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With the development of technology and the widespread use of high static magnetic fields (SMFs) in medical diagnosis, such as MRI (magnetic resonance imaging) in hospitals, patients have more and more chances to encounter high SMFs (higher than 1 T), which invokes increasing public concerns about human health. However, due to the experimental limitations, there are very few studies of high SMFs (above 1 T) on animals and human bodies. In contrast, cell, as a basic unit of various organisms, is the primary research target for most researches of the biological effects under the action of magnetic fields. However, due to the differences in magnetic field parameter, exposure condition and cell type, there are diverse experimental outcomes reported by individual studies in the literature. Here in this review, we summarize the results about the cellular effects under SMFs above 1 T, including changes of cell orientation, cell proliferation, microtubule and mitotic spindle orientation, DNA and cell cycle. Moreover, we also compare and analyze the factors that could cause these experimental variations, including the differential effects of high SMFs on cell type, such as cancer and non-cancer cells, as well as magnetic field intensity-induced experimental variations. The most well studied cellular effects are SMF-induced cell and polymer orientation changes, and the cellular composition is a key factor that determines the exact orientation of a cell in an SMF. For example, the normal red blood cell is aligned parallelly to the SMF direction, but the whole bull sperm is aligned perpendicularly to the SMF direction. Among the magnetic field parameters, the magnetic field intensity is especially critical. The red blood cells can only be partially aligned by 1 T SMF, but an 8 T SMF could align the red blood cells 100% along the magnetic direction. Overall, the biological research of high SMFs above 1 T, especially above 10 T, is still at an initial stage. Biological experiments in high SMFs above 20 T are especially lacking. This review could help provide some biological bases for future high SMF investigations, which is important not only for the basic understanding of the biological effects of high SMFs, but also for the applications of high SMFs in medicine, such as high field MRI.
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Keywords:
- high static magnetic fields /
- cell orientation /
- cell proliferation /
- cell type
[1] He Y Z 2013 Acta Phys. Sin. 62 084105 (in Chinese) [何永周 2013 物理学报 62 084105]
[2] van der Kolk A G, Hendrikse J, Zwanenburg J J M, Visser F, Luijten P R 2013 Eur. J. Radiol. 82 708
[3] Vaughan T T, Snyder C J, DelaBarre L J, Bolan P J, Tian J, Bolinger L, Adriany G, Andersen P, Strupp J, Ugurbil K 2009 Magnet. Reson. Med. 61 244
[4] Budde J, Shajan G, Scheffler K, Pohmann R 2014 Neuroimage 86 592
[5] Budinger T F, Bird M D 2017 Neuroimage 168 509
[6] Worcester D L 1978 P. Natl. Acad. Sci. USA 75 5475
[7] Pauling L 1979 Proc. Natl. Acad. Sci. USA 76 2293
[8] Bras W, Torbet J, Diakun G P, Rikken G L, Diaz J F 2014 J. Biophys. 2014 985082
[9] Albuquerque W W, Costa R M, de Fernandes T S, Porto A L 2016 Prog. Biophys. Mol. Biol. 121 16
[10] Zablotskii V, Polyakova T, Lunov O, Dejneka A 2016 Sci. Rep. 6 37407
[11] Iwasaka M, Miyakoshi J, Ueno S 2003 In. Vitro. Cell. Dev-An 39 120
[12] Umeno A, Kotani H, Iwasaka M, Ueno S 2001 IEEE T. Magn. 37 2909
[13] Zhang L, Wang J H, Wang H L, Wang W C, Li Z Y, Liu J J, Yang X X, Ji X M, Luo Y, Hu C, Hou Y B, He Q Q, Fang J, Wang J F, Liu Q S, Li G H, Lu Q Y, Zhang X 2016 Oncotarget 7 41527
[14] Sakurai H, Okuno K, Kubo A, Nakamura K, Shoda M 1999 Bioelectroch. Bioener. 49 57
[15] Hsieh C H, Lee M C, Tsai-Wu J J, Chen M H, Lee H S, Chiang H, Wu C H H, Jiang C C 2008 Osteoarthr. Cartilage. 16 343
[16] Ghibelli L, Cerella C, Cordisco S, Clavarino G, Marazzi S, De Nicola M, Nuccitelli S, D'Alessio M, Magrini A, Bergamaschi A, Guerrisi V, Porfiri L M 2006 Apoptosis 11 359
[17] Higashi T, Yamagishi A, Takeuchi T, Kawaguchi N, Sagawa S, Onishi S, Date M 1993 Blood 82 1328
[18] Zhang X, Yarema K, Xu A 2017 Biological Effects of Static Magnetic Fields (Singapore: Springer) p94
[19] Higashi T, Yamagishi A, Takeuchi T, Date M 1995 Bioelectroch. Bioener. 36 101
[20] Shiga T, Okazaki M, Maeda N, Seiyama A 1996 Biological Effects of Magnetic and Electromagnetic Fields (New York: Springer) p185
[21] Takeuchi T, Mizuno T, Higashi T, Yamagishi A, Date M 1995 J. Magn. Magn. Mater. 140 1462
[22] Kotani H, Iwasaka M, Ueno S, Curtis A 2000 J. Appl. Phys. 87 6191
[23] Kotani H, Kawaguchi H, Shimoaka T, Iwasaka M, Ueno S, Ozawa H, Nakamura K, Hoshi K 2002 J. Bone. Miner. Res. 17 1814
[24] Eguchi Y, Ogiue-Ikeda M, Ueno S 2003 Neurosci. Lett. 351 130
[25] Eguchi Y, Ueno S 2005 IEEE T. Magn. 41 4146
[26] Sakurai T, Hashimoto A, Kiyokawa T, Kikuchi K, Miyakoshi J 2012 Bioelectromagnetics 33 421
[27] Emura R, Takeuchi T, Nakaoka Y, Higashi T 2003 Bioelectromagnetics 24 347
[28] Hirose H, Nakahara T, Miyakoshi J 2003 Neurosci. Lett. 338 88
[29] Zhang X, Yarema K, Xu A 2017 Biological Effects of Static Magnetic Fields (Singapore: Springer) pp81-122 [张欣, 雅瑞玛 K, 徐安合 著 (张磊, 刘娟娟 译) 2017 稳态磁场的生物学效应 (北京: 科学出版社)第81–122页]
[30] Ogiue-Ikeda M, Ueno S 2004 IEEE T. Magn. 40 3024
[31] Emura R, Ashida N, Higashi T, Takeuchi T 2001 Bioelectromagnetics 22 60
[32] Raylman R R, Clavo A C, Wahl R L 1996 Bioelectromagnetics 17 358
[33] Zhang L, Yang X X, Liu J J, Luo Y, Li Z Y, Ji X M, Wang W C, Zhang X 2015 Sci. Bull. 60 2120
[34] Luo Y, Ji X M, Liu J J, Li Z Y, Wang W C, Chen W, Wang J F, Liu Q S, Zhang X 2016 Bioelectrochemistry 109 31
[35] Short W O, Goodwill L, Taylor C W, Job C, Arthur M E, Cress A E 1992 Invest. Radiol. 27 836
[36] Nakahara T, Yaguchi H, Yoshida M, Miyakoshi J 2002 Radiology 224 817
[37] Gao W M, Liu Y Q, Zhou J Z, Pan H J 2005 Bioelectromagnetics 26 558
[38] Reddig A, Fatahi M, Friebe B, Guttek K, Hartig R, Godenschweger F, Roggenbuck D, Ricke J, Reinhold D, Speck O 2015 PLoS One 10 e0132702
[39] Iachininoto M G, Camisa V, Leone L, Pinto R, Lopresto V, Merla C, Giorda E, Carsetti R, Zaffina S, Podda M V, Teofili L, Grassi C 2016 Bioelectromagnetics 37 201
[40] Vassilev P M, Dronzine R T, Vassileva M P, Georgiev G A 1982 Bioscience. Rep. 2 1025
[41] Bras W, Diakun G P, Diaz J F, Maret G, Kramer H, Bordas J, Medrano F J 1998 Biophys. J. 74 1509
[42] Glade N, Tabony J 2005 Biophys. Chem. 115 29
[43] Denegre J M, Valles J M, Jr, Lin K, Jordan W B, Mowry K L 1998 P. Natl. Acad. Sci. USA 95 14729
[44] Eguchi Y, Ueno S, Kaito C, Sekimizu K, Shiokawa K 2006 Bioelectromagnetics 27 307
[45] Valles J M 2002 Biophys. J. 82 1260
[46] Valles J M, Wasserman Jr S R, Schweidenback C, Edwardson J, Denegre J M, Mowry K L 2002 Exp. Cell. Res. 274 112
[47] Valiron O, Peris L, Rikken G, Schweitzer A, Saoudi Y, Remy C, Job D 2005 J. Magn. Reson. Imaging 22 334
[48] Zhang L, Hou Y B, Li Z Y, Ji X M, Wang Z, Wang H Z, Tian X F, Yu F Z, Yang Z Y, Pi L, Mitchison T J, Lu Q Y, Zhang X 2017 Elife 6 e22911
[49] Sato K, Yamaguchi H, Miyamoto H, Kinouchi Y 1992 Biochim. Biophys. Acta 1136 231
[50] Muroski M E, Morshed R A, Cheng Y, Vemulkar T, Mansell R, Han Y, Zhang L, Aboody K S, Cowburn R P, Lesniak M S 2016 PLoS One 11 e0145129
[51] Cheng Y, Muroski M E, Petit D, Mansell R, Vemulkar T, Morshed R A, Han Y, Balyasnikova I V, Horbinski C M, Huang X, Zhang L, Cowburn R P, Lesniak M S 2016 J. Control Release 223 75
[52] Hapuarachchige S, Kato Y, Ngen E J, Smith B, Delannoy M, Artemov D 2016 PLoS One 11 e0156294
[53] Shen Y J, Cheng Y, Uyeda T Q P, Plaza G R 2017 Ann. Biomed. Eng. 45 2475
[54] Son B, Kim H D, Kim M, Kim J A, Lee J, Shin H, Hwang N S, Park T H 2015 Adv. Healthc. Mater. 4 1339
[55] Takashima Y, Miyakoshi J, Ikehata M, Iwasaka M, Ueno S, Koana T 2004 J. Radiat. Res. 45 393
[56] Schwenzer N F, Bantleon R, Maurer B, Kehlbach R, Schraml C, Claussen C D, Rodegerdts E 2007 J. Magn. Reson. Imaging 26 1308
[57] Fatahi M, Reddig A, Vijayalaxmi, Friebe B, Hartig R, Prihoda T J, Ricke J, Roggenbuck D, Reinhold D, Speck O 2016 Neuroimage 133 288
[58] Schiffer I B, Schreiber W G, Graf R, Schreiber E M, Jung D, Rose D M, Hehn M, Gebhard S, Sagemuller J, Spiess H W, Oesch F, Thelen M, Hengstler J G 2003 Bioelectromagnetics 24 241
[59] Zhao G P, Chen S P, Zhao Y, Zhu L Y, Huang P, Bao L Z, Wang J, Wang L, Wu L J, Wu Y J, Xu A 2010 Plasma Sci. Technol. 12 123
[60] Zhang L, Ji X M, Yang X X, Zhang X 2017 Oncotarget 8 13126
[61] Prina-Mello A, Farrell E, Prendergast P J, Campbell V, Coey J M D 2006 Bioelectromagnetics 27 35
[62] Yang J, Zhang J, Ding C, Dong D, Shang P 2017 Biol. Trace. Elem. Res. 184 214
[63] Aldinucci C, Garcia J B, Palmi M, Sgaragli G, Benocci A, Meini A, Pessina F, Rossi C, Bonechi C, Pessina G P 2003 Bioelectromagnetics 24 109
[64] Hackett S, Hamzah J, Davis T M, St Pierre T G 2009 Bba-Mol. Basis. Dis. 1792 93
[65] Lee J, Kim M S, Kim Y J, Choi Y J, Lee Y, Chung H 2011 Bioelectromagnetics 32 535
[66] Zablotskii V, Syrovets T, Schmidt Z W, Dejneka A, Simmet T 2014 Biomaterials 35 3164
[67] Zborowski M, Ostera G R, Moore L R, Milliron S, Chalmers J J, Schechter A N 2003 Biophys. J. 84 2638
[68] Zablotskii V, Dejneka A, Kubinova S, Le-Roy D, Dumas-Bouchiat F, Givord D, Dempsey N M, Sykova E 2013 Plos One 8 e70416
[69] Zhao G, Chen S, Wang L, Zhao Y, Wang J, Wang X, Zhang W, Wu R, Wu L, Wu Y, Xu A 2011 Bioelectromagnetics 32 94
[70] Wang J, Yang G, Liu F 2015 Acta Phys. Sin. 64 058707 (in Chinese) [王璟, 杨根, 刘峰 2015 物理学报 64 058707]
[71] Liu R C, Chen G, Liu L Y 2017 Physics 46 627 (in Chinese) [刘如川, 陈果, 刘雳宇 2017 物理 46 627]
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[1] He Y Z 2013 Acta Phys. Sin. 62 084105 (in Chinese) [何永周 2013 物理学报 62 084105]
[2] van der Kolk A G, Hendrikse J, Zwanenburg J J M, Visser F, Luijten P R 2013 Eur. J. Radiol. 82 708
[3] Vaughan T T, Snyder C J, DelaBarre L J, Bolan P J, Tian J, Bolinger L, Adriany G, Andersen P, Strupp J, Ugurbil K 2009 Magnet. Reson. Med. 61 244
[4] Budde J, Shajan G, Scheffler K, Pohmann R 2014 Neuroimage 86 592
[5] Budinger T F, Bird M D 2017 Neuroimage 168 509
[6] Worcester D L 1978 P. Natl. Acad. Sci. USA 75 5475
[7] Pauling L 1979 Proc. Natl. Acad. Sci. USA 76 2293
[8] Bras W, Torbet J, Diakun G P, Rikken G L, Diaz J F 2014 J. Biophys. 2014 985082
[9] Albuquerque W W, Costa R M, de Fernandes T S, Porto A L 2016 Prog. Biophys. Mol. Biol. 121 16
[10] Zablotskii V, Polyakova T, Lunov O, Dejneka A 2016 Sci. Rep. 6 37407
[11] Iwasaka M, Miyakoshi J, Ueno S 2003 In. Vitro. Cell. Dev-An 39 120
[12] Umeno A, Kotani H, Iwasaka M, Ueno S 2001 IEEE T. Magn. 37 2909
[13] Zhang L, Wang J H, Wang H L, Wang W C, Li Z Y, Liu J J, Yang X X, Ji X M, Luo Y, Hu C, Hou Y B, He Q Q, Fang J, Wang J F, Liu Q S, Li G H, Lu Q Y, Zhang X 2016 Oncotarget 7 41527
[14] Sakurai H, Okuno K, Kubo A, Nakamura K, Shoda M 1999 Bioelectroch. Bioener. 49 57
[15] Hsieh C H, Lee M C, Tsai-Wu J J, Chen M H, Lee H S, Chiang H, Wu C H H, Jiang C C 2008 Osteoarthr. Cartilage. 16 343
[16] Ghibelli L, Cerella C, Cordisco S, Clavarino G, Marazzi S, De Nicola M, Nuccitelli S, D'Alessio M, Magrini A, Bergamaschi A, Guerrisi V, Porfiri L M 2006 Apoptosis 11 359
[17] Higashi T, Yamagishi A, Takeuchi T, Kawaguchi N, Sagawa S, Onishi S, Date M 1993 Blood 82 1328
[18] Zhang X, Yarema K, Xu A 2017 Biological Effects of Static Magnetic Fields (Singapore: Springer) p94
[19] Higashi T, Yamagishi A, Takeuchi T, Date M 1995 Bioelectroch. Bioener. 36 101
[20] Shiga T, Okazaki M, Maeda N, Seiyama A 1996 Biological Effects of Magnetic and Electromagnetic Fields (New York: Springer) p185
[21] Takeuchi T, Mizuno T, Higashi T, Yamagishi A, Date M 1995 J. Magn. Magn. Mater. 140 1462
[22] Kotani H, Iwasaka M, Ueno S, Curtis A 2000 J. Appl. Phys. 87 6191
[23] Kotani H, Kawaguchi H, Shimoaka T, Iwasaka M, Ueno S, Ozawa H, Nakamura K, Hoshi K 2002 J. Bone. Miner. Res. 17 1814
[24] Eguchi Y, Ogiue-Ikeda M, Ueno S 2003 Neurosci. Lett. 351 130
[25] Eguchi Y, Ueno S 2005 IEEE T. Magn. 41 4146
[26] Sakurai T, Hashimoto A, Kiyokawa T, Kikuchi K, Miyakoshi J 2012 Bioelectromagnetics 33 421
[27] Emura R, Takeuchi T, Nakaoka Y, Higashi T 2003 Bioelectromagnetics 24 347
[28] Hirose H, Nakahara T, Miyakoshi J 2003 Neurosci. Lett. 338 88
[29] Zhang X, Yarema K, Xu A 2017 Biological Effects of Static Magnetic Fields (Singapore: Springer) pp81-122 [张欣, 雅瑞玛 K, 徐安合 著 (张磊, 刘娟娟 译) 2017 稳态磁场的生物学效应 (北京: 科学出版社)第81–122页]
[30] Ogiue-Ikeda M, Ueno S 2004 IEEE T. Magn. 40 3024
[31] Emura R, Ashida N, Higashi T, Takeuchi T 2001 Bioelectromagnetics 22 60
[32] Raylman R R, Clavo A C, Wahl R L 1996 Bioelectromagnetics 17 358
[33] Zhang L, Yang X X, Liu J J, Luo Y, Li Z Y, Ji X M, Wang W C, Zhang X 2015 Sci. Bull. 60 2120
[34] Luo Y, Ji X M, Liu J J, Li Z Y, Wang W C, Chen W, Wang J F, Liu Q S, Zhang X 2016 Bioelectrochemistry 109 31
[35] Short W O, Goodwill L, Taylor C W, Job C, Arthur M E, Cress A E 1992 Invest. Radiol. 27 836
[36] Nakahara T, Yaguchi H, Yoshida M, Miyakoshi J 2002 Radiology 224 817
[37] Gao W M, Liu Y Q, Zhou J Z, Pan H J 2005 Bioelectromagnetics 26 558
[38] Reddig A, Fatahi M, Friebe B, Guttek K, Hartig R, Godenschweger F, Roggenbuck D, Ricke J, Reinhold D, Speck O 2015 PLoS One 10 e0132702
[39] Iachininoto M G, Camisa V, Leone L, Pinto R, Lopresto V, Merla C, Giorda E, Carsetti R, Zaffina S, Podda M V, Teofili L, Grassi C 2016 Bioelectromagnetics 37 201
[40] Vassilev P M, Dronzine R T, Vassileva M P, Georgiev G A 1982 Bioscience. Rep. 2 1025
[41] Bras W, Diakun G P, Diaz J F, Maret G, Kramer H, Bordas J, Medrano F J 1998 Biophys. J. 74 1509
[42] Glade N, Tabony J 2005 Biophys. Chem. 115 29
[43] Denegre J M, Valles J M, Jr, Lin K, Jordan W B, Mowry K L 1998 P. Natl. Acad. Sci. USA 95 14729
[44] Eguchi Y, Ueno S, Kaito C, Sekimizu K, Shiokawa K 2006 Bioelectromagnetics 27 307
[45] Valles J M 2002 Biophys. J. 82 1260
[46] Valles J M, Wasserman Jr S R, Schweidenback C, Edwardson J, Denegre J M, Mowry K L 2002 Exp. Cell. Res. 274 112
[47] Valiron O, Peris L, Rikken G, Schweitzer A, Saoudi Y, Remy C, Job D 2005 J. Magn. Reson. Imaging 22 334
[48] Zhang L, Hou Y B, Li Z Y, Ji X M, Wang Z, Wang H Z, Tian X F, Yu F Z, Yang Z Y, Pi L, Mitchison T J, Lu Q Y, Zhang X 2017 Elife 6 e22911
[49] Sato K, Yamaguchi H, Miyamoto H, Kinouchi Y 1992 Biochim. Biophys. Acta 1136 231
[50] Muroski M E, Morshed R A, Cheng Y, Vemulkar T, Mansell R, Han Y, Zhang L, Aboody K S, Cowburn R P, Lesniak M S 2016 PLoS One 11 e0145129
[51] Cheng Y, Muroski M E, Petit D, Mansell R, Vemulkar T, Morshed R A, Han Y, Balyasnikova I V, Horbinski C M, Huang X, Zhang L, Cowburn R P, Lesniak M S 2016 J. Control Release 223 75
[52] Hapuarachchige S, Kato Y, Ngen E J, Smith B, Delannoy M, Artemov D 2016 PLoS One 11 e0156294
[53] Shen Y J, Cheng Y, Uyeda T Q P, Plaza G R 2017 Ann. Biomed. Eng. 45 2475
[54] Son B, Kim H D, Kim M, Kim J A, Lee J, Shin H, Hwang N S, Park T H 2015 Adv. Healthc. Mater. 4 1339
[55] Takashima Y, Miyakoshi J, Ikehata M, Iwasaka M, Ueno S, Koana T 2004 J. Radiat. Res. 45 393
[56] Schwenzer N F, Bantleon R, Maurer B, Kehlbach R, Schraml C, Claussen C D, Rodegerdts E 2007 J. Magn. Reson. Imaging 26 1308
[57] Fatahi M, Reddig A, Vijayalaxmi, Friebe B, Hartig R, Prihoda T J, Ricke J, Roggenbuck D, Reinhold D, Speck O 2016 Neuroimage 133 288
[58] Schiffer I B, Schreiber W G, Graf R, Schreiber E M, Jung D, Rose D M, Hehn M, Gebhard S, Sagemuller J, Spiess H W, Oesch F, Thelen M, Hengstler J G 2003 Bioelectromagnetics 24 241
[59] Zhao G P, Chen S P, Zhao Y, Zhu L Y, Huang P, Bao L Z, Wang J, Wang L, Wu L J, Wu Y J, Xu A 2010 Plasma Sci. Technol. 12 123
[60] Zhang L, Ji X M, Yang X X, Zhang X 2017 Oncotarget 8 13126
[61] Prina-Mello A, Farrell E, Prendergast P J, Campbell V, Coey J M D 2006 Bioelectromagnetics 27 35
[62] Yang J, Zhang J, Ding C, Dong D, Shang P 2017 Biol. Trace. Elem. Res. 184 214
[63] Aldinucci C, Garcia J B, Palmi M, Sgaragli G, Benocci A, Meini A, Pessina F, Rossi C, Bonechi C, Pessina G P 2003 Bioelectromagnetics 24 109
[64] Hackett S, Hamzah J, Davis T M, St Pierre T G 2009 Bba-Mol. Basis. Dis. 1792 93
[65] Lee J, Kim M S, Kim Y J, Choi Y J, Lee Y, Chung H 2011 Bioelectromagnetics 32 535
[66] Zablotskii V, Syrovets T, Schmidt Z W, Dejneka A, Simmet T 2014 Biomaterials 35 3164
[67] Zborowski M, Ostera G R, Moore L R, Milliron S, Chalmers J J, Schechter A N 2003 Biophys. J. 84 2638
[68] Zablotskii V, Dejneka A, Kubinova S, Le-Roy D, Dumas-Bouchiat F, Givord D, Dempsey N M, Sykova E 2013 Plos One 8 e70416
[69] Zhao G, Chen S, Wang L, Zhao Y, Wang J, Wang X, Zhang W, Wu R, Wu L, Wu Y, Xu A 2011 Bioelectromagnetics 32 94
[70] Wang J, Yang G, Liu F 2015 Acta Phys. Sin. 64 058707 (in Chinese) [王璟, 杨根, 刘峰 2015 物理学报 64 058707]
[71] Liu R C, Chen G, Liu L Y 2017 Physics 46 627 (in Chinese) [刘如川, 陈果, 刘雳宇 2017 物理 46 627]
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