Processing of liposome-encapsulated natural herbs derived from Silybum marianum plants for the treatment of breast cancer cells

Document Type : Article

Authors

1 Institute for Nanoscience & Nanotechnology (INST), Sharif University of Technology, Azadi Avenue, 14588 Tehran, P.O. Box 11155-9466, Iran

2 - Department of Toxicology and Pharmacology, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran - Toxicology and Poisoning Research Centre, Tehran University of Medical Sciences, Tehran, Iran

3 - Institute for Nanoscience & Nanotechnology (INST), Sharif University of Technology, Azadi Avenue, 14588 Tehran, P.O. Box 11155-9466, Iran - Department of Materials Science and Engineering, Sharif University of Technology, Azadi Avenue, 14588 Tehran, P.O. Box 11155-9466, Iran

Abstract

It has been long known that Silibinin, a naturally derived herbal phytochemical, is an effective drug for the treatment of toxic thyroid damage; however, its role in cancer treatment is still not approved and is under investigation. Besides, due to the poor water solubility and bioavailability of Silibinin and the side effects that drug payloads cause, its delivery to the point of care with a controlled release rate is challenging. In this work, we propose a protocol to prepare liposome-encapsulated Silibinin (LES) with the ability to produce reactive oxygen species (ROS) for the treatment of MCF-7 breast cancer cells. Spherical-shaped LES nanoparticles with an average size of 60 nm and narrow size distribution (PDI=0.11) were synthesized by the thin film hydration method. Studies of the pharmacokinetics showed that a burst release occurred during the first 12 h that was followed by a sustained release over the next 12 days. MTT assays and the analysis of the drug effect determined that LES nanoparticles displayed a significant cytotoxic effect to kill breast cancer cells. IC50 values for LES nanoparticles were experimentally determined to be 20 μМ which was significantly lower than that of the pristine drug (38 μМ).....

Keywords

References

References:
1. Balmain, A. "Cancer genetics: from Boveri and Mendel to microarrays", Nat. Rev. Cancer, 1(1), pp. 77-82 (2001). DOI: 10.1038/35094086.
2. Siegel, R.L., Miller, K.D., Fuchs, H.E., et al. "Cancer statistics, 2022", CA. Cancer J. Clin., 72(1), pp. 7-33 (2022). DOI: https://doi.org/10.3322/caac.21708.
3. Nyst, H.J., Tan, I.B., Stewart, F.A., et al. "Is photodynamic therapy a good alternative to surgery and radiotherapy in the treatment of head and neck cancer?", Photodiagnosis Photodyn. Ther., 6(1), pp. 3-11 (2009). DOI: https://doi.org/10.1016/j.pdpdt.2009.03.002.
4. Nguyen, M.-H., Pham, N.-D., Dong, B., et al. "Radioprotective activity of curcumin-encapsulated liposomes against genotoxicity caused by Gamma Cobalt-60 irradiation in human blood cells", Int. J. Radiat. Biol., 93(11), pp. 1267-1273 (Nov. 2017). DOI: 10.1080/09553002.2017.1380329.
5. Batta, A., Kalra, B.S., and Khirasaria, R. "Trends in FDA drug approvals over last 2 decades: An observational study.", J. Fam. Med. Prim. Care, 9(1), pp. 105-114 (Jan. 2020). DOI: 10.4103/jfmpc.jfmpc 578 19.
6. Makovec, T. "Cisplatin and beyond: molecular mechanisms of action and drug resistance development in cancer chemotherapy", Radiol. Oncol., 53(2), pp. 148- 158 (2019). DOI: 10.2478/raon-2019-0018.
7. Lin, K.H., Rutter, J.C., Xie, A., et al. "Using antagonistic pleiotropy to design a chemotherapy-induced evolutionary trap to target drug resistance in cancer", Nat. Genet., 52(4), pp. 408-417 (2020). DOI:10.1038/s41588-020-0590-9.
8. Leary, M., Heerboth, S., Lapinska, K., et al. "Sensitization of drug resistant cancer cells: A matter of combination therapy", Cancers, 10(12), pp. 483-501 (2018). DOI: 10.3390/cancers10120483.
9. Mathur, P., Rawal, S., Patel, B., et al. "Oral delivery of anticancer agents using nanoparticulate drug delivery system", Curr. Drug Metab., 20(14), pp. 1132-1140 (2019). DOI: 10.2174/1389200220666191007154017.
10. Agarwal, C., Singh, R.P., Dhanalakshmi, S., et al. "Silibinin upregulates the expression of cyclindependent kinase inhibitors and causes cell cycle arrest and apoptosis in human colon carcinoma HT-29 cells", Oncogene, 22(51), pp. 8271-8282 (2003). DOI:10.1038/sj.onc.1207158.
11. Dheeraj, A., Tailor, D., Singh, S.P., et al. "Chapter 10 - Anticancer Attributes of Silibinin: Chemoand Radiosensitization of Cancer", in Cancer Sensitizing Agents for Chemotherapy, 2, A.C. Bharti and B.B. Aggarwal, Eds., Academic Press, pp. 199-
220 (2018). DOI: https://doi.org/10.1016/B978-0-12-812373-7.00010-3.
12. Taheri, M., Ghafouri-Fard, S., Najafi, S., et al. "Hormonal regulation of telomerase activity and hTERT expression in steroid-regulated tissues and cancer", Cancer Cell Int., 22(1), p. 258 (2022). DOI:10.1186/s12935-022-02678-9.
13. Tiwari, P. and Mishra, K. "Silibinin in cancer therapy: A promising prospect", Cancer Res. Front., 1(3), pp.303-318 (2015). DOI: 10.17980/2015.303.
14. Takke, A. and Shende, P. "Nanotherapeutic silibinin: An insight of phytomedicine in healthcare reformation", Nanomedicine Nanotechnology, Biol. Med., 21, p. 102057 (2019). DOI: https://doi.org/10.1016/j.nano.2019.102057.
15. Hamdy, R., Mostafa, A., Abo Shama, N.M., et al. "Comparative evaluation of  avonoids reveals the superiority and promising inhibition activity of silibinin against SARS-CoV-2", Phyther. Res., 36(7), pp. 2921-2939 (Jul. 2022). DOI: https://doi.org/10.1002/ptr.7486.
16. Yazdi Rouholamini, S.E., Moghassemi, S., Maharat, Z., et al. "Effect of silibinin-loaded nanoniosomal coated with trimethyl chitosan on miRNAs expression in 2D and 3D models of T47D breast cancer cell line", Artif. Cells, Nanomedicine, Biotechnol., 46(3), pp. 524-535 (May 2018). DOI: 10.1080/21691401.2017.1326928.
17. Bajpai, S., Tiwary, S.K., Sonker, M., et al. "Recent advances in nanoparticle-based cancer treatment: A review", ACS Appl. Nano Mater., 4(7), pp. 6441-6470(Jul. 2021). DOI: 10.1021/acsanm.1c00779.
18. Alamdari, S.G., Amini, M., Jalilzadeh, N., et al. "Recent advances in nanoparticle-based photothermal therapy for breast cancer", J. Control. Release, 349, pp. 269-303 (2022). DOI: https://doi.org/10.1016/j.jconrel.2022.06.050.
19. Gupta, B. and Kim, J.O. "Recent progress in cancer immunotherapy approaches based on nanoparticle delivery devices", J. Pharm. Investig., 51(4), pp. 399- 412 (2021). DOI: 10.1007/s40005-021-00527-x.
20. Pivetta, T.P., Botteon, C.E.A., Ribeiro, P.A., et al. "Nanoparticle systems for cancer phototherapy: An overview", Nanomaterials, 11(11), pp. 3132-3169(2021). DOI: 10.3390/nano11113132.
21. Dang, Y. and Guan, J. "Nanoparticle-based drug delivery systems for cancer therapy", Smart Mater. Med., 1, pp. 10-19 (2020). DOI:https://doi.org/10.1016/j.smaim.2020.04.001.
22. Ebrahimnezhad, Z., Zarghami, N., Keyhani, M., et al. "Inhibition of hTERT gene expression by silibininloaded PLGA-PEG-Fe3O4 in T47D breast cancer cell line", Bioimpacts, 3(2), pp. 67-74 (2013). DOI:10.5681/bi.2013.005.
23. Varghese, L., Agarwal, C., Tyagi, A., et al. "Silibinin efficacy against human hepatocellular carcinoma", Clin. Cancer Res. an Off. J. Am. Assoc. Cancer Res., 11(23), pp. 8441-8448 (Dec. 2005). DOI:10.1158/1078-0432.CCR-05-1646.
24. Ferreira, D.D.S., Faria, S.D., Lopes, S.C. de A., et al."Development of a bone-targeted pH-sensitive liposomal formulation containing doxorubicin: physicochemicalcharacterization, cytotoxicity, and biodistribution evaluation in a mouse model of bone metastasis", Int. J. Nanomedicine, 11, pp. 3737-3751 (Aug. 2016). DOI: 10.2147/IJN.S109966.
25. Rao, X., Huang, X., Zhou, Z., et al. "An improvement of the 2 (-delta delta CT) method for quantitative realtime polymerase chain reaction data analysis", Biostat. Bioinforma. Biomath., 3(3), pp. 71-85 (Aug. 2013).
26. Ge, L., Shao, W., Zhang, Y., et al. "RNAi targeting of hTERT gene expression induces apoptosis and inhibits the proliferation of lung cancer cells", Oncol. Lett., 2(6), pp. 1121-1129 (Nov. 2011). DOI: 10.3892/ol.2011.388.
27. Xiang, B. and Cao, D.-Y., Preparation of Drug Liposomes by Thin-Film Hydration and Homogenization BT- Liposome-Based Drug Delivery Systems, W.-L. Lu and X.-R. Qi, Eds. Berlin, Heidelberg: Springer, Berlin Heidelberg, pp. 25-35 (2021). DOI: 10.1007/978-3-662- 49320-5 2.
28. Bashyal, S., Seo, J.-E., Keum, T., et al. "Development, characterization, and Ex vivo assessment of elastic liposomes for enhancing the buccal delivery of insulin", Pharmaceutics, 13(4), pp. 565-581 (2021).DOI: 10.3390/pharmaceutics13040565.
29. Sang, R., Stratton, B., Engel, A., et al. "Liposome technologies towards colorectal cancer therapeutics", Acta Biomater., 127, pp. 24-40 (2021). DOI:https://doi.org/10.1016/j.actbio.2021.03.055.
30. Gabizon, A.A. "Liposome circulation time and tumor targeting: implications for cancer chemotherapy", Adv. Drug Deliv. Rev., 16(2), pp. 285-294 (1995).DOI: https://doi.org/10.1016/0169-409X(95)00030-B.
31. Liu, D., Mori, A., and Huang, L. "Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes", Biochim. Biophys. Acta, 1104(1), pp. 95-101 (Feb. 1992). DOI:10.1016/0005-2736(92)90136-a.
32. Hu, Y.-J., Ju, R.-J., Zeng, F., et al., Liposomes in Drug Delivery: Status and Advances BT - Liposome-Based Drug Delivery Systems, W.-L. Lu and X.-R. Qi,Eds., Berlin, Heidelberg: Springer Berlin Heidelberg,pp. 3-24 (2021). DOI: 10.1007/978-3-662-49320-5 1.
33. Tavakoli, F., Jahanban-Esfahlan, R., Seidi, K., et al. "Effects of nano-encapsulated curcumin-chrysin on telomerase, MMPs and TIMPs gene expression in mouse B16F10 melanoma tumour model", Artif. Cells, Nanomedicine, Biotechnol., 46(sup2), pp. 75-86 (Nov. 2018). DOI: 10.1080/21691401.2018.1452021.
34. Petrini, M., Lokerse, W.J.M., Mach, A., et al. "Effects of surface charge, PEGylation and functionalization with dipalmitoyl phosphatidyldiglycerol on liposomecell interactions and local drug delivery to solid tumors via thermosensitive liposomes", Int. J. Nanomedicine, 16, pp. 4045-4061 (2021). DOI: 10.2147/IJN.S305106.
35. Lotfi-Attari, J., Pilehvar-Soltanahmadi, Y., Dadashpour, M., et al. "Co-delivery of curcumin and chrysin by polymeric nanoparticles inhibit synergistically growth and hTERT gene expression in human colorectal cancer cells", Nutr. Cancer, 69(8), pp. 1290- 1299 (2017). DOI: 10.1080/01635581.2017.1367932.
36. Subhan, M.A., Yalamarty, S.S.K., Filipczak, N., et al. "Recent advances in tumor targeting via EPR effect for cancer treatment", J. Pers. Med., 11(6) (Jun. 2021). DOI: 10.3390/jpm11060571.
37. Sahibzada, M.U.K., Sadiq, A., Khan, S., et al. "Fabrication, characterization and in vitro evaluation of silibinin nanoparticles: an attempt to enhance its oral bioavailability.", Drug Des. Devel. Ther., 11, pp. 1453-1464 (2017). DOI: 10.2147/DDDT.S133806.
38. Ghalehkhondabi, V., Soleymani, M., and Fazlali, A. "Folate-targeted nano-micelles containing silibinin as an active drug delivery system for liver cancer therapy", J. Drug Deliv. Sci. Technol., 61, p. 102157 (2021). DOI: https://doi.org/10.1016/j.jddst.2020.102157.
39. Wu, J.-W., Lin, L.-C., Hung, S.-C., et al. "Analysis of silibinin in rat plasma and bile for hepatobiliary excretion and oral bioavailability application", J. Pharm. Biomed. Anal., 45(4), pp. 635-641 (2007).DOI: https://doi.org/10.1016/j.jpba.2007.06.026.
40. Trucillo, P. "Drug carriers: classification, administration, release profiles, and industrial approach", Processes, 9(3), pp. 470-488 (2021). DOI: 10.3390/pr9030470.
41. De Leo, V., Milano, F., Agostiano, A., et al. "Recent advancements in polymer/liposome assembly for drug delivery: From surface modifications to hybrid vesicles", Polymers, 13(7), pp. 1027-1051 (2021). DOI:10.3390/polym13071027.
42. Sawaftah, N.A., Paul, V., Awad, N., et al. "Modeling of anti-cancer drug release kinetics from liposomes and micelles: A review", IEEE Trans. Nanobioscience, 20(4), pp. 565-576 (2021). DOI: 10.1109/TNB.2021.3097909.
43. Large, D.E., Abdelmessih, R.G., Fink, E.A., et al. "Liposome composition in drug delivery design, synthesis, characterization, and clinical application", Adv. Drug Deliv. Rev., 176, p. 113851 (2021). DOI:https://doi.org/10.1016/j.addr.2021.113851.
44. Guimaraes, D., Cavaco-Paulo, A., and Nogueira, E., "Design of liposomes as drug delivery system for therapeutic applications", Int. J. Pharm., 601, p. 120571 (2021). DOI: https://doi.org/10.1016/j.ijpharm.2021.120571.
45. Chatran, M., Pilehvar-Soltanahmadi, Y., Dadashpour, M., et al. "Synergistic anti-proliferative effects of metformin and silibinin combination on T47D breast cancer cells via hTERT and cyclin D1 inhibition", Drug Res. (Stuttg)., 68(12), pp. 710-716 (Dec. 2018). DOI: 10.1055/a-0631-8046.
46. Javidfar, S., Pilehvar-Soltanahmadi, Y., Farajzadeh, R., et al. "The inhibitory effects of nanoencapsulated metformin on growth and hTERT expression in breast cancer cells", J. Drug Deliv. Sci. Technol., 43, pp. 19-26 (2018). DOI: https://doi.org/10.1016/j.jddst.2017.09.013.
47. Kim, S.-H., Kim, K.-Y., Yu, S.-N., et al. "Silibinin induces mitochondrial NOX4-mediated endoplasmic reticulum stress response and its subsequent apoptosis", BMC Cancer, 16(1), p. 452 (2016). DOI:10.1186/s12885-016-2516-6.
48. Zheng, N., Liu, L., Liu, W., et al. "Crosstalk of ROS/RNS and autophagy in silibinin-induced apoptosis of MCF-7 human breast cancer cells in vitro", Acta Pharmacol. Sin., 38(2), pp. 277-289 (2017). DOI: 10.1038/aps.2016.117.
49. Tsai, C.-C., Chuang, T.-W., Chen, L.-J., et al. "Increase in apoptosis by combination of metformin with silibinin in human colorectal cancer cells", World J. Gastroenterol., 21(14), pp. 4169-4177 (Apr. 2015).DOI: 10.3748/wjg.v21.i14.4169.
50. Hardwick, J.M. and Soane, L. "Multiple functions of BCL-2 family proteins", Cold Spring Harb. Perspect. Biol., 5(2), pp. 1-22 (2013). DOI: 10.1101/cshperspect. a008722.
51. Warren, C.F.A., Wong-Brown, M.W., and Bowden, N.A. "BCL-2 family isoforms in apoptosis and cancer", Cell Death Dis., 10(3), p. 177 (2019). DOI:10.1038/s41419-019-1407-6.
52. Brentnall, M., Rodriguez-Menocal, L., De Guevara, R.L., et al. "Caspase-9, caspase-3 and caspase-7 have distinct roles during intrinsic apoptosis", BMC Cell Biol., 14(1), p. 32 (2013). DOI: 10.1186/1471-2121-14-32.
53. Allan, L.A. and Clarke, P.R. "Apoptosis and autophagy: Regulation of caspase-9 by phosphorylation", FEBS J., 276(21), pp. 6063-6073 (Nov. 2009). DOI:https://doi.org/10.1111/j.1742-4658.2009.07330.x.
54. Asadi, M., Shanehbandi, D., Asvadi Kermani, T., et al. "Expression level of caspase genes in colorectal cancer", Asian Pac. J. Cancer Prev., 19(5), pp. 1277-1280 (May 2018). DOI: 10.22034/APJCP.2018.19.5.1277.
55. Jelinek, M., Balusikova, K., Schmiedlova, M., et al. "The role of individual caspases in cell death induction by taxanes in breast cancer cells", Cancer Cell Int., 15(1), p. 8 (2015). DOI: 10.1186/s12935-015-0155-7.
56. Russo, A., Cardile, V., Graziano, A.C.E., et al.  Involvement of Bax and Bcl-2 in induction of apoptosis by essential oils of three Lebanese salvia species in human prostate cancer cells", Int. J. Mol. Sci., 19(1) (Jan. 2018). DOI: 10.3390/ijms19010292.
57. Carneiro, B.A. and El-Deiry, W.S. "Targeting apoptosis in cancer therapy", Nat. Rev. Clin. Oncol., 17(7), pp. 395-417 (Jul. 2020). DOI: 10.1038/s41571-020-0341-y.
58. Zavari-Nematabad, A., Alizadeh-Ghodsi, M., Hamishehkar, H., et al. "Development of quantum-dotencapsulated liposome-based optical nanobiosensor for detection of telomerase activity without target amplification", Anal. Bioanal. Chem., 409(5), pp. 1301-1310 (Feb. 2017). DOI: 10.1007/s00216-016-0058-z.
59. Pirmoradi, S., Fathi, E., Farahzadi, R., et al. "Curcumin affects adipose tissue-derived mesenchymal stem cell aging through TERT gene expression", Drug Res. (Stuttg)., 68(4), pp. 213-221 (Apr. 2018). DOI:10.1055/s-0043-119635.
60. Liang, Q., Wang, X., and Chen, T. "Resveratrol protects rabbit articular chondrocyte against sodium nitroprusside-induced apoptosis via scavenging ROS", Apoptosis, 19(9), pp. 1354-1363 (Sep. 2014). DOI:10.1007/s10495-014-1012-1.
Scientia Iranica
Volume 29, Issue 6 - Serial Number 6
Transactions on Nanotechnology (F)
November and December 2022
Pages 3619-3627

Files

History

  • Receive Date: 04 September 2022
  • Accept Date: 19 September 2022

Share

How to cite

Statistics