Skip to main content

Combined effects of electromagnetic field and low-level laser increase proliferation and alter the morphology of human adipose tissue-derived mesenchymal stem cells

Lasers in Medical Science volume 32, pages 151–160 (2017)Cite this article

Abstract

In recent years, electromagnetic field (EMF) and low-level laser (LLL) have been found to affect various biological processes, the growth and proliferation of cells, and especially that of stem cells. The aim of this study was to investigate the effects of EMF and LLL on proliferation of human adipose tissue-derived mesenchymal stem cells (hAT-MSCs) and thus to examine the impact of these therapeutic physical modalities on stem cell engraftment. hAT-MSCs were isolated from subcutaneous adipose tissue of six persons ranging in age from 21 to 56 years. EMF was applied for a period of 7 days, once a day for 30 min, via a magnetic cushion surface at a frequency of 50 Hz and an intensity of 3 mT. LLL was applied also for 7 days, once a day for 5 min, at radiation energies of 3 J/cm2, with a wavelength of 808 nm, power output of 200 mW, and power density of 0.2 W/cm2. Nonexposed cells (control) were cultivated under the same culture conditions. Seven days after treatment, the cells were examined for cell viability, proliferation, and morphology. We found that after 7 days, the number of EMF-treated hAT-MSCs was significantly higher than the number of the untreated cells, LLL-treated hAT-MSCs were more numerous than EMF-treated cells, and hAT-MSCs that were treated with the combination of EMF and LLL were the most numerous. EMF and/or LLL treatment did not significantly affect hAT-MSC viability by itself. Changes in cell morphology were also observed, in terms of an increase in cell surface area and fractal dimension in hAT-MSCs treated with EMF and the combination of EMF and LLL. In conclusion, EMF and/or LLL treatment accelerated the proliferation of hAT-MSCs without compromising their viability, and therefore, they may be used in stem cell tissue engineering.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Saliev T, Mustapova Z, Kulsharova G, Bulanin D, Mikhalovsky S (2014) Therapeutic potential of electromagnetic fields for tissue engineering and wound healing. Cell Prolif 47(6):485–493

    CAS  Article  PubMed  Google Scholar 

  2. Abrahamse H (2012) Regenerative medicine, stem cells, and low level laser therapy: future directives. Photomed Laser Surg 30(12):681–682

    Article  PubMed  Google Scholar 

  3. Volarevic V, Nurkovic J, Arsenijevic N, Stojkovic M (2014) Concise review: Therapeutic potential of mesenchymal stem cells for the treatment of acute liver failure and cirrhosis. Stem Cells 32(11):2818–2823

    CAS  Article  PubMed  Google Scholar 

  4. Nurkovic J, Volarevic V, Lako M, Armstrong L, Arsenijevic N, Stojkovic M (2016) Aging of stem and progenitor cells: mechanisms, impact on the therapeutic potential and rejuvenation. Rejuvenation Res 19(1):3–12

    Article  PubMed  Google Scholar 

  5. Nurkovic J, Dolicanin Z, Mustafic F, Mujanovic R, Memic M, Grbovic V, Jurisic Skevin A, Nurkovic S (2016) Mesenchymal stem cells in regenerative rehabilitation. J Phys Ther Sci 28(6):1943–1948

    Article  PubMed  PubMed Central  Google Scholar 

  6. Salehinejad P, Alitheen NB, Mandegary A, Nematollahi-Mahani SN, Janzamin E (2013) Effect of EGF and FGF on the expansion properties of human umbilical cord mesenchymal cells. Vitro Cell Dev Biol Anim 49(7):515–523

    CAS  Article  Google Scholar 

  7. Patil S, Paul S (2014) A comprehensive review on the role of various materials in the osteogenic differentiation of mesenchymal stem cells with a special focus on the association of heat shock proteins and nanoparticles. Cells Tissues Organs 199(2-3):81–102

    CAS  Article  PubMed  Google Scholar 

  8. Dehghani Soltani S, Babaee A, Shojaei M, Salehinejad P, Seyedi F, JalalKamali M, Nematollahi-Mahani SN (2016) Different effects of energy dependent irradiation of red and green lights on proliferation of human umbilical cord matrix-derived mesenchymal cells. Lasers Med Sci 31(2):255–261

    Article  PubMed  Google Scholar 

  9. Mvula B, Moore TJ, Abrahamse H (2010) Effect of low-level laser irradiation and epidermal growth factor on adult human adipose-derived stem cells. Lasers Med Sci 25(1):33–39

    CAS  Article  PubMed  Google Scholar 

  10. Mester E, Spiry T, Szende B, Tota JG (1971) Effect of laser rays on wound healing. Am J Surg 122(4):532–535

    CAS  Article  PubMed  Google Scholar 

  11. Kushibiki T, Hirasawa T, Okawa S, Ishihara M (2015) Low reactive level laser therapy for mesenchymal stromal cells therapies. Stem Cells Int 2015:974864

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chung SH, Mazur E (2009) Surgical applications of femtosecond lasers. J Biophotonics 2(10):557–572

    Article  PubMed  Google Scholar 

  13. Khatri KA, Mahoney DL, McCartney MJ (2011) Laser scar revision: a review. J Cosmet Laser Ther 13(2):54–62

    Article  PubMed  Google Scholar 

  14. Funk RH, Monsees TK, Ozkucur N (2009) Electromagnetic effects—from cell biology to medicine. Prog Histochem Cytochem 43(4):177–264

    Article  PubMed  Google Scholar 

  15. Kim HJ, Jung J, Park JH, Kim JH, Ko KN, Kim CW (2013) Extremely low-frequency electromagnetic fields induce neural differentiation in bone marrow derived mesenchymal stem cells. Exp Biol Med (Maywood) 238(8):923–931

    Article  Google Scholar 

  16. Mousavi M, Baharara J, Shahrokhabadi K (2014) The synergic effects of Crocus sativus L. and low frequency electromagnetic field on VEGFR2 gene expression in human breast cancer cells. Avicenna J Med Biotechnol 6(2):123–127

    PubMed  PubMed Central  Google Scholar 

  17. Ross CL, Siriwardane M, Almeida-Porada G, Porada CD, Brink P, Christ GJ, Harrison BS (2015) The effect of low-frequency electromagnetic field on human bone marrow stem/progenitor cell differentiation. Stem Cell Res 15(1):96–108

    Article  PubMed  PubMed Central  Google Scholar 

  18. Zhong C, Zhang X, Xu Z, He R (2012) Effects of low-intensity electromagnetic fields on the proliferation and differentiation of cultured mouse bone marrow stromal cells. Phys Ther 92(9):1208–1219

    Article  PubMed  Google Scholar 

  19. Passarella S, Karu T (2014) Absorption of monochromatic and narrow band radiation in the visible and near IR by both mitochondrial and non-mitochondrial photoacceptors results in photobiomodulation. J Photochem Photobiol B 140:344–358

    CAS  Article  PubMed  Google Scholar 

  20. Oberoi S, Zamperlini-Netto G, Beyene J, Treister NS, Sung L (2014) Effect of prophylactic low level laser therapy on oral mucositis: a systematic review and meta-analysis. PLoS ONE 9(9):e107418

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45(2):115–120

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Nurkovic J, Dolicanin Z, Tutic I, Hajrovic S, Mustafic F, Todorovic V, Kovacevic-Filipovic M (2013) Adipose tissue mesenchymal stem cells - isolation, cultivation and induced differentiation. Praxis Medica 42(3):45–50

    Google Scholar 

  23. Mitchell JB, McIntosh K, Zvonic S, Garrett S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24(2):376–385

    Article  PubMed  Google Scholar 

  24. Lv FJ, Tuan RS, Cheung KM, Leung VY (2014) Concise review: The surface markers and identity of human mesenchymal stem cells. Stem Cells 32(6):1408–1419

    CAS  Article  PubMed  Google Scholar 

  25. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT1 (2014) Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 12:8

    Article  PubMed  PubMed Central  Google Scholar 

  26. Höfig I, Ingawale Y, Atkinson MJ, Hertlein H, Nelson PJ, Rosemann M (2016) p53-dependent senescence in mesenchymal stem cells under chronic normoxia is potentiated by low-dose γ-irradiation. Stem Cells Int 2016:6429853

    Article  PubMed  Google Scholar 

  27. Christodoulou I, Kolisis FN, Papaevangeliou D, Zoumpourlis V (2013) Comparative evaluation of human mesenchymal stem cells of fetal (Wharton’s jelly) and adult (adipose tissue) origin during prolonged in vitro expansion: considerations for cytotherapy. Stem Cells Int 2013:246134

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Milosevic NT, Ristanovic D, Jelinek HF, Rajkovic K (2009) Quantitative analysis of dendritic morphology of the α and δ retinal ganglion cells in the rat: a cell classification study. J Theor Biol 259:142–50

    Article  PubMed  Google Scholar 

  29. Zaletel I, Ristanovic D, Stefanovic BD, Puskas N (2015) Modified Richardson’s method versus the box-counting method in neuroscience. J Neurosci Methods 242:93–96

    Article  PubMed  Google Scholar 

  30. Puskas N, Zaletel I, Stefanovis BD, Ristanovic D (2015) Fractal dimension of apical dendritic arborization differs in the superficial and the deep pyramidal neurons of the rat cerebral neocortex. Neurosci Lett 589:88–91

    CAS  Article  PubMed  Google Scholar 

  31. Murray IR, West CC, Hardy WR, James AW, Park TS, Nguyen A, Tawonsawatruk T, Lazzari L, Soo C, Péault B (2014) Natural history of mesenchymal stem cells, from vessel walls to culture vessels. Cell Mol Life Sci 71(8):1353–1374

    CAS  Article  PubMed  Google Scholar 

  32. De Haas WG, Watson J, Morrison DM (1980) Non-invasive treatment of ununited fractures of the tibia using electrical stimulation. J Bone Joint Surg (Br) 62-B:465–470

    Google Scholar 

  33. Aaron RK, Ciombor DM (1996) Acceleration of experimental endochondral ossification by biophysical stimulation of the progenitor cell pool. J Orthop Res 14(4):582–589

    CAS  Article  PubMed  Google Scholar 

  34. Maziarz A, Kocan B, Bester M, Budzik S, Cholewa M, Ochiya T, Banas A (2016) How electromagnetic fields can influence adult stem cells: positive and negative impacts. Stem Cell Res Ther 7:54

    Article  PubMed  PubMed Central  Google Scholar 

  35. 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 34:74–80

    Article  PubMed  Google Scholar 

  36. Tsai MT, Li WJ, Tuan RS, Chang WH (2009) Modulation of osteogenesis in human mesenchymal stem cells by specific pulsed electromagnetic field stimulation. J Orthop Res 27(9):1169–1174

    Article  PubMed  PubMed Central  Google Scholar 

  37. Schwartz Z, Fisher M, Lohmann CH, Simon BJ, Boyan BD (2009) Osteoprotegerin (OPG) production by cells in the osteoblast lineage is regulated by pulsed electromagnetic fields in cultures grown on calcium phosphate substrates. Ann Biomed Eng 37:437–444

    Article  PubMed  Google Scholar 

  38. 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 29:165–176

    CAS  Article  PubMed  Google Scholar 

  39. de Villiers JA, Houreld NN, Abrahamse H (2011) Influence of low intensity laser irradiation on isolated human adipose derived stem cells over 72 hours and their differentiation potential into smooth muscle cells using retinoic acid. Stem Cell Rev 7(4):869–882

    CAS  Article  PubMed  Google Scholar 

  40. Hudson DE, Hudson DO, Wininger JM, Richardson BD (2013) Penetration of laser light at 808 and 980 nm in bovine tissue samples. Photomed Laser Surg 31(4):163–168

    Article  PubMed  PubMed Central  Google Scholar 

  41. Joensen J, Ovsthus K, Reed RK, Hummelsund S, Iversen VV, Lopes-Martins RÁ, Bjordal JM (2012) Skin penetration time-profiles for continuous 810 nm and superpulsed 904 nm lasers in a rat model. Photomed Laser Surg 30(12):688–694

    Article  PubMed  Google Scholar 

  42. Park SH, Shin JW, Kang YG, Hyun J-S, Oh MJ, Shin J-W (2014) Texture analyses show synergetic effects of biomechanical and biochemical stimulation on mesenchymal stem cell differentiation into early phase osteoblasts. Microsc Microanal 20(1):219–227

    CAS  Article  PubMed  Google Scholar 

  43. Chalut KJ, Kulangara K, Wax A, Leong KW (2011) Stem cell differentiation indicated by noninvasive photonic characterization and fractal analysis of subcellular architecture. Integr Biol (Camb) 3(8):863–867

    CAS  Article  Google Scholar 

  44. Ishikawa K (2015) Intracoronary injection of large stem cells: size matters. Circ Cardiovasc Interv 8(5)

  45. Koç ON (2006) Clinical trials of human mesenchymal stem cells to support hematopoietic stem cell transplantation. In: Nolta JA (ed) Genetic engineering of mesenchymal stem cells. Springer, Houten, pp 151–162

    Chapter  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Ervin Sejdić and Dr. Vladislav Volarević for the critical review of the paper. This article was supported by a grant (no. 175061) from the Ministry of Education, Sciences and Technological Development of the Republic of Serbia.

Author information

Affiliations

  1. Department of Biomedical Sciences, State University of Novi Pazar, Novi Pazar, Serbia

    Jasmin Nurković, Fahrudin Mustafić & Zana Dolićanin

  2. Center for Molecular Medicine and Stem Cell Research, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia

    Jasmin Nurković & Selmina Nurković

  3. Center for Physical Medicine and Rehabilitation, Clinical Center Kragujevac, Kragujevac, Serbia

    Jasmin Nurković, Aleksandra Jurišić Škevin & Vesna Grbović

  4. Institute of Histology and Embryology “Aleksandar Đ. Kostic,” School of Medicine, University of Belgrade, Belgrade, Serbia

    Ivan Zaletel & Jovan Isma

  5. General Hospital Novi Pazar, Novi Pazar, Serbia

    Selmina Nurković, Šefćet Hajrović & Zana Dolićanin

  6. Department of Physical Medicine and Rehabilitation, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia

    Aleksandra Jurišić Škevin & Vesna Grbović

  7. Faculty of Veterinary Medicine, University of Belgrade, Belgrade, Serbia

    Milica Kovačević Filipović

Authors
  1. Jasmin Nurković
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Zaletel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Selmina Nurković
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Šefćet Hajrović
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fahrudin Mustafić
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jovan Isma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aleksandra Jurišić Škevin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vesna Grbović
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Milica Kovačević Filipović
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zana Dolićanin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jasmin Nurković.

Ethics declarations

The present experiment, which includes human subjects, was approved by the Ethics Committee of State University of Novi Pazar and the General Hospital of Novi Pazar. All of the protocols were approved in advance by the State University of Novi Pazar, Novi Pazar, Serbia. All patients provided a written informed consent to participate. All of the investigations have been conducted according to the ethical principles suggested in the Declaration of Helsinki. Measures have been made to protect the privacy of research subjects and the confidentiality of their personal information.

Conflict of interest

The authors declare that they have no conflict of interests.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nurković, J., Zaletel, I., Nurković, S. et al. Combined effects of electromagnetic field and low-level laser increase proliferation and alter the morphology of human adipose tissue-derived mesenchymal stem cells. Lasers Med Sci 32, 151–160 (2017). https://doi.org/10.1007/s10103-016-2097-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-016-2097-2

Keywords

  • Mesenchymal stem cells
  • Electromagnetic field
  • Low-level laser
  • Treatment
  • Therapeutic application
  • Fractal analysis