Electromagnetic fields mediate efficient cell reprogramming into a pluripotent state

ACS Nano

Volumn 8, Issue 10, 2014, Pages 10125-10138

  Baek, Soonbong ^a   Quan, Xiaoyuan ^a   Kim, Soochan ^b   Lengner, Christopher ^c   Park, Jung Keug ^a   Kim, Jongpil ^a  

^a Dongguk University   (South Korea)

^b Hankyong National University   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

cell reprogramming; electromagnetic fields; epigenetic changes

Indexed keywords

AMINO ACIDS; CYTOLOGY; ELECTROMAGNETIC FIELDS;

BIOLOGICAL PROCESS; CELL REPROGRAMMING; EPIGENETIC CHANGES; EXTREMELY LOW FREQUENCY ELECTROMAGNETIC FIELDS; FUNDAMENTAL MECHANISMS; METHYLTRANSFERASES; NATURAL ELECTROMAGNETIC FIELDS; NATURALLY OCCURRING;

CELLS;

ANIMAL; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; ELECTROMAGNETIC FIELD; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; HEK293 CELL LINE; HUMAN; MOUSE; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLULAR REPROGRAMMING; CHROMATIN IMMUNOPRECIPITATION; ELECTROMAGNETIC FIELDS; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; MICE; PLURIPOTENT STEM CELLS; POLYMERASE CHAIN REACTION;

EID: 84908439331     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn502923s     Document Type: Article

References (46)

1. Hollenbach, D. F.; Herndon, J. M. Deep-Earth Reactor: Nuclear Fission, Helium, and the Geomagnetic Field Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 11085-11090
2. Lacy-Hulbert, A.; Metcalfe, J. C.; Hesketh, R. Biological Responses to Electromagnetic Fields FASEB J. 1998, 12, 395-420
3. Doucet, I. L. Biological Effects of Low Frequency Electromagnetic Fields Med. War 1992, 8, 205-212
4. Arendash, G. W.; Sanchez-Ramos, J.; Mori, T.; Mamcarz, M.; Lin, X.; Runfeldt, M.; Wang, L.; Zhang, G.; Sava, V.; Tan, J. et al. Electromagnetic Field Treatment Protects Against and Reverses Cognitive Impairment in Alzheimers Disease Mice J. Alzheimers Dis. 2010, 19, 191-210
5. Caprani, A.; Richert, A.; Flaud, P. Experimental Evidence of a Potentially Increased Thrombo-Embolic Disease Risk by Domestic Electromagnetic Field Exposure Bioelectromagnetics 2004, 25, 313-315
6. Danilenko, S. R.; Shatrov, A. A.; Gerasimovich, O. I. The Efficacy of Using an Electromagnetic Field of Extremely High Frequency (54-78 GHz) in Treating Patients with Chronic Nonspecific Lung Disease Vopr. Kurortol., Fizioter. Lech. Fiz. Kult. 1995, 16-18
7. Sadlonova, J.; Korpas, J.; Vrabec, M.; Salat, D.; Buchancova, J.; Kudlicka, J. The Effect of the Pulsatile Electromagnetic Field in Patients Suffering from Chronic Obstructive Pulmonary Disease and Bronchial Asthma Bratisl. Lek. Listy 2002, 103, 260-265
8. Bakhmutskii, N. G.; Golubtsov, V. I.; Pyleva, T. A.; Sinitskii, D. A.; Frolov, V. E. A Case of Successful Treatment of a Patient with Breast Cancer Using Rotational Electromagnetic Field Sov. Med. 1991, 86-87
9. Del Vecchio, G.; Giuliani, A.; Fernandez, M.; Mesirca, P.; Bersani, F.; Pinto, R.; Ardoino, L.; Lovisolo, G. A.; Giardino, L.; Calza, L. Effect of Radiofrequency Electromagnetic Field Exposure on In Vitro Models of Neurodegenerative Disease Bioelectromagnetics 2009, 30, 564-572
10. Wang, Q.; Wu, W.; Chen, X.; He, C.; Liu, X. Effect of Pulsed Electromagnetic Field with Different Frequencies on the Proliferation, Apoptosis and Migration of Human Ovarian Cancer Cells Shengwu Yixue Gongchengxue Zazhi 2012, 29, 291-295
11. Maaroufi, K.; Save, E.; Poucet, B.; Sakly, M.; Abdelmelek, H.; Had-Aissouni, L. Oxidative Stress and Prevention of the Adaptive Response to Chronic Iron Overload in the Brain of Young Adult Rats Exposed to a 150 Kilohertz Electromagnetic Field Neuroscience 2011, 186, 39-47
12. Ceccarelli, G.; Bloise, N.; Mantelli, M.; Gastaldi, G.; Fassina, L.; De Angelis, M. G.; Ferrari, D.; Imbriani, M.; Visai, L. A Comparative Analysis of the In Vitro Effects of Pulsed Electromagnetic Field Treatment on Osteogenic Differentiation of Two Different Mesenchymal Cell Lineages BioRes. Open Access 2013, 2, 283-294
13. An, G. Z.; Zhou, Y.; Hou, Q. X.; Li, Y. R.; Jiang, D. P.; Guo, G. Z.; Zhang, C.; Ding, G. R. Effect of Long-Term Power Frequency Electromagnetic Field Exposure on Proliferation and Apoptosis of SRA01/04 Cells Zhonghua Laodong Weisheng Zhiyebing Zazhi 2013, 31, 246-250
14. Seong, Y.; Moon, J.; Kim, J. Egr1 Mediated the Neuronal Differentiation Induced by Extremely Low-Frequency Electromagnetic Fields Life Sci. 2014, 102, 16-27
15. Juutilainen, J. Developmental Effects of Electromagnetic Fields Bioelectromagnetics 2005, 26, S107-S115
16. Hotary, K. B.; Robinson, K. R. Endogenous Electrical Currents and the Resultant Voltage Gradients in the Chick Embryo Dev. Biol. 1990, 140, 149-160
17. Levin, M. Large-Scale Biophysics: Ion Flows and Regeneration Trends Cell Biol. 2007, 17, 261-270
18. Hiraki, Y.; Endo, N.; Takigawa, M.; Asada, A.; Takahashi, H.; Suzuki, F. Enhanced Responsiveness to Parathyroid Hormone and Induction of Functional Differentiation of Cultured Rabbit Costal Chondrocytes by a Pulsed Electromagnetic Field Biochim. Biophys. Acta 1987, 931, 94-100
19. Kang, K. S.; Hong, J. M.; Kang, J. A.; Rhie, J. W.; Jeong, Y. H.; Cho, D. W. Regulation of Osteogenic Differentiation of Human Adipose-Derived Stem Cells by Controlling Electromagnetic Field Conditions Exp. Mol. Med. 2013, 45, e6
20. Meng, D.; Xu, T.; Guo, F.; Yin, W.; Peng, T. The Effects of High-Intensity Pulsed Electromagnetic Field on Proliferation and Differentiation of Neural Stem Cells of Neonatal Rats In vitro J. Huazhong Univ. Sci. Technol., Med. Sci. 2009, 29, 732-736
21. Pesce, M.; Patruno, A.; Speranza, L.; Reale, M. Extremely Low Frequency Electromagnetic Field and Wound Healing: Implication of Cytokines as Biological Mediators Eur. Cytokine Network 2013, 24, 1-10
22. Takahashi, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors Cell 2006, 126, 663-676
23. Lengner, C. J.; Camargo, F. D.; Hochedlinger, K.; Welstead, G. G.; Zaidi, S.; Gokhale, S.; Scholer, H. R.; Tomilin, A.; Jaenisch, R. Oct4 Expression Is Not Required for Mouse Somatic Stem Cell Self-Renewal Cell Stem Cell 2007, 1, 403-415
24. Carey, B. W.; Markoulaki, S.; Hanna, J.; Saha, K.; Gao, Q.; Mitalipova, M.; Jaenisch, R. Reprogramming of Murine and Human Somatic Cells Using a Single Polycistronic Vector Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 157-162
25. Maherali, N.; Sridharan, R.; Xie, W.; Utikal, J.; Eminli, S.; Arnold, K.; Stadtfeld, M.; Yachechko, R.; Tchieu, J.; Jaenish, R. et al. Directly Reprogrammed Fibroblasts Show Global Epigenetic Remodeling and Widespread Tissue Contribution Cell Stem Cell 2007, 1, 55-70
26. Esteban, M. A.; Wang, T.; Qin, B.; Yang, J.; Qin, D.; Cai, J.; Li, W.; Weng, Z.; Chen, J.; Ni, S. et al. Vitamin C Enhances the Generation of Mouse and Human Induced Pluripotent Stem Cells Cell Stem Cell 2010, 6, 71-79
27. Huangfu, D.; Maehr, R.; Guo, W.; Eijkelenboom, A.; Snitow, M.; Chen, A. E.; Melton, D. A. Induction of Pluripotent Stem Cells by Defined Factors is Greatly Improved by Small-Molecule Compounds Nat. Biotechnol. 2008, 26, 795-797
28. Wernig, M.; Lengner, C. J.; Hanna, J.; Lodato, M. A.; Steine, E.; Foreman, R.; Staerk, J.; Markoulaki, S.; Jaenisch, R. A Drug-Inducible Transgenic System for Direct Reprogramming of Multiple Somatic Cell Types Nat. Biotechnol. 2008, 26, 916-924
29. Hanna, J.; Saha, K.; Pando, B.; van Zon, J.; Lengner, C. J.; Creyghton, M. P.; van Oudenaarden, A.; Jaenisch, R. Direct Cell Reprogramming Is a Stochastic Process Amenable to Acceleration Nature 2009, 462, 595-601
30. Antony, J.; Oback, F.; Chamley, L. W.; Oback, B.; Laible, G. Transient JMJD2B-Mediated Reduction of H3K9me3 Levels Improves Reprogramming of Embryonic Stem Cells into Cloned Embryos Mol. Cell. Biol. 2013, 33, 974-983
31. Mansour, A. A.; Gafni, O.; Weinberger, L.; Zviran, A.; Ayyash, M.; Rais, Y.; Krupalnik, V.; Zerbib, M.; Amann-Zalcenstein, D.; Maza, I. et al. The H3K27 Demethylase Utx Regulates Somatic and Germ Cell Epigenetic Reprogramming Nature 2012, 488, 409-413
32. Mattout, A.; Biran, A.; Meshorer, E. Global Epigenetic Changes During Somatic Cell Reprogramming to iPS Cells J. Mol. Cell Biol. 2011, 3, 341-350
33. Belyaev, I. Y.; Hillert, L.; Protopopova, M.; Tamm, C.; Malmgren, L. O.; Persson, B. R.; Selivanova, G.; Harms-Ringdahl, M. 915 MHz Microwaves and 50 Hz Magnetic Field Affect Chromatin Conformation and 53BP1 Foci in Human Lymphocytes from Hypersensitive and Healthy Persons Bioelectromagnetics 2005, 26, 173-184
34. Zhang, Y.; She, F.; Li, L.; Chen, C.; Xu, S.; Luo, X.; Li, M.; He, M.; Yu, Z. p25/CDK5 Is Partially Involved in Neuronal Injury Induced by Radiofrequency Electromagnetic Field Exposure Int. J. Radiat. Biol. 2013, 89, 976-984
35. FitzGerald, K. T.; Diaz, M. O. MLL2: A New Mammalian Nember of the Trx/MLL Family of Genes Genomics 1999, 59, 187-192
36. Marino, S.; Vooijs, M.; van Der Gulden, H.; Jonkers, J.; Berns, A. Induction of Medulloblastomas in p53-null Mutant Mice by Somatic Inactivation of Rb in the External Granular Layer Cells of The Cerebellum Genes Dev. 2000, 14, 994-1004
37. Gyawali, S. R. Design and Construction of Helmholtz Coil for Biomagnetic Studies on Soybean, University of Missouri-Columbia, 2008.
38. Chen, J.; Liu, H.; Liu, J.; Qi, J.; Wei, B.; Yang, J.; Liang, H.; Chen, Y.; Chen, J.; Wu, Y. et al. H3K9 Methylation Is a Barrier during Somatic Cell Reprogramming Into iPSCs Nat. Genet. 2013, 45, 34-42
39. Feng, B.; Ng, J. H.; Heng, J. C.; Ng, H. H. Molecules That Promote or Enhance Reprogramming of Somatic Cells to Induced Pluripotent Stem Cells Cell Stem Cell 2009, 4, 301-312
40. Berg, H. Problems of Weak Electromagnetic Field Effects in Cell Biology Bioelectrochem. Bioenerg. 1999, 48, 355-360
41. Loginov, V. A. Accumulation of Calcium Ions in Myocardial Sarcoplasmic Reticulum of Restrained Rats Exposed to the Pulsed Electromagnetic Field Aviakosm. Ekol. Med. 1992, 26, 49-51
42. Cho, H.; Seo, Y. K.; Yoon, H. H.; Kim, S. C.; Kim, S. M.; Song, K. Y.; Park, J. K. Neural Stimulation on Human Bone Marrow-Derived Mesenchymal Stem Cells by Extremely Low Frequency Electromagnetic Fields Biotechnol. Prog. 2012, 28, 1329-1335
43. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors Cell 2007, 131, 861-872
44. Mahmood, T.; Yang, P. C. Western Blot: Technique, Theory, and Trouble Shooting North Am. J. Med. Sci. 2012, 4, 429-34
45. Doege, C. A.; Inoue, K.; Yamashita, T.; Rhee, D. B.; Travis, S.; Fujita, R.; Guarnieri, P.; Bhagat, G.; Vanti, W. B.; Shih, A. et al. Early-Stage Epigenetic Modification during Somatic Cell Reprogramming by Parp1 and Tet2 Nature 2012, 488, 652-625
46. Kim, J.; Lengner, C. J.; Kirak, O.; Hanna, J.; Cassady, J. P.; Lodato, M. A.; Wu, S.; Faddah, D. A.; Steine, E. J.; Gao, Q. et al. Reprogramming of Postnatal Neurons into Induced Pluripotent Stem Cells by Defined Factors Stem Cells 2011, 29, 992-1000