytotoxic activities. Propolis extract, which is a natural product that can be used against Acanthamoeba trophozoites can be an alternative source of therapeutic drugs in the treatment of Acanthamoeba, supported by in vivo studies.

References

  • 1. Przybyłek I, Karpiński TM. Antibacterial Properties of Propolis. Molecules. 2019; 24(11):2047.
  • 2. Duran G, Duran N, Culha G, Ozcan B, Oztas H, Ozer B. In vitro antileishmanial activity of Adana propolis samples on Leishmania tropica: a preliminary study. Parasitol Res. 2008; 102:1217-1225.
  • 3. Bankova V. Chemical diversity of propolis and the problem of standardization. J Ethnopharmacol. 2005; 100:114-117.
  • 4. Nina N, Quispe C, Jiménez-Aspee F, Theoduloz C, Feresín GE, Lima B, Leiva E. Schmeda-Hirschmann, G. Antibacterial activity, antioxidant effect and chemical composition of propolis from the Región del Maule, Central Chile. Molecules. 2015; 20: 18144–18167.
  • 5. De Mendonca IC, Porto IC, do Nascimento TG, de Souza NS, Oliveira JM, Arruda RE, Mousinho KC, dos Santos AF, Basilio-Junior ID, Parolia A, Barreto FS. Brazilian red propolis: phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complement Altern Med. 2015; 15:357.
  • 6. Olczyk P, Wisowski G, Komosinska-Vassev K, Stojko J, Klimek K, Olczyk M, Kozma EM. Propolis modifies collagen types I and III accumulation in the matrix of burnt tissue. Evid Based Complementary Altern Med. 2013:423809.
  • 7. Topalkara A, Vural A, Polat Z, Toker MI, Arici MK, Ozan F, Cetin A. In vitro amoebicidal activity of propolis on Acanthamoeba castellanii. J Ocul Pharmacol Ther. 2007; 23:40-45.
  • 8. Asfaram S, Fakhar M, Keighobadi M, Akhtari J. Promising Anti-Protozoan Activities of Propolis (Bee Glue) as Natural Product: A Review. Acta Parasit. 2021; 66: 1–12.
  • 9. Dağcı H, Gül S, Emre S, Türk M, Sönmez G, Tünger A, Yağcı A. Planned interchangeable soft contact lenses Acanthamoeba and bacterial contamination. J Infect. 2001;15:357-362.
  • 10. Kaynak B, Koloren Z, Karaman U. Investigation of In Vitro Amoebicidal Activities of Trachystemon orientalis on Acanthamoeba castellanii Cysts and Trophozoites. Van Med J. 2019; 26 (4):483-490.
  • 11. Baldemir A, Karaman Ü, Yusufbeyoğlu S, Eken A, Ildız N, İlgün S, Çolak C, Kaçmaz G, Öçsoy İ, Çankaya S. A new strategy for enhancing acanthamoebicidal activity with synthesis of nanoflower of Laurocerausus officinalis roemer (Cherry laurel) fruit extracts. Mikrobiyol Bul. 2018; 52(1):56-71.
  • 12. Malatyali E, Tepe B, Degerli S, Berk S. In vitro amoebicidal activities of Satureja cuneifolia and Melissa officinalis on Acanthamoeba castellanii cysts and trophozoites. Parasitol Res. 2012; 110(6): 2175-2180.
  • 13. Tepe B, Malatyali E, Degerli S, Berk, S. In vitro amoebicidal activities of Teucrium polium and T. chamaedrys on Acanthamoeba castellanii trophozoites and cysts. Parasitol Res. 2012; 110(5):1773-1778.
  • 14. Mohamed H., Marusich E, Afanasev Y, Leonov S. Fatty acids-enriched fractions of Hermetia illucens (Black soldier fly) larvae fat can combat MDR pathogenic fish bacteria Aeromonas spp. Int J Mol Sci. 2021; 22, 8829.
  • 15. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983; 65(1-2):55-63.
  • 16. Natarajan K, Singh S, Burke TR, Jr. Grunberger D., and Aggarwal, B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. The Proceedings of the National Academy of Sciences (PNAS). 1996; 93, 9090-9095.
  • 17. Banskota AH, Tezuka Y, Kadota S. Recent progress in pharmacological research of propolis. Phytother Res. 2001; 15:561-571.
  • 18. Bueno-Silva B, Alencar SM, Koo H, Ikegaki M, Silva GV, Napimoga MH, Rosalen PL Anti-inflammatory and antimicrobial evaluation of neovestitol and vestitol isolated from Brazilian red propolis. J Agric Food Chem. 2013; 61:4546-4550.
  • 19. Sforcin JM, Bankova V, Kuropatnicki AK. Medical benefits of honeybee products. Evid Based Complementary Altern Med. 2017; 2702106.
  • 20. Brito GAB, Chaves MH. β- amyrin, a natural triterpenoidameliorates L-arginine-induced acute pancreatitis in rats. World J Gastroenterol. 2010; 16:4272-4280.
  • 21. Bankova V. New biologically active compounds from Kenyan propolis. Fitoterapia. 2010; 81:509-514.
  • 22. Sforcin JM. Biological properties and therapeutic applications of propolis. Phytother Res. 2016; 30:894-905.
  • 23. Dewi LK, Sahlan M, Pratami DK, Agus A, Agussalim Sabir A. Identifying propolis compounds potential to be covid-19 therapies by targeting sars-cov-2 main protease. Int J Appl Pharm. 2021;13:103-110.
  • 24. Vural A, Polat ZA, Topalkara A, Toker MI, Erdogan H, Arici MK, Cetin A. The effect of propolis in experimental Acanthamoeba keratitis. Clin Exp Ophthalmol. 2007; 35:749-754.
  • 25. Duran G, Duran N, Culha G, Ozcan B, Oztas H, Ozer B. In vitro antileishmanial activity of Adana propolis samples on Leishmania tropica: a preliminary study. Parasitol Res. 2008; 102:1217–1225.
  • 26. Duran N, Muz M, Culha G, Duran G, Ozer B. GC-MS analysis and antileishmanial activities of two Turkish propolis types. Parasitol Res. 2011; 108:95-105.
  • 27. Almuhayawi MS. Propolis as a novel antibacterial agent. Saudi J Biol Sci. 2020; 27:3079-3086.
  • 28. Ma X, Guo Z, Zhang Z, Li X, Wang X, Liu Y, Wang X Ferulic acid isolated from propolis inhibits porcine parvovirus replication potentially through Bid-mediate apoptosis. Int Immunopharmacoly. 2020; 83.
  • 29. De Castro PA, Bom VLP, Brown NA, de Almeida RSC, Ramalho LNZ, Savoldi M, Goldman MHS, Berretta AA, Goldman GH. Identification of the cell targets important for propolis-induced cell death in Candida albicans. Fungal Genet Biol. 2013; 60:74-86.
  • 30. Antwi CA, Amisigo CM, Adjimani JP, Gwira TM. In vitro activity and mode of action of phenolic compounds on leishmania donovani. PLoS Negl Trop Dis. 2019;13(2):e0007206.
  • 31. Kılıç Altun, S Aydemir, ME. Phenolic characterization of some propolis samples of Anatolia. Bahri Dağdaş Hayvancılık Araştırma Dergisi. 2020; 9(2): 97-104
  • 32. Coşkun I, Duymaz GM, Dastan T, Sonmezer OE, Acar S, Akyıldız E, Raday S. The characterization and bioactive composition of Turkish propolis. Apiterapi ve Doğa Dergisi, 2018; 1(3): 39-39 33. Sorucu A, Oruç HH. Determination of biologically active phenolic compounds in propolis by LC–MS/MS according to seasons and altitudes. Journal of Food Measurement and Characterization. 2019; 13(3): 2461-2469.
  • 34. Celińska-Janowicz K, Zaręba I, Lazarek U, Teul J, Tomczyk M, Pałka J, Miltyk W. Constituents of propolis: chrysin, caffeic acid, p-coumaric acid, and ferulic acid ınduce PRODH/POX-Dependent apoptosis in human tongue squamous cell carcinoma cell (CAL-27). Front Pharmacol. 2018; 9:336.
  • 35. Mirza AC, Panchal SS. Safety assessment of vanillic acid: Subacute oral toxicity studies in Wistar rats. Turkish Journal of Pharmaceutical Science. 2020;17(4), 432.
  • 36. Ozkul Y, Silici S, Eroğlu E. The anticarcinogenic effect of propolis in human lymphocyte culture. Phytomedicine 2005; 12(10):742-747.
  • 37. Ozkul Y, Eroglu HE, Ok E. Genotoxic potential of Turkish propolis in peripheral blood lymphocytes. Pharmazie, 2006; 61(7):638-640.
  • 38. Demir S, Aliyazicioglu Y, Turan I, Misir S, Mentese A, Yaman SO, Akbulut K, Kilinc K, Deger O. Antiproliferative and proapoptotic activity of Turkish propolis on human lung cancer cell line. Nutr Cancer. 2016; 68:165-172.
  • 39. Seyhan MF, Yılmaz E, Timirci-Kahraman Ö, Saygılı N, Kısakesen Hİ, Gazioğlu S, Gören AC, Eronat AP, Ceviz AB, Öztürk T, Yılmaz-Aydoğan H, Öztürk O. Different propolis samples, phenolic content, and breast cancer cell lines: Variable cytotoxicity ranging from ineffective to potent. IUBMB Life. 2019; 71(5):619-631.
  • 40. Ilhan-Ayisigi E, Ulucan F, Saygili E, Saglam-Metiner P, Gulce-Iz S, Yesil-Celiktas O. Nano-vesicular formulation of propolis and cytotoxic effects in a 3D spheroid model of lung cancer. J Sci Food
Year 2023, Volume: 9 Issue: 2, 312 - 324, 31.05.2023
https://doi.org/10.19127/mbsjohs.1253511

Abstract

References

  • 1. Przybyłek I, Karpiński TM. Antibacterial Properties of Propolis. Molecules. 2019; 24(11):2047.
  • 2. Duran G, Duran N, Culha G, Ozcan B, Oztas H, Ozer B. In vitro antileishmanial activity of Adana propolis samples on Leishmania tropica: a preliminary study. Parasitol Res. 2008; 102:1217-1225.
  • 3. Bankova V. Chemical diversity of propolis and the problem of standardization. J Ethnopharmacol. 2005; 100:114-117.
  • 4. Nina N, Quispe C, Jiménez-Aspee F, Theoduloz C, Feresín GE, Lima B, Leiva E. Schmeda-Hirschmann, G. Antibacterial activity, antioxidant effect and chemical composition of propolis from the Región del Maule, Central Chile. Molecules. 2015; 20: 18144–18167.
  • 5. De Mendonca IC, Porto IC, do Nascimento TG, de Souza NS, Oliveira JM, Arruda RE, Mousinho KC, dos Santos AF, Basilio-Junior ID, Parolia A, Barreto FS. Brazilian red propolis: phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complement Altern Med. 2015; 15:357.
  • 6. Olczyk P, Wisowski G, Komosinska-Vassev K, Stojko J, Klimek K, Olczyk M, Kozma EM. Propolis modifies collagen types I and III accumulation in the matrix of burnt tissue. Evid Based Complementary Altern Med. 2013:423809.
  • 7. Topalkara A, Vural A, Polat Z, Toker MI, Arici MK, Ozan F, Cetin A. In vitro amoebicidal activity of propolis on Acanthamoeba castellanii. J Ocul Pharmacol Ther. 2007; 23:40-45.
  • 8. Asfaram S, Fakhar M, Keighobadi M, Akhtari J. Promising Anti-Protozoan Activities of Propolis (Bee Glue) as Natural Product: A Review. Acta Parasit. 2021; 66: 1–12.
  • 9. Dağcı H, Gül S, Emre S, Türk M, Sönmez G, Tünger A, Yağcı A. Planned interchangeable soft contact lenses Acanthamoeba and bacterial contamination. J Infect. 2001;15:357-362.
  • 10. Kaynak B, Koloren Z, Karaman U. Investigation of In Vitro Amoebicidal Activities of Trachystemon orientalis on Acanthamoeba castellanii Cysts and Trophozoites. Van Med J. 2019; 26 (4):483-490.
  • 11. Baldemir A, Karaman Ü, Yusufbeyoğlu S, Eken A, Ildız N, İlgün S, Çolak C, Kaçmaz G, Öçsoy İ, Çankaya S. A new strategy for enhancing acanthamoebicidal activity with synthesis of nanoflower of Laurocerausus officinalis roemer (Cherry laurel) fruit extracts. Mikrobiyol Bul. 2018; 52(1):56-71.
  • 12. Malatyali E, Tepe B, Degerli S, Berk S. In vitro amoebicidal activities of Satureja cuneifolia and Melissa officinalis on Acanthamoeba castellanii cysts and trophozoites. Parasitol Res. 2012; 110(6): 2175-2180.
  • 13. Tepe B, Malatyali E, Degerli S, Berk, S. In vitro amoebicidal activities of Teucrium polium and T. chamaedrys on Acanthamoeba castellanii trophozoites and cysts. Parasitol Res. 2012; 110(5):1773-1778.
  • 14. Mohamed H., Marusich E, Afanasev Y, Leonov S. Fatty acids-enriched fractions of Hermetia illucens (Black soldier fly) larvae fat can combat MDR pathogenic fish bacteria Aeromonas spp. Int J Mol Sci. 2021; 22, 8829.
  • 15. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983; 65(1-2):55-63.
  • 16. Natarajan K, Singh S, Burke TR, Jr. Grunberger D., and Aggarwal, B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. The Proceedings of the National Academy of Sciences (PNAS). 1996; 93, 9090-9095.
  • 17. Banskota AH, Tezuka Y, Kadota S. Recent progress in pharmacological research of propolis. Phytother Res. 2001; 15:561-571.
  • 18. Bueno-Silva B, Alencar SM, Koo H, Ikegaki M, Silva GV, Napimoga MH, Rosalen PL Anti-inflammatory and antimicrobial evaluation of neovestitol and vestitol isolated from Brazilian red propolis. J Agric Food Chem. 2013; 61:4546-4550.
  • 19. Sforcin JM, Bankova V, Kuropatnicki AK. Medical benefits of honeybee products. Evid Based Complementary Altern Med. 2017; 2702106.
  • 20. Brito GAB, Chaves MH. β- amyrin, a natural triterpenoidameliorates L-arginine-induced acute pancreatitis in rats. World J Gastroenterol. 2010; 16:4272-4280.
  • 21. Bankova V. New biologically active compounds from Kenyan propolis. Fitoterapia. 2010; 81:509-514.
  • 22. Sforcin JM. Biological properties and therapeutic applications of propolis. Phytother Res. 2016; 30:894-905.
  • 23. Dewi LK, Sahlan M, Pratami DK, Agus A, Agussalim Sabir A. Identifying propolis compounds potential to be covid-19 therapies by targeting sars-cov-2 main protease. Int J Appl Pharm. 2021;13:103-110.
  • 24. Vural A, Polat ZA, Topalkara A, Toker MI, Erdogan H, Arici MK, Cetin A. The effect of propolis in experimental Acanthamoeba keratitis. Clin Exp Ophthalmol. 2007; 35:749-754.
  • 25. Duran G, Duran N, Culha G, Ozcan B, Oztas H, Ozer B. In vitro antileishmanial activity of Adana propolis samples on Leishmania tropica: a preliminary study. Parasitol Res. 2008; 102:1217–1225.
  • 26. Duran N, Muz M, Culha G, Duran G, Ozer B. GC-MS analysis and antileishmanial activities of two Turkish propolis types. Parasitol Res. 2011; 108:95-105.
  • 27. Almuhayawi MS. Propolis as a novel antibacterial agent. Saudi J Biol Sci. 2020; 27:3079-3086.
  • 28. Ma X, Guo Z, Zhang Z, Li X, Wang X, Liu Y, Wang X Ferulic acid isolated from propolis inhibits porcine parvovirus replication potentially through Bid-mediate apoptosis. Int Immunopharmacoly. 2020; 83.
  • 29. De Castro PA, Bom VLP, Brown NA, de Almeida RSC, Ramalho LNZ, Savoldi M, Goldman MHS, Berretta AA, Goldman GH. Identification of the cell targets important for propolis-induced cell death in Candida albicans. Fungal Genet Biol. 2013; 60:74-86.
  • 30. Antwi CA, Amisigo CM, Adjimani JP, Gwira TM. In vitro activity and mode of action of phenolic compounds on leishmania donovani. PLoS Negl Trop Dis. 2019;13(2):e0007206.
  • 31. Kılıç Altun, S Aydemir, ME. Phenolic characterization of some propolis samples of Anatolia. Bahri Dağdaş Hayvancılık Araştırma Dergisi. 2020; 9(2): 97-104
  • 32. Coşkun I, Duymaz GM, Dastan T, Sonmezer OE, Acar S, Akyıldız E, Raday S. The characterization and bioactive composition of Turkish propolis. Apiterapi ve Doğa Dergisi, 2018; 1(3): 39-39 33. Sorucu A, Oruç HH. Determination of biologically active phenolic compounds in propolis by LC–MS/MS according to seasons and altitudes. Journal of Food Measurement and Characterization. 2019; 13(3): 2461-2469.
  • 34. Celińska-Janowicz K, Zaręba I, Lazarek U, Teul J, Tomczyk M, Pałka J, Miltyk W. Constituents of propolis: chrysin, caffeic acid, p-coumaric acid, and ferulic acid ınduce PRODH/POX-Dependent apoptosis in human tongue squamous cell carcinoma cell (CAL-27). Front Pharmacol. 2018; 9:336.
  • 35. Mirza AC, Panchal SS. Safety assessment of vanillic acid: Subacute oral toxicity studies in Wistar rats. Turkish Journal of Pharmaceutical Science. 2020;17(4), 432.
  • 36. Ozkul Y, Silici S, Eroğlu E. The anticarcinogenic effect of propolis in human lymphocyte culture. Phytomedicine 2005; 12(10):742-747.
  • 37. Ozkul Y, Eroglu HE, Ok E. Genotoxic potential of Turkish propolis in peripheral blood lymphocytes. Pharmazie, 2006; 61(7):638-640.
  • 38. Demir S, Aliyazicioglu Y, Turan I, Misir S, Mentese A, Yaman SO, Akbulut K, Kilinc K, Deger O. Antiproliferative and proapoptotic activity of Turkish propolis on human lung cancer cell line. Nutr Cancer. 2016; 68:165-172.
  • 39. Seyhan MF, Yılmaz E, Timirci-Kahraman Ö, Saygılı N, Kısakesen Hİ, Gazioğlu S, Gören AC, Eronat AP, Ceviz AB, Öztürk T, Yılmaz-Aydoğan H, Öztürk O. Different propolis samples, phenolic content, and breast cancer cell lines: Variable cytotoxicity ranging from ineffective to potent. IUBMB Life. 2019; 71(5):619-631.
  • 40. Ilhan-Ayisigi E, Ulucan F, Saygili E, Saglam-Metiner P, Gulce-Iz S, Yesil-Celiktas O. Nano-vesicular formulation of propolis and cytotoxic effects in a 3D spheroid model of lung cancer. J Sci Food
There are 39 citations in total.

Details

Primary Language English
Subjects Health Care Administration
Journal Section Research articles
Authors

Zeynep Koloren 0000-0001-9708-2716

Ömer Ertürk 0000-0001-5837-6893

Zülal Atlı Şekeroğlu 0000-0002-3552-3819

Ülkü Karaman 0000-0001-7027-1613

Publication Date May 31, 2023
Published in Issue Year 2023 Volume: 9 Issue: 2

Cite

Vancouver Koloren Z, Ertürk Ö, Atlı Şekeroğlu Z, Karaman Ü. Amoebicidal and Cytotoxic Activity of Propolis collected from Different Regions in Turkey on Acanthamoeba castellanii Trophozoites. Mid Blac Sea J Health Sci. 2023;9(2):312-24.

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