Abstract
Controlling stem cell (SC) fate is an extremely important topic in the realm of SC research. A variety of different external cues mainly mechanical, chemical, or electrical stimulations individually or in combination have been incorporated to control SC fate. Here, we will deconstruct the probable relationship between the functioning of electromagnetic (EMF) and SC fate of a variety of different SCs. The electromagnetic (EM) nature of the cells is discussed with the emphasis on the effects of EMF on the determinant factors that directly and/or indirectly influence cell fate. Based on the EM effects on a variety of cellular processes, it is believed that EMFs can be engineered to provide a controlled signal with the highest impact on the SC fate decision. Considering the novelty and broad applications of applying EMFs to change SC fate, it is necessary to shed light on many unclear mechanisms underlying this phenomenon.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adams DS, Levin M (2013) Endogenous voltage gradients as mediators of cell-cell communication: strategies for investigating bioelectrical signals during pattern formation. Cell Tissue Res 352:95–122
Adam-Vizi V, Chinopoulos C (2006) Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol Sci 27:639–645
Ahmed S, Passos JF, Birket MJ, Beckmann T, Brings S, Peters H, Birch-Machin MA, von Zglinicki T, Saretzki G (2008) Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J Cell Sci 121:1046–1053
Alwaal A, Zaid UB, Lin C-S, Lue TF (2015) Stem cell treatment of erectile dysfunction. Adv Drug Deliv Rev 82:137–144
Andreyev AY, Kushnareva YE, Starkov A (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70:200–214
Armstrong L, Saretzki G, Peters H, Wappler I, Evans J, Hole N, Von Zglinicki T, Lako M (2005) Overexpression of telomerase confers growth advantage, stress resistance, and enhanced differentiation of ESCs toward the hematopoietic lineage. Stem Cells 23:516–529
Asashima M, Shimada K, Pfeiffer CJ (1991) Magnetic shielding induces early developmental abnormalities in the newt, Cynops pyrrhogaster. Bioelectromagnetics 12:215–224
Baek S, Quan X, Kim S, Lengner C, Park J-K, Kim J (2014) Electromagnetic fields mediate efficient cell reprogramming into a pluripotent state. ACS Nano 8:10125–10138
Bagheri S, Nosrati M, Li S, Fong S, Torabian S, Rangel J, Moore DH, Federman S, LaPosa RR, Baehner FL (2006) Genes and pathways downstream of telomerase in melanoma metastasis. Proc Natl Acad Sci 103:11306–11311
Bauréus Koch C, Sommarin M, Persson B, Salford L, Eberhardt J (2003) Interaction between weak low frequency magnetic fields and cell membranes. Bioelectromagnetics 24:395–402
Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313
Bernardi P, Di Lisa F (2015) The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection. J Mol Cell Cardiol 78:100–106
Bernhard O, Palsson SNB (2004) Tissue engineering. Pearson Prentice Hall
Blank M, Goodman R (2009) Electromagnetic fields stress living cells. Pathophysiology 16:71–78
Blank U, Karlsson G, Karlsson S (2008) Signaling pathways governing stem-cell fate. Blood 111:492–503
Bowne‐Anderson H, Zanic M, Kauer M, Howard J (2013) Microtubule dynamic instability: a new model with coupled GTP hydrolysis and multistep catastrophe. Bioessays 35:452–461
Brown MJ, Loew LM (1994) Electric field-directed fibroblast locomotion involves cell surface molecular reorganization and is calcium independent. J Cell Biol 127:117–128
Cairns RA, Harris IS, Mak TW (2011) Regulation of cancer cell metabolism. Nat Rev Cancer 11:85–95
Calabrò E, Condello S, Currò M, Ferlazzo N, Vecchio M, Caccamo D, Magazù S, Ientile R (2013) 50 Hz electromagnetic field produced changes in FTIR spectroscopy associated with mitochondrial transmembrane potential reduction in neuronal-like SH-SY5Y cells. Oxid Med Cell Longev 2013:414393
Celso CL, Wu JW, Lin CP (2009) In vivo imaging of hematopoietic stem cells and their microenvironment. J Biophotonics 2:619–631
Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia A mechanism of o2 sensing. J Biol Chem 275:25130–25138
Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37–40
Chen G, Upham BL, Sun W, Chang C-C, Rothwell EJ, Chen K-M, Yamasaki H, Trosko JE (2000) Effect of electromagnetic field exposure on chemically induced differentiation of friend erythroleukemia cells. Environ Health Perspect 108:967
Cho MR, Thatte HS, Silvia MT, Golan DE (1999) Transmembrane calcium influx induced by ac electric fields. FASEB J 13:677–683
Cho YM, Kwon S, Pak YK, Seol HW, Choi YM, Park DJ, Park KS, Lee HK (2006) Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells. Biochem Biophys Res Commun 348:1472–1478
Chu L, Hao H, Luo M, Huang Y, Chen Z, Lu T, Zhao X, Verfaillie CM, Zweier JL, Liu Z (2011) Ox‐LDL modifies the behaviour of bone marrow stem cells and impairs their endothelial differentiation via inhibition of Akt phosphorylation. J Cell Mol Med 15:423–432
Chung S, Dzeja PP, Faustino RS, Perez-Terzic C, Behfar A, Terzic A (2007) Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med 4:S60–S67
Clapham DE (2007) Calcium signaling. Cell 131:1047–1058
Consales C, Merla C, Marino C, Benassi B (2012) Electromagnetic fields, oxidative stress, and neurodegeneration. Int J Cell Biol 2012, 683897
Denegre JM, Valles JM, Lin K, Jordan W, Mowry KL (1998) Cleavage planes in frog eggs are altered by strong magnetic fields. Proc Natl Acad Sci 95:14729–14732
Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:780–783
Doyle MJ, Lohr JL, Chapman CS, Koyano-Nakagawa N, Garry MG, Garry DJ (2015) Human induced pluripotent stem cell-derived cardiomyocytes as a model for heart development and congenital heart disease. Stem Cell Rev Rep 11:710–727
Dzierzak E, Enver T (2008) Stem cell researchers find their niche. Development 135:1569–1573
Eliasson P, Jönsson JI (2010) The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol 222:17–22
Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102:4783–4788
Facucho-Oliveira J, John JS (2009) The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev Rep 5:140–158
Falone S, Grossi MR, Cinque B, D’Angelo B, Tettamanti E, Cimini A, Di Ilio C, Amicarelli F (2007) Fifty hertz extremely low-frequency electromagnetic field causes changes in redox and differentiative status in neuroblastoma cells. Int J Biochem Cell Biol 39:2093–2106
Feng B, Qiu L, Ye C, Chen L, Fu Y, Sun W (2016) Exposure to a 50-Hz magnetic field induced mitochondrial permeability transition through the ROS/GSK-3β signaling pathway. Int J Radiat Biol 92:148–155
Fijalkowska I, Xu W, Comhair SA, Janocha AJ, Mavrakis LA, Krishnamachary B, Zhen L, Mao T, Richter A, Erzurum SC (2010) Hypoxia inducible-factor1α regulates the metabolic shift of pulmonary hypertensive endothelial cells. Am J Pathol 176:1130–1138
Forristal CE, Wright KL, Hanley NA, Oreffo RO, Houghton FD (2010) Hypoxia inducible factors regulate pluripotency and proliferation in human embryonic stem cells cultured at reduced oxygen tensions. Reproduction 139:85–97
Funes JM, Quintero M, Henderson S, Martinez D, Qureshi U, Westwood C, Clements MO, Bourboulia D, Pedley RB, Moncada S (2007) Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production. Proc Natl Acad Sci 104:6223–6228
Furse C, Christensen DA, Durney CH (2009) Basic introduction to bioelectromagnetics. CRC Press, Boca Raton
Gaetani R, Ledda M, Barile L, Chimenti I, De Carlo F, Forte E, Ionta V, Giuliani L, D'Emilia E, Frati G (2009) Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc Res 82:411–420
Gattazzo F, Urciuolo A, Bonaldo P (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim Biophys Acta 1840:2506–2519
Gerardi G, De Ninno A, Prosdocimi M, Ferrari V, Barbaro F, Mazzariol S, Bernardini D, Talpo G (2008) Effects of electromagnetic fields of low frequency and low intensity on rat metabolism. Biomagn Res Technol 6:3
Gherardini L, Ciuti G, Tognarelli S, Cinti C (2014) Searching for the perfect wave: the effect of radiofrequency electromagnetic fields on cells. Int J Mol Sci 15:5366–5387
Gillo B, Ma Y-S, Marks A (1993) Calcium influx in induced differentiation of murine erythroleukemia cells. Blood 81:783–792
Goldstein LS, Reyna S, Woodruff G (2015) Probing the secrets of Alzheimer’s disease using human-induced pluripotent stem cell technology. Neurotherapeutics 12:121–125
Grassi C, D’Ascenzo M, Torsello A, Martinotti G, Wolf F, Cittadini A, Azzena GB (2004) Effects of 50Hz electromagnetic fields on voltage-gated Ca < sup > 2 + </sup > channels and their role in modulation of neuroendocrine cell proliferation and death. Cell Calcium 35:307–315
Graziewicz MA, Day BJ, Copeland WC (2002) The mitochondrial DNA polymerase as a target of oxidative damage. Nucleic Acids Res 30:2817–2824
Guo Y, Einhorn L, Kelley M, Hirota K, Yodoi J, Reinbold R, Scholer H, Ramsey H, Hromas R (2004) Redox regulation of the embryonic stem cell transcription factor oct‐4 by thioredoxin. Stem Cells 22:259–264
Guo Y-L, Chakraborty S, Rajan SS, Wang R, Huang F (2010) Effects of oxidative stress on mouse embryonic stem cell proliferation, apoptosis, senescence, and self-renewal. Stem Cells Dev 19:1321–1331
Halgamuge MN, Perssont BR, Salford LG, Mendis P, Eberhardt J (2009) Comparison between two models for interactions between electric and magnetic fields and proteins in cell membranes. Environ Eng Sci 26:1473–1480
Hamanaka RB, Chandel NS (2009) Mitochondrial reactive oxygen species regulate hypoxic signaling. Curr Opin Cell Biol 21:894–899
Hamanaka RB, Chandel NS (2010) Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 35:505–513
Han J, Won E-J, Lee B-Y, Hwang U-K, Kim I-C, Yim JH, Leung KMY, Lee YS, Lee J-S (2014) Gamma rays induce DNA damage and oxidative stress associated with impaired growth and reproduction in the copepod Tigriopus japonicus. Aquat Toxicol 152:264–272
Harris VK, Sadiq SA (2015) Stem cell therapy in multiple sclerosis: a future perspective. Neurodegener Dis Manag 5:167–170
Havelka D, Cifra M, Kučera O, Pokorný J, Vrba J (2011) High-frequency electric field and radiation characteristics of cellular microtubule network. J Theor Biol 286:31–40
Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN (2009) The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 8:3274–3284
Hochedlinger K, Plath K (2009) Epigenetic reprogramming and induced pluripotency. Development 136:509–523
Holland JD, Klaus A, Garratt AN, Birchmeier W (2013) Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol 25:254–264
Hosokawa K, Arai F, Yoshihara H, Nakamura Y, Gomei Y, Iwasaki H, Miyamoto K, Shima H, Ito K, Suda T (2007) Function of oxidative stress in the regulation of hematopoietic stem cell-niche interaction. Biochem Biophys Res Commun 363:578–583
Houghton FD (2006) Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation 74:11–18
Huang X, Cho S, Spangrude G (2007) Hematopoietic stem cells: generation and self-renewal. Cell Death Differ 14:1851–1859
Inaba M, Yamashita YM (2012) Asymmetric stem cell division: precision for robustness. Cell Stem Cell 11:461–469
James AW, Shen J, Zhang X, Asatrian G, Goyal R, Kwak JH, Jiang L, Bengs B, Culiat CT, Turner AS (2015) NELL-1 in the treatment of osteoporotic bone loss. Nat Commun 6
Jelenković A, Janać B, Pešić V, Jovanović D, Vasiljević I, Prolić Z (2006) Effects of extremely low-frequency magnetic field in the brain of rats. Brain Res Bull 68:355–360
Jelınek F, Pokorný J, Šaroch J, Trkal V, Hašek J, Palán B (1999) Microelectronic sensors for measurement of electromagnetic fields of living cells and experimental results. Bioelectrochem Bioenerg 48:261–266
Ji A-R, Ku S-Y, Cho MS, Kim YY, Kim YJ, Oh SK, Kim SH, Moon SY, Choi YM (2010) Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp Mol Med 42:175–186
Jiang F-Y, Tang L-L, Zeng C, Liu H, Liang K-D, Mi Y, Sun C-X (2008) Effects of electric pulses on apoptosis induction and mitochondrial transmembrane potential of cancer cells. In: 7th Asian-Pacific conference on medical and biological engineering. Springer, pp 511–513
Juntilla MM, Patil VD, Calamito M, Joshi RP, Birnbaum MJ, Koretzky GA (2010) AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115:4030–4038
Kang J, Shakya A, Tantin D (2009a) Stem cells, stress, metabolism and cancer: a drama in two Octs. Trends Biochem Sci 34:491–499
Kang J, Gemberling M, Nakamura M, Whitby FG, Handa H, Fairbrother WG, Tantin D (2009b) A general mechanism for transcription regulation by Oct1 and Oct4 in response to genotoxic and oxidative stress. Genes Dev 23:208–222
Kang KS, Hong JM, Kang JA, Rhie J-W, Jeong YH, Cho D-W (2013) Regulation of osteogenic differentiation of human adipose-derived stem cells by controlling electromagnetic field conditions. Exp Mol Med 45, e6
Katsir G, Parola AH (1998) Enhanced proliferation caused by a low frequency weak magnetic field in chick embryo fibroblasts is suppressed by radical scavengers. Biochem Biophys Res Commun 252:753–756
Kemp K, Redondo J, Mallam E, Scolding N, Wilkins A (2015) The use of mesenchymal stem cells for treating neurodegenerative diseases. In: Stem cells and cancer stem cells, vol 13. Springer, pp 3–20
Knoblich JA (2001) Asymmetric cell division during animal development. Nat Rev Mol Cell Biol 2:11–20
Knoblich JA (2008) Mechanisms of asymmetric stem Cell Division. Cell 132:583–597
Kobayashi-Miura M, Nakamura H, Yodoi J, Shiota K (2002) Thioredoxin, an anti-oxidant protein, protects mouse embryos from oxidative stress-induced developmental anomalies. Free Radic Res 36:949–956
Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, Bernard D, Gil J, Beach D (2007) A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 9:293–299
Kristián T, Gertsch J, Bates TE, Siesjö BK (2000) Characteristics of the calcium‐triggered mitochondrial permeability transition in nonsynaptic brain mitochondria. J Neurochem 74:1999–2009
Larsimont JC, Blanpain C (2015) Single stem cell gene therapy for genetic skin disease. EMBO Mol Med 7:366–367
Lee B-C, Johng H-M, Lim J-K, Jeong JH, Baik KY, Nam TJ, Lee JH, Kim J, Sohn UD, Yoon G (2004) Effects of extremely low frequency magnetic field on the antioxidant defense system in mouse brain: a chemiluminescence study. J Photochem Photobiol B 73:43–48
Lee MK, Hande MP, Sabapathy K (2005) Ectopic mTERT expression in mouse embryonic stem cells does not affect differentiation but confers resistance to differentiation-and stress-induced p53-dependent apoptosis. J Cell Sci 118:819–829
Leszczynski D, Joenväärä S, Reivinen J, Kuokka R (2002) Non‐thermal activation of the hsp27/p38MAPK stress pathway by mobile phone radiation in human endothelial cells: molecular mechanism for cancer‐and blood‐brain barrier‐related effects. Differentiation 70:120–129
Levin M (2003) Bioelectromagnetics in morphogenesis. Bioelectromagnetics 24:295–315
Li L, Jiang J (2011) Stem cell niches and endogenous electric fields in tissue repair. Front Med 5:40–44
Li L, Neaves WB (2006) Normal stem cells and cancer stem cells: the niche matters. Cancer Res 66:4553–4557
Li S, Crothers J, Haqq CM, Blackburn EH (2005) Cellular and gene expression responses involved in the rapid growth inhibition of human cancer cells by RNA interference-mediated depletion of telomerase RNA. J Biol Chem 280:23709–23717
Li H-J, Guo L-M, Yang L-L, Zhou Y-C, Zhang Y-J, Guo J, Xie X-J, Guo G-Z (2013) Electromagnetic-pulse-induced activation of p38 MAPK pathway and disruption of blood-retinal barrier. Toxicol Lett 220:35–43
Lim K-T, Kim J-H, Seonwoo H, Son H-M, Baik S-J, Park J-Y, Jeon S-H, Kim E-S, Choung Y-H, Cho C-S (2009) In vitro effects of electromagnetic field stimulation on cells in tissue engineering. Tissue Eng Regener Med 6:675–684
Lin CC, Lin RW, Chang CW, Wang GJ, Lai KA (2015) Single‐pulsed electromagnetic field therapy increases osteogenic differentiation through Wnt signaling pathway and sclerostin downregulation. Bioelectromagnetics 36:494–505
Liu C, Duan W, Xu S, Chen C, He M, Zhang L, Yu Z, Zhou Z (2013) Exposure to 1800MHz radiofrequency electromagnetic radiation induces oxidative DNA base damage in a mouse spermatocyte-derived cell line. Toxicol Lett 218:2–9
Lonergan T, Brenner C, Bavister B (2006) Differentiation‐related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol 208:149–153
Lonergan T, Bavister B, Brenner C (2007) Mitochondria in stem cells. Mitochondrion 7:289–296
Loureiro R, Mesquita KA, Oliveira PJ, Vega-Naredo I (2013) Mitochondria in cancer stem cells: a target for therapy. Recent Pat Endocr Metab Immune Drug Dis 7:102–114
Lu T, Parthasarathy S, Hao H, Luo M, Ahmed S, Zhu J, Luo S, Kuppusamy P, Sen CK, Verfaillie CM (2010) Reactive oxygen species mediate oxidized low-density lipoprotein-induced inhibition of oct-4 expression and endothelial differentiation of bone marrow stem cells. Antioxid Redox Signal 13:1845–1856
Ma Q, Deng P, Zhu G, Liu C, Zhang L, Zhou Z, Luo X, Li M, Zhong M, Yu Z (2014) Extremely low-frequency electromagnetic fields affect transcript levels of neuronal differentiation-related genes in embryonic neural stem cells. PLoS One 9, e90041
Maioli M, Rinaldi S, Santaniello S, Castagna A, Pigliaru G, Gualini S, Cavallini C, Fontani V, Ventura C (2013) Radio electric conveyed fields directly reprogram human dermal skin fibroblasts toward cardiac, neuronal, and skeletal muscle-like lineages. Cell Transplant 22:1227–1235
Malmivuo J, Plonsey R (1995) Bioelectromagnetism: principles and applications of bioelectric and biomagnetic fields. Oxford University Press
Masri FA, Comhair SA, Dostanic‐Larson I, Kaneko FT, Dweik RA, Arroliga AC, Erzurum SC (2008) Deficiency of lung antioxidants in idiopathic pulmonary arterial hypertension. Clin Transl Sci 1:99–106
Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CM, Hubaud A, Stadler B, Choi M, Bar M (2011) HIF induces human embryonic stem cell markers in cancer cells. Cancer Res 71:4640–4652
Matthews RE (2007) Harold burr's biofields measuring the electromagnetics of life. Subtle Energies Energy Med J Arch 18
Mayer‐Wagner S, Passberger A, Sievers B, Aigner J, Summer B, Schiergens TS, Jansson V, Müller PE (2011) Effects of low frequency electromagnetic fields on the chondrogenic differentiation of human mesenchymal stem cells. Bioelectromagnetics 32:283–290
Megha K, Deshmukh PS, Banerjee BD, Tripathi AK, Ahmed R, Abegaonkar MP (2015) Low intensity microwave radiation induced oxidative stress, inflammatory response and DNA damage in rat brain. Neurotoxicology 51:158–165
Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642
Moon J-H, Heo JS, Kim JS, Jun EK, Lee JH, Kim A, Kim J, Whang KY, Kang Y-K, Yeo S (2011) Reprogramming fibroblasts into induced pluripotent stem cells with Bmi1. Cell Res 21:1305–1315
Moon SH, Jenkins CM, Kiebish MA, Sims HF, Mancuso DJ, Gross RW (2012) Genetic ablation of calcium-independent phospholipase A2γ (iPLA2γ) attenuates calcium-induced opening of the mitochondrial permeability transition pore and resultant cytochrome c release. J Biol Chem 287:29837–29850
Morabito C, Rovetta F, Bizzarri M, Mazzoleni G, Fanò G, Mariggiò MA (2010) Modulation of redox status and calcium handling by extremely low frequency electromagnetic fields in C2C12 muscle cells: a real-time, single-cell approach. Free Radic Biol Med 48:579–589
Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068–1074
Mycielska ME, Djamgoz MB (2004) Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease. J Cell Sci 117:1631–1639
Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2007) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26:101–106
Nakamura M, Bhatnagar A, Sadoshima J (2012) Overview of pyridine nucleotides review series. Circ Res 111:604–610
Napotnik TB, Wu YH, Gundersen MA, Miklavčič D, Vernier PT (2012) Nanosecond electric pulses cause mitochondrial membrane permeabilization in Jurkat cells. Bioelectromagnetics 33:257–264
Neumüller RA, Knoblich JA (2009) Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23:2675–2699
Nichols J (2001) Introducing embryonic stem cells. Curr Biol 11:R503–R505
Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Schöler H, Smith A (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391
Nicotera P, Thor H, Orrenius S (1989) Cytosolic-free Ca2+ and cell killing in hepatoma 1c1c7 cells exposed to chemical anoxia. FASEB J 3:59–64
Nordberg J, Arner ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312
Nusse R (2008) Wnt signaling and stem cell control. Cell Res 18:523–527
Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448:313–317
Oktem F, Ozguner F, Mollaoglu H, Koyu A, Uz E (2005) Oxidative damage in the kidney induced by 900-MHz-emitted mobile phone: protection by melatonin. Arch Med Res 36:350–355
Onuma EK, Hui S-W (1988) Electric field-directed cell shape changes, displacement, and cytoskeletal reorganization are calcium dependent. J Cell Biol 106:2067–2075
Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115–128
Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922
Panagopoulos DJ (2014) Electromagnetic interaction between environmental fields and living systems determines health and well-being. Int J Condens Matter Adv Mater Superconductivity Res 13:99
Panagopoulos DJ, Karabarbounis A, Margaritis LH (2002) Mechanism for action of electromagnetic fields on cells. Biochem Biophys Res Commun 298:95–102
Papayannopoulou T, Scadden DT (2008) Stem-cell ecology and stem cells in motion. Blood 111:3923–3930
Park J-E, Seo Y-K, Yoon H-H, Kim C-W, Park J-K, Jeon S (2013) Electromagnetic fields induce neural differentiation of human bone marrow derived mesenchymal stem cells via ROS mediated EGFR activation. Neurochem Int 62:418–424
Parker GC, Acsadi G, Brenner CA (2009) Mitochondria: determinants of stem cell fate? Stem Cells Dev 18:803–806
Pauklin S, Vallier L (2013) The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135–147
Pesce M, Schöler HR (2000) Oct‐4: Control of totipotency and germline determination. Mol Reprod Dev 55:452–457
Pesce M, Schöler HR (2001) Oct-4:gatekeeper in the beginnings of mammalian development. Stem Cells 19:271–278
Pienta KJ, Hoover CN (1994) Coupling of cell structure to cell metabolism and function. J Cell Biochem 55:16–21
Pokorný J (2004) Excitation of vibrations in microtubules in living cells. Bioelectrochemistry 63:321–326
Pokorný J (2012) Physical aspects of biological activity and cancer. AIP Adv 2:011207
Pokorný J, Jelínek F, Trkal V, Lamprecht I, Hölzel R (1997) Vibrations in microtubules. J Biol Phys 23:171–179
Pokorný J, Hašek J, Jelínek F, Šaroch J, Palán B (2001) Electromagnetic activity of yeast cells in the M phase. Electro- Magnetobiol 20:371–396
Rafalski VA, Brunet A (2011) Energy metabolism in adult neural stem cell fate. Prog Neurobiol 93:182–203
Rahnama M, Tuszynski JA, Bokkon I, Cifra M, Sardar P, Salari V (2011) Emission of mitochondrial biophotons and their effect on electrical activity of membrane via microtubules. J Integr Neurosci 10:65–88
Ramalho R, Soares H, Melo L (2007) Microtubule behavior under strong electromagnetic fields. Mater Sci Eng C 27:1207–1210
Ramalho‐Santos M (2004) Stem cells as probabilistic self‐producing entities. Bioessays 26:1013–1016
Rattis FM, Voermans C, Reya T (2004) Wnt signaling in the stem cell niche. Curr Opin Hematol 11:88–94
Rehman J (2010) Empowering self-renewal and differentiation: the role of mitochondria in stem cells. J Mol Med 88:981–986
Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111
Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423:409–414
Rodda DJ, Chew J-L, Lim L-H, Loh Y-H, Wang B, Ng H-H, Robson P (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280:24731–24737
Rollwitz J, Lupke M, Simkó M (2004) Fifty-hertz magnetic fields induce free radical formation in mouse bone marrow-derived promonocytes and macrophages. Biochim Biophys Acta 1674:231–238
Roman A, Tombarkiewicz B (2009) Prolonged weakening of the geomagnetic field (GMF) affects the immune system of rats. Bioelectromagnetics 30:21–28
Rump A, Scholz T, Thiel C, Hartmann FK, Uta P, Hinrichs MH, Taft MH, Tsiavaliaris G (2011) Myosin-1C associates with microtubules and stabilizes the mitotic spindle during cell division. J Cell Sci 124:2521–2528
Ryan AK, Rosenfeld MG (1997) POU domain family values: flexibility, partnerships, and developmental codes. Genes Dev 11:1207–1225
Samudio I, Fiegl M, McQueen T, Clise-Dwyer K, Andreeff M (2008) The Warburg effect in leukemia-stroma cocultures is mediated by mitochondrial uncoupling associated with uncoupling protein 2 activation. Cancer Res 68:5198–5205
Samudio I, Fiegl M, Andreeff M (2009) Mitochondrial uncoupling and the Warburg effect: molecular basis for the reprogramming of cancer cell metabolism. Cancer Res 69:2163–2166
Saretzki G (2005) Telomerase and oxidative stress in embryonic stem cells. Embryonic stem cells: the hormonal regulation of pluripotency and embryogenesis. Lippincott & Williams, Philadelphia
Saretzki G, Walter T, Atkinson S, Passos JF, Bareth B, Keith WN, Stewart R, Hoare S, Stojkovic M, Armstrong L (2008) Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells 26:455–464
Saretzki G (2009) Telomerase, mitochondria and oxidative stress. Exp Gerontol 44:485–492
Sauer H, Wartenberg M (2005) Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxid Redox Signal 7:1423–1434
Sauer H, Rahimi G, Hescheler J, Wartenberg M (1999) Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J Cell Biochem 75:710–723
Scarpa A, Graziotti P (1973) Mechanisms for intracellular calcium regulation in heart I. Stopped-flow measurements of Ca++ uptake by cardiac mitochondria. J Gen Physiol 62:756–772
Schmelter M, Ateghang B, Helmig S, Wartenberg M, Sauer H (2006) Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 20:1182–1184
Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9:726–735
Serena E, Figallo E, Tandon N, Cannizzaro C, Gerecht S, Elvassore N, Vunjak-Novakovic G (2009) Electrical stimulation of human embryonic stem cells: cardiac differentiation and the generation of reactive oxygen species. Exp Cell Res 315:3611–3619
Shakya A, Cooksey R, Cox JE, Wang V, McClain DA, Tantin D (2009) Oct1 loss of function induces a coordinate metabolic shift that opposes tumorigenicity. Nat Cell Biol 11:320–327
Siller KH, Doe CQ (2009) Spindle orientation during asymmetric cell division. Nat Cell Biol 11:365–374
Simeonova M, Wachner D, Gimsa J (2002) Cellular absorption of electric field energy: influence of molecular properties of the cytoplasm. Bioelectrochemistry 56:215–218
Simkó M (2004) Induction of cell activation processes by low frequency electromagnetic fields. Scientific World Journal 4:4–22
Simko M (2007) Cell type specific redox status is responsible for diverse electromagnetic field effects. Curr Med Chem 14:1141–1152
Singh AM, Dalton S (2014) Cell cycle regulation of pluripotent stem cells. Stem cells: from basic research to therapy: basic stem cell biology, tissue formation during development, and model organisms 1:3
Soda A, Ikehara T, Kinouchi Y, Yoshizaki K (2008) Effect of exposure to an extremely low frequency-electromagnetic field on the cellular collagen with respect to signaling pathways in osteoblast-like cells. J Med Invest 55:267–278
Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104
Šrobár F (2012) Fröhlich systems in cellular physiology. Prague Med Rep 113:95–104
Šrobár F (2013) Impact of mitochondrial electric field on modal occupancy in the Fröhlich model of cellular electromagnetism. Electromagn Biol Med 32:401–408
St. John JC, Ramalho-Santos J, Gray HL, Petrosko P, Rawe VY, Navara CS, Simerly CR, Schatten GP (2005) The expression of mitochondrial DNA transcription factors during early cardiomyocyte in vitro differentiation from human embryonic stem cells. Cloning Stem Cells 7:141–153
Stracke R, Böhm K, Wollweber L, Tuszynski J, Unger E (2002) Analysis of the migration behaviour of single microtubules in electric fields. Biochem Biophys Res Commun 293:602–609
Suda T, Arai F, Hirao A (2005) Hematopoietic stem cells and their niche. Trends Immunol 26:426–433
Suda T, Takubo K, Semenza GL (2011) Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9:298–310
Taylor GW, Harvey EN (1931) The theory of mitogenetic radiation. Biol Bull 61:280–293
Thar R, Kühl M (2004) Propagation of electromagnetic radiation in mitochondria? J Theor Biol 230:261–270
Torres-Duran PV, Ferreira-Hermosillo A, Juarez-Oropeza MA, Elias-Viñas D, Verdugo-Diaz L (2007) Effects of whole body exposure to extremely low frequency electromagnetic fields (ELF-EMF) on serum and liver lipid levels, in the rat. Lipids Health Dis 6:31
Trushko A, Schäffer E, Howard J (2013) The growth speed of microtubules with XMAP215-coated beads coupled to their ends is increased by tensile force. Proc Natl Acad Sci 110:14670–14675
Tsai M-T, Li W-J, Tuan RS, Chang WH (2009) Modulation of osteogenesis in human mesenchymal stem cells by specific pulsed electromagnetic field stimulation. J Orthop Res 27:1169
Valles JM (2002) Model of magnetic field-induced mitotic apparatus reorientation in frog eggs. Biophys J 82:1260–1265
Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM (2012) p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149:1536–1548
Vladimirov YA, Proskurnina E (2009) Free radicals and cell chemiluminescence. Biochemistry (Moscow) 74:1545–1566
Walczak CE, Cai S, Khodjakov A (2010) Mechanisms of chromosome behaviour during mitosis. Nat Rev Mol Cell Biol 11:91–102
Walleczek J (1992) Electromagnetic field effects on cells of the immune system: the role of calcium signaling. FASEB J 6:3177–3185
Wang B (2010) Phosphoproteome studies of human mitotic spindle proteinslmu
Wang C, Zhou H, Peng R, Wang L, Su Z, Chen P, Wang S, Wang S, Liu Y, Cong J (2013) Electromagnetic pulse reduces free radical generation in rat liver mitochondria in vitro. Free Radic Res 47:276–282
Waris G, Ahsan H (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 5:14
Watt FM, Hogan B (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430
Watt FM, Huck WT (2013) Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 14:467–473
Waypa GB, Marks JD, Mack MM, Boriboun C, Mungai PT, Schumacker PT (2002) Mitochondrial reactive oxygen species trigger calcium increases during hypoxia in pulmonary arterial myocytes. Circ Res 91:719–726
Wesbuer S, Lanvers-Kaminsky C, Duran-Seuberth I, Bolling T, Schafer K-L, Braun Y, Willich N, Greve B (2010) Association of telomerase activity with radio-and chemosensitivity of neuroblastomas. Radiat Oncol 5:66
White J, Dalton S (2005) Cell cycle control of embryonic stem cells. Stem Cell Rev 1:131–138
Wolff EF, Mutlu L, Massasa EE, Elsworth JD, Eugene Redmond D, Taylor HS (2015) Endometrial stem cell transplantation in MPTP‐exposed primates: an alternative cell source for treatment of Parkinson's disease. J Cell Mol Med 19:249–256
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
Yang C, Przyborski S, Cooke MJ, Zhang X, Stewart R, Anyfantis G, Atkinson SP, Saretzki G, Armstrong L, Lako M (2008) A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 26:850–863
Yang Y, Tao C, Zhao D, Li F, Zhao W, Wu H (2010) EMF acts on rat bone marrow mesenchymal stem cells to promote differentiation to osteoblasts and to inhibit differentiation to adipocytes. Bioelectromagnetics 31:277–285
Ye XQ, Li Q, Wang GH, Sun FF, Huang GJ, Bian XW, Yu SC, Qian GS (2011) Mitochondrial and energy metabolism‐related properties as novel indicators of lung cancer stem cells. Int J Cancer 129:820–831
Young RA (2011) Control of the embryonic stem cell state. Cell 144:940–954
Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920
Zang L-Y, Cosma G, Gardner H, Vallyathan V (1998) Scavenging of reactive oxygen species by melatonin. Biochim Biophys Acta 1425:469–477
Zeni O, Di Pietro R, d'Ambrosio G, Massa R, Capri M, Naarala J, Juutilainen J, Scarfì MR (2007) Formation of reactive oxygen species in L929 cells after exposure to 900 MHz RF radiation with and without co-exposure to 3-chloro-4-(dichloromethyl)-5-hydroxy-2 (5H)-furanone. Radiat Res 167:306–311
Zhai M, Jing D, Tong S, Wu Y, Wang P, Zeng Z, Shen G, Wang X, Xu Q, Luo E (2016) Pulsed electromagnetic fields promote in vitro osteoblastogenesis through a Wnt/β‐catenin signaling‐associated mechanism. Bioelectromagnetics 37:152–162
Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12:9–18
Zhang H, Wang ZZ (2008) Mechanisms that mediate stem cell self‐renewal and differentiation. J Cell Biochem 103:709–718
Zhang J, Khvorostov I, Hong JS, Oktay Y, Vergnes L, Nuebel E, Wahjudi PN, Setoguchi K, Wang G, Do A (2011) UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 30:4860–4873
Zhao Y, Zhan Q (2012) Electric fields generated by synchronized oscillations of microtubules, centrosomes and chromosomes regulate the dynamics of mitosis and meiosis. Theor Biol Med Model 9:26
Zhao M, Forrester JV, McCaig CD (1999) A small, physiological electric field orients cell division. Proc Natl Acad Sci 96:4942–4946
Zhou J, He H, Yang L, Chen S, Guo H, Xia L, Liu H, Qin Y, Liu C, Wei X (2012a) Effects of pulsed electromagnetic fields on bone mass and Wnt/β-catenin signaling pathway in ovariectomized rats. Arch Med Res 43:274–282
Zhou W, Choi M, Margineantu D, Margaretha L, Hesson J, Cavanaugh C, Blau CA, Horwitz MS, Hockenbery D, Ware C (2012b) HIF1α induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J 31:2103–2116
Zmyślony M, Politanski P, Rajkowska E, Szymczak W, Jajte J (2004) Acute exposure to 930 MHz CW electromagnetic radiation in vitro affects reactive oxygen species level in rat lymphocytes treated by iron ions. Bioelectromagnetics 25:324–328
Zwirska-Korczala K, Jochem J, Adamczyk-Sowa M, Sowa P, Polaniak R, Birkner E, Latocha M, Pilc K, Suchanek R (2005) Effect of extremely low frequency of electromagnetic fields on cell proliferation, antioxidative enzyme activities and lipid peroxidation in 3T3-L1 preadipocytes-an in vitro study. J Physiol Pharmacol 56:101
Acknowledgments
The authors thank Dr. Mehran Solati for insightful discussions that greatly assisted the research.
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Tamrin, S.H., Majedi, F.S., Tondar, M., Sanati-Nezhad, A., Hasani-Sadrabadi, M.M. (2016). Electromagnetic Fields and Stem Cell Fate: When Physics Meets Biology. In: Nilius, B., de Tombe, P., Gudermann, T., Jahn, R., Lill, R., Petersen, O. (eds) Reviews of Physiology, Biochemistry and Pharmacology, Vol. 171. Reviews of Physiology, Biochemistry and Pharmacology, vol 171. Springer, Cham. https://doi.org/10.1007/112_2016_4
Download citation
DOI: https://doi.org/10.1007/112_2016_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-43813-9
Online ISBN: 978-3-319-43814-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)