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Table 1 Effects of EMFs with different parameters on stem cell biology

From: How electromagnetic fields can influence adult stem cells: positive and negative impacts

Stem cell type

EMF characteristics

Exposure duration

Differentiation type

Stimulation effects

Reference

Sinusoidal EMF

BM-MSCs

ELF-EMF

 Magnetic flux density: 1 mT

 Frequency: 50 or 100 Hz

Continuous for up to 8 days

Neurogenic

No effects on cell viability

Increase in the expression of neuronal markers (NeuroD1, MAP2, NF-L)

Stimulation of neural differentiation

Park et al. 2013 [17]

BM-MSCs

ELF-EMF

 Magnetic flux density: 1 mT

 Frequency: 50 Hz

Continuous for 12 days

Neurogenic

Inhibition of MSC growth

Decrease of the neural stem cell marker expression (nestin)

Increase of the neural cell marker expression (MAP2, NeuroD1, NF-L, and Tau)

Cho et al. 2012 [39]

BM-MSCs

ELF-EMF

 Magnetic flux density: 5 mT

 Frequency: 15 Hz

Three times a day (45 min every 8 h) for 21 days

Chondrogenic

More compact structure

Varied effects on cartilage-specific marker expression (increase in COL II, decrease in COL X, or no impact on aggrecan, SOX9)

Higher glycosaminoglycan/DNA content

Improvement of chondrogenic differentiation in combination with growth factor treatment

Mayer-Wagner et al. 2011 [23]

BM-MSCs (derived from fetus)

ELF-EMF

 Magnetic flux density: 20 mT

 Frequency: 50 Hz

12 h/day for up to 23 days

Osteogenic

Decrease of MSC growth and metabolism

No significant effect on MSC differentiation

Yan et al. 2010 [38]

ASCs

EMF

 Magnetic flux density: 1 mT

 Frequency: 30/45 Hz (positive differentiation conditions); 7.5 Hz (negative differentiation conditions)

8 h/day

Osteogenic

Alterations in ALP expression level

Alterations in osteogenic differentiation level

Alterations in the expression of osteogenic markers

Enhancement of matrix mineralization

Kang et al. 2013 [6]

ESCs

Low-frequency EMF

 Magnetic flux density: 5 mT

 Frequency: 1, 10, and 50 Hz

30 min/day for 3, 5, or 7 days

–

Increase in cell proliferation rate, in a frequency-dependent manner (the highest rate in the 50 Hz group)

Alterations in the cell cycle

No effect on cell morphology and cell phenotype

Zhang et al. 2013 [35]

Combination of static and sinusoidal EMF

CSCs

Static MF

 Magnetic flux density: 10 μT

Sinusoidal ELF-EMF

 Magnetic flux density: 2.5 μT

 Frequency: 7 Hz (Ca2+ ICR)

Up to 5 days

Cardiogenic

Increase in metabolic activity

Increase in proliferation rate

Increase in the expression of cardiac markers (TnI, MHC, Nkx2.5)

Decrease (SMA) or no change (VEGF, KDR) in the expression of vascular markers

Alterations in the intracellular calcium distribution

Gaetani et al. 2009 [11]

CSCs/BM-MSCs

Static MF

 Magnetic flux density: 10 μT

Sinusoidal ELF-EMF

 Frequency: 7 Hz (Ca2+ ICR)

For 5 days

Cardiogenic/osteogenic

Upregulation of cardiac markers (TnI, MHC)

Downregulation of angiogenic markers (VEGF, KDR)

Increase in the expression of osteogenic markers (ALP, OC, OPN)

Alterations in plasma membrane morphology accompanied by a rearrangement in actin filaments

Lisi et al. 2008 [43]

Pulsed EMF

     

BM-MSCs

Magnetic flux density: 1.1 mT

Frequency: 5, 25, 50, 75, 100, and 150 Hz

30 min/day for 21 days

Osteogenic

Alterations in cell morphology

Increase in ALP expression and activity

Increase in the expression of osteogenic markers (COL I, OC)

Stimulation of osteogenic differentiation

Enhancement of matrix mineralization

Luo et al. 2012 [7]

BM-MSCs

Magnetic flux density: 1.8–3 mT

Frequency: 75 Hz

8 h/day for 14 days

Osteogenic

Acceleration of cell proliferation

Alterations in cell cycle

Increase in ALP expression level

Enhancement of the osteogenic differentiation

Esposito et al. 2012 [45]

BM-MSCs

Time of pulses: 300 μs (repetitive single quasi-rectangular pulses)

Magnetic flux density: 0.13 mT

Frequency: 7.5 Hz

2 h/day for 14 days

Osteogenic

Time-dependent alterations in cell proliferation rate

Stimulation of ALP activity at day 7

Enhancement of early osteogenic genes expression (Runx2/Cbfa1 and ALP) during the mid-stage of osteogenic differentiation

Tsai et al. 2009 [5]

BM-MSCs

Time of bursts: 5 ms

Time of pulses: 5 μs

Magnetic flux density: 0.1 mT

Frequency:15 Hz

Continuous exposure

Osteogenic

Increase of matrix mineralization

No effect on ALP activity

Upregulation of several osteogenic marker genes (BMP-2, OC, OPG, IBSP, MMP-1, MMP-3)

Stimulation of osteogenic differentiation

Jansen et al. 2010 [41]

BM-MSCs/osteoblast-like cells

Time of bursts: 5 ms

Time of pulses: 1 μs

Magnetic flux density: 0.1 mT

Frequency:15 Hz

Continuous exposure

Osteogenic

Increase of cell viability rate

No effect on osteo-induction

Kaivosoja et al. 2015 [47]

BM-MSCs

Time of bursts: 4.5 ms

Number of pulses: 20

Magnetic flux density: 1.8 mT (increase from 0 to 1.8 mT in 200 μs steps and then decrease to 0 mT in 25 μs steps during each pulse)

Frequency: 15 Hz

8 h/day during culture period

Osteogenic, adipogenic, neurogenic

Enhancement of cell proliferation rate

Increase of cell densities

Alterations of cell cycle progression

No effect on the surface phenotype or multilineage differentiation potential

Sun et al. 2009 [21]

BM-MSCs

Time of bursts: 4.5 ms

Number of pulses: 20

Magnetic flux density: 1.8 mT (increase from 0 to 1.8 mT in 200 μs steps and then decrease to 0 mT in 25 μs steps during each pulse)

Frequency: 15 Hz

8 h/day during the culture period

Osteogenic

Increase in cell proliferation

Increase in ALP expression and activity

Time-dependent alterations of osteogenic marker expression (BMP-2, Cbfa1, COL I, OC)

Enhancement of matrix mineralization

Sun et al. 2010 [33]

BM-MSCs/osteoblast-like cells

Time of bursts: 4.5 ms

Number of pulses: 20

Magnetic flux density: 1.6 mT (increase from 0 to 1.6 mT in 200 μs steps and then decrease to 0 mT in 25 μs steps during each pulse)

Frequency: 15 Hz

8 h/day

Osteogenic

Surface-dependent decrease in cell number

Increase in OPG expression level

Schwartz et al. 2009 [37]

BM-MSCs/ASCs

Number of pulses: 10

Time of pulses: 1.3 ms

Magnetic flux density: 1.5 mT

Frequency: 75 Hz

Whole differentiation time (28 days)

Osteogenic

Increase in ALP activity

Increase in OC expression

Induction of ASC osteogenic differentiation

Enhancement of matrix mineralization

Ongaro et al. 2014 [49]

BM-MSCs

Time of bursts: 4.5 ms

Number of pulses: 20

Magnetic flux density: 1.6 mT (increase from 0 to 1.6 mT in 200 μs steps and then decrease to 0 mT in 25 μs steps during each pulse)

Frequency: 15 Hz

8 h/day for 24 days

Osteogenic

Synergistic increase in ALP activity over that caused by BMP-2

Enhancement of the stimulatory effect of BMP-2 on OC

Schwartz et al. 2008 [40]

WJ-MSCs

Magnetic flux density: 1.8 or 3 mT

Frequency: 75 Hz

8 h/day for up to 21 days

Chondrogenic

Increase in cell division

Increase in cell densities

Increase in COL II expression level

Induction of early chondrogenic differentiation

Esposito et al. 2013 [36]

Sinusoidal PEMF

ESCs

Magnetic flux density: 5 mT

Frequency: 50 Hz

30 min/day for 14 days

–

Increase in proliferation rate

Bai et al. 2012 [32]

Low-frequency pulsed EMF (BEMER type)

BM-MSCs/chondrocytes

Time of pulses: 30 ms

Magnetic flux density: 35 μT (increase from 0 to 35 μT in 30 ms steps)

Frequency: 30 Hz

Five times at 12-h intervals for 8 min

–

Impact on cell metabolism and cell matrix structure

No increased expression of cancer-related genes

Walther et al. 2007 [48]

Pulsed EMF and single-pulse EMF

ASCs

PEMF

 Time of bursts: 67.1 ms

 Number of pulses: 21

 Time of pulses: 5.46 ms

 Magnetic flux density: 2 mT

 Frequency: 15 Hz

SPEMF

 Time of bursts: 5 s

 Number of pulses: 30

 Time of pulses: 5 ms

 Magnetic flux density: 1 T

PEMF: 8 h/day

SPEMF: 3 min/day

Osteogenic/chondrogenic

No effects on cell viability

Increase of the cartilaginous matrix deposition with both PEMF and SPEMF

Enhancement of chondrogenic gene expression (SOX-9, COL II, and aggrecan) with both PEMF and SPEMF

Enhancement of bone matrix gene expression (OC, COL I) only with PEMF

Chen et al. 2013 [42]

  1. ALP alkaline phosphatase, ASC adipose tissue-derived mesenchymal stem cell, BM-MSC bone marrow-mesenchymal stem cell, BMP bone morphogenetic protein, COL collagen type, CSC cardiac stem cell, ELF extremely low frequency, EMF electromagnetic field, ESC epidermal stem cell, IBSP bone sialoprotein, ICR ion cyclotron resonance, KDR kinase domain receptor, MAP2 mitogen activated protein 2, MF magnetic field, MHC myosin heavy chain, MMP matrix metalloproteinase, ms milliseconds, MSC mesenchymal stem cell, NeuroD1 neurogenic differentiation 1, NF-L low-molecular weight neurofilament, Nkx2.5 NK2 transcription factor related, locus 5, OC osteocalcin, OPG osteoprotegerin, OPN osteopontin, OSX osterix, PEMF pulsed electromagnetic field, Runx runt-related transcription factor, SMA smooth muscle actin, SOX9 sex-determining region Y box 9, SPEMF single-pulse electromagnetic field, Tau microtubule associated protein tau, TnI troponin I, VEGF vascular endothelial growth factor, WJ-MSC Wharton’s jelly-mesenchymal stem cell