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Biological Trace Element Research

, Volume 184, Issue 2, pp 529–535 | Cite as

Zinc Sulphate Mediates the Stimulation of Cell Proliferation of Rat Adipose Tissue-Derived Mesenchymal Stem Cells Under High Intensity of EMF Exposure

  • Ezzatollah Fathi
  • Raheleh Farahzadi
Article

Abstract

Unlike the role of mesenchymal stem cells (MSCs) in regenerative medicine, their application in cell therapy can be complicated by factors such as a reduction in the proliferation potential, senescent tendency of MSCs to expand, and an age-dependent decline in their number and functions. It was shown that there is an association between exposure to electromagnetic fields (EMFs) and response to stress, cell proliferation, aging, and cell death. Furthermore, the zinc ion, as an essential trace element, was reported to be involved in the regulation of the growth and cell proliferation. In this report, ratadipose tissue-derived mesenchymal stem cells (rADSCs) were randomly divided into four groups—group I (control without any ZnSO4 and EMF); group II (ZnSO4 treatment without EMF exposed); group III (EMF exposed without ZnSO4); and group ІV (EMF exposed with ZnSO4)—to evaluate whether 0.14 μg/ml Zinc sulfate (ZnSO4) could affect cell proliferation of rADSCs under extremely low frequency-electromagnetic field (ELF-EMF). The methyl thiazoltetrazolium (MTT) method was used to determine the cell proliferation of rADSCs following exposure to ELF-EMF in the presence of ZnSO4. The immunocytochemistry method as well as flow-cytometry was used to identify the cell surface markers. Next, oil red O, alizarin red, toluidine blue, and cresyl violet staining was done to evaluate the adipogenic, osteogenic, chondrogenic, and neurogenic differentiation of rADSCs as the pluripotent capacity of rADSCs, respectively. The results showed that an exposure to ELF-EMF caused a decrease in the proliferation of rADSCs. However, the ZnSO4 supplementation significantly increased the cell proliferation of ELF-EMF-exposed rADSCs. In addition, in the presence of 0.14 μg/ml ZnSO4, rADSCs appeared to be growing faster than the control group and ZnSO4 significantly decreased the doubling time of ELF-EMF-exposed rADSCs. It seems that ZnSO4 would be a good element to induce the cell proliferation of ELF-EMF-exposed rADSCs.

Keywords

Rat adipose tissue-derived mesenchymal stem cells Cell proliferation Electromagnetic field Zinc sulphate 

Notes

Acknowledgements

The authors wish to thank Prof. M.A. Hossein Pour Feizi for providing magnetic field system.

Funding

This work was supported by a grant (No. S/146, 30/11/1394) from the University of Tabriz, Tabriz, Iran.

Compliance with Ethical Standards

Conflict of Interest

The authors have no conflicting financial interest.

References

  1. 1.
    Yan J, Dong L, Zhang B, Qi N (2010) Effects of extremely low-frequency magnetic field on growth and differentiation of human mesenchymal stem cells. Electromagn Biol Med 29(4):165–176.  https://doi.org/10.3109/01676830.2010.505490 CrossRefPubMedGoogle Scholar
  2. 2.
    Wolf FI, Torsello A, Tedesco B, Fasanella S, Boninsegna A, D’Ascenzo M, Grassi C, Azzena GB, Cittadini A (2005) 50-Hz extremely low frequency electromagnetic fields enhance cell proliferation and DNA damage: possible involvement of a redox mechanism. Biochim Biophys Acta 1743(1–2):120–129.  https://doi.org/10.1016/j.bbamcr.2004.09.005 CrossRefPubMedGoogle Scholar
  3. 3.
    Jadidi M, Safari M, Baghian A (2013) Effects of extremely low frequency electromagnetic fields on cell proliferation. Koomesh:1–10Google Scholar
  4. 4.
    Zheng T, Holford TR, Mayne ST, Owens PH, Zhang B, Boyle P, Carter D, Ward B, Zhang Y, Zahm SH (2000) Exposure to electromagnetic fields from use of electric blankets and other in-home electrical appliances and breast cancer risk. Am J Epidemiol 151(11):1103–1111.  https://doi.org/10.1093/oxfordjournals.aje.a010154 CrossRefPubMedGoogle Scholar
  5. 5.
    Fathi E, Farahzadi R (2012) Effect of electromagnetic field on acetylcholinesterase activity: in vitro study. Afr J Biochem Res 6(1):8–13Google Scholar
  6. 6.
    Saino E, Fassina L, Van Vlierberghe S, Avanzini MA, Dubruel P, Magenes G, Visai L, Benazzo F (2011) Effects of electromagnetic stimulation on osteogenic differentiation of human mesenchymal stromal cells seeded onto gelatin cryogel. Int J Immunopathol Pharmacol 24(1 Suppl 2):1–6.  https://doi.org/10.1177/03946320110241s201 CrossRefPubMedGoogle Scholar
  7. 7.
    Martinez-Samano J, Torres-Duran PV, Juarez-Oropeza MA, Verdugo-Diaz L (2012) Effect ofacute extremely low frequency electromagnetic field exposure on the antioxidant status and lipid levels in rat brain. Arch Med Res 43(3):183–189.  https://doi.org/10.1016/j.arcmed.2012.04.003 CrossRefPubMedGoogle Scholar
  8. 8.
    Srdjenovic B, Mrdjanovic J, Galovic A, Kladar N, BozinB JV, Bogdanovic G (2014) Effect of ELF-EMF on antioxidant status and micronuclei in K562 cells and normal lymphocytes. Open Life Sci 9(10):931–940Google Scholar
  9. 9.
    Fathi E, Farhzadi R (2015) Survey on impact of trace elements (Cu, Se and Zn) on veterinary and human mesenchymal stem cells. Rom J Biochem 52:67–77Google Scholar
  10. 10.
    Fathi E, Farahzadi R (2012) Investigation of the effect of sodium selenate on acetylcholinesterase activity under extremely low frequency electromagnetic field. J Biol Life Sci 4(1)Google Scholar
  11. 11.
    Farahzadi R, Mesbah-Namin SA, Zarghami N, Fathi E (2016) L-carnitine effectively induces hTERT gene expression of human adipose tissue-derived mesenchymal stem cells obtained from the aged subjects. Int J Stem Cells 9(1):107–114.  10.15283/ijsc.2016.9.1.107 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Levenson CW, Morris D (2011) Zinc and neurogenesis: making new neurons from development to adulthood. Adv Nutr (Bethesda, Md) 2(2):96–100.  https://doi.org/10.3945/an.110.000174 CrossRefGoogle Scholar
  13. 13.
    Ghasemzadeh-Hasankolai M, Batavani R, Eslaminejad MB, Sedighi-Gilani M (2012) Effect of zinc ions on differentiation of bone marrow-derived mesenchymal stem cells to male germ cells and some germ cell-specific gene expression in rams. Biol Trace Elem Res 150(1–3):137–146.  https://doi.org/10.1007/s12011-012-9484-8 CrossRefPubMedGoogle Scholar
  14. 14.
    Oh SA, Kim SH, Won JE, Kim JJ, Shin US, Kim HW (2011) Effects on growth and osteogenic differentiation of mesenchymal stem cells by the zinc-added sol-gel bioactive glass granules. J Tissue Eng 2010(1):475260.  https://doi.org/10.4061/2010/475260 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Brazvan B, Farahzadi R, Mohammadi SM, Montazer Saheb S, Shanehbandi D, Schmied L, Soleimani Rad J, Darabi M, Nozad Charoudeh H (2016) Key immune cell cytokines affects the telomere activity of cord blood cells in vitro. Adv Pharm Bull 6(2):153–161.  10.15171/apb.2016.022 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Fathi E, Farahzadi R (2016) Isolation, culturing, characterization and aging of adipose tissue-derived mesenchymal stem cells: a brief overview. Braz Arch Biol Technol 59. doi:  https://doi.org/10.1590/1678-4324-2016150383
  17. 17.
    Ejtehadifar M, Shamsasenjan K, Movassaghpour A, Akbarzadehlaleh P, Dehdilani N, Abbasi P, Molaeipour Z, Saleh M (2015) The effect of hypoxia on mesenchymal stem cell biology. Adv Pharm Bull 5(2):141–149.  10.15171/apb.2015.021 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ghorbani A, Jalali SA, Varedi M (2014) Isolationof adipose tissue mesenchymal stem cells without tissue destruction: a non-enzymatic method. Tissue & cell 46(1):54–58.  https://doi.org/10.1016/j.tice.2013.11.002 CrossRefGoogle Scholar
  19. 19.
    Amirkhani MA, Mohseni R, Soleimani M, Shoae-Hassani A, Nilforoushzadeh MA (2016) A rapid sonicationbased method for preparation of stromal vascular fraction and mesenchymal stem cells from fat tissue. BioImpacts : BI 6(2):99–104.  10.15171/bi.2016.14 CrossRefPubMedGoogle Scholar
  20. 20.
    Fathi E, Farahzadi R, Charoudeh HN (2017) L-carnitine contributes to enhancement of neurogenesis from mesenchymal stem cells through Wnt/beta-catenin and PKA pathway. Exp Biol Med (Maywood, NJ) 242(5):482–486.  https://doi.org/10.1177/1535370216685432 CrossRefGoogle Scholar
  21. 21.
    Mohammadian A, Naderali E, Mohammadi SM, Movasaghpour A, Valipour B, Nouri M, NozadCharoudeh H (2017) Cord blood cells responses to IL2, IL7 and IL15 cytokines for mTOR expression. Adv Pharm Bull 7(1):81–85.  10.15171/apb.2017.010 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Mobarak H, Fathi E, Farahzadi R, Zarghami N, Javanmardi S (2017) L-carnitine significantly decreased aging of rat adipose tissue-derived mesenchymal stem cells. Vet Res Commun 41(1):41–47.  https://doi.org/10.1007/s11259-016-9670-9 CrossRefPubMedGoogle Scholar
  23. 23.
    Pirmoradi S, Fathi E, Farahzadi R, Pilehvar-Soltanahmadi Y, Zarghami N (2017) Curcumin affects adipose tissue-derived mesenchymal stem cell aging through TERT gene expression. Drug ResGoogle Scholar
  24. 24.
    Fathi E, Farahzadi R (2017) Enhancement of osteogenic differentiation of rat adipose tissue-derived mesenchymal stem cells by zinc sulphate under electromagnetic field via the PKA, ERK1/2 andWnt/beta-catenin signaling pathways. PLoS One 12(3):e0173877.  https://doi.org/10.1371/journal.pone.0173877 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Luo F, Hou T, Zhang Z, Xie Z, Wu X, Xu J (2012) Effects of pulsed electromagnetic field frequencies on the osteogenic differentiation of human mesenchymalstem cells. Orthopedics 35(4):e526–e531.  https://doi.org/10.3928/01477447-20120327-11 CrossRefPubMedGoogle Scholar
  26. 26.
    Consales C, Merla C, Marino C, Benassi B (2012) Electromagnetic fields, oxidative stress, and neurodegeneration. Int J Cell Biol 2012:1–16.  https://doi.org/10.1155/2012/683897 CrossRefGoogle Scholar
  27. 27.
    Patruno A, Tabrez S, Pesce M, Shakil S, Kamal MA, Reale M (2015) Effects of extremely low frequency electromagnetic field (ELF-EMF) on catalase, cytochrome P450 and nitric oxide synthase in erythro-leukemic cells. Life Sci 121:117–123.  https://doi.org/10.1016/j.lfs.2014.12.003 CrossRefPubMedGoogle Scholar
  28. 28.
    Rafi MA (2011) Gene and stem cell therapy: alone or in combination? BioImpacts : BI 1(4):213–218.  https://doi.org/10.5681/bi.2011.030 PubMedCrossRefGoogle Scholar
  29. 29.
    Park JE, Seo YK, Yoon HH, Kim CW, Park JK, Jeon S (2013) Electromagnetic fields induce neural differentiation of human bonemarrow derived mesenchymal stem cells via ROS mediated EGFR activation. Neurochem Int 62(4):418–424.  https://doi.org/10.1016/j.neuint.2013.02.002 CrossRefPubMedGoogle Scholar
  30. 30.
    Cho H, Seo YK, Yoon HH, Kim SC, Kim SM, Song KY, Park JK (2012) Neural stimulation on human bone marrow-derived mesenchymal stem cells by extremely low frequency electromagnetic fields. Biotechnol Prog 28(5):1329–1335.  https://doi.org/10.1002/btpr.1607 CrossRefPubMedGoogle Scholar
  31. 31.
    Zhang M, Li X, Bai L, Uchida K, Bai W, Wu B, Xu W, Zhu H, Huang H (2013) Effects of low frequency electromagnetic field on proliferation of human epidermal stem cells: an in vitro study. Bioelectromagnetics 34(1):74–80.  https://doi.org/10.1002/bem.21747 CrossRefPubMedGoogle Scholar
  32. 32.
    Esposito M, Lucariello A, Riccio I, Riccio V, Esposito V, Riccardi G (2012) Differentiation of human osteoprogenitor cells increases after treatment with pulsed electromagnetic fields. In Vivo (Athens, Greece) 26(2):299–304Google Scholar
  33. 33.
    Bai WF, Zhang MS, Huang H, Zhu HX, Xu WC (2012) Effects of 50 Hz electromagnetic fields on human epidermal stem cells cultured on collagen sponge scaffolds. Int J Radiat Biol 88(7):523–530.  https://doi.org/10.3109/09553002.2012.692496 CrossRefPubMedGoogle Scholar
  34. 34.
    Yamaguchi S, Miura C, Kikuchi K, Celino FT, Agusa T, Tanabe S, Miura T (2009) Zinc is an essential trace element for spermatogenesis. Proc Natl Acad Sci U S A 106(26):10859–10864.  https://doi.org/10.1073/pnas.0900602106 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Sengupta P (2013) Environmental and occupational exposure of metals and their role in male reproductive functions. Drug Chem Toxicol 36(3):353–368.  https://doi.org/10.3109/01480545.2012.710631 CrossRefPubMedGoogle Scholar
  36. 36.
    Fathi E, Farahzadi R, Rahbarghazi R, Samadi Kafil H, Yolmeh R (2017) Rat adipose-derived mesenchymal stem cells aging reduction by zinc sulfate under extremely low frequency electromagnetic field exposure is associated with increased telomerase reverse transcriptase gene expression. In: Veterinary research forum. vol 2. Faculty of Veterinary Medicine, Urmia University, pp 89–96Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Clinical Sciences, Faculty of Veterinary MedicineUniversity of TabrizTabrizIran
  2. 2.Hematology and Oncology Research CenterTabriz University of Medical SciencesTabrizIran

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