High-frequency repetitive transcranial magnetic stimulation (rTMS) improves functional recovery by enhancing neurogenesis and activating BDNF/TrKB signaling in ischemic rats

International Journal of Molecular Sciences

Volumn 18, Issue 2, 2017, Pages

  Luo, Jing ^a   Zheng, Haiqing ^a   Zhang, Liying ^a   Zhang, Qingjie ^a   Li, Lili ^a   Pei, Zhong ^a   Hu, Xiquan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

BDNF; MCAO; Neural stem cells; Neurological function; rTMS; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE FUNCTION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; RAT; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BRAIN INFARCTION; CELL MOTION; CEREBROVASCULAR ACCIDENT; CONVALESCENCE; CORPUS STRIATUM; CYTOLOGY; DISEASE MODEL; METABOLISM; NEURAL STEM CELL; PATHOLOGY; PROCEDURES; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; MALE; NEURAL STEM CELLS; NEUROGENESIS; RATS; RECEPTOR, TRKB; RECOVERY OF FUNCTION; SIGNAL TRANSDUCTION; STROKE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 85013852196     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18020455     Document Type: Article

References (46)

1. Langhorne, P.; Coupar, F.; Pollock, A. Motor recovery after stroke: A systematic review. Lancet Neurol. 2009, 8, 741–754.
2. Thorsén, A.M.; Holmqvist, L.W.; de Pedro-Cuesta, J.; von Koch, L. A randomized controlled trial of early supported discharge and continued rehabilitation at home after stroke: Five-year follow-up of patient outcome. Stroke 2005, 36, 297–303.
3. Bellenchi, G.C.; Volpicelli, F.; Piscopo, V.; Perrone-Capano, C.; di Porzio, U. Adult neural stem cells: An endogenous tool to repair brain injury? J. Neurochem. 2013, 124, 159–167.
4. Arvidsson, A.; Collin, T.; Kirik, D.; Kokaia, Z.; Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8, 963–970.
5. Gage, F.H. Mammalian neural stem cells. Science 2000, 287, 1433–1438.
6. Thored, P.; Arvidsson, A.; Cacci, E.; Ahlenius, H.; Kallur, T.; Darsalia, V.; Ekdahl, C.T.; Kokaia, Z.; Lindvall, O. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 2006, 24, 739–747.
7. Yozbatiran, N.; Alonso-Alonso, M.; See, J.; Demirtas-Tatlidede, A.; Luu, D.; Motiwala, R.R.; Pascual-Leone, A.; Cramer, S.C. Safety and behavioral effects of high-frequency repetitive transcranial magnetic stimulation in stroke. Stroke 2009, 40, 309–312.
8. Houdayer, E.; Degardin, A.; Cassim, F.; Bocquillon, P.; Derambure, P.; Devanne, H. The effects of low-and high-frequency repetitive TMS on the input/output properties of the human corticospinal pathway. Exp. Brain Res. 2008, 187, 207–217.
9. Huang, Y.Z.; Edwards, M.J.; Rounis, E.; Bhatia, K.P.; Rothwell, J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45, 201–206.
10. Chung, S.W.; Hoy, K.E.; Fitzgerald, P.B. Theta-burst stimulation: A new form of TMS treatment for depression? Depress. Anxiety 2015, 32, 182–192.
11. Barry, M.D.; Boddington, L.J.; Igelström, K.M. Utility of intracerebral theta burst electrical stimulation to attenuate interhemispheric inhibition and to promote motor recovery after cortical injury in an animal model. Exp. Neurol. 2014, 261, 258–266.
12. Inoue, Y. Repetitive transcranial magnetic stimulation (rTMS) for higher brain function deficits. Brain Nerve 2016, 68, 1459–1470.
13. Guo, F.; Han, X.; Zhang, J.; Zhao, X.; Lou, J.; Chen, H.; Huang, X. 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, 10, e109267.
14. Müller, M.B.; Toschi, N.; Kresse, A.E.; Post, A.; Keck, M.E. Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology 2000, 23, 205–215.
15. Berretta, A.; Tzeng, Y.C.; Clarkson, A.N. Post-stroke recovery: The role of activity-dependent release of brain-derived neurotrophic factor. Expert Rev. Neurother. 2014, 14, 1335–1344.
16. Bath, K.G.; Lee, F.S. Neurotrophic factor control of adult SVZ neurogenesis. Dev. Neurobiol. 2010, 70, 339–349.
17. Jansson, L.C.; Louhivuori, L.; Wigren, H.K. Brain-derived neurotrophic factor increases the motility of a particular N-methyl-D-aspartate/GABA-responsive subset of neural progenitor cells. Neuroscience 2012, 224, 223–234.
18. Balthazart, J.; Ball, G.F. Endogenous versus exogenous markers of adult neurogenesis in canaries and other birds: Advantages and disadvantages. J. Comp. Neurol. 2014, 522, 4100–4120.
19. Park, D.; Xiang, A.P.; Mao, F.F. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 2010, 28, 2162–2171.
20. Li, W.L.; Yu, S.P.; Ogle, M.; Ding, X.S.; Wei, L. Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice. Dev. Neurobiol. 2008, 68, 1474–1486.
21. Christie, K.J.; Turnley, A.M. Regulation of endogenous neural stem/progenitor cells for neural repair—Factors that promote neurogenesis and gliogenesis in the normal and damaged brain. Front. Cell. Neurosci. 2013, 6, 70.
22. Le, Q.; Qu, Y.; Tao, Y.; Zhu, S. Effects of repetitive transcranial magnetic stimulation on hand function recovery and excitability of the motor cortex after stroke: A meta-analysis. Am. J. Phys. Med. Rehabil. 2014, 93, 422–430.
23. Yoon, K.J.; Lee, Y.T.; Han, T.R. Mechanism of functional recovery after repetitive transcranial magnetic stimulation (rTMS) in the subacute cerebral ischemic rat model: Neural plasticity or anti-apoptosis? Exp. Brain Res. 2011, 214, 549–556.
24. Barreto, G.; White, R.E.; Ouyang, Y. Astrocytes: Targets for neuroprotection in stroke. Cent. Nerv. Syst. Agents Med. Chem. 2011, 11, 164–173.
25. Liu, Z.; Chopp, M. Astrocytes, therapeutic targets for neuroprotection and neurorestoration in ischemic stroke. Prog. Neurobiol. 2016, 144, 103–120.
26. Bagley, J.A.; Belluscio, L. Dynamic imaging reveals that brain-derived neurotrophic factor can independently regulate motility and direction of neuroblasts within the rostral migratory stream. Neuroscience 2010, 169, 1449–1461.
27. Schäbitz, W.R.; Steigleder, T.; Cooper-Kuhn, C.M. Intravenous brain-derived neurotrophic factor enhances poststroke sensorimotor recovery and stimulates neurogenesis. Stroke 2007, 38, 2165–2172.
28. Chiaramello, S.; Dalmasso, G.; Bezin, L.; Marcel, D.; Jourdan, F.; Peretto, P.; Fasolo, A.; de Marchis, S. BDNF/TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur. J. Neurosci. 2007, 26, 1780–1790.
29. Young, C.C.; Brooks, K.J.; Buchan, A.M.; Szele, F.G. Cellular and molecular determinants of stroke-induced changes in subventricular zone cell migration. Antioxid. Redox Signal. 2011, 14, 1877–1888.
30. Chen, Y.H.; Zhang, R.G.; Xue, F.; Wang, H.N.; Chen, Y.C.; Hu, G.T.; Peng, Y.; Peng, Z.W.; Tan, Q.R. Quetiapine and repetitive transcranial magnetic stimulation ameliorate depression-like behaviors and up-regulate the proliferation of hippocampal-derived neural stem cells in a rat model of depression: The involvement of the BDNF/ERK signal pathway. Pharmacol. Biochem. Behav. 2015, 136, 39–46.
31. Luo, J.; Hu, X.Q.; Zhang, L.Y.; Li, L.L.; Zheng, H.Q.; Li, M.L.; Zhang, Q.J. Physical exercise regulates neural stem cells proliferation and migration via SDF-1α/CXCR4 pathway in rats after ischemic stroke. Neurosci. Lett. 2014, 578, 203–208.
32. Lee, Y.S.; Chio, C.C.; Chang, C.P. Long course hyperbaric oxygen stimulates neurogenesis and attenuates inflammation after ischemic stroke. Mediators Inflamm. 2013, 2013, 512978.
33. Morris, D.C.; Chopp, M.; Zhang, L. Thymosin β4 improves functional neurological outcome in a rat model of embolic stroke. Neuroscience 2010, 169, 674–682.
34. Chang, D.J.; Lee, N.; Choi, C. Therapeutic effect of BDNF-overexpressing human neural stem cells (HB1.F3.BDNF) in a rodent model of middle cerebral artery occlusion. Cell. Transplant. 2013, 22, 1441–1452.
35. Ridding, M.C.; Rothwell, J.C. Is there a future for therapeutic use of transcranial magnetic stimulation? Nat. Rev. Neurosci. 2007, 8, 559–567.
36. Richter, L.; Neumann, G.; Oung, S.; Schweikard, A.; Trillenberg, P. Optimal coil orientation for transcranial magnetic stimulation. PLoS ONE 2013, 8, e60358.
37. Ogiue-Ikeda, M.; Kawato, S.; Ueno, S. Acquisition of ischemic tolerance by repetitive transcranial magnetic stimulation in the rat hippocampus. Brain Res. 2005, 1037, 7–11.
38. Cárdenas-Morales, L.; Nowak, D.A.; Kammer, T.; Wolf, R.C.; Schönfeldt-Lecuona, C. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr. 2010, 22, 294–306.
39. Hoogendam, J.M.; Ramakers, G.M.; Di Lazzaro, V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul. 2010, 3, 95–118.
40. Benninger, D.H.; Iseki, K.; Kranick, S. Controlled study of 50-Hz repetitive transcranial magnetic stimulation for the treatment of Parkinson disease. Neurorehabil. Neural Repair 2012, 26, 1096–1105.
41. Kanno, M.; Matsumoto, M.; Togashi, H. Effects of repetitive transcranial magnetic stimulation on behavioral and neurochemical changes in rats during an elevated plus-maze test. J. Neurol. Sci. 2003, 211, 5–14.
42. Swanson, R.A.; Morton, M.T.; Tsao-Wu, G.; Savalos, R.A.; Davidson, C.; Sharp, F.R. A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 1990, 10, 290–293.
43. Li, C.; Wen, H.; Wang, Q.; Zhang, C.; Jiang, L.; Dou, Z.; Luo, X.; Zeng, J. Exercise training inhibits the Nogo-A/NgR1/Rho-A signals in the cortical peri-infarct area in hypertensive stroke rats. Am. J. Phys. Med. Rehabil. 2015, 94, 1083–1094.
44. Zhang, L.Y.; Hu, X.Q.; Luo, J.; Li, L.L.; Chen, X.Y.; Huang, R.X.; Pei, Z. Physical exercise improves functional recovery through mitigation of autophagy, attenuation of apoptosis and enhancement of neurogenesis after MCAO in rats. BMC Neurosci. 2013, 14, 46.
45. Imai, H.; Harland, J.; McCulloch, J.; Graham, D.I.; Brown, S.M.; Macrae, I.M. Specific expression of the cell cycle regulation proteins, GADD34 and PCNA, in the peri-infarct zone after focal cerebral ischemia in the rat. Eur. J. Neurosci. 2002, 15, 1929–1936.
46. Zhang, J.; Zhang, Y.S.; Li, J.J.; Xing, S.; Li, C.; Li, Y.; Dang, C.; Fan, Y.; Yu, J.; Pei, Z.; et al. Autophagosomes accumulation is associated with β-amyloid deposits and secondary damage in the thalamus after focal cortical infarction in hypertension rats. J. Neurochem. 2012, 120, 564–573.