Advertisement

Cell Biochemistry and Biophysics

, Volume 77, Issue 3, pp 213–225 | Cite as

Externally Controlled Cellular Transport of Magnetic Iron Oxide Particles with Polysaccharide Surface Coatings

  • Kwan Hyung Cho
  • Meong Cheol Shin
  • Kyoung Ah MinEmail author
Original Paper
  • 36 Downloads

Abstract

Recently, due to their promising applications in biomedicine, magnetic iron oxide nanoparticles (MPs) have become one of the research hotspots in the nanomedicine field. Since various synthetic modifications have been widely applied to these nanoparticles for better targeting behaviors, it is meaningful to apply the optimal magnetic field condition for each case. This will enable creating a safe and efficient drug targeting using different types of MPs. In the present study, we aimed to find out any changes of transepithelial transport of polysaccharide-coated MPs by applying the continuous or the pulsatile magnetic field condition. Our results with heparin-functionalized MPs indicate that the particle concentrations and the external magnetic field could influence the transepithelial permeability of the particles. In the presence of a continuously applied magnetic density, heparin-MPs at high concentrations, by forming magnetically-induced aggregation of particles over the cell surface layer, showed a lower cellular transport than those at low concentrations. Furthermore, the results from the quantitative chemical assays and imaging analyses showed that transepithelial transport of heparin-MPs (negatively charged) under the pulsatile magnetic field was higher than that under the continuous magnetic field (CP), whereas the starch-MPs (neutrally charged) showed a small difference in transepithelial transport or cell retention between pulsatile vs. continuous magnetic field conditions. Taken together, our results suggest that the external magnetic field should be differentially applied to control the cellular drug transport depending on the physicochemical properties of the surface chemistry of magnetic particles.

Keywords

Magnetic nanoparticles Polysaccharide Controlled magnetic field Transepithelial transport Cell surface 

Notes

Acknowledgements

This work was supported by the 2016 Inje University research grant. We thank Anjila Maharjan for the technical support.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12013_2019_874_MOESM1_ESM.pdf (56 kb)
Supplementary Information

References

  1. 1.
    Chomoucka, J., Drbohlavova, J., Huska, D., Adam, V., Kizek, R., & Hubalek, J. (2010). Magnetic nanoparticles and targeted drug delivering. Pharmacological Research, 62, 144–149.CrossRefGoogle Scholar
  2. 2.
    Cardoso, V. F., Francesko, A., Ribeiro, C., Banobre-Lopez, M., Martins, P., & Lanceros-Mendez, S. (2018). Advances in Magnetic Nanoparticles for Biomedical Applications. Advanced healthcare materials, 7, 1700845.CrossRefGoogle Scholar
  3. 3.
    Kumar, C. S., & Mohammad, F. (2011). Magnetic nanomaterials for hyperthermia-based therapy and controlled drug delivery. Advanced Drug Delivery Reviews, 63, 789–808.CrossRefGoogle Scholar
  4. 4.
    Rumenapp, C., Gleich, B., & Haase, A. (2012). Magnetic nanoparticles in magnetic resonance imaging and diagnostics. Pharmaceutical Research, 29, 1165–1179.CrossRefGoogle Scholar
  5. 5.
    Gobbo, O. L., Sjaastad, K., Radomski, M. W., Volkov, Y., & Prina-Mello, A. (2015). Magnetic nanoparticles in cancer theranostics. Theranostics, 5, 1249–1263.CrossRefGoogle Scholar
  6. 6.
    McBain, S. C., Yiu, H. H., & Dobson, J. (2008). Magnetic nanoparticles for gene and drug delivery. International Journal of Nanomedicine, 3, 169–180.Google Scholar
  7. 7.
    Miao, L., Liu, C., Ge, J., Yang, W., Liu, J., Sun, W., et al. (2014). Antitumor effect of TRAIL on oral squamous cell carcinoma using magnetic nanoparticle-mediated gene expression. Cell Biochemistry and Biophysics, 69, 663–672.CrossRefGoogle Scholar
  8. 8.
    Reddy, L. H., Arias, J. L., Nicolas, J., & Couvreur, P. (2012). Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chemical Reviews, 112, 5818–5878.CrossRefGoogle Scholar
  9. 9.
    Laurent, S., Saei, A. A., Behzadi, S., Panahifar, A., & Mahmoudi, M. (2014). Superparamagnetic iron oxide nanoparticles for delivery of therapeutic agents: opportunities and challenges. Expert Opinion on Drug Delivery, 11, 1449–1470.CrossRefGoogle Scholar
  10. 10.
    Lu, A. H., Salabas, E. L., & Schuth, F. (2007). Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angewandte Chemie, 46, 1222–1244.CrossRefGoogle Scholar
  11. 11.
    Branquinho, L. C., Carriao, M. S., Costa, A. S., Zufelato, N., Sousa, M. H., Miotto, R., et al. (2013). Effect of magnetic dipolar interactions on nanoparticle heating efficiency: implications for cancer hyperthermia. Scientific Reports, 3, 2887.CrossRefGoogle Scholar
  12. 12.
    Gupta, A. K., Naregalkar, R. R., Vaidya, V. D., & Gupta, M. (2007). Recent advances on surface engineering of magnetic iron oxide nanoparticles and their biomedical applications. Nanomedicine, 2, 23–39.CrossRefGoogle Scholar
  13. 13.
    Easo, S. L., & Mohanan, P. V. (2013). Dextran stabilized iron oxide nanoparticles: synthesis, characterization and in vitro studies. Carbohydrate Polymers, 92, 726–732.CrossRefGoogle Scholar
  14. 14.
    Hubatsch, I., Ragnarsson, E. G., & Artursson, P. (2007). Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nature Protocols, 2, 2111–2119.CrossRefGoogle Scholar
  15. 15.
    Volpe, D. A. (2011). Drug-permeability and transporter assays in Caco-2 and MDCK cell lines. Future Medicinal Chemistry, 3, 2063–2077.CrossRefGoogle Scholar
  16. 16.
    Beddoes, C. M., Case, C. P., & Briscoe, W. H. (2015). Understanding nanoparticle cellular entry: A physicochemical perspective. Advances in Colloid and Interface Science, 218, 48–68.CrossRefGoogle Scholar
  17. 17.
    Min, K. A., Yu, F., Yang, V. C., Zhang, X., & Rosania, G. R. (2010). Transcellular transport of heparin-coated magnetic iron oxide nanoparticles (Hep-MION) under the influence of an applied magnetic field. Pharmaceutics, 2, 119–135.CrossRefGoogle Scholar
  18. 18.
    Min, K. A., Shin, M. C., Yu, F., Yang, M., David, A. E., Yang, V. C., et al. (2013). Pulsed magnetic field improves the transport of iron oxide nanoparticles through cell barriers. ACS Nano, 7, 2161–2171.CrossRefGoogle Scholar
  19. 19.
    Riemer, J., Hoepken, H. H., Czerwinska, H., Robinson, S. R., & Dringen, R. (2004). Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Analytical Biochemistry, 331, 370–375.CrossRefGoogle Scholar
  20. 20.
    Arbab, A. S., Bashaw, L. A., Miller, B. R., Jordan, E. K., Lewis, B. K., Kalish, H., 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, 838–846.CrossRefGoogle Scholar
  21. 21.
    Min, K. A., Rosania, G. R., & Shin, M. C. (2016). Human Airway primary epithelial cells show distinct architectures on Membrane supports under different culture conditions. Cell Biochemistry and Biophysics, 74, 191–203.CrossRefGoogle Scholar
  22. 22.
    Konsoula, R., & Barile, F. A. (2005). Correlation of in vitro cytotoxicity with paracellular permeability in Caco-2 cells. Toxicology In vitro, 19, 675–684.Google Scholar
  23. 23.
    Lacombe, O., Woodley, J., Solleux, C., Delbos, J. M., Boursier-Neyret, C., & Houin, G. (2004). Localisation of drug permeability along the rat small intestine, using markers of the paracellular, transcellular and some transporter routes. European Journal of Pharmaceutical Sciences, 23, 385–391.CrossRefGoogle Scholar
  24. 24.
    Chertok, B., Moffat, B. A., David, A. E., Yu, F., Bergemann, C., Ross, B. D., et al. (2008). Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials, 29, 487–496.CrossRefGoogle Scholar
  25. 25.
    Cole, A. J., David, A. E., Wang, J., Galban, C. J., Hill, H. L., & Yang, V. C. (2011). Polyethylene glycol modified, cross-linked starch-coated iron oxide nanoparticles for enhanced magnetic tumor targeting. Biomaterials, 32, 2183–2193.CrossRefGoogle Scholar
  26. 26.
    Laurent, S., Forge, D., Port, M., Roch, A., Robic, C., Vander Elst, L., et al. (2008). Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chemical Reviews, 108, 2064–2110.CrossRefGoogle Scholar
  27. 27.
    Neuberger, T., Schöpf, B., Hofmann, H., Hofmann, M., & Von Rechenberg, B. (2005). Superparamagnetic nanoparticles for biomedical applications: possibilities and limitations of a new drug delivery system. Journal of Magnetism and Magnetic Materials, 293, 483–496.CrossRefGoogle Scholar
  28. 28.
    Nel, A. E., Madler, L., Velegol, D., Xia, T., Hoek, E. M., Somasundaran, P. et al. (2009). Understanding biophysicochemical interactions at the nano-bio interface. Nature Materials, 8, 543–557.CrossRefGoogle Scholar
  29. 29.
    Limbach, L. K., Li, Y., Grass, R. N., Brunner, T. J., Hintermann, M. A., Muller, M., et al. (2005). Oxide nanoparticle uptake in human lung fibroblasts: effects of particle size, agglomeration, and diffusion at low concentrations. Environmental Science & Technology, 39, 9370–9376.CrossRefGoogle Scholar
  30. 30.
    Corchero, J. L., & Villaverde, A. (2009). Biomedical applications of distally controlled magnetic nanoparticles. Trends in Biotechnology, 27, 468–476.CrossRefGoogle Scholar
  31. 31.
    Polyak, B., & Friedman, G. (2009). Magnetic targeting for site-specific drug delivery: applications and clinical potential. Expert Opinion on Drug Delivery, 6, 53–70.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Pharmacy and Inje Institute of Pharmaceutical Sciences and ResearchInje UniversityGimhaeRepublic of Korea
  2. 2.College of Pharmacy and Research Institute of Pharmaceutical SciencesGyeongsang National UniversityJinjuRepublic of Korea

Personalised recommendations