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Teriflunomide Loaded SPION Nanoparticles Induced Apoptosis in MDA-MB-231 Breast Cancer Cells

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Abstract

Introduction

Teriflunomide (TFN), an immunomodulatory drug, has demonstrated cytotoxic effects in recent studies. This potential can be combined with nano-drug delivery to achieve an improved anticancer formulation.

Methods

In this study, super paramagnetic iron oxide nanoparticles (SPIONs) were coated with polydopamine (PD-SPIONs) and used to deliver TFN to the breast cancer cell lines, MDA-MB-231 and MCF-7. Nanoparticles were characterized in terms of size, polydispersity index, zeta potential, morphology. The cytotoxicity of PD-SPIONs, free-TFN and TFN loaded PD-SPIONs was investigated on the cell lines. MDA-MB-231 cells were examined for TP53 and BAX gene expression, cellular apoptosis, and cell cycle analysis.

Methods

In this study, super paramagnetic iron oxide nanoparticles (SPIONs) were coated with polydopamine (PD-SPIONs) and used to deliver TFN to the breast cancer cell lines, MDA-MB-231 and MCF-7. Nanoparticles were characterized in terms of size, polydispersity index, zeta potential, morphology. The cytotoxicity of PD-SPIONs, free-TFN and TFN loaded PD-SPIONs was investigated on the cell lines. MDA-MB-231 cells were examined for TP53 and BAX gene expression, cellular apoptosis, and cell cycle analysis.

Results

Nanoparticles with the size of 163 ± 8 nm and zeta potential of − 38 ± 4 mv were obtained. In comparison to cells treated with free-TFN, cells treated with TFN loaded PD-SPIONs showed significantly higher cytotoxicity. TFN loaded PD-SPIONs treated cells showed significant increase in TP53 (P \(<\) 0.001) and BAX (P \(<\) 0.01) gene expressions compared to free-TFN treated cells. MDA-MB-231 cells also showed an increased percentage of apoptosis and cell cycle arrest in the S and G2 phases.

Conclusion

The designed TFN loaded nanoparticles showed promising potentials that can be considered in future breast cancer therapy research.

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References

  1. H. Sung, J. Ferlay, R. L. Siegel, M. Laversanne, et al. (2021). Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71, 209. https://doi.org/10.3322/caac.21660.

    Article  PubMed  Google Scholar 

  2. Z. Momenimovahed and H. Salehiniya (2019). Epidemiological characteristics of and risk factors for breast cancer in the world. Breast Cancer 11, 151. https://doi.org/10.2147/BCTT.S176070.

    Article  PubMed  PubMed Central  Google Scholar 

  3. WHO. Cancer. 3 February 2022; https://www.who.int/news-room/fact-sheets/detail/cancer

  4. S. Tran, P. J. DeGiovanni, B. Piel, and P. Rai (2017). Cancer nanomedicine: a review of recent success in drug delivery. Clin Transl Med 6, 44. https://doi.org/10.1186/s40169-017-0175-0.

    Article  PubMed  PubMed Central  Google Scholar 

  5. R. Sebastian (2017). Nanomedicine - the future of cancer treatment: a review. J Cancer Prevent Curr Res 8, 1. https://doi.org/10.15406/jcpcr.2017.08.00265.

    Article  CAS  Google Scholar 

  6. A. Jurj, C. Braicu, L. A. Pop, C. Tomuleasa, et al. (2017). The new era of nanotechnology, an alternative to change cancer treatment. Drug Des Devel Ther 11, 2871. https://doi.org/10.2147/DDDT.S142337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. A. C. Anselmo and S. Mitragotri (2016). Nanoparticles in the clinic. Bioeng Transl Med 1, 10. https://doi.org/10.1002/btm2.10003.

    Article  PubMed  PubMed Central  Google Scholar 

  8. J. Kudr, Y. Haddad, L. Richtera, Z. Heger, et al. (2017). Magnetic nanoparticles: from design and synthesis to real world applications. Nanomaterials 7, 9. https://doi.org/10.3390/nano7090243.

    Article  CAS  Google Scholar 

  9. Y. Yao, Y. Zhou, L. Liu, Y. Xu, et al. (2020). Nanoparticle-based drug delivery in cancer therapy and its role in overcoming drug resistance. Front Mol Biosci 2020, 193.

    Article  Google Scholar 

  10. M. I. Anik, M. K. Hossain, I. Hossain, A. Mahfuz, et al. (2021). Recent progress of magnetic nanoparticles in biomedical applications: a review. Nano Select 2, 1146.

    Article  CAS  Google Scholar 

  11. H. Kheiri Manjili, L. Ma’mani, S. Tavaddod, M. Mashhadikhan, et al. (2016). D, L-sulforaphane loaded Fe3O4@ gold core shell nanoparticles: a potential sulforaphane delivery system. PLoS ONE 11, e0151344.

    Article  PubMed  PubMed Central  Google Scholar 

  12. R. Nosrati, K. Abnous, M. Alibolandi, J. Mosafer, et al. (2021). Targeted SPION siderophore conjugate loaded with doxorubicin as a theranostic agent for imaging and treatment of colon carcinoma. Sci Rep 11, 1.

    Article  Google Scholar 

  13. R. A. Revia and M. Zhang (2016). Magnetite nanoparticles for cancer diagnosis, treatment, and treatment monitoring: recent advances. Mater Today (Kidlington) 19, 157. https://doi.org/10.1016/j.mattod.2015.08.022.

    Article  CAS  PubMed  Google Scholar 

  14. R. Hergt, S. Dutz, R. Müller, and M. Zeisberger (2006). Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy. J Phys: Condens Matter 18, S2919.

    CAS  Google Scholar 

  15. N. Singh, G. J. Jenkins, R. Asadi, and S. H. Doak (2010). Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev. https://doi.org/10.3402/nano.v1i0.5358.

    Article  PubMed  PubMed Central  Google Scholar 

  16. R. Kumar, A. Chauhan, S. K. Jha, and B. K. Kuanr (2018). Localized cancer treatment by radio-frequency hyperthermia using magnetic nanoparticles immobilized on graphene oxide: from novel synthesis to in vitro studies. J Mater Chem B 6, 5385. https://doi.org/10.1039/c8tb01365a.

    Article  CAS  PubMed  Google Scholar 

  17. A. S. Arbab, L. B. Wilson, P. Ashari, E. K. Jordan, et al. (2005). A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: implications for cellular magnetic resonance imaging. NMR Biomed 18, 383. https://doi.org/10.1002/nbm.970.

    Article  CAS  PubMed  Google Scholar 

  18. Wahajuddin and S. Arora (2012). Superparamagnetic iron oxide nanoparticles: magnetic nanoplatforms as drug carriers. Int J Nanomed. 7, 3445. https://doi.org/10.2147/ijn.S30320.

    Article  CAS  Google Scholar 

  19. S. M. Mousavi, M. Zarei, and S. A. R. Hashemi (2018). Polydopamine for biomedical application and drug delivery system. Med Chem. https://doi.org/10.4172/2161-0444.1000516.

    Article  Google Scholar 

  20. L. S. Lin, Z. X. Cong, J. B. Cao, K. M. Ke, et al. (2014). Multifunctional Fe(3)O(4)@polydopamine core-shell nanocomposites for intracellular mRNA detection and imaging-guided photothermal therapy. ACS Nano 8, 3876. https://doi.org/10.1021/nn500722y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. P. Gottle, A. Manousi, D. Kremer, L. Reiche, et al. (2018). Teriflunomide promotes oligodendroglial differentiation and myelination. J Neuroinflammation 15, 76. https://doi.org/10.1186/s12974-018-1110-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. J. Oh and P. W. O’Connor (2013). An update of teriflunomide for treatment of multiple sclerosis. Ther Clin Risk Manag 9, 177. https://doi.org/10.2147/TCRM.S30947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. S. Zhu, X. Yan, Z. Xiang, H. F. Ding, et al. (2013). Leflunomide reduces proliferation and induces apoptosis in neuroblastoma cells in vitro and in vivo. PLoS ONE 8, e71555. https://doi.org/10.1371/journal.pone.0071555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. N. Hail, P. Chen, J. Rower, and L. R. Bushman (2010). Teriflunomide encourages cytostatic and apoptotic effects in premalignant and malignant cutaneous keratinocytes. Apoptosis 15, 1234. https://doi.org/10.1007/s10495-010-0518-4.

    Article  CAS  PubMed  Google Scholar 

  25. P. Baumann, S. Mandl-Weber, A. Volkl, C. Adam, et al. (2009). Dihydroorotate dehydrogenase inhibitor A771726 (leflunomide) induces apoptosis and diminishes proliferation of multiple myeloma cells. Mol Cancer Ther 8, 366. https://doi.org/10.1158/1535-7163.MCT-08-0664.

    Article  CAS  PubMed  Google Scholar 

  26. N. Hail, P. Chen, and L. R. Bushman (2010). Teriflunomide (leflunomide) promotes cytostatic, antioxidant, and apoptotic effects in transformed prostate epithelial cells: evidence supporting a role for teriflunomide in prostate cancer chemoprevention. Neoplasia 12, 464. https://doi.org/10.1593/neo.10168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. O. Huang, Z. Xie, W. Zhang, Y. Lou, et al. (2014). A771726, an anti-inflammatory drug, exerts an anticancer effect and reverses tamoxifen resistance in endocrine-resistant breast cancer cells. Oncol Rep 32, 627. https://doi.org/10.3892/or.2014.3249.

    Article  PubMed  Google Scholar 

  28. O. Huang, W. Zhang, Q. Zhi, X. Xue, et al. (2015). Teriflunomide, an immunomodulatory drug, exerts anticancer activity in triple negative breast cancer cells. Exp Biol Med (Maywood) 240, 426. https://doi.org/10.1177/1535370214554881.

    Article  CAS  PubMed  Google Scholar 

  29. A. K. MohamadFairus, B. Choudhary, S. Hosahalli, N. Kavitha, et al. (2017). Dihydroorotate dehydrogenase (DHODH) inhibitors affect ATP depletion, endogenous ROS and mediate S-phase arrest in breast cancer cells. Biochimie 135, 154. https://doi.org/10.1016/j.biochi.2017.02.003.

    Article  CAS  Google Scholar 

  30. M. Ladds, I. M. M. van Leeuwen, C. J. Drummond, S. Chu, et al. (2018). A DHODH inhibitor increases p53 synthesis and enhances tumor cell killing by p53 degradation blockage. Nat Commun 9, 1107. https://doi.org/10.1038/s41467-018-03441-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. M. Gomez-Lazaro, F. J. Fernandez-Gomez, and J. Jordán (2004). p53: twenty five years understanding the mechanism of genome protection. J Physiol Biochem 60, 287. https://doi.org/10.1007/bf03167075.

    Article  CAS  PubMed  Google Scholar 

  32. B. J. Aubrey, G. L. Kelly, A. Janic, M. J. Herold, et al. (2018). How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death Differ 25, 104. https://doi.org/10.1038/cdd.2017.169.

    Article  CAS  PubMed  Google Scholar 

  33. Y. Tsujimoto and S. Shimizu (2000). VDAC regulation by the Bcl-2 family of proteins. Cell Death Differ 7, 1174. https://doi.org/10.1038/sj.cdd.4400780.

    Article  CAS  PubMed  Google Scholar 

  34. H. Nosrati, M. Salehiabar, M. Fridoni, M.-A. Abdollahifar, et al. (2019). New insight about biocompatibility and biodegradability of iron oxide magnetic nanoparticles: stereological and in vivo MRI monitor. Sci Rep 9, 1.

    Article  CAS  Google Scholar 

  35. J. Jiang, X. Sun, Y. Li, C. Deng, et al. (2018). Facile synthesis of Fe3O4@PDA core-shell microspheres functionalized with various metal ions: a systematic comparison of commonly-used metal ions for IMAC enrichment. Talanta 178, 600. https://doi.org/10.1016/j.talanta.2017.09.071.

    Article  CAS  PubMed  Google Scholar 

  36. C.-P. Segeritz and L. Vallier, Cell culture: growing cells as model systems in vitro,. Basic Science Methods for Clinical Researchers. Elsevier, pp 151–172.

    Chapter  Google Scholar 

  37. J. Ye, G. Coulouris, I. Zaretskaya, I. Cutcutache, et al. (2012). Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf 13, 134. https://doi.org/10.1186/1471-2105-13-134.

    Article  CAS  Google Scholar 

  38. H. Singh, J. Du, P. Singh, G. T. Mavlonov, et al. (2018). Development of superparamagnetic iron oxide nanoparticles via direct conjugation with ginsenosides and its in-vitro study. J Photochem Photobiol B 185, 100. https://doi.org/10.1016/j.jphotobiol.2018.05.030.

    Article  CAS  PubMed  Google Scholar 

  39. H. J. Cox, J. Li, P. Saini, J. R. Paterson, et al. (2021). Bioinspired and eco-friendly high efficacy cinnamaldehyde antibacterial surfaces. J Mater Chem B 9, 2918. https://doi.org/10.1039/d0tb02379e.

    Article  CAS  PubMed  Google Scholar 

  40. Y. Wang, S. Wang, H. Niu, Y. Ma, et al. (2013). Preparation of polydopamine coated Fe(3)O(4) nanoparticles and their application for enrichment of polycyclic aromatic hydrocarbons from environmental water samples. J Chromatogr A 1283, 20. https://doi.org/10.1016/j.chroma.2013.01.110.

    Article  CAS  PubMed  Google Scholar 

  41. M. Oroujeni, B. Kaboudin, W. Xia, P. Jönsson, et al. (2018). Conjugation of cyclodextrin to magnetic Fe3O4 nanoparticles via polydopamine coating for drug delivery. Progr Org Coat 114, 154. https://doi.org/10.1016/j.porgcoat.2017.10.007.

    Article  CAS  Google Scholar 

  42. H. Xi, D. Cun, R. Xiang, Y. Guan, et al. (2013). Intra-articular drug delivery from an optimized topical patch containing teriflunomide and lornoxicam for rheumatoid arthritis treatment: does the topical patch really enhance a local treatment? J Control Release 169, 73. https://doi.org/10.1016/j.jconrel.2013.03.028.

    Article  CAS  PubMed  Google Scholar 

  43. J. Kolosnjaj-Tabi and C. Wilhelm (2017). Magnetic nanoparticles in cancer therapy: how can thermal approaches help? Nanomedicine (Lond) 12, 573. https://doi.org/10.2217/nnm-2017-0014.

    Article  CAS  PubMed  Google Scholar 

  44. V. K. Singh, A. Saini, and R. Chandra (2017). The implications and future perspectives of nanomedicine for cancer stem cell targeted therapies. Front Mol Biosci 4, 52. https://doi.org/10.3389/fmolb.2017.00052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. M. J. Ansari, S. A. Jasim, T. Z. Taban, D. O. Bokov, et al. (2022). Anticancer drug-loading capacity of green synthesized porous magnetic iron nanocarrier and cytotoxic effects against human cancer cell line. J Clust Sci 2022, 1.

    Google Scholar 

  46. M. Zhu, G. Nie, H. Meng, T. Xia, et al. (2013). Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Acc Chem Res 46, 622. https://doi.org/10.1021/ar300031y.

    Article  CAS  PubMed  Google Scholar 

  47. P. Foroozandeh and A. A. Aziz (2018). Insight into cellular uptake and intracellular trafficking of nanoparticles. Nanoscale Res Lett 13, 339. https://doi.org/10.1186/s11671-018-2728-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. A. Panariti, G. Miserocchi, and I. Rivolta (2012). The effect of nanoparticle uptake on cellular behavior: disrupting or enabling functions? Nanotechnol Sci Appl 5, 87. https://doi.org/10.2147/nsa.S25515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. J. Rejman, V. Oberle, I. S. Zuhorn, and D. Hoekstra (2004). Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377, 159. https://doi.org/10.1042/bj20031253.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. S. Khoee and K. Hemati (2013). Synthesis of magnetite/polyamino-ester dendrimer based on PCL/PEG amphiphilic copolymers via convergent approach for targeted diagnosis and therapy. Polymer 54, 5574.

    Article  CAS  Google Scholar 

  51. R. Bafkary and S. Khoee (2016). Carbon nanotube-based stimuli-responsive nanocarriers for drug delivery. RSC Adv 6, 82553.

    Article  CAS  Google Scholar 

  52. B. Davodi, M. Jahangiri, and M. Ghorbani (2019). Magnetic Fe3O4@ polydopamine biopolymer: synthesis, characterization and fabrication of promising nanocomposite. J Vinyl Addit Technol 25, 41–47.

    Article  CAS  Google Scholar 

  53. Z. Wang, Y. Duan, and Y. Duan (2018). Application of polydopamine in tumor targeted drug delivery system and its drug release behavior. J Control Release 290, 56–74.

    Article  CAS  PubMed  Google Scholar 

  54. B. Poinard, S. Kamaluddin, A. Q. Q. Tan, K. G. Neoh, et al. (2019). Polydopamine coating enhances mucopenetration and cell uptake of nanoparticles. ACS Appl Mater Interfaces 11, 4777. https://doi.org/10.1021/acsami.8b18107.

    Article  CAS  PubMed  Google Scholar 

  55. Q. Wu, T. Miao, T. Feng, C. Yang, et al. (2018). Dextrancoated superparamagnetic iron oxide nanoparticles activate the MAPK pathway in human primary monocyte cells. Mol Med Rep 18, 564. https://doi.org/10.3892/mmr.2018.8972.

    Article  CAS  PubMed  Google Scholar 

  56. X. Mu, F. Zhang, C. Kong, H. Zhang, et al. (2017). EGFR-targeted delivery of DOX-loaded Fe3O4@ polydopamine multifunctional nanocomposites for MRI and antitumor chemo-photothermal therapy. Int J Nanomed 12, 2899. https://doi.org/10.2147/IJN.S131418.

    Article  CAS  Google Scholar 

  57. A. S. Arbab, L. A. Bashaw, B. R. Miller, E. K. Jordan, et al. (2003). Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229, 838. https://doi.org/10.1148/radiol.2293021215.

    Article  PubMed  Google Scholar 

  58. R. Mrówczyński, J. Jurga-Stopa, R. Markiewicz, E. L. Coy, et al. (2016). Assessment of polydopamine coated magnetic nanoparticles in doxorubicin delivery. RSC Adv 6, 5936. https://doi.org/10.1039/c5ra24222c.

    Article  Google Scholar 

  59. S. Boukalova, S. Hubackova, M. Milosevic, Z. Ezrova, et al. (2020). Dihydroorotate dehydrogenase in oxidative phosphorylation and cancer. Biochim Biophys Acta Mol Basis Dis 1866, 165759. https://doi.org/10.1016/j.bbadis.2020.165759.

    Article  CAS  PubMed  Google Scholar 

  60. M. Löffler, L. D. Fairbanks, E. Zameitat, A. M. Marinaki, et al. (2005). Pyrimidine pathways in health and disease. Trends Mol Med 11, 430. https://doi.org/10.1016/j.molmed.2005.07.003.

    Article  CAS  PubMed  Google Scholar 

  61. A. N. Lane and T. W. Fan (2015). Regulation of mammalian nucleotide metabolism and biosynthesis. Nucleic Acids Res 43, 2466. https://doi.org/10.1093/nar/gkv047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. M. Hosseini, L. Dousset, W. Mahfouf, M. Serrano-Sanchez, et al. (2018). Energy metabolism rewiring precedes UVB-induced primary skin tumor formation. Cell Rep 23, 3621. https://doi.org/10.1016/j.celrep.2018.05.060.

    Article  CAS  PubMed  Google Scholar 

  63. E. A. Corbin, O. O. Adeniba, O. V. Cangellaris, W. P. King, et al. (2017). Evidence of differential mass change rates between human breast cancer cell lines in culture. Biomed Microdev 19, 10. https://doi.org/10.1007/s10544-017-0151-x.

    Article  CAS  Google Scholar 

  64. M. Nedeljković and A. Damjanović (2019). Mechanisms of chemotherapy resistance in triple-negative breast cancer-how we can rise to the challenge. Cells 8, 9. https://doi.org/10.3390/cells8090957.

    Article  CAS  Google Scholar 

  65. M. Ladds and S. Laín (2019). Small molecule activators of the p53 response. J Mol Cell Biol 11, 245. https://doi.org/10.1093/jmcb/mjz006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. J. Chen (2016). The cell-cycle arrest and apoptotic functions of p53 in tumor initiation and progression. Cold Spring Harb Perspect Med 6, a026104. https://doi.org/10.1101/cshperspect.a026104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. W. R. Taylor, S. E. DePrimo, A. Agarwal, M. L. Agarwal, et al. (1999). Mechanisms of G2 arrest in response to overexpression of p53. Mol Biol Cell 10, 3607. https://doi.org/10.1091/mbc.10.11.3607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. D. B. Sykes, Y. S. Kfoury, F. E. Mercier, M. J. Wawer, et al. (2016). Inhibition of dihydroorotate dehydrogenase overcomes differentiation blockade in acute myeloid leukemia. Cell 167, 171. https://doi.org/10.1016/j.cell.2016.08.057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. E. F. O’Donnell, P. R. Kopparapu, D. C. Koch, H. S. Jang, et al. (2012). The aryl hydrocarbon receptor mediates leflunomide-induced growth inhibition of melanoma cells. PLoS ONE 7, e40926. https://doi.org/10.1371/journal.pone.0040926.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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The authors greatly appreciate the staffs of school of Pharmacy, Tehran University of Medical Sciences and Science and Research Branch, Azad Islamic University.

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Rabizadeh, T., Varshochian, R., Mahdieh, A. et al. Teriflunomide Loaded SPION Nanoparticles Induced Apoptosis in MDA-MB-231 Breast Cancer Cells. J Clust Sci 34, 1511–1525 (2023). https://doi.org/10.1007/s10876-022-02327-1

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