Skip to main content

Advertisement

SpringerLink
Log in

An In Vitro Analysis of Pattern Cell Migration of Equine Adipose Derived Mesenchymal Stem Cells (EqASCs) Using Iron Oxide Nanoparticles (IO) in Static Magnetic Field

  • Published:
Cellular and Molecular Bioengineering Aims and scope Submit manuscript

Abstract

The aim of this work was to investigate the effects of various combinations of a static magnetic field and iron oxide nanoparticles on the growth, proliferation rate, morphology and ultrastructure of equine adipose-derived mesenchymal stem cells (ASCs). Cell migration patterns were also evaluated in order to determine whether the stem cells could be attracted using a magnetic field after iron oxide uptake. Proliferation activity of cells after magnetic field and iron oxide treatment was determined with a resazurin based cytotoxic assay whereas morphology, cytophisiological activity and ultrastructure were evaluated utilizing light, fluorescent and scanning electron microscopy. Morphological and ultrastructural examination of equine ASCs showed that exposure to a magnetic field did not cause any significant changes in cell morphology, however a shift of nuclei to the peripheral parts of the cell was observed in ultrastructural examinations. Although the cells had a lower proliferation factor after the uptake of iron nanoparticles, they could still be attracted to the desired area using a static magnetic field. This method may allow ASCs to be directed and retained within the desired area. These findings support the potential value of the combination of static magnetic fields and iron oxide nanoparticles in the treatment of equine injures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Ahmadinejad, M., J. Pishkar, H. Pashzanoussi, and S. Tavakoli. Common injuries in athletic horses at riding clubs in Tehran, Iran. Int. J. Vet. Res. 5(1):17–20, 2011.

    Google Scholar 

  2. Bekhite, M., A. Finkensieper, F. A. Abou-Zaid, I. K. El-Shourbagy, K. M. Omar, H. R. Figulla, H. Sauer, and M. Wartenberg. Static electromagnetic fields induce vasculogenesis and chondro-osteogenesis of mouse embryonic stem cells by reactive oxygen species-mediated up-regulation of vascular endothelial growth factor. Stem Cells Dev. 19(5):731–743, 2010.

    Article  Google Scholar 

  3. Biancone, L., S. Bruno, M. C. Deregibus, C. Tetta, and G. Camussi. Therapeutic potential of mesenchymal stem cell-derived microvesicles. Nephrol. Dial. Transplant. 27:3037–3042, 2012.

    Article  Google Scholar 

  4. Carvalho, A. D., P. R. Badial, L. E. Alvarez, A. L. Yamada, A. S. Borges, E. Deffune, C. A. Hussni, and A. L. Garcia Alves. Equine tendonitis therapy using mesenchymal stem cells and platelet concentrates: a randomized controlled trial. Stem Cell Res. Ther. 4(4):85, 2013.

    Article  Google Scholar 

  5. Colbert, A. P., H. Wahbeh, N. Harling, E. Connelly, H. C. Schiffke, C. Forsten, W. L. Gregory, M. S. Markov, J. J. Souder, P. Elmer, and V. King. Static magnetic field therapy: a critical review of treatment parameters. Evid. Based Complement. Alternat. Med. 6(2):133–139, 2009.

    Article  Google Scholar 

  6. Esposito, M., A. Lucariello, C. Costanzo, A. Fiumarella, A. Giannini, G. Riccardi, and I. Riccio. Differentiation of human umbilical cord-derived mesenchymal stem cells, WJ-MSCs, into chondrogenic cells in the presence of pulsed electromagnetic fields. In Vivo 27(4):495–500, 2013.

    Google Scholar 

  7. Gimble, J. M., A. J. Katz, and B. A. Bunnell. Adipose-derived stem cells for regenerative medicine. Circ. Res. 100(9):1249–1260, 2007.

    Article  Google Scholar 

  8. Godwin, E. E., N. J. Young, J. Dudhia, I. C. Beamish, and R. K. Smith. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon. Equine Vet. J. 44:25–32, 2012.

    Article  Google Scholar 

  9. Grzesiak, J., K. Marycz, J. Czogała, K. Wrzeszcz, and J. Nicpoń. Comparison of behavior, morphology and morphometry of equine and canine adipose derived mesenchymal stem cells in culture. Int. J. Morphol. 29:1012–1017, 2011.

    Article  Google Scholar 

  10. Grzesiak, J., K. Marycz, D. Szarek, and W. Jarmundowicz. Morphological characterization of gecko’s (Eublepharis macularius) glial cells in culture. Int. J. Morphol. 31(3):826–831, 2013.

    Article  Google Scholar 

  11. Guest, D. J., M. R. Smith, and W. R. Allen. Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study. Equine Vet. J. 40:178–181, 2008.

    Article  Google Scholar 

  12. Hattori, H., K. Masuoka, M. Sato, M. Ishihara, T. Asazuma, B. Takase, M. Kikuchi, K. Nemoto, and M. Ishihara. Bone formation using human adipose tissue-derived stromal cells and a biodegradable scaffold. J. Biomed. Mater. Res. B 76(1):230–239, 2006.

    Article  Google Scholar 

  13. Hill, T., D. Carmichael, G. Maylin, and L. Krook. Track condition and racing injuries in thoroughbred horses. Cornell Vet. 76(4):361–379, 1986.

    Google Scholar 

  14. Hsu, S. H., and J. C. Chang. The static magnetic field accelerates the osteogenic differentiation and mineralization of dental pulp cells. Cytotechnology 2:143–155, 2010.

    Article  Google Scholar 

  15. Jasmin, A. L. Torres, H. M. Nunes, J. A. Passipieri, L. A. Jelicks, E. L. Gasparetto, D. C. Spray, A. C. Campos de Carvalho, and R. Mendez-Otero. Optimized labeling of bone marrow mesenchymal cells with superparamagnetic iron oxide nanoparticles and in vivo visualization by magnetic resonance imaging. J. Nanobiotechnol. 9:4, 2011.

    Article  Google Scholar 

  16. Kotani, H., H. Kawaguchi, T. Shimoaka, M. Iwasaka, S. Ueno, H. Ozawa, K. Nakamura, and K. Hoshi. Strong static magnetic field stimulates bone formation to a definite orientation in vitro and in vivo. J. Bone Miner. Res. 17(10):1814–1821, 2002.

    Article  Google Scholar 

  17. Lacy-Hulbert, A., J. C. Metcalfe, and R. Hesketh. Biological responses to electromagnetic fields. FASEB J. 12(6):395–420, 1998.

    Google Scholar 

  18. Lai, R. C., T. S. Chen, and S. K. Lim. Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease. Regen. Med. 6:481–492, 2011.

    Article  Google Scholar 

  19. Lee, S. W., P. Padmanabhan, and P. Ray. Stem cell-mediated accelerated bone healing observed with in vivo molecular and small animal imaging technologies in a model of skeletal injury. J Orthop. Res. 27:295–302, 2009.

    Article  Google Scholar 

  20. Luo, F., T. Hou, Z. Zhang, Z. Xie, X. Wu, and J. Xu. Effects of pulsed electromagnetic field frequencies on the osteogenic differentiation of human mesenchymal stem cells. Orthopedics 35(4):526–531, 2012.

    Article  Google Scholar 

  21. Marędziak, M., K. Marycz, A. Śmieszek, D. Lewandowski, and N. Y. Toker. The influence of static magnetic fields on canine and equine mesenchymal stem cells derived from adipose tissue. In Vitro Cell Dev. Biol. Anim. 50(6):562–571, 2014.

    Article  Google Scholar 

  22. Markov, M. S. Therapeutic application of static magnetic fields. Environmentalist 27:457–463, 2007.

    Article  Google Scholar 

  23. Marycz, K., J. Grzesiak, K. Wrzeszcz, and P. Golonka. Adipose stem cell combined with plasma-based implant bone tissue differentiation in vitro and in a horse with a phalanx digitalis distalis fracture: a case report. Vet. Med. 57(11):610–617, 2012.

    Google Scholar 

  24. Marycz, K., A. Śmieszek, J. Grzesiak, A. Donesz-Sikorska, and J. Krzak-Roś. Application of bone marrow and adipose-derived stem cells for testing the biocompatibility of metal-based biomaterials functionalized with ascorbic acid. Biomed. Mater. 8(6):065004, 2013.

    Article  Google Scholar 

  25. Marycz, K., N. Y. Toker, J. Grzesiak, K. Wrzeszcz, and P. Golonka. The therapeutic effect of autogenic adipose derived stem cells combined with autogenic platelet rich plasma in tendons disorders in horses in vitro and in vivo research. J. Anim. Vet. Adv. 11(23):4324–4331, 2012.

    Google Scholar 

  26. Marycz, K., N. Y. Toker, A. Śmieszek, and J. Nicpoń. The morphology and proliferation rate of canine and equine adipose derived stem cells cultured with flunixin meglumine—in vitro. Kafkas Univ. Vet. Fak. Derg. 9:1–7, 2013.

    Google Scholar 

  27. Mizuno, H., M. Tobita, and A. C. Uysal. Concise review: adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells 30(5):804–810, 2012.

    Article  Google Scholar 

  28. Nicpoń, J., K. Marycz, and J. Grzesiak. Therapeutic effect of adipose-derived mesenchymal stem cell injection in horses suffering from bone spavin. Pol. J. Vet. Sci. 16(4):753–754, 2013.

    Google Scholar 

  29. Pesce, M., A. Patruno, L. Speranza, and M. Reale. Extremely low frequency electromagnetic field and wound healing: implication of cytokines as biological mediators. Eur. Cytokine Netw. 24(1):1–10, 2013.

    Google Scholar 

  30. Pislaru, S. V., A. Harbuzariu, and R. Gulati. Magnetically targeted endothelial cell localization in stented vessels. J. Am. Coll. Cardiol. 48:1839–1845, 2006.

    Article  Google Scholar 

  31. Ross, C. L., and B. S. Harrison. The use of magnetic field for the reduction of inflammation: a review of the history and therapeutic results. Altern. Ther. Health Med. 19(2):47–54, 2013.

    Google Scholar 

  32. Sato, K., H. Yamaguchi, H. Miyamoto, and Y. Kinouchi. Growth of human cultured cells exposed to a non-homogeneous static magnetic field generated by Sm-Co magnets. Biochim. Biophys. Acta 1136(3):231–238, 1992.

    Article  Google Scholar 

  33. Schäfer, R., R. Bantleon, R. Kehlbach, G. Siegel, J. Wiskirchen, H. Wolburg, T. Kluba, F. Eibofner, H. Northoff, C. D. Claussen, and H. P. Schlemmer. Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol. 11:22, 2010.

    Article  Google Scholar 

  34. Schäfer, R., R. Kehlbach, M. Müller, R. Bantleon, T. Kluba, M. Ayturan, G. Siegel, H. Wolburg, H. Northoff, K. Dietz, C. D. Claussen, and J. Wiskirchen. Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 11(1):68–78, 2009.

    Article  Google Scholar 

  35. Tenuzzo, B., A. Chionna, E. Panzarini, R. Lanubile, P. Tarantino, B. Di Jeso, M. Dwikat, and L. Dini. Biological effects of 6 mT static magneticfields: a comparative study in different cell types. Bioelectromagnetics 27(7):560–577, 2006.

    Article  Google Scholar 

  36. Tetta, C., A. L. Consiglio, S. Bruno, E. Tetta, E. Gatti, M. Dobreva, F. Cremonesi, and G. Camussi. The role of microvesicles derived from stem cells in tissue regeneration; a dream for tendon repair? Muscles Ligaments Tendons J. 2(3):212–221, 2012.

    Google Scholar 

  37. Torbet, J., and M. C. Ronzière. Magnetic alignment of collagen during self-assembly. Biochem. J. 219(3):1057–1059, 1984.

    Article  Google Scholar 

  38. Vergallo, C., L. Dini, Z. Szamosvölgyi, B. A. Tenuzzo, E. Carata, E. Panzarini, and J. F. Laszlo. In vitro analysis of the anti-inflammatory effect of inhomogeneous static magnetic field-exposure on human macrophages and lymphocytes. PLoS One 2013. doi:10.1371/journal.pone.0072374.

    Google Scholar 

  39. Yamamoto, Y., Y. Ohsaki, T. Goto, A. Nakasima, and T. Iijima. Effects of static magnetic fields on bone formation in rat osteoblast cultures. J. Dent. Res. 82(12):962–966, 2003.

    Article  Google Scholar 

Download references

Acknowlegments

The research was supported by Wroclaw Research Centre EIT+ under the Project “Biotechnologies and Advanced Medical Technologies” – BioMed (POIG.01.01.02-02-003/08) financed from the European Regional Development Fund (Operational Programmed Innovative Economy, 1.1.2.). Publication supported by Wrocław Centre of Biotechnology, programme the Leading National Research Centre (KNOW) for years 2014–2018.

Conflict of interests

Monika Marędziak, Krzysztof Marycz, Agnieszka Śmieszek, and Daniel Lewandowski declare that they have no conflicts of interest.

Ethical Standards

All animal studies were approved by the Second Local Ethic Commission (Chelmonskiego 38C, 51-630 Wroclaw, Poland; decision No. 84/2012). No human subjects research was performed by the authors for this study.

Author information

Authors and Affiliations

  1. Electron Microscopy Laboratory, University of Environmental and Life Sciences, Kożuchowska 5b, 50-631, Wroclaw, Poland

    Monika Marędziak, Krzysztof Marycz & Agnieszka Śmieszek

  2. Institute of Materials Science and Applied Mechanics, Wroclaw University of Technology, Smoluchowskiego 25, 50-370, Wroclaw, Poland

    Daniel Lewandowski

  3. Wrocław Research Centre EIT+, Stablowicka 147, 54-066, Wroclaw, Poland

    Krzysztof Marycz & Agnieszka Śmieszek

Authors
  1. Monika Marędziak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Krzysztof Marycz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agnieszka Śmieszek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Lewandowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monika Marędziak.

Additional information

Associate Editor Michael R. King oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marędziak, M., Marycz, K., Śmieszek, A. et al. An In Vitro Analysis of Pattern Cell Migration of Equine Adipose Derived Mesenchymal Stem Cells (EqASCs) Using Iron Oxide Nanoparticles (IO) in Static Magnetic Field. Cel. Mol. Bioeng. 8, 566–576 (2015). https://doi.org/10.1007/s12195-015-0402-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-015-0402-y

Keywords

Search

Navigation