Advances in nano research

Techno-Press (테크노프레스)
권호 표지
DOI QR코드

DOI QR Code

Antioxidative and antiproliferative effects of propolis-reduced silver nanoparticles

  • Tan, Gamze (Department of Biology, Faculty of Science and Letters, Aksaray University) ;
  • Ilk, Sedef (Department of Immunology, Faculty of Medicine, Nigde O mer Halisdemir University) ;
  • Foto, Fatma Z. (Department of Biochemistry, Faculty of Science, Selcuk University) ;
  • Foto, Egemen (Department of Biotechnology, Faculty of Science, Necmettin Erbakan University) ;
  • Saglam, Necdet (Department of Nanotechnology and Nanomedicine, Institute of Science and Engineering, Hacettepe University)
  • Received : 2019.12.22
  • Accepted : 2020.12.08
  • Published : 2021.02.25
⟨ Previous Next ⟩

Abstract

In this study, phytochemicals present in Propolis Extract (PE) were employed as reducing and stabilizing reagents to synthesize silver nanoparticles. Three propolis-reduced silver nanoparticles (P-AgNPs1-3) were synthesized using increasing amounts of PE. P-AgNPs were treated with different cancer cells-lung (A549), cervix (HeLa) and colon (WiDr) - for 24, 48 and 72 h to evaluate their anti-proliferative activities. A non-cancerous cell type (L929) was also used to test whether suppressive effects of P-AgNPs on cancer cell proliferation were due to a general cytotoxic effect. The characterization results showed that the bioactive contents in propolis successfully induced particle formation. As the amount of PE increased, the particle size decreased; however, the size distribution range expanded. The antioxidant capacity of the particles increased with increased propolis amounts. P-AgNP1 exhibited almost equal inhibitory effects across all cancer cell types; however, P-AgNP2 was more effective on HeLa cells. P-AgNPs3 showed greater inhibitory effects in almost all cancer cells compared to other NPs and pure propolis. Consequently, the biological effects of P-AgNPs were highly dependent on PE amount, NP concentration, and cell type. These results suggest that AgNPs synthesized utilizing propolis phytochemicals might serve as anti-cancer agents, providing greater efficacy against cancer cells.

Keywords

Acknowledgement

The authors would like to thank Ph.D. candidate Ezgi Emul for her technical guidance. There are no conflicts of interest.

References

  1. Abdel Raheem, I.A., Abdul Razek, A., Elgendy, A.A., Labah, D.A. and Saleh, N.M. (2020), "Egyptian propolis-loaded nanoparticles as a root canal nanosealer: Sealing ability and in vivo biocompatibility", Int. J. Nanomed., 15, 5265-5277. https://doi.org/10.2147/IJN.S258888.
  2. Arokiyaraj, S., Vincent, S., Saravanan, M., Lee, Y., Oh, Y.K. and Kim, K.H. (2017), "Green synthesis of silver nanoparticles using Rheum palmatum root extract and their antibacterial activity against Staphylococcus aureus and Pseudomonas aeruginosa", Artif. Cells Nanomed. Biotechnol., 45(2), 372-379. https://doi.org/10.3109/21691401.2016.1160403.
  3. Baltas, N., Yildiz, O. and Kolayli, S. (2016), "Inhibition properties of propolis extracts to some clinically important enzymes", J. Enzyme Inhib. Med. Chem., 31, 52-55. https://doi.org/10.3109/14756366.2016.1167049.
  4. Barbosa, V.T., Souza, J.K.C., Alvino, V., Meneghetti, M.R., Florez-Rodriguez, P.P., Moreira, R.E., Paulino, G.V.B., Landell, M.F., Basilio-Junior, I.D., Do Nascimento, T.G., Grillo, L.A.M. and Dornelas, C.B. (2019), "Biogenic synthesis of silver nanoparticles using Brazilian propolis", Biotechnol. Prog., 35(6), 2888. https://doi.org/10.1002/btpr.2888.
  5. Baygar, T. (2020), "Characterization of silk sutures coated with propolis and biogenic silver nanoparticles (AgNPs): An eco-friendly solution with wound healing potential against surgical site infections (SSIs)", Turk. J. Med. Sci., 50(1), 258-266. https://doi.org/10.3906/sag-1906-48.
  6. Benedec, D., Oniga, I., Cuibus, F., Sevastre, B., Stiufiuc, G., Duma, M., Hanganu, D., Iacovita, C., Stiufiuc, R. and Lucaciu, C.M. (2018), "Origanum vulgare mediated green synthesis of biocompatible gold nanoparticles simultaneously possessing plasmonic, antioxidant and antimicrobial properties", Int. J. Nanomed., 13, 1041-1058. https://doi.org/10.2147/IJN.S149819.
  7. Clement, J.L. and Jarrett, P.S. (1994), "Antibacterial silver", Met. Based Drugs, 1(5-6), 467-482. https://doi.org/10.1155/MBD.1994.467.
  8. De Barros, C.H.N., Cruz, G.C.F., Mayrink, W. and Tasic, L. (2018), "Bio-based synthesis of silver nanoparticles from orange waste: effects of distinct biomolecule coatings on size, morphology, and antimicrobial activity", Nanotechnol. Sci. Appl., 11, 1-14. https://doi.org/10.2147/NSA.S156115.
  9. De Figueiredo, S.M., Nogueira-Machado, J.A., Almeida, B.D.M., Abreu, S.R.L., De Abreu, J.A.S., Filho, S.A.V., Binda, N.S. and Caligiorne, R.B. (2014), "Immunomodulatory properties of green propolis", Recent Pat. Endocr. Metab. Immune Drug Discov., 8(2), 85-94. https://doi.org/10.2174/1872214808666140619115319.
  10. Dehpour, A.A., Ebrahimzadeh, M.A., Seyed Fazel, N. and Seyed Mohammad, N. (2009), "Antioxidant activity of the methanol extract of Ferula assafoetida and its essential oil composition", Grasas Aceites, 60(4), 405-412. https://doi.org/10.3989/gya.010109.
  11. Dhas, S.P., Mukerjhee, A. and Chandrasekaran, N. (2013), "Phytosynthesis of silver nanoparticles using Ceriops tagal and its antimicrobial potential against human pathogens", Int. J. Pharm. Pharm. Sci., 5(3), 349-352.
  12. Do Nascimento, T.G., Da Silva, P.F., Azevedo, L.F., Da Rocha, L.G., De Moraes Porto, I.C.C., Lima e Moura, T.F.A., Basilio-Junior, I.D., Grillo, L.A.M., Dornelas, C.B., Fonseca, E.J.D.S., De Jesus Oliveira, E., Zhang, A.T. and Watson, D.G. (2016), "Polymeric nanoparticles of Brazilian red propolis extract: Preparation, characterization, antioxidant and leishmanicidal activity", Nanoscale Res. Lett., 11(301), 1-16. https://doi.org/10.1186/s11671-016-1517-3.
  13. El-Deeb, N.M., El-Sherbiny, I.M., El-Aassara, M.R. and Hafez, E.E. (2015), "Novel trend in colon cancer therapy using silver nanoparticles synthesized by honeybee", J. Nanomed. Nanotechnol., 6(1), 265-271. http://dx.doi.org/10.4172/2157-7439.1000265.
  14. Gardea-Torresdey, J.L., Tiemann, K.J., Gamez, G., Dokken, K., Tehuacanero, S. and Jose-Yacaman, M. (1999), "Gold nanoparticles obtained by bio-precipitation from gold(III) solutions", J. Nanopart. Res., 1(3), 397-404. https://doi.org/10.1023/A:1010008915465.
  15. Gatea, F., Teodor, E.D., Seciu, A.M., Covaci, O.I., Manoiu, S., Lazar, V. and Radu, G.L. (2015), "Antitumour, antimicrobial and catalytic activity of gold nanoparticles synthesized by different pH propolis extracts", J. Nanopart. Res., 17(320), 1-13. https://doi.org/10.1007/s11051-015-3127-x.
  16. Gericke, M. and Pinches, A. (2006), "Microbial production of gold nanoparticles", Gold Bull., 39(1), 22-28. https://doi.org/10.1007/BF03215529.
  17. Gulcelik, N.E., Zeybek, D., Kaymaz, F., Gencay, O., Salih, B., Asan, E., Sorkun, K. and Usman, A. (2012), "Antitumor activity of propolis on differantiated cancer cell lines", Med. Sci., 1(4), 292-300. https://doi.org/10.5455/medscience.2012.01.8029.
  18. Gurunathan, S., Raman, J., Abd Malek, S.N., John, P.A. and Vikineswary, S. (2013), "Green synthesis of silver nanoparticles using Ganoderma neo-japonicum Imazeki: A potential cytotoxic agent against breast cancer cells", Int. J. Nanomed., 8(1), 4399-4413. https://doi.org/10.2147/IJN.S51881.
  19. Hyllested, J.E., Palanco, M.E., Hagen, N., Mogensen, K.B. and Kneipp, K. (2015), "Green preparation and spectroscopic characterization of plasmonic silver nanoparticles using fruits as reducing agents", Beilstein J. Nanotechnol., 6, 293-299. https://doi.org/10.3762/bjnano.6.27.
  20. Karlidag, S.K. and Ferat, G. (2007), "Resin yield of propolis samples produced by different honeybee races and methods", Uludag Bee J., 7(2), 52-58.
  21. Khacha-Ananda, S., Tragoolpua, K., Chantawannakul, P. and Tragoolpua, Y. (2013), "Antioxidant and anti-cancer cell proliferation activity of propolis extracts from two extraction methods", Asian Pac. J. Cancer Prev., 14(11), 6991-6995. https://doi.org/10.7314/apjcp.2013.14.11.6991.
  22. Kim, D.M., Lee, G.D., Aum, S.H. and Kim, H.J. (2008), "Preparation of propolis nanofood and application to human cancer", Biol. Pharm. Bull., 31(9), 1704-1710. https://doi.org/10.1248/bpb.31.1704.
  23. Kim, J.I., Pant, H.R., Sim, H.J., Lee, K.M. and Kim, C.S. (2014), "Electrospun propolis/polyurethane composite nanofibers for biomedical applications", Mater. Sci. Eng. C, 44, 52-57. https://doi.org/10.1016/j.msec.2014.07.062.
  24. Kirby, A.J. and Schmidt, R.J. (1997), "The antioxidant activity of Chinese herbs for eczema and of placebo herbs-I", J. Ethnopharmacol., 56(2), 103-108. https://doi.org/10.1016/S0378-8741(97)01510-9.
  25. othai, S. and Jayanthi, B. (2014), "Anti cancer activity of silver nano particles bio-synthesized using stingless bee propolis (Tetragonula iridipennis) of Tamilnadu", Asian J. Biomed. Pharm. Sci., 4(40), 30-37. https://doi.org/10.15272/ajbps.v4i40.654.
  26. Krishnaraj, C., Jagan, E., Rajasekar, S., Selvakumar, P., Kalaichelvan, P. and Mohan, N. (2010), "Synthesis of silver nanoparticles using Acalypha indica leaf extracts and its antibacterial activity against water borne pathogens", Colloids Surf. B, 76(1), 50-56. https://doi.org/10.1016/j.colsurfb.2009.10.008.
  27. Matei, P.M., Martin-Ramos, P., Sanchez-Bascones, M., Hernandez-Navarro, S., Correa-Guimaraes, A., Navas-Gracia, L.M., Rufino, C.A., Ramos-Sanchez, M.C. and Martin-Gil, J. (2015), "Synthesis of chitosan oligomers/propolis/silver nanoparticles composite systems and study of their activity against Diplodia seriata", Int. J. Polym. Sci., 2015, 1-11. https://doi.org/10.1155/2015/864729.
  28. Mittal, A.K., Chisti, Y. and Banerjee, U.C. (2013), "Synthesis of metallic nanoparticles using plant extracts", Biotechnol. Adv., 31(2), 346-356. https://doi.org/10.1016/j.biotechadv.2013.01.003.
  29. Mukherjee, S., Chowdhury, D., Kotcherlakota, R., Patra, S., Vinothkumar, B., Bhadra, M.P., Sreedhar, B. and Patra, C.R. (2014), "Potential theranostics application of bio-synthesized silver nanoparticles (4-in-1 system)", Theranostics, 4(3), 316-335. https://doi.org/10.7150/thno.7819.
  30. Orsolic, N. and Basic, I. (2003), "Immunomodulation by water-soluble derivative of propolis: a factor of antitumor reactivity", J. Ethnopharmacol., 84(2-3), 265-273. https://doi.org/10.1016/S0378-8741(02)00329-X.
  31. Ozgen, M., Reese, R.N., Tulio, A.Z., Scheerens, J.C. and Miller, A. R. (2006), "Modified 2,2-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2,2-diphenyl-1-picryl-hydrazyl (DPPH) methods", J. Agric. Food Chem., 54(4), 1151-1157. https://doi.org/10.1021/jf051960d.
  32. Parolia, A., Kumar, H., Ramamurthy, S., Davamani, F. and Pau, A. (2020), "Effectiveness of chitosan-propolis nanoparticle against Enterococcus faecalis biofilms in the root canal", BMC Oral Health, 20, 339. https://doi.org/10.1186/s12903-020-01330-0.
  33. Patel, S. (2016), "Emerging adjuvant therapy for cancer: propolis and its constituents", J. Diet. Suppl., 13(3), 245-268. https://doi.org/10.3109/19390211.2015.1008614.
  34. Patil, S., Desai, N., Mahadik, K. and Paradkar, A. (2015), "Can green synthesized propolis loaded silver nanoparticulate gel enhance wound healing caused by burns?", Eur. J. Integr. Med., 7(3), 243-250. https://doi.org/10.1016/j.eujim.2015.03.002.
  35. Prior, R.L., Wu, X. and Schaich, K. (2005), "Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements", J. Agric. Food Chem., 53(10), 4290-4302. https://doi.org/10.1021/jf0502698.
  36. Priyadarshini, J.F., Sivakumari, K., Selvaraj, R., Ashok, K., Jayaprakash, P. and Rajesh, S. (2018), "Green synthesis of silver nanoparticles from propolis", Res. J. Life Sci. Bioinform. Pharm. Chem. Sci., 4(4), 23-36. https://doi.org/10.26479/2018.0404.02.
  37. Roy, N., Mondal, S., Laskar, R.A., Basu, S., Mandal, D. and Begum, N.A. (2010), "Biogenic synthesis of Au and Ag nanoparticles by Indian propolis and its constituents", Colloids Surf. B, 76(1), 317-325. https://doi.org/10.1016/j.colsurfb.2009.11.011.
  38. Ryaidh, S. and Al-Qayim, M. (2017), "Bio-synthesis and characterizations of magnetic iron oxide nanoparticles mediated by Iraq propolis extract", IOSR J. Pharm. Biol. Sci., 12(6), 65-73. 10.9790/3008-1206056573.
  39. Saghafi, N., Yousofi, Z., Homaei Shandiz, F., Afzal Aghaee, M. and Javedanmehr, M. (2015), "Comparison of efficacy and side effects of propolis with chemotherapy and chemotherapy alone for neoadjuant therapy of ovarian cancer", Iran. J. Obstet. Gynecol. Infertil., 18(146), 1-5.
  40. Sahin, B., Demir, E., Aygun, A., Gunduz, H. and Sen, F. (2017), "Investigation of the effect of pomegranate extract and monodisperse silver nanoparticle combination on MCF-7 cell line", J. Biotechnol., 260, 79-83. https://doi.org/10.1016/j.jbiotec.2017.09.012.
  41. Sathishkumar, M., Sneha, K., Kwak, I.S., Mao, J., Tripathy, S.J. and Yun, Y.S. (2009), "Phyto-crystallization of palladium through reduction process using Cinnamom zeylanicum bark extract", J. Hazard. Mater., 171(1-3), 400-404. https://doi.org/10.1016/j.jhazmat.2009.06.014.
  42. Shubharani, R., Mahesh, M. and Murthy, V.N.Y. (2019), "Biosynthesis and characterization, antioxidant and antimicrobial activities of selenium nanoparticles from ethanol extract of bee propolis", J. Nanomed. Nanotechnol., 10(1), 522. https://doi.org/10.4172/2157-7439.1000522.
  43. Skandalis, N., Dimopoulou, A., Georgopoulou, A., Gallios, N., Papadopoulos, D., Tsipas, D., Theologidis, I., Michailidis, N. and Chatzinikolaidou, M. (2017), "The effect of silver nanoparticles size, produced using plant extract from Arbutus unedo, on their antibacterial efficacy", Nanomaterials, 7(178), 1-14. https://doi.org/10.3390/nano7070178.
  44. Sosa, I.O., Noguez, C. and Barrera, R. G. (2003), "Optical properties of metal nanoparticles with arbitrary shapes", J. Phys. Chem. B, 107(26), 6269-6275. https://doi.org/10.1021/jp0274076.
  45. Suarez, D., Zayas, D. and Guisado, F. (2005), "Propolis: Patents and technology trends for health applications", J. Bus. Chem., 2(3), 119-125.
  46. Tan, G., Saglam, S., Emul, E., Erdonmez, D. and Saglam, N. (2016), "Synthesis and characterization of silver nanoparticles integrated in polyvinyl alcohol nanofibers for bionanotechnological applications", Turk. J. Biol., 40(3), 643-651. https://doi.org/10.3906/biy-1505-71.
  47. Tepe, B., Daferera, D., Sokmen, A., Sokmen, M. and Polissiou, M. (2005), "Antimicrobial and antioxidant activities of the essential oil and various extracts of Salvia tomentosa Miller (Lamiaceae)", Food Chem., 90(3), 333-340. https://doi.org/10.1016/j.foodchem.2003.09.013.
  48. Toreti, V.C., Sato, H.H., Pastore, G.M. and Park, Y.K. (2013), "Recent progress of propolis for its biological and chemical compositions and its botanical origin", Evid. Based Complementary Altern. Med., 2013, 1-13. https://doi.org/10.1155/2013/697390.
  49. Turan, I., Demir, S., Misir, S., Kilinc, K., Mentese, A., Aliyazicioglu, Y. and Deger, O. (2015), "Cytotoxic effect of Turkish propolis on liver, colon, breast, cervix and prostate cancer cell lines", Trop. J. Pharm. Res., 14(5), 777-782. http://dx.doi.org/10.4314/tjpr.v14i5.5.
  50. Vatansever, H.S., Sorkun, K., Gurhan, S.I.D., Ozdal-Kurt, F., Turkoz, E., Gencay, O. and Salih, B. (2010), "Propolis from Turkey induces apoptosis through activating caspases in human breast carcinoma cell lines", Acta Histochem., 112(6), 546-556. https://doi.org/10.1016/j.acthis.2009.06.001.
  51. Vichai, V. and Kirtikara, K. (2006), "Sulforhodamine B colorimetric assay for cytotoxicity screening", Nat. Protoc., 1, 1112. https://doi.org/10.1038/nprot.2006.179.
  52. Wasukan, N., Srisung, S., Kulthong, K., Boonrungsiman, S. and Maniratanachote, R. (2015), "Determination of silver in personal care nanoproducts and effects on dermal exposure", J. Nanopart. Res., 17(11), 1-11. https://doi.org/10.1007/s11051-015-3220-1.