Magnetic stimulation modulates structural synaptic plasticity and regulates BDNF-TrkB signal pathway in cultured hippocampal neurons

Neurochemistry International

Volumn 62, Issue 1, 2013, Pages 84-91

  Ma, Jun ^a   Zhang, Zhanchi ^a   Su, Yuhong ^a   Kang, Lin ^a   Geng, Dandan ^a   Wang, Yanyong ^a   Luan, Feng ^a   Wang, Mingwei ^a   Cui, Huixian ^a  

^a HEBEI MEDICAL UNIVERSITY   (China)

Author keywords

Cultured hippocampal neurons; Magnetic stimulation; Signal pathway; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NEUROMODULIN; PHOSPHATIDYLINOSITOL 3 KINASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN KINASE B; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL STRUCTURE; DENDRITIC CELL; GENETIC TRANSCRIPTION; HIPPOCAMPUS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRANIAL MAGNETIC STIMULATION; UPREGULATION;

ACTINS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; ELECTROMAGNETIC FIELDS; GAP-43 PROTEIN; GUANYLATE KINASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; NEURONAL PLASTICITY; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTOPHYSIN; TRANSCRIPTION, GENETIC;

EID: 84871152550     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.11.010     Document Type: Article

References (46)

1. Keith T. Akama, and Bruce S. McEwen Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase b pathway J. Neurosci. 23 6 2003 2333 2339
2. R.D. Almeida, B.J. Manadas, C.V. Melo, J.R. Gomes, C.S. Mendes, M.M. Grãos, R.F. Carvalho, A.P. Carvalho, and C.B. Duarte Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways Cell Death Differ. 12 10 2005 1329 1343
3. S. Aydin-Abidin, J. Trippe, K. Funke, U.T. Eysel, and A. Benali High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain Exp. Brain Res. 188 2 2008 249 261
4. S. Bashir, D. Edwards, and A. Pascual-Leone Neuronavigation increases the physiologic and behavioral effects of low-frequency rTMS of primary motor cortex in healthy subjects Brain Topogr. 24 1 2011 54 64
5. C.R. Bramham, and E. Messaoudi BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis Prog. Neurobiol. 76 2005 99 125
6. E. Caparelli, W. Backus, F. Telang, G. Wang, T. Maloney, R. Goldstein, and F. Henn Is 1 Hz rTMS always inhibitory in healthy individuals? Open Neuroimaging J. 6 2012 69 74
7. L.G. Cohen, B.J. Roth, J. Nilsson, N. Dang, M. Panizza, S. Bandinelli, W. Friauf, and M. Hallett Effects of coil design on delivery of focal magnetic stimulation. Technical considerations Electroencephalogr. Clin. Neurophysiol. 75 4 1990 350 357
8. G. Cosentino, B. Fierro, P. Paladino, S. Talamanca, S. Vigneri, A. Palermo, G. Giglia, and F. Brighina Transcranial direct current stimulation preconditioning modulates the effect of high-frequency repetitive transcranial magnetic stimulation in the human motor cortex Eur. J. Neurosci. 35 1 2012 119 124
9. S.P. Cregan, J.G. MacLaurin, C.G. Craig, G.S. Robertson, D.W. Nicholson, D.S. Park, and R.S. Slack Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons J. Neurosci. 19 18 1999 7860 7869
10. J. Diaz, C. Pilon, B. Le Foll, C. Gros, A. Triller, J.C. Schwartz, and P. Sokoloff Dopamine D3 receptors expressed by all mesencephalic dopamine neurons J. Neurosci. 20 23 2000 8677 8684
11. P.A. Dijkhuizen, and A. Ghosh Regulation of dendritic growth by calcium and neurotrophin signaling Prog. Brain Res. 147 2005 17 27
12. S.L. Donovan, L.A. Mamounas, A.M. Andrews, M.E. Blue, and J.S. McCasland GAP-43 is critical for normal development of the serotonergic innervation in forebrain J. Neurosci. 22 9 2002 3543 3552
13. T.H. Emara, R.R. Moustafa, N.M. Elnahas, A.M. Elganzoury, T.A. Abdo, S.A. Mohamed, and M.A. Eletribi Repetitive transcranial magnetic stimulation at 1 Hz and 5 Hz produces sustained improvement in motor function and disability after ischaemic stroke Eur. J. Neurol. 17 9 2010 1203 1209
14. A. Ferreira, H.Q. Han, P. Greengard, and K.S. Kosik Suppression of sunapsin II inhibits the formation and maintenance of synapases in hippocampal culture Proc. Natl. Acad. Sci. USA 92 1995 9225 9229
15. R. Gersner, E. Kravetz, J. Feil, G. Pell, and A. Zangen Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals J. Neurosci. 31 20 2011 7521 7526
16. M.R. Goldsworthy, J.B. Pitcher, and M.C. Ridding The application of spaced theta burst protocols induces long-lasting neuroplastic changes in the human motor cortex Eur. J. Neurosci. 35 1 2012 125 134
17. H.J. Gundersen Notes on the estimation of the numerical density of arbitrary particles: the edge effect J. Microsc. 111 1977 219 223
18. F.H. Güldner, and C.A. Ingham Increase in postsynaptic density material in optic target neurons of the rat suprachiasmatic nucleus after bilateral enucleation Neurosci. Lett. 17 1-2 1980 27 31
19. B.H. Han, and D.M. Holtzman BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway J. Neurosci. 20 15 2000 5775 5781
20. N.G. Harris, Y.A. Mironova, D.A. Hovda, and R.L. Sutton Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury J. Neuropathol. Exp. Neurol. 69 2 2010 139 154
21. A. Hasan, M.A. Nitsche, B. Rein, T. Schneider-Axmann, B. Guse, O. Gruber, P. Falkai, and T. Wobrock Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation Behav. Brain Res. 224 1 2011 15 22
22. E. Houdayer, A. Degardin, F. Cassim, P. Bocquillon, P. Derambure, and H. Devanne The effects of low- and high-frequency repetitive TMS on the input/output properties of the human corticospinal pathway Exp. Brain Res. 187 2008 207 217
23. E.J. Huang, and L.F. Reichardt Neurotrophins: roles in neuronal development and function Annu. Rev. Neurosci. 24 2001 677 736
24. Y.Z. Huang, M.J. Edwards, E. Rounis, K.P. Bhatia, and J.C. Rothwell Theta burst stimulation of the human motor cortex Neuron 45 2005 201 206
25. S. Kaech, and G. Banker Culturing hippocampal neurons Nat. Protoc. 1 2006 2406 2415
26. L. Lee, H.R. Siebner, J.B. Rowe, V. Rizzo, J.C. Rothwell, R.S. Frackowiak, and K.J. Friston Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation J. Neurosci. 23 12 2003 5308 5318
27. W. Li, and J. Keifer Rapid enrichment of presynaptic protein in boutons undergoing classical conditioning is mediated by brain-derived neurotrophic factor Neuroscience 203 2012 50 58
28. X. Li, Z. Nahas, F.A. Kozel, B. Anderson, D.E. Bohning, and M.S. George Acute left prefrontal transcranial magnetic stimulation in depressed patients is associated with immediately increased activity in prefrontal cortical as well as subcortical regions Biol. Psychiatry 55 9 2004 882 890
29. T.M. Mayhew A review of recent advances in stereology for quantifying neural structure J. Neurocytol. 21 1992 313 328
30. C. Miniussi, and P.M. Rossini Transcranial magnetic stimulation in cognitive rehabilitation Neuropsychol. Rehabil. 21 5 2011 579 601
31. M.B. Muller, N. Toschi, A.E. Kresse, A. Post, and M.E. Keck Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokin in mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain Neuropsychopharmacology 23 2000 205 215
32. M. Ogiue-Ikeda, S. Kawato, and S. Ueno The effect of repetitive transcranial magnetic stimulation on long-term potentiation in rat hippocampus depends on stimulus intensity Brain Res. 993 1-2 2003 222 226
33. Adlane Ould-yahoui, Evelyne Tremblay, Oualid Sbai, Lotfi Ferhat, Anne Bernard, Eliane Charrat, Yatma Gueye, Ngee Han Lim, Keith Brew, Jean-Jacques Risso, Vincent Dive, Michel Khrestchatisky, and Santiago Rivera A new role for TIMP-1 in modulating neurite outgrowth and morphology of cortical neurons PLoS ONE 4 12 2009 e8289
34. B. Pan, D.W. Yang, and T.Z. Han Changes of synaptic structure after long-lasting LTP induced by high and low frequency tetanus in slices of the rat visual cortex Sheng Li Xue Bao 57 1 2005 77 82
35. B. Pleger, F. Blankenburg, S. Bestmann, C.C. Ruff, K. Wiech, K.E. Stephan, K.J. Friston, and R.J. Dolan Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans J. Neurosci. 26 7 2006 1945 1952
36. C. Robinet, and L. Pellerin Brain-derived neurotrophic factor enhances the hippocampal expression of key postsynaptic proteins in vivo including the monocarboxylate transporter MCT2 Neuroscience 29 192 2011 155 163
37. A. Saito, Y. Takayama, H. Moriguchi, K. Kotani, and Y. Jimbo Developmental effects of low frequency magnetic fields on P19-derived neuronal cells Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009 5942 5945
38. H.M. Schambra, L. Sawaki, and L.G. Cohen Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1 Clin. Neurophysiol. 114 1 2003 130 133
39. B. Schutte, R. Nuydens, H. Geerts, and F. Ramaekers Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells J. Neurosci. Methods 86 1998 63 69
40. H.R. Siebner, N. Lang, V. Rizzo, M.A. Nitsche, W. Paulus, R.N. Lemon, and J.C. Rothwell Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex J. Neurosci. 24 13 2004 3379 3385
41. F. Wang, X. Geng, H.Y. Tao, and Y. Cheng The restoration after repetitive transcranial magnetic stimulation treatment on cognitive ability of vascular dementia rats and its impacts on synaptic plasticity in hippocampal CA1 area J. Mol. Neurosci. 41 1 2010 145 155
42. E.G. Waterhouse, and B. Xu New insights into the role of brain-derived neurotrophic factor in synaptic plasticity Mol. Cell. Neurosci. 42 2009 81 89
43. A.J. Weber, and C.D. Harman BDNF preserves the dendritic morphology of alpha and beta ganglion cells in the cat retina after optic nerve injury Invest. Ophthalmol. Vis. Sci. 49 2008 2456 2463
44. H. Xu, H.L. Gao, W. Zheng, N. Xin, Z.H. Chi, S.L. Bai, and Z.Y. Wang Lactational zinc deficiency-induced hippocampal neuronal apoptosis by a BDNF-independent TrkB signaling pathway Hippocampus 21 5 2011 495 501
45. 2+-independent signaling pathway to extracellular signal-regulated protein kinase by coactivation of NMDA receptors and metabotropic glutamate receptor 5 in neurons J. Neurosci. 24 48 2004 10846 10857
46. A. Zangen, and K. Hyodo Transcranial magnetic stimulation induces increases in extracellular levels of dopamine and glutamate in the nucleus accumbens NeuroReport 13 18 2002 2401 2405