RESEARCH ARTICLE

Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells

  • Jing-Peng Fu 1,3 ,
  • Wei-Chuan Mo 1,2 ,
  • Ying Liu , 1,3 ,
  • Perry F. Bartlett 2 ,
  • Rong-Qiao He , 1,3,4
Expand
  • 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

Received date: 04 Jun 2016

Accepted date: 07 Jul 2016

Published date: 27 Sep 2016

Copyright

2016 The Author(s) 2016. This article is published with open access at Springerlink.com and journal.hep.com.cn

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.

Cite this article

Jing-Peng Fu , Wei-Chuan Mo , Ying Liu , Perry F. Bartlett , Rong-Qiao He . Elimination of the geomagnetic field stimulates the proliferation of mouse neural progenitor and stem cells[J]. Protein & Cell, 2016 , 7(9) : 624 -637 . DOI: 10.1007/s13238-016-0300-7

1
Ahmed S (2009) The culture of neural stem cells. J Cell Biochem 106:1–6

DOI

2
Asashima M, Shimada K, Pfeiffer CJ (1991) Magnetic shielding induces early developmental abnormalities in the newt, Cynops pyrrhogaster. Bioelectromagnetics 12:215–224

DOI

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

DOI

5
Bliss VL, Heppner FH (1976) Circadian activity rhythm influenced by near zero magnetic field. Nature 261:411–412

DOI

6
Bull ND, Bartlett PF (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 25:10815–10821

DOI

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

DOI

10
Cho JH, Tsai MJ (2004) The role of BETA2/NeuroD1 in the development of the nervous system. Mol Neurobiol 30:35–47

DOI

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

DOI

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

DOI

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

DOI

16
Fu JP (2016) Decline of cell viability and mitochondrial activity in mouse skeletal muscle cell in a hypomagnetic field. Bioelectromagnetics 37:212–222

DOI

17
Gage FH, Temple S (2013) Neural stem cells: generating and regenerating the brain. Neuron 80:588–601

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

27
Lohmann KJ (2010) Animal behavior: magnetic-field perception. Nature 464:1140–1142

DOI

28
Louis SA (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 26:988–996

DOI

29
Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146:18–36

DOI

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

DOI

32
Merkle FT, Alvarez-Buylla A (2006) Neural stem cells in mammalian development. Curr Opin Cell Biol 18:704–709

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

45
Oh J, Lee YD, Wagers AJ (2014) Stem cell aging: mechanisms, regulators and therapeutic opportunities. Nat Med 20:870–880

DOI

46
Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115–128

DOI

47
Park D (2010) Nestinis required for the proper self-renewalof neural stem cells. Stem Cells 28:2162–2171

DOI

48
Portelli LA (2012) Reduction of the earth’s magnetic field inhibits Drosophila melanogaster ability to survive ionizing radiation. Bioelectromagnetics 33:706–709

DOI

49
Prato FS (2005) Daily repeated magnetic field shielding induces analgesia in CD-1 mice. Bioelectromagnetics 26:109–117

DOI

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

DOI

53
Stine RR, Matunis EL (2013) Stem cell competition: finding balance in the niche. Trends Cell Biol 23:357–364

DOI

54
Tsukamoto A (2013) Clinical translationof human neural stem cells. Stem Cell Res Ther 4:102

DOI

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

DOI

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

DOI

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

DOI

61
Wojtowicz JM, Kee N (2006) BrdU assay for neurogenesis in rodents. Nat Protoc 1:1399–1405

DOI

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

DOI

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

DOI

66
Zhang B (2004) Exposure to hypomagnetic field space for multiple generations causes amnesia in Drosophila melanogaster. Neurosci Lett 371:190–195

DOI

Outlines

/