The morphological and molecular changes of brain cells exposed to direct current electric field stimulation

International Journal of Neuropsychopharmacology

Volumn 18, Issue 5, 2015, Pages 1-16

  Pelletier, Simon J ^a   Lagace, Marie ^a   St Amour, Isabelle ^b   Arsenault, Dany ^c   Cisbani, Giulia ^d   Chabrat, Audrey ^e   Fecteau, Shirley ^a   Levsque, Martin ^a   Cicchetti, Francesca ^a  

^a University Laval   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^d Centre de Recherche de L'Institut Universitaire en Sant Mentale de   (Canada)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

GAP 43; Inflammation; Transcranial Direct Current Stimulation

Indexed keywords

CYCLOOXYGENASE 2; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUROMODULIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BRAIN CELL; CELL BODY; CELL DEATH; CELL DIFFERENTIATION; CELL POPULATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; DIRECT CURRENT; DIRECT CURRENT ELECTRICAL FIELD; DOPAMINERGIC NERVE CELL; ELECTROSTIMULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPLANT; FETUS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; MESENCEPHALON; MICROGLIA; MOUSE; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRANIAL DIRECT CURRENT STIMULATION; ANIMAL; CELL CULTURE TECHNIQUE; CYTOLOGY; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; PSEUDOPODIUM;

ANIMALS; ASTROCYTES; CELL CULTURE TECHNIQUES; CYCLOOXYGENASE 2; ELECTRIC STIMULATION; GAP-43 PROTEIN; IN VITRO TECHNIQUES; LIPOPOLYSACCHARIDES; MICE; MICROGLIA; NEURITES; NEURONS; PSEUDOPODIA;

EID: 84931269735     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu090     Document Type: Article

References (82)

1. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner HR, Caroni P (1995) Overexpression of the neural growth-Associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278
2. Alais S, Simoes S, Baas D, Lehmann S, Raposo G, Darlix JL, Leblanc P (2008) Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol Cell 100:603-615
3. Alexander JK, Fuss B, Colello RJ (2006) Electric field-induced astrocyte alignment directs neurite outgrowth. Neuron Glia Biol 2:93-103
4. Alhouayek M, Muccioli GG (2014) COX-2-derived endocannabinoid metabolites as novel inflammatory mediators. Trends Pharmacol Sci 35:284-292
5. Auvichayapat N, Rotenberg A, Gersner R, Ngodklang S, Tiamkao S, Tassaneeyakul W, Auvichayapat P (2013) Transcranial direct current stimulation for treatment of refractory childhood focal epilepsy. Brain Stimul 6:696-700
6. Babona-Pilipos R, Droujinine IA, Popovic MR, Morshead CM (2011) Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric fields. PLoS One 6:e23808
7. Baetge EE, Hammang JP (1991) Neurite outgrowth in PC12 cells deficient in GAP-43. Neuron 6:21-30
8. Bai H, McCaig CD, Forrester JV, Zhao M (2004) DC electric fields induce distinct preangiogenic responses in microvascular and macrovascular cells. Arterioscler Thromb Vasc Biol 24:1234-1239
9. Bedlack RS Jr, Wei M, Loew LM (1992) Localized membrane depolarizations and localized calcium influx during electric fieldguided neurite growth. Neuron 9:393-403
10. Benninger DH, Lomarev M, Lopez G, Wassermann EM, Li X, Considine E, Hallett M (2010) Transcranial direct current stimulation for the treatment of Parkinson's disease. J Neurol Neurosurg Psychiatry 81:1105-1111
11. Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20:84-91
12. Biewenga JE, Schrama LH, Gispen WH (1996) Presynaptic phosphoprotein B-50/GAP-43 in neuronal and synaptic plasticity. Acta Biochim Pol 43:327-338
13. Biffo S, Verhaagen J, Schrama LH, Schotman P, Danho W, Margolis FL (1990) B-50/GAP43 expression correlates with process outgrowth in the embryonic mouse nervous system. Eur J Neurosci 2:487-499
14. Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys JG (2004) Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol 557:175-190
15. Bikson M, Datta A, Elwassif M (2009) Establishing safety limits for transcranial direct current stimulation. Clin Neurophysiol 120:1033-1034
16. Bikson M, Reato D, Rahman A (2012) Cellular and network effects of transcranial direct current stimulation: insights from animal models and brain slice. In: transcranial brain stimulation (Miniussi C, Paulus W, Rossini PM, eds), pp 55-92. Boca Raton, FL: CRC Press/Taylor & Francis
17. Boggio PS, Ferrucci R, Rigonatti SP, Covre P, Nitsche M, Pascual- Leone A, Fregni F (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J Neurol Sci 249:31-38
18. Booth R, Kim H (2012) Characterization of a microfluidic in vitro model of the blood-brain barrier (muBBB). Lab Chip 12:1784-1792
19. Borgens RB (1999) Electrically mediated regeneration and guidance of adult mammalian spinal axons into polymeric channels. Neuroscience 91:251-264
20. Borgens RB, Shi R, Mohr TJ, Jaeger CB (1994) Mammalian cortical astrocytes align themselves in a physiological voltage gradient. Exp Neurol 128:41-49
21. Buffo A, Holtmaat AJ, Savio T, Verbeek JS, Oberdick J, Oestreicher AB, Gispen WH, Verhaagen J, Rossi F, Strata P (1997) Targeted overexpression of the neurite growth-Associated protein B-50/GAP-43 in cerebellar Purkinje cells induces sprouting after axotomy but not axon regeneration into growth-permissive transplants. J Neurosci 17:8778-8791
22. Cicchetti F, Barker RA (2014) The glial response to intracerebrally delivered therapies for neurodegenerative disorders: is this a critical issue? Front Pharmacol 5:139
23. Cork RJ, McGinnis ME, Tsai J, Robinson KR (1994) The growth of PC12 neurites is biased towards the anode of an applied electrical field. J Neurobiol 25:1509-1516
24. Dell'osso B, Dobrea C, Arici C, Benatti B, Ferrucci R, Vergari M, Priori A, Altamura AC (2013) Augmentative transcranial direct current stimulation (tDCS) in poor responder depressed patients: a follow-up study. CNS Spectr:1-8
25. del Zoppo G, Ginis I, Hallenbeck JM, Iadecola C, Wang X, Feuerstein GZ (2000) Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol 10:95-112
26. Erskine L, Stewart R, McCaig CD (1995) Electric field-directed growth and branching of cultured frog nerves: effects of aminoglycosides and polycations. J Neurobiol 26:523-536
27. Evangelopoulos ME, Weis J, Kruttgen A (2005) Signalling pathways leading to neuroblastoma differentiation after serum withdrawal: HDL blocks neuroblastoma differentiation by inhibition of EGFR. Oncogene 24:3309-3318
28. Fenoy AJ, Goetz L, Chabardes S, Xia Y (2014) Deep brain stimulation: are astrocytes a key driver behind the scene? CNS Neurosci Ther 20:191-201
29. Franke K, Gruler H (1990) Galvanotaxis of human granulocytes: electric field jump studies. Eur Biophys J 18:335-346
30. Gil V, del Rio JA (2012) Analysis of axonal growth and cell migration in 3D hydrogel cultures of embryonic mouse CNS tissue. Nat Protoc 7:268-280
31. Goslin K, Schreyer DJ, Skene JH, Banker G (1988) Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature 336:672-674
32. Henn A, Lund S, Hedtjarn M, Schrattenholz A, Porzgen P, Leist M (2009) The suitability of BV2 cells as alternative model system for primary microglia cultures or for animal experiments examining brain inflammation. ALTEX 26:83-94
33. Hinkle L, McCaig CD, Robinson KR (1981) The direction of growth of differentiating neurones and myoblasts from frog embryos in an applied electric field. J Physiol 314:121-135
34. Huang R, Peng L, Hertz L (1997) Effects of a low-voltage static electric field on energy metabolism in astrocytes. Bioelectromagnetics 18:77-80
35. Jacobsson SO, Fowler CJ (2001) Characterization of palmitoylethanolamide transport in mouse Neuro-2a neuroblastoma and rat RBL-2H3 basophilic leukaemia cells: comparison with anandamide. Br J Pharmacol 132:1743-1754
36. Jaffe LF, Poo MM (1979) Neurites grow faster towards the cathode than the anode in a steady field. J Exp Zool 209:115-128
37. Jain S, Sharma A, Basu B (2013) Vertical electric field stimulated neural cell functionality on porous amorphous carbon electrodes. Biomaterials 34:9252-9263
38. Jiang T, Xu RX, Zhang AW, Di W, Xiao ZJ, Miao JY, Luo N, Fang YN (2012) Effects of transcranial direct current stimulation on hemichannel pannexin-1 and neural plasticity in rat model of cerebral infarction. Neuroscience 226:421-426
39. Joung Lee S, Chun MH (2013) Combination transcranial direct current stimulation and virtual reality therapy for upper extremity training in subacute stroke patients. Arch Phys Med Rehabil 95:431-438
40. Kabakov AY, Muller PA, Pascual-Leone A, Jensen FE, Rotenberg A (2012) Contribution of axonal orientation to pathwaydependent modulation of excitatory transmission by direct current stimulation in isolated rat hippocampus. J Neurophysiol 107:1881-1889
41. Kamida T, Kong S, Eshima N, Abe T, Fujiki M, Kobayashi H (2011) Transcranial direct current stimulation decreases convulsions and spatial memory deficits following pilocarpineinduced status epilepticus in immature rats. Behav Brain Res 217:99-103
42. Kim SJ, Kim BK, Ko YJ, Bang MS, Kim MH, Han TR (2010) Functional and histologic changes after repeated transcranial direct current stimulation in rat stroke model. J Korean Med Sci 25:1499-1505
43. Knott C, Stern G, Wilkin GP (2000) Inflammatory regulators in Parkinson's disease: iNOS, lipocortin-1, and cyclooxygenases- 1 and -2. Mol Cell Neurosci 16:724-739
44. Koppes AN, Seggio AM, Thompson DM (2011) Neurite outgrowth is significantly increased by the simultaneous presentation of Schwann cells and moderate exogenous electric fields. J Neural Eng 8:046023
45. Li J, Nandagopal S, Wu D, Romanuik SF, Paul K, Thomson DJ, Lin F (2011) Activated T lymphocytes migrate toward the cathode of DC electric fields in microfluidic devices. Lab Chip 11:1298-1304
46. Li X, Kolega J (2002) Effects of direct current electric fields on cell migration and actin filament distribution in bovine vascular endothelial cells. J Vasc Res 39:391-404
47. Liebetanz D, Koch R, Mayenfels S, Konig F, Paulus W, Nitsche MA (2009) Safety limits of cathodal transcranial direct current stimulation in rats. Clin Neurophysiol 120:1161-1167
48. Lin F, Baldessari F, Gyenge CC, Sato T, Chambers RD, Santiago JG, Butcher EC (2008) Lymphocyte electrotaxis in vitro and in vivo. J Immunol 181:2465-2471
49. McCaig CD (1987) Spinal neurite reabsorption and regrowth in vitro depend on the polarity of an applied electric field. Development 100:31-41
50. McCaig CD, Sangster L, Stewart R (2000) Neurotrophins enhance electric field-directed growth cone guidance and directed nerve branching. Dev Dyn 217:299-308
51. McCaig CD, Rajnicek AM, Song B, Zhao M (2005) Controlling cell behavior electrically: current views and future potential. Physiol Rev 85:943-978
52. Meiri KF, Pfenninger KH, Willard MB (1986) Growth-Associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci U S A 83:3537-3541
53. Michaud JP, Halle M, Lampron A, Theriault P, Prefontaine P, Filali M, Tribout-Jover P, Lanteigne AM, Jodoin R, Cluff C, Brichard V, Palmantier R, Pilorget A, Larocque D, Rivest S (2013) Toll-like receptor 4 stimulation with the detoxified ligand monophosphoryl lipid A improves Alzheimer's disease-related pathology. Proc Natl Acad Sci U S A 110:1941-1946
54. Minhas P, Bikson M, Woods AJ, Rosen AR, Kessler SK (2012) Transcranial direct current stimulation in pediatric brain: a computational modeling study. Conf Proc IEEE Eng Med Biol Soc 2012:859-862
55. Mollace V, Muscoli C, Masini E, Cuzzocrea S, Salvemini D (2005) Modulation of prostaglandin biosynthesis by nitric oxide and nitric oxide donors. Pharmacol Rev 57:217-252
56. Moriarty LJ, Borgens RB (2001) An oscillating extracellular voltage gradient reduces the density and influences the orientation of astrocytes in injured mammalian spinal cord. J Neurocytol 30:45-57
57. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1:206-223
58. Oberheim NA, Wang X, Goldman S, Nedergaard M (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547-553
59. Orida N, Feldman JD (1982) Directional protrusive pseudopodial activity and motility in macrophages induced by extracellular electric fields. Cell Motil 2:243-255
60. Palmer AM, Messerli MA, Robinson KR (2000) Neuronal galvanotropism is independent of external Ca(2+) entry or internal Ca(2+) gradients. J Neurobiol 45:30-38
61. Patel N, Poo MM (1982) Orientation of neurite growth by extracellular electric fields. J Neurosci 2:483-496
62. Pelletier SJ, Cicchetti F (2014) Cellular and molecular mechanisms of action of transcranial direct current stimulation: evidence from in vitro and in vivo models. Int J Neuropsychopharmacol. doi:10.1093/ijnp/pyu047
63. Pereira JB, Junque C, Bartres-Faz D, Marti MJ, Sala-Llonch R, Compta Y, Falcon C, Vendrell P, Pascual-Leone A, Valls-Sole J, Tolosa E (2013) Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson's disease. Brain Stimul 6:16-24
64. Peruzzotti-Jametti L, Cambiaghi M, Bacigaluppi M, Gallizioli M, Gaude E, Mari S, Sandrone S, Cursi M, Teneud L, Comi G, Musco G, Martino G, Leocani L (2013) Safety and efficacy of transcranial direct current stimulation in acute experimental ischemic stroke. Stroke 44:3166-3174
65. Rajnicek AM, Foubister LE, McCaig CD (2006a) Temporally and spatially coordinated roles for Rho, Rac, Cdc42 and their effectors in growth cone guidance by a physiological electric field. J Cell Sci 119:1723-1735
66. Rajnicek AM, Foubister LE, McCaig CD (2006b) Growth cone steering by a physiological electric field requires dynamic microtubules, microfilaments and Rac-mediated filopodial asymmetry. J Cell Sci 119:1736-1745
67. Rueger MA, Keuters MH, Walberer M, Braun R, Klein R, Sparing R, Fink GR, Graf R, Schroeter M (2012) Multi-session transcranial direct current stimulation (tDCS) elicits inflammatory and regenerative processes in the rat brain. PLoS One 7:e43776
68. Shapiro S, Borgens R, Pascuzzi R, Roos K, Groff M, Purvines S, Rodgers RB, Hagy S, Nelson P (2005) Oscillating field stimulation for complete spinal cord injury in humans: a phase 1 trial. J Neurosurg Spine 2:3-10
69. Sheng W, Zong Y, Mohammad A, Ajit D, Cui J, Han D, Hamilton JL, Simonyi A, Sun AY, Gu Z, Hong JS, Weisman GA, Sun GY (2011) Pro-inflammatory cytokines and lipopolysaccharide induce changes in cell morphology, and upregulation of ERK1/2, iNOS and sPLA(2)-IIA expression in astrocytes and microglia. J Neuroinflammation 8:121
70. Song B, Gu Y, Pu J, Reid B, Zhao Z, Zhao M (2007) Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo. Nat Protoc 2:1479-1489
71. Spezia Adachi LN, Caumo W, Laste G, Fernandes Medeiros L, Ripoll Rozisky J, de Souza A, Fregni F, Torres IL (2012) Reversal of chronic stress-induced pain by transcranial direct current stimulation (tDCS) in an animal model. Brain Res 1489:17-26
72. Stewart R, Erskine L, McCaig CD (1995) Calcium channel subtypes and intracellular calcium stores modulate electric fieldstimulated and -oriented nerve growth. Dev Biol 171:340-351
73. Teismann P, Tieu K, Cohen O, Choi DK, Wu DC, Marks D, Vila M, Jackson-Lewis V, Przedborski S (2003) Pathogenic role of glial cells in Parkinson's disease. Mov Disord 18:121-129
74. Vejlstrup NG, Bouloumie A, Boesgaard S, Andersen CB, Nielsen- Kudsk JE, Mortensen SA, Kent JD, Harrison DG, Busse R, Alder shvile J (1998) Inducible nitric oxide synthase (iNOS) in the human heart: expression and localization in congestive heart failure. J Mol Cell Cardiol 30:1215-1223
75. Wang X, Zhang S, Sun C, Yuan ZG, Wu X, Wang D, Ding Z, Hu R (2011) Proteomic profiles of mouse neuro N2a cells infected with variant virulence of rabies viruses. J Microbiol Biotechnol 21:366-373
76. Wood MD, Willits RK (2009) Applied electric field enhances DRG neurite growth: influence of stimulation media, surface coating and growth supplements. J Neural Eng 6:046003
77. Yoon KJ, Oh BM, Kim DY (2012) Functional improvement and neuroplastic effects of anodal transcranial direct current stimulation (tDCS) delivered 1 day vs. 1 week after cerebral ischemia in rats. Brain Res 1452:61-72
78. Yu Y, Matsuyama Y, Nakashima S, Yanase M, Kiuchi K, Ishiguro N (2004) Effects of MPSS and a potent iNOS inhibitor on traumatic spinal cord injury. Neuroreport 15:2103-2107
79. Zhao M, Bai H, Wang E, Forrester JV, McCaig CD (2004a) Electrical stimulation directly induces pre-Angiogenic responses in vascular endothelial cells by signaling through VEGF receptors. J Cell Sci 117:397-405
80. Zhao M, Song B, Pu J, Wada T, Reid B, Tai G, Wang F, Guo A, Walczysko P, Gu Y, Sasaki T, Suzuki A, Forrester JV, Bourne HR, Devreotes PN, McCaig CD, Penninger JM (2006) Electrical signals control wound healing through phosphatidylinositol- 3-OH kinase-gamma and PTEN. Nature 442:457-460
81. Zhao S, Maxwell S, Jimenez-Beristain A, Vives J, Kuehner E, Zhao J, O'Brien C, de Felipe C, Semina E, Li M (2004b) Generation of embryonic stem cells and transgenic mice expressing green fluorescence protein in midbrain dopaminergic neurons. Eur J Neurosci 19:1133-1140
82. Zhu Y, Zhu M, Lance P (2012) iNOS signaling interacts with COX-2 pathway in colonic fibroblasts. Exp Cell Res 318:2116-2127