Please wait a minute...
Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Protein Cell    2016, Vol. 7 Issue (9) : 624-637    https://doi.org/10.1007/s13238-016-0300-7
RESEARCH ARTICLE
Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells
Jing-Peng Fu1,3,Wei-Chuan Mo1,2,Ying Liu1,3(),Perry F. Bartlett2,Rong-Qiao He1,3,4()
1. State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
2. Queensland Brain Institute, University of Queensland, Brisbane, QLD 4072, Australia
3. University of the Chinese Academy of Sciences, Beijing 100049, China
4. Alzheimer’s Disease Center, Beijing Institute for Brain Disorders, Capital Medical University, Beijing 100069, China
 Download: PDF(2234 KB)  
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

Living organisms are exposed to the geomagnetic field (GMF) throughout their lifespan. Elimination of the GMF, resulting in a hypogeomagnetic field (HMF), leads to central nervous system dysfunction and abnormal development in animals. However, the cellular mechanisms underlying these effects have not been identified so far. Here, we show that exposure to an HMF (<200 nT), produced by a magnetic field shielding chamber, promotes the proliferation of neural progenitor/stem cells (NPCs/NSCs) from C57BL/6 mice. Following seven-day HMF-exposure, the primary neurospheres (NSs) were significantly larger in size, and twice more NPCs/NSCs were harvested from neonatal NSs, when compared to the GMF controls. The self-renewal capacity and multipotency of the NSs were maintained, as HMF-exposed NSs were positive for NSC markers (Nestin and Sox2), and could differentiate into neurons and astrocyte/glial cells and be passaged continuously. In addition, adult mice exposed to the HMF for one month were observed to have a greater number of proliferative cells in the subventricular zone. These findings indicate that continuous HMF-exposure increases the proliferation of NPCs/NSCs,in vitro and in vivo. HMF-disturbed NPCs/ NSCs production probably Affects brain development and function, which provides a novel clue for elucidating the cellular mechanisms of the bio-HMF response.

Keywords hypomagnetic field      neural progenitor/stem cells      neurosphere      proliferation      stemness      multipotency     
Corresponding Author(s): Ying Liu,Rong-Qiao He   
Issue Date: 27 September 2016
 Cite this article:   
Jing-Peng Fu,Wei-Chuan Mo,Ying Liu, et al. Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells[J]. Protein Cell, 2016, 7(9): 624-637.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-016-0300-7
https://academic.hep.com.cn/pac/EN/Y2016/V7/I9/624
1 Ahmed S (2009) The culture of neural stem cells. J Cell Biochem 106:1–6
https://doi.org/10.1002/jcb.21972
2 Asashima M, Shimada K, Pfeiffer CJ (1991) Magnetic shielding induces early developmental abnormalities in the newt, Cynops pyrrhogaster. Bioelectromagnetics 12:215–224
https://doi.org/10.1002/bem.2250120403
3 Azari H (2010) Isolation and expansion of the adult mouse neural stem cells using the neurosphere assay. JoVE 45:2393
4 Biskup T (2009) Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew Chem Int Ed Engl 48:404–407
https://doi.org/10.1002/anie.200803102
5 Bliss VL, Heppner FH (1976) Circadian activity rhythm influenced by near zero magnetic field. Nature 261:411–412
https://doi.org/10.1038/261411a0
6 Bull ND, Bartlett PF (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 25:10815–10821
https://doi.org/10.1523/JNEUROSCI.3249-05.2005
7 Cameron HA, Glover LR (2015) Adult neurogenesis: beyond learning and memory. Annu Rev Psychol 3:53–81
8 Carreira BP (2010) Nitric oxide stimulates the proliferation of neural stem cells bypassingthe epidermal growth factor receptor. Stem Cells 28:1219–1230
9 Castello PR (2014) Inhibition of cellular proliferation and enhancement of hydrogen peroxide production in fibrosarcoma cell line by weak radio frequency magnetic fields. Bioelectromagnetics 35:598–602
https://doi.org/10.1002/bem.21858
10 Cho JH, Tsai MJ (2004) The role of BETA2/NeuroD1 in the development of the nervous system. Mol Neurobiol 30:35–47
https://doi.org/10.1385/MN:30:1:035
11 Ciccolini F, Svendsen CN (1998) Fibroblast growth factor2(FGF-2) promotes acquisition of epidermal growth factor (EGF) responsiveness in mouse striatal precursor cells: Identification of neural precursors responding to both EGF and FGF-2. J Neurosci 18:7869–7880
12 Destici E (2011) Mammalian cryptochromes impinge on cell cycle progression in a circadian clock-independent manner. Cell Cycle 10:3788–3797
https://doi.org/10.4161/cc.10.21.17974
13 Di Lazzaro VF (2013) A consensus panel review of central nervous system effects of the exposure to low-intensity extremely low-frequency magnetic fields. Brain Stimul 6:469–476
https://doi.org/10.1016/j.brs.2013.01.004
14 Ding H (2014) The hematopoietic system responses to one-month continuous hypomagnetic field exposure in adult mice. Prog Mod Biomed 26:5001–5004
15 Fesenko EE (2010) Effect of the “zero” magnetic field on early embryogenesis in mice. Electromagn Biol Med 29:1–8
https://doi.org/10.3109/15368371003627290
16 Fu JP (2016) Decline of cell viability and mitochondrial activity in mouse skeletal muscle cell in a hypomagnetic field. Bioelectromagnetics 37:212–222
https://doi.org/10.1002/bem.21968
17 Gage FH, Temple S (2013) Neural stem cells: generating and regenerating the brain. Neuron 80:588–601
https://doi.org/10.1016/j.neuron.2013.10.037
18 Gegear RJ (2012) Animal cryptochromes mediate magnetoreception by an unconventional photochemicalmechanism. Nature 463:804–807
19 Golmohammadi MG (2008) Comparative analysis of the frequency and distribution of stem and progenitor cells in the adult mouse brain. Stem Cells 26:979–987
https://doi.org/10.1634/stemcells.2007-0919
20 Gould JL, Gould CG (2012) Nature’s compass: the mystery of animal navigation. Princeton University Press, Princeton
21 Graham V (2003) SOX2 functionsto maintain neural progenitor identity. Neuron 39:749–765
https://doi.org/10.1016/S0896-6273(03)00497-5
22 Jia C (2007) EGF receptor clustering is induced by a 0.4 mT power frequency magnetic field and blocked by the EGF receptor tyrosine kinase inhibitor PD153035. Bioelectromagnetics 28:197–207
https://doi.org/10.1002/bem.20293
23 Jiang JC (1998) Effect of magnetic free field space (MFFS) on vocal behavior in melop sittacus undulafus. Acta Seismol Sin 20:421–426 (In Chinese)
24 Jogler C, Schuler D (2009) Genomics, genetics, and cell biology of magnetosome formation. Annu Rev Microbiol 63:501–521
https://doi.org/10.1146/annurev.micro.62.081307.162908
25 Le Belle JE (2014) Maternal inflammation contributes to brain overgrowth and autism-associated behaviors through altered redox signaling in stem and progenitor cells. Stem Cell Rep 3:725–734
https://doi.org/10.1016/j.stemcr.2014.09.004
26 Lisi A (2005) Exposure to 50 Hz electromagnetic radiation promote early maturation and differentiation in newborn rat cerebellar granule neurons. J Cell Physiol 204:532–538
https://doi.org/10.1002/jcp.20322
27 Lohmann KJ (2010) Animal behavior: magnetic-field perception. Nature 464:1140–1142
https://doi.org/10.1038/4641140a
28 Louis SA (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 26:988–996
https://doi.org/10.1634/stemcells.2007-0867
29 Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146:18–36
https://doi.org/10.1016/j.cell.2011.06.030
30 Martino CF, Castello PR (2011) Modulation of hydrogen peroxide production in cellular systems by low level magnetic fields. PLoS One 6:e22753
31 Martino CF (2010) Reduction of the Earth’s magnetic field inhibits growth rates of cancer cells. Bioelectromagnetics 31:649–655
https://doi.org/10.1002/bem.20606
32 Merkle FT, Alvarez-Buylla A (2006) Neural stem cells in mammalian development. Curr Opin Cell Biol 18:704–709
https://doi.org/10.1016/j.ceb.2006.09.008
33 Mo WC, Liu Y, He RQ (2012a) A biological perspective of the hypomagnetic field: from definition towards mechanism. Prog Biochem Biophys 399:835–842 (In Chinese)
34 Mo WC (2012b) Altered development of Xenopus embryos in a hypogeomagnetic field. Bioelectromagnetics 33:238–246
35 Mo WC (2013) Magnetic shielding accelerates the proliferation of human neuroblastoma cell by promoting G1-phase progression. PLoS One 8:e54775
36 Mo W, Liu Y, He R (2014a) Hypomagnetic field, an ignorable environmental factor in space? Sci China Life Sci 57:726–728
37 Mo W (2014b) Transcriptome profile of human neuroblastoma cells in the hypomagnetic field. Sci China Life Sci 57:448–461
38 Mo WC (2015) Hypomagnetic field alters circadian rhythm and increases algesia in adult male mice. Prog Biochem Biophys 42 (7):639–646
39 Mo W (2016) Shielding of the geomagnetic field alters actin assembly and inhibits cell motility in human neuroblastoma cells. Sci Rep 6:22624
https://doi.org/10.1038/srep22624
40 Müller P, Ahmad M (2011) Light-activated cryptochrome reacts with molecular oxygen to form a flavin-superoxide radical pair consistent with magnetoreception. J Biol Chem 286:21033–21040
https://doi.org/10.1074/jbc.M111.228940
41 Nakamichi N (2009) Possible promotion of neuronal differentiation in fetal rat brain neural progenitor cells after sustained exposure to static magnetism. J Neurosci Res 87:2406–2417
https://doi.org/10.1002/jnr.22087
42 Namiki J(2012) Nestin proteinis phosphorylatedin adult neural stem/progenitor cells and not endothelial progenitor cells. Stem Cells Int 2012:430138
43 Nathan FP (2014) An inherited magnetic map guides ocean navigation in Juvenile Pacific Salmon. Curr Biol 24:446–450
https://doi.org/10.1016/j.cub.2014.01.017
44 Nordahl CW (2013) Maternal autoantibodies are associated with abnormal brain enlargement in a subgroup of children with autism spectrum disorder. Brain Behav Immun 30:61–65
https://doi.org/10.1016/j.bbi.2013.01.084
45 Oh J, Lee YD, Wagers AJ (2014) Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat Med 20:870–880
https://doi.org/10.1038/nm.3651
46 Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115–128
https://doi.org/10.1038/nrg2269
47 Park D (2010) Nestinis required for the proper self-renewalof neural stem cells. Stem Cells 28:2162–2171
https://doi.org/10.1002/stem.541
48 Portelli LA (2012) Reduction of the earth’s magnetic field inhibits Drosophila melanogaster ability to survive ionizing radiation. Bioelectromagnetics 33:706–709
https://doi.org/10.1002/bem.21720
49 Prato FS (2005) Daily repeated magnetic field shielding induces analgesia in CD-1 mice. Bioelectromagnetics 26:109–117
https://doi.org/10.1002/bem.20056
50 Qin S (2016) A magnetic protein biocompass. Nat Mater 15:217–226
51 Quah BJC, Parish CR (2010) The use of Carboxyfluorescein Diacetate Succinimidyl Ester (CFSE) to monitor lymphocyte proliferation. JoVE 44:2259–2261
52 Simons BD, Clevers H (2011) Strategies for homeostatic stem cell self-renewalin adult tissues. Cell 145:851–862
https://doi.org/10.1016/j.cell.2011.05.033
53 Stine RR, Matunis EL (2013) Stem cell competition: finding balance in the niche. Trends Cell Biol 23:357–364
https://doi.org/10.1016/j.tcb.2013.03.001
54 Tsukamoto A (2013) Clinical translationof human neural stem cells. Stem Cell Res Ther 4:102
https://doi.org/10.1186/scrt313
55 Usselman R (2014) Spin biochemistry modulates reactive oxygen species (ROS) production by radio frequency magnetic fields. PLoS One 9:e93065
56 Ventura C (2005) Turning on stem cell cardiogenesis with extremely low frequency magnetic fields. FASEBJ 19:155–157
57 Walker TL (2008) Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 28:5240–5247
https://doi.org/10.1523/JNEUROSCI.0344-08.2008
58 Wan GJ (2014) Bio-effectsof near-zero magnetic fields on the growth, development and reproduction of small brown planthopper, Laodelphax striatellus and brown planthopper, Nilaparvata lugens. J Insect Physiol 68:7–15
https://doi.org/10.1016/j.jinsphys.2014.06.016
59 Wang XB (2002) Long-term memory was impaired in one-trial passive avoidance task of day-old chicks hatching from hypo-magnetic field space. Chin Sci Bull 48:2042–2045 (In Chinese)
60 Wang X (2012) PrimerBank: a PCR primer database for quantitative gene expression analysis, 2012 update. Nucleic Acids Res 40:1144–11499
https://doi.org/10.1093/nar/gkr1013
61 Wojtowicz JM, Kee N (2006) BrdU assay for neurogenesis in rodents. Nat Protoc 1:1399–1405
https://doi.org/10.1038/nprot.2006.224
62 Wu H (2005) Effect of electromagnetic fields on proliferation and differentiation of cultured mouse bone marrow mesenchymal stem cells. JHuazhong Univ SciTechnol Med Sci 25:185–187 (In Chinese)
63 Wu X (2014) Weak power frequency magnetic field acting similarly to EGF stimulation, induces acute activations of the EGFR sensitive actin cytoskeleton motility in human amniotic cells. PLoS One 9:e87626
64 Xu C (2014) Blue light-dependent phosphorylations of cryptochromes are Affected by magnetic fields in Arabidopsis. Adv Space Res 53:1118–1124
https://doi.org/10.1016/j.asr.2014.01.033
65 Yau SY (2014) Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc Natl Acad Sci USA 111:15810–15815
https://doi.org/10.1073/pnas.1415219111
66 Zhang B (2004) Exposure to hypomagnetic field space for multiple generations causes amnesia in Drosophila melanogaster. Neurosci Lett 371:190–195
https://doi.org/10.1016/j.neulet.2004.08.072
[1] PAC-0624-16127-HRQ_suppl_1 Download
[1] Xiao-Shuai Han, Chen Wang, Fang-hao Guo, Shuang Huang, Yong-Wen Qin, Xian-Xian Zhao, Qing Jing. Neoblast-enriched zinc finger protein FIR1 triggers local proliferation during planarian regeneration[J]. Protein Cell, 2019, 10(1): 43-59.
[2] Hai-tao Zhang, Zi-jian Zhang, Wei-chuan Mo, Ping-dong Hu, Hai-min Ding, Ying Liu, Qian Hua, Rong-qiao He. Shielding of the geomagnetic field reduces hydrogen peroxide production in human neuroblastoma cell and inhibits the activity of CuZn superoxide dismutase[J]. Protein Cell, 2017, 8(7): 527-537.
[3] Yuanyuan Gu, Shuoxin Liu, Xiaodan Zhang, Guimin Chen, Hongwei Liang, Mengchao Yu, Zhicong Liao, Yong Zhou, Chen-Yu Zhang, Tao Wang, Chen Wang, Junfeng Zhang, Xi Chen. Oncogenic miR-19a and miR-19b co-regulate tumor suppressor MTUS1 to promote cell proliferation and migration in lung cancer[J]. Protein Cell, 2017, 8(6): 455-466.
[4] Kegan Zhu,Lei Liu,Junliang Zhang,Yanbo Wang,Hongwei Liang,Gentao Fan,Zhenhuan Jiang,Chen-Yu Zhang,Xi Chen,Guangxin Zhou. MiR-29b suppresses the proliferation and migration of osteosarcoma cells by targeting CDK6[J]. Protein Cell, 2016, 7(6): 434-444.
[5] Haiyang Zhang,Jingjing Duan,Yanjun Qu,Ting Deng,Rui Liu,Le Zhang,Ming Bai,Jialu Li,Tao Ning,Shaohua Ge,Xia Wang,Zhenzhen Wang,Qian Fan,Hongli Li,Guoguang Ying,Dingzhi Huang,Yi Ba. Onco-miR-24 regulates cell growth and apoptosis by targeting BCL2L11 in gastric cancer[J]. Protein Cell, 2016, 7(2): 141-151.
[6] Qian Fan,Xiangrui Meng,Hongwei Liang,Huilai Zhang,Xianming Liu,Lanfang Li,Wei Li,Wu Sun,Haiyang Zhang,Ke Zen,Chen-Yu Zhang,Zhen Zhou,Xi Chen,Yi Ba. miR-10a inhibits cell proliferation and promotes cell apoptosis by targeting BCL6 in diffuse large B-cell lymphoma[J]. Protein Cell, 2016, 7(12): 899-912.
[7] Chao Lu,Yang Yang,Ran Zhao,Bingxuan Hua,Chen Xu,Zuoqin Yan,Ning Sun,Ruizhe Qian. Role of circadian gene Clock during differentiation of mouse pluripotent stem cells[J]. Protein Cell, 2016, 7(11): 820-832.
[8] Jiwei Zhang,Zehua Bian,Jialiang Zhou,Mingxu Song,Zhihui Liu,Yuyang Feng,Li Zhe,Binbin Zhang,Yuan Yin,Zhaohui Huang. MicroRNA-638 inhibits cell proliferation by targeting phospholipase D1 in human gastric carcinoma[J]. Protein Cell, 2015, 6(9): 680-688.
[9] Qiu Li,Zhi-Chun Lai. Recent progress in studies of factors that elicit pancreatic β-cell expansion[J]. Protein Cell, 2015, 6(2): 81-87.
[10] Chunji Quan,Moon Kyun Cho,Yuan Shao,Laurel E. Mianecki,Eric Liao,Daniel Perry,Taihao Quan. Dermal fibroblast expression of stromal cellderived factor-1 (SDF-1) promotes epidermal keratinocyte proliferation in normal and diseased skin[J]. Protein Cell, 2015, 06(12): 890-903.
[11] Chuankai Zhang,Yunda Zhang,Weiji Ding,Yancheng Lin,Zhengjie Huang,Qi Luo. MiR-33a suppresses breast cancer cell proliferation and metastasis by targeting ADAM9 and ROS1[J]. Protein Cell, 2015, 06(12): 881-889.
[12] Peng Jiang,Wenjing Du,Mian Wu. Regulation of the pentose phosphate pathway in cancer[J]. Protein Cell, 2014, 5(8): 592-602.
[13] Youguang Luo,Dengwen Li,Jie Ran,Bing Yan,Jie Chen,Xin Dong,Zhu Liu,Ruming Liu,Jun Zhou,Min Liu. End-binding protein 1 stimulates paclitaxel sensitivity in breast cancer by promoting its actions toward microtubule assembly and stability[J]. Protein Cell, 2014, 5(6): 469-479.
[14] Dengwen Li,Xiaodong Sun,Linlin Zhang,Bing Yan,Songbo Xie,Ruming Liu,Min Liu,Jun Zhou. Histone deacetylase 6 and cytoplasmic linker protein 170 function together to regulate the motility of pancreatic cancer cells[J]. Protein Cell, 2014, 5(3): 214-223.
[15] Dan Wang, Peng Xue, Xiu Lan Chen, Zhen Sheng Xie, Fu Quan Yang, Li Zheng, Tao Xu. Angiotensin IV upregulates the activity of protein phosphatase 1α in Neura-2A cells[J]. Prot Cell, 2013, 4(7): 520-528.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed