10.1007/s40204-021-00178-z

Fe3O4 nanoparticles coated with carboxymethyl chitosan containing curcumin in combination with hyperthermia induced apoptosis in breast cancer cells

  1. Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, IR
  2. Department of Polymer and Color Engineering, Amirkabir University of Technology, Tehran, IR
  3. Department of Nanobiotechnology, Pasteur Institute of Iran, Tehran, IR

Published in Issue 2022-01-13

How to Cite

Pazouki, N., Irani, S., Olov, N., Atyabi, S. M., & Bagheri-Khoulenjani, S. (2022). Fe3O4 nanoparticles coated with carboxymethyl chitosan containing curcumin in combination with hyperthermia induced apoptosis in breast cancer cells. Progress in Biomaterials, 11(1 (March 2022). https://doi.org/10.1007/s40204-021-00178-z

Abstract

Abstract Many studies have demonstrated that curcumin has potential anticancer properties. This research aims to study the effect of iron (II, III) oxide (Fe 3 O 4 ) nanoparticles coated with carboxymethyl chitosan containing curcumin combination with hyperthermia on breast cancer cells. Magnetic nanoparticles coated with carboxymethyl chitosan containing curcumin (MNP-CMC-CUR) were prepared and specified. MCF-7, MDA-MB-231, and human fibroblast cells were treated with free curcumin and MNP-CMC-CUR at concentrations of 0–60 µM and at different time points. A combined therapy of MNP-CMC-CUR and hyperthermia was performed on MCF-7 cells. The cytotoxicity of curcumin and MNP-CMC-CUR combined with hyperthermia was assessed by MTT. The changes in TP53 and CASPASE3 gene expression were evaluated using real-time PCR. Both cell apoptosis and cell cycle were studied by Annexin/PI staining. The results of MTT showed that the IC 50 amount of MNP-CMC-CUR has significantly decreased compared to free curcumin ( p  < 0.05) and MNP-CMC-CUR in combination with the hyperthermia, and significantly reducing the metabolic activity of the cells ( p  < 0.05). Real-time PCR results revealed the up-regulation of TP53 and CASPASE3 ( p  < 0.05). The combinational therapy-induced cell apoptosis (64.51%) and sub-G1 cell cycle were arrested in MCF-7 cells. Based on these observations, a combination of MNP-CMC-CUR with hyperthermia could inhibit the proliferation of MCF-7 cells.

Keywords

  • Curcumin,
  • Breast cancer,
  • Carboxymethyl chitosan,
  • Magnetic nanoparticle,
  • Hyperthermia

References

  1. Ali and Smiley (2018) Curcumin induces apoptosis via the capase-8 activated extrinsic pathway in MDA-MB-231 breast cancer cells (pp. 664-666) https://doi.org/10.1096/fasebj.2018.32.1_supplement.664.6
  2. Banerjee et al. (2016) Role of nanoparticle size, shape and surface chemistry in oral drug delivery https://doi.org/10.1016/j.jconrel.2016.07.051
  3. Bani et al. (2019) Casein-coated iron oxide nanoparticles for in vitro hyperthermia for cancer therapy 9(2) (pp. 1-10) https://doi.org/10.1142/S2010324719400034
  4. Barahuie et al. (2017) Sustained release of anticancer agent phytic acid from its chitosan-coated magnetic nanoparticles for drug-delivery system https://doi.org/10.2147/IJN.S126245
  5. Boice and Bouchier-Hayes (2020) Targeting apoptotic caspases in cancer https://doi.org/10.1016/j.bbamcr.2020.118688
  6. Chang et al. (2018) Biologically targeted magnetic hyperthermia: potential and limitations https://doi.org/10.3389/fphar.2018.00831
  7. Dhanavel et al. (2017) In vitro cytotoxicity study of dual drug loaded chitosan/palladium nanocomposite towards HT-29 cancer cells https://doi.org/10.1016/j.msec.2017.03.058
  8. Espinosa et al. (2016) Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment https://doi.org/10.1021/acsnano.5b07249
  9. Gao et al. (2015) Heat stress inhibits proliferation, promotes growth, and induces apoptosis in cultured Lantang swine skeletal muscle satellite cells https://doi.org/10.1631/jzus.B1400339
  10. Gu et al. (2020) Magnetic hyperthermia with ϵ-Fe2O3 nanoparticles 10(48) (pp. 28786-28797) https://doi.org/10.1039/d0ra04361c
  11. Hallman et al. (2017) The effects of turmeric (Curcumin) on tumor suppressor protein (p53) and estrogen receptor (ERα) in breast cancer cells (pp. 153-161) https://doi.org/10.2147/BCTT.S125783
  12. Heydari et al. (2015) Magnetic fluid hyperthermia in a cylindrical gel contains water flow 15(5) (pp. 1-16) https://doi.org/10.1142/S0219519415500888
  13. Hossen et al. (2019) Smart nanocarrier-based drug delivery systems for cancer therapy and toxicity studies: a review (pp. 1-18) https://doi.org/10.1016/j.jare.2018.06.005
  14. Hou et al. (2014) Hyperthermia induces apoptosis through endoplasmic reticulum and reactive oxygen species in human Osteosarcoma cells https://doi.org/10.3390/ijms151017380
  15. Jose et al. (2020) Magnetic nanoparticles for hyperthermia in cancer treatment: an emerging tool 27(16) (pp. 19214-19225) https://doi.org/10.1007/s11356-019-07231-2
  16. Khan et al. (2016) Characterization and anti-proliferative activity of curcumin loaded chitosan nanoparticles in cervical cancer https://doi.org/10.1016/j.ijbiomac.2016.08.050
  17. Khan et al. (2017) Polymeric nano-encapsulation of curcumin enhances its anticancer activity in breast (MDA-MB231) and lung (A549) cancer cells through reduction in expression of hif-1α and nuclear p65 (Rel A) https://doi.org/10.2174/1567201814666171019104002
  18. Klochkov et al. (2021) Implications of nanotechnology for the treatment of cancer: recent advances 69(August) (pp. 190-199) https://doi.org/10.1016/j.semcancer.2019.08.028
  19. Laffon B, Fernández-bertólez N, Costa C, Brandão F, Teixeira JP, Pásaro E, Valdiglesias V (2018) Cellular and molecular toxicity of iron oxide nanoparticles. In: Saquib Q, Faisal M, Al-Khedhairy A, Alatar A (eds) Cellular and Molecular Toxicology of Nanoparticles. Advances in Experimental Medicine and Biology, vol 1048. Springer, Cham
  20. Liao et al. (2019) Synergistic action of microwave-induced mild hyperthermia and paclitaxel in inducing apoptosis in the human breast cancer cell line MCF-7 https://doi.org/10.3892/ol.2018.9629
  21. Manso et al. (2021) Plant natural compounds in the treatment of adrenocortical tumors (pp. 1-18) https://doi.org/10.1155/2021/5516285
  22. Mansouri et al. (2020) Clinical effects of curcumin in enhancing cancer therapy: a systematic review (pp. 1-11) https://doi.org/10.1186/s12885-020-07256-8
  23. Materón et al. (2021) Magnetic nanoparticles in biomedical applications: a review https://doi.org/10.1016/j.apsadv.2021.100163
  24. Miller et al. (2019) Cancer treatment and survivorship statistics, 2019 https://doi.org/10.3322/caac.21565
  25. Minaei et al. (2019) In vitro anticancer efficacy of multi-functionalized magnetite nanoparticles combining alternating magnetic hyperthermia in glioblastoma cancer cells 101(April) (pp. 575-587) https://doi.org/10.1016/j.msec.2019.04.007
  26. Mirakabad et al. (2016) A Comparison between the cytotoxic effects of pure curcumin and curcumin-loaded PLGA-PEG nanoparticles on the MCF-7 human breast cancer cell line https://doi.org/10.3109/21691401.2014.955108
  27. Mirzaie et al. (2016) Docetaxel-Chitosan nanoparticles for breast cancer treatment: cell viability and gene expression study https://doi.org/10.1111/cbdd.12814
  28. Moideen et al. (2021) Preparation of soluble complex of curcumin for the potential antagonistic effects on human colorectal adenocarcinoma cells https://doi.org/10.3390/ph14090939
  29. Mortezaee and Rosengren (2019) Mechanisms of apoptosis modulation by curcumin: implications for cancer therapy https://doi.org/10.1002/jcp.28122
  30. Olanipekun et al. (2021) Comparative studies of chitosan and carboxymethyl chitosan doped with nickel and copper: characterization and antibacterial potential 183(March) (pp. 1971-1977) https://doi.org/10.1016/j.ijbiomac.2021.05.162
  31. Ozkan et al. (2020) The anti-proliferative and apoptotic effects of curcumin on feline mammary gland tumor cells in vitro
  32. Parsian et al. (2016) Loading of Gemcitabine on chitosan magnetic nanoparticles increases the anticancer efficacy of the drug https://doi.org/10.1016/j.ejphar.2016.05.016
  33. Pham et al. (2016) Synthesis and characterization of chitosan-coated magnetite nanoparticles and their application in curcumin drug delivery https://doi.org/10.1088/2043-6262/7/4/045010
  34. Rao et al. (2014) Thermally responsive nanoparticle-encapsulated curcumin and its combination with mild hyperthermia for enhanced cancer cell destruction https://doi.org/10.1016/j.actbio.2013.10.020
  35. Salatin et al. (2015) Effect of the surface modification, size, and shape on cellular uptake of nanoparticles https://doi.org/10.1002/cbin.10459
  36. Sanhaji et al. (2019) The phenotype of target pancreatic cancer cells influences cell death by magnetic hyperthermia with nanoparticles carrying gemicitabine and the pseudo-peptide NucAnt https://doi.org/10.1016/j.nano.2018.12.019
  37. Saxena et al. (2021) Antibacterial nano-biocomposite scaffolds of Chitosan, Carboxymethyl Cellulose and Zn & Fe integrated Hydroxyapatite (Chitosan-CMC-FZO@HAp) for bone tissue engineering 28(14) (pp. 9207-9226) https://doi.org/10.1007/s10570-021-04072-6
  38. Shariatinia (2018) Carboxymethyl chitosan: Properties and biomedical applications (pp. 1406-1419) https://doi.org/10.1016/j.ijbiomac.2018.09.131
  39. Subramani et al. (2017) Curcumin nanotechnologies and its anticancer activity https://doi.org/10.1080/01635581.2017.1285405
  40. Sun et al. (2018) Mechanistic study of nonivamide enhancement of hyperthermia-induced apoptosis in U937 cells https://doi.org/10.1016/j.freeradbiomed.2018.03.017
  41. Vakili-Ghartavol et al. (2020) Toxicity assessment of superparamagnetic iron oxide nanoparticles in different tissues 48(1) (pp. 443-451) https://doi.org/10.1080/21691401.2019.1709855
  42. Valencia et al. (2017) The role of genetic testing in patients with breast cancer a review https://doi.org/10.1001/jamasurg.2017.0552
  43. Waks and Winer (2019) Breast cancer treatment: a review 321(3) (pp. 288-300) https://doi.org/10.1001/jama.2018.19323
  44. Wong et al. (2019) Curcumin nanoformulations for colorectal cancer: a review https://doi.org/10.3389/fphar.2019.00152
  45. Yahya and Alqadhi (2021) Recent trends in cancer therapy: a review on the current state of gene delivery 269(December 2020) https://doi.org/10.1016/j.lfs.2021.119087
  46. Yalcin and Gündüz (2021) Iron oxide-based polymeric magnetic nanoparticles for drug and gene delivery: in vitro and in vivo applications in cancer https://doi.org/10.1007/978-3-030-40513-7_38
  47. Zavisova et al. (2019) Effect of magnetic nanoparticles coating on cell proliferation and uptake https://doi.org/10.1016/j.jmmm.2018.09.116
  48. Zhou et al. (2012) The targets of curcumin https://doi.org/10.2174/138945011794815356
  49. Zhou et al. (2019) Mutant p53 in cancer therapy-the barrier or the path (pp. 293-305) https://doi.org/10.1093/jmcb/mjy072
  50. Zou et al. (2015) Doxorubicin-loaded mesoporous magnetic nanoparticles to induce apoptosis in breast cancer cells https://doi.org/10.1016/j.biopha.2014.12.012