Repetitive magnetic stimulation promotes neural stem cells proliferation by upregulating MiR-106b in vitro

Journal of Huazhong University of Science and Technology - Medical Science

Volumn 35, Issue 5, 2015, Pages 766-772

  Liu, Hua ^a   Han, Xiao hua ^a   Chen, Hong ^a   Zheng, Cai xia ^a   Yang, Yi ^b   Huang, Xiao lin ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WUHAN SPORTS UNIVERSITY   (China)

Author keywords

cyclin dependent kinase; cyclin dependent kinase inhibitor; EdU; ki67; microRNA 106b; neural stem cells; repetitive magnetic stimulation

Indexed keywords

BIOLOGICAL MARKER; CDK2 PROTEIN, RAT; CDK4 PROTEIN, RAT; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1C; CYCLINE; KI 67 ANTIGEN; MICRORNA;

ANIMAL; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; MAGNETIC FIELD; METABOLISM; NEURAL STEM CELL; NEWBORN; PRIMARY CELL CULTURE; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BIOMARKERS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P57; CYCLINS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; KI-67 ANTIGEN; MAGNETIC FIELDS; MICRORNAS; NEURAL STEM CELLS; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84944679780     PISSN: 16720733     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11596-015-1505-3     Document Type: Article

References (50)

1. Pell GS, Roth Y, Zangen A. Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol, 2011,93(1):59–98
2. Touge T, Gerschlager W, Brown P, et al. Are the after- effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol, 2001,112(11):2138–2145
3. Bilek E, Schafer A, Ochs E, et al. Application of high-frequency repetitive transcranial magnetic stimulation to the DLPFC alters human prefrontal-hippocampal functional interaction. J Neurosci, 2013,33(16):7050–7056
4. Lisanby SH, Datto CJ, Szuba MP. ECT and TMS: past, present, and future. Depress Anxiety, 2000,12(3):115–117
5. Rothkegel H, Sommer M, Paulus W. Breaks during 5Hz rTMS are essential for facilitatory after effects. Clin Neurophysiol, 2009,121(3):426–430
6. Guo F, Han X, Zhang J, et al. Repetitive transcranial magnetic stimulation promotes neural stem cell proliferation via the regulation of MiR-25 in a rat model of focal cerebral ischemia. PLoS One, 2014,9(10):e109267
7. Zeng Y, Yi R, Cullen BR. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J, 2005,24(1):138–148
8. Saito K, Ishizuka A, Siomi H, et al. Processing of pre-microRNAs by the Dicer-1-Loquacious complex in Drosophila cells. PLoS Biol, 2005,3(7):e235
9. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol, 2009,10(2):126–139
10. Cremisi F. MicroRNAs and cell fate in cortical and retinal development. Front Cell Neurosci, 2013,7:141
11. Perruisseau-Carrier C, Jurga M, Forraz N, et al. miRNAs stem cell reprogramming for neuronal induction and differentiation. Mol Neurobiol, 2011,43(3):215–227
12. Zhao C, Sun G, Li S, et al. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol, 2009,16(4):365–371
13. Brett JO, Renault VM, Rafalski VA, et al. The microRNA cluster miR-106b~25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging, 2011,3(2):108–124
14. Peck B, Schulze A. A role for the cancer-associated miR-106b~25 cluster in neuronal stem cells. Aging, 2011,3(4):329–331
15. Landgraf P, Rusu M, Sheridan R, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 2007,129(7):1401–1414
16. Morte MI, Carreira BP, Machado V, et al. Evaluation of proliferation of neural stem cells in vitro and in vivo. Curr Protoc Stem Cell Biol, 2013, Chapter 2: Unit 2D.14 doi: 10.1002/9780470151808.sc02d14s24.
17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 2001,25(4):402–408
18. Conti L, Cattaneo E. Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci, 2010,11(3):176–187
19. Salic A, Mitchison TJ. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A, 2008,105(7):2415–2420
20. Hayashi Y, Takei H, Kurosumi M. Ki67 immunohistochemical staining: the present situation of diagnostic criteria. Nihon Rinsho, 2013,70(Suppl 7):428–432
21. Reif A, Fritzen S, Finger M, et al. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry, 2006,11(5):514–522
22. Arias-Carrion O, Verdugo-Diaz L, Feria-Velasco A, et al. Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J Neurosci Res, 2004,78(1):16–28
23. Werner S, Unsicker K, von Bohlen und Halbach O. Fibroblast growth factor-2 deficiency causes defects in adult hippocampal neurogenesis, which are not rescued by exogenous fibroblast growth factor-2. J Neurosci Res, 2011,89(10):1605–1617
24. Jeong CH, Kim SM, Lim JY, et al. Mesenchymal stem cells expressing brain-derived neurotrophic factor enhance endogenous neurogenesis in an ischemic stroke model. Biomed Res Int, 2014,2014:129–145
25. Emsley JG, Hagg T. Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice. Exp Neurol, 2003,183(2):298–310
26. Rotem A, Moses E. Magnetic stimulation of one-dimensional neuronal cultures. Biophys J, 2008, 94(12):5065–5078
27. Kim JY, Choi GS, Cho YW, et al. Attenuation of spinal cord injury-induced astroglial and microglial activation by repetitive transcranial magnetic stimulation in rats. J Korean Med Sci, 2013,28(2):295–299
28. Ueyama E, Ukai S, Ogawa A, et al. Chronic repetitive transcranial magnetic stimulation increases hippocampal neurogenesis in rats. Psychiatry Clin Neurosci, 2011,65(1):77–81
29. Sontag W, Kalka D. No effect of pulsed electromagnetic fields on PC12 and HL-60 cells. Radiat Environ Biophys, 2006,45(1):63–71
30. Vlachos A, Muller-Dahlhaus F, Rosskopp J, et al. Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J Neurosci, 2012,32(48): 17514–17523
31. Gilio F, Conte A, Vanacore N, et al. Excitatory and inhibitory after-effects after repetitive magnetic transcranial stimulation (rTMS) in normal subjects. Exp Brain Res, 2007,176(4):588–593
32. Yang TS, Yang XH, Chen X, et al. MicroRNA-106b in cancer-associated fibroblasts from gastric cancer promotes cell migration and invasion by targeting PTEN. FEBS Lett, 2014,588(13):2162–2169
33. Tan W, Li Y, Lim SG, et al. miR-106b-25/miR-17-92 clusters: polycistrons with oncogenic roles in hepatocellular carcinoma. World J Gastroenterol, 2014,20(20):5962–5972
34. Semo J, Sharir R, Afek A, et al. The 106b~25 microRNA cluster is essential for neovascularization after hindlimb ischaemia in mice. Eur Heart J, 2013,35(45):3212–3223
35. Zhang XY, Tang LZ, Ren BG, et al. Interaction of MCM7 and RACK1 for activation of MCM7 and cell growth. Am J Pathol, 2013,182(3):796–805
36. Ying SY, Chang CP, Lin SL. Intron-mediated RNA interference, intronic microRNAs, and applications. Methods Mol Biol, 2010,629:205–237
37. Lutter D, Marr C, Krumsiek J, et al. Intronic microRNAs support their host genes by mediating synergistic and antagonistic regulatory effects. BMC Genomics, 2010, 11:224
38. Kippin TE, Martens DJ, van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev, 2005,19(6):756–767
39. Ivey KN, Srivastava D. MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell, 2010,7(1):36–41
40. Ivanovska I, Ball AS, Diaz RL, et al. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol, 2008,28(7):2167–2174
41. Joaquin M, Gubern A, Posas F. A novel G1 checkpoint mediated by the p57 CDK inhibitor and p38 SAPK promotes cell survival upon stress. Cell Cycle, 2012,11(18): 3339–3340
42. Kan T, Sato F, Ito T, et al. The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology, 2009,136(5):1689–1700
43. Nishioka S, Nakano D, Kitada K, et al. The cyclin- dependent kinase inhibitor p21 is essential for the beneficial effects of renal ischemic preconditioning on renal ischemia/reperfusion injury in mice. Kidney Int, 2013,85(4):871–879
44. von Harsdorf R, Hauck L, Mehrhof F, et al. E2F-1 overexpression in cardiomyocytes induces downregulation of p21CIP1 and p27KIP1 and release of active cyclin- dependent kinases in the presence of insulin-like growth factor I. Circ Res, 1999,85(2):128–136
45. Puri PL, Balsano C, Burgio VL, et al. MyoD prevents cyclinA/cdk2 containing E2F complexes formation in terminally differentiated myocytes. Oncogene, 1997,14 (10):1171–1184
46. Marques-Torrejon MA, Porlan E, Banito A, et al. Cyclin- dependent kinase inhibitor p21 controls adult neural stem cell expansion by regulating Sox2 gene expression. Cell Stem Cell, 2012,12(1):88–100
47. Miyagi S, Nishimoto M, Saito T, et al. The Sox2 regulatory region 2 functions as a neural stem cell-specific enhancer in the telencephalon. J Biol Chem, 2006,281 (19):13374–13381
48. Lange C, Huttner WB, Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell, 2009,5(3):320–331
49. Lim S, Kaldis P. Loss of Cdk2 and Cdk4 induces a switch from proliferation to differentiation in neural stem cells. Stem Cells, 2012,30(7):1509–1520
50. Devgan V, Mammucari C, Millar SE, et al. p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev, 2005,19(12):1485–1495