Advances in Clinical and Experimental Medicine

Adv Clin Exp Med
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Advances in Clinical and Experimental Medicine

2018, vol. 27, nr 9, September, p. 1181–1193

doi: 10.17219/acem/90872

Publication type: original article

Language: English

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Creative Commons BY-NC-ND 3.0 Open Access

Migration of human mesenchymal stem cells stimulated with pulsed electric field and the dynamics of the cell surface glycosylation

Katarzyna Jezierska-Woźniak1,A,B,C,D, Seweryn Lipiński2,C,D, Margaret Huflejt3,A,C,D, Łukasz Grabarczyk3,B, Monika Barczewska3,A,C, Aleksandra Habich4,B, Joanna Wojtkiewicz,C, Wojciech Maksymowicz3,A,F

1 Department of Neurology and Neurosurgery, Faculty of Medical Sciences, Laboratory for Regenerative Medicine, University of Warmia and Mazury in Olsztyn, Poland

2 Department of Electric and Power Engineering, Electronics and Automatics, Faculty of Technical Sciences, University of Warmia and Mazury in Olsztyn, Poland

3 Center of Innovative Research in Medical and Natural Sciences, Faculty of Medicine, University of Rzeszów, Poland



Background. The analysis of the stem cells’ glycome dynamics at different stages of differentiation and migration makes possible the exploration of the cell surface glycans as markers of the stem cell functional status, and, in the future, compatibility between transplanted cell and host environment.
Objectives. The objective of our study was to develop novel techniques of investigating cell motility and to assess whether the electric field of the therapeutic spinal cord stimulation system used in vivo contributes to the migration of human mesenchymal stem cells (hMSCs) in vitro.
Material and Methods. We have investigated the electrotaxis of bone marrow-derived MSCs using pulsed electric field (PEF) in the range of 16–80 mV/mm and the frequency of 130 Hz and 240 Hz. The PEF-related dynamics of the cell surface glycosylation was evaluated using 6 plant lectins recognizing individual glycans.
Results. Pulsed electric field at physiological levels (10 mV/mm; 130 Hz) did not influence cellular motility in vitro, which may correspond to the maintenance of the transplanted cells at the lesion site in vivo. An increase of the PEF intensity and the frequency exceeding physiological levels resulted in an increase in the cellular migration rate in vitro. Pulsed electric field elevated above physiological intensity and frequency (40–80 mV/mm; 240 Hz), but not at physiological levels, resulted in changes of the cell surface glycosylation.
Conclusion. We found the described approach convenient for investigations and for the in vitro modeling of the cellular systems intended for the regenerative cell transplantations in vivo. Probing cell surface glycomes may provide valuable biomarkers to assess the competence of transplanted cells.

Key words

translational medicine, mesenchymal stem cells migration, stem cells homing, pulsed electric field, stem cell glycosylation

References (40)

  1. Okano H, Sawamoto K. Neural stem cells: Involvement in adult neurogenesis and CNS repair. Philos Trans R Soc Lond B Biol Sci. 2008;363:2111–2122.
  2. Breitbach M, Bostani T, Roell W, et al. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood. 2007;110(4):1362–1369.
  3. McCaig CD, Rajnicek AM, Song B, Zhao M. Controlling cell behavior electrically: Current views and future potential. Physiol Rev. 2005;85:943–978.
  4. Barker AT, Jaffe LF, Vanable Jr JW. The glabrous epidermis of cavies contains a powerful battery. Am J Physiol. 1982;242:R358–R366.
  5. Zhao M, Song B, Pu J, et al. X Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature. 1982;442:457–460.
  6. Ozkucur N, Monsees TK, Perike S, Do HQ, Funk RH. Local calcium elevation and cell elongation initiate guided motility in electrically stimulated osteoblast-like cells. PLoS One. 2009;4:e6131.
  7. Zhao Z, Qin L, Reid B, Pu J, Hara T, Zhao M. Directing migration of endothelial progenitor cells with applied DC electric fields. Stem Cell Res. 2011;8:38–48.
  8. Zhao M, Bai H, Wang E, Forrester JV, McCaig CD. Electrical stimulation directly induces preangiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J Cell Sci. 2004;117:397–405.
  9. McCaig CD, Zhao M. Physiological electrical fields modify cell behavior. Bioessays. 1997;19:819–826.
  10. Sato MJ, Ueda M, Takagi H, Watanabe TM, Yanagida T. Input-output relationship in galvanotactic response of Dictyostelium cells. Biosystems. 2007;88:261.
  11. Li J, Zhu L, Zhang M, Lin F. Microfluidic device for studying cell migration in single or co-existing chemical gradients and electric fields. Biomicrofluidics. 2012;6(2):24121–2412113.
  12. Huang C, Cheng J, Yen M, Young T. Electrotaxis of lung cancer cells in a multiple-electricfield chip. Biosens Bioelectron. 2009;24:3510.
  13. Huang J, Hu X, Lu L, Ye Z, Zhang Q, Luo Z. Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers. J Biomed Mater Res. 2009;93:164–174.
  14. Rezai P, Salam S, Selvaganapathy PR, Gupta BP. Electrical sorting of Caenorhabditis elegans. Lab Chip. 2012;12:1831.
  15. Alley WR Jr, Mann BF, Novotny MV. High-sensitivity analytical approaches for the structural characterization of glycoproteins. Chem Rev. 2013;113(4):2668–2732.
  16. Malina W, Smiatacz M. Methods of Digital Image Processing. Warszawa, Poland: Academic Publishing House – Exit; 2005:159–176.
  17. Batchelor B, Waltz F. Interactive Image Processing for Machine Vision. London, UK: Springer-Verlag; 2012:17–45.
  18. Zieliński KW, Strzelecki M. Computer Analysis of Biomedical Image. Warszawa, Poland: Scientific Publishing House – PWN; 2002:170–178.
  19. Jezierska-Woźniak K, Wojtkiewicz J, Grabarczyk Ł, Habich A, Lipiński S, Maksymowicz W. The effect of pulsed electric field on mesenchymal stem cell direct migration. IFMBE Proceedings. 2016;53:159–162.
  20. Pu J, Zhao M. Golgi polarization in a strong electric field. J Cell Sci. 2005;118:1117–1128.
  21. Li J, Lin F. Microfluidic devices for studying chemotaxis and electrotaxis. Trends Cell Biol. 2011;21:489.
  22. Huang Y-J, Samorajski J, Kreimer R, Searson PC. The influence of electric fields and confinement on cell motility. PLoS One. 2013;8:1–9.
  23. Zhao Z, Watt C, Karystinou A, et al. Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. Eur Cell Mater. 2011;29(22):344–358.
  24. Hart FX, Laird M, Riding A, Pullar CE. Keratinocyte galvanotaxis in combined DC and AC electric fields supports an electromechanical transduction sensing mechanism. Bioelectromagnetics. 2013;34:85–94.
  25. Jahanshahi A, Schonfeld L, Janssen ML, et al. Electrical stimulation of the motor cortex enhances progenitor cell migration in the adult rat brain. Exp Brain Res. 2013;231(2):165–177.
  26. Fong EL, Chan CK, Goodman SB. Stem cell homing in musculoskeletal injury. Biomaterials. 2011;32:395–409.
  27. Miller RJ, Banisadr G, Bhattachary BJ. CXCR4 signaling in the regulation of stem cell migration and development. J Neuroimmunol. 2008;198:31–38.
  28. Puc M, Corovic S, Flisar K, Petkovsek M, Nastran J, Miklavcic D. Techniques of signal generation required for electropermeabilization. Survey of electropermeabilization devices. Bioelectrochemistry. 2004; 64:113–124.
  29. Kojima J, Shinohara H, Ikariyama Y, Aizawa M, Nagaike K, Morioka S. Electrically promoted protein production by mammalian cells cultured on the electrode surface. Biotechnol Bioeng. 1992;39:27–32.
  30. Fang KS, Ionides E, Oster G, Nuccitelli R, Isseroff RR. Epidermal growth factor receptor relocalization and kinase activity are necessary for directional migration of keratinocytes in DC electric fields. J Cell Sci. 1999;112:1967–1978.
  31. Huang L, Cormie P, Messerli MA, Robinson KR. The involvement of Ca2+ and integrins in directional responses of zebrafish keratocytes to electric fields. J Cell Physiol. 2009;219:162–172.
  32. Wu D, Ma X, Lin F. DC electric fields direct breast cancer cell migration, induce EGFR polarization, and increase the intracellular level of calcium ions. Cell Biochem Biophys. 2013;67;1115–1125.
  33. Yura H, Kanatani Y, Ishihara M, et al. Selection of hematopoietic stem cells with a combination of galactose-bound vinyl polymer and soybean agglutinin, a galactose-specific lectin. Transfusion. 2008;48: 561–566.
  34. Naeem A, Saleemuddin M, Khan RH. Glycoprotein targeting and other applications of lectins in biotechnology. Curr Protein Pept Sci. 2007;8:261–271.
  35. Tao SC, Li Y, Zhou J, Qian J, Schnaar RL, Zhang Y, et al. Lectin microarrays identify cell-specific and functionally significant cell surface glycan markers. Glycobiology. 2008;18:761–769.
  36. Kullolli M, Hancock WS, Hincapie M. Preparation of a high-performance multi-lectin affinity chromatography (HP-M-LAC) adsorbent for the analysis of human plasma glycoproteins. J Sep Sci. 2008;31: 2733–2739.
  37. Hardy CL, Tavassoli M. Homing of hemopoietic stem cells to hemopoietic stroma. Adv Exp Med Biol. 1988;241:129–133.
  38. Hinge AS, Limaye LS, Surolia A, Kale VP. In vitro protection of umbilical cord blood-derived primitive hematopoietic stem progenitor cell pool by mannose-specific lectins via antioxidant mechanisms. Transfusion. 2010;50(8):1815–1826.
  39. Li K, Ooi VE, Chuen CK, et al. The plant mannose-binding lectin NTL preserves cord blood haematopoietic stem/progenitor cells in long-term culture and enhances their ex vivo expansion. Br J Haematol. 2008;140(1):90–98.
  40. Amano M, Yamaguchi M, Takegawa Y, et al. Threshold in stage-specific embryonic glycotypes uncovered by a full portrait of dynamic N-glycan expression during cell differentiation. Mol Cell Proteomics. 2010;9:523–537.