Electrical stimulation promotes the survival of oligodendrocytes in mixed cortical cultures

Journal of Neuroscience Research

Volumn 90, Issue 1, 2012, Pages 72-83

  Gary, Devin S ^a,b   Malone, Misti ^a,b   Capestany, Paul ^a   Houdayer, Thierry ^a   Mcdonald, John W ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Electrical stimulation; Neuron; Neuronal activity; Oligodendrocyte

Indexed keywords

CASPASE 3; GALACTOSYLCERAMIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEIN; PROTEOCHONDROITIN SULFATE; PROTEOCHONDROITIN SULFATE NG2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN NERVE CELL; CELL CONTACT; CELL COUNT; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE FIBER; NERVE STIMULATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT;

AMINO ACID CHLOROMETHYL KETONES; ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; ANTIGENS; BIOPHYSICS; BROMODEOXYURIDINE; CASPASE 3; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CYSTEINE PROTEINASE INHIBITORS; ELECTRIC STIMULATION; FEMALE; GALACTOSYLCERAMIDASE; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN BASIC PROTEINS; NEURONS; OLIGODENDROGLIA; PHOSPHOPYRUVATE HYDRATASE; PREGNANCY; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; TETRODOTOXIN;

EID: 81255171507     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22717     Document Type: Article

References (79)

1. Abe Y, Yamamoto T, Sugiyama Y, Watanabe T, Saito N, Kayama H, Kumagai T. 1999. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J Neurotrauma 16: 945-952.
2. Abe Y, Yamamoto T, Sugiyama Y, Watanabe T, Saito N, Kayama H, Kumagai T. 2004."Anoikis" of oligodendrocytes induced by Wallerian degeneration: ultrastructural observations. J Neurotrauma 21: 119-124.
3. Ahlborn P, Schachner M, Irintchev A. 2007. One hour electrical stimulation accelerates functional recovery after femoral nerve repair. Exp Neurol 208: 137-144.
4. Al-Majed AA, Brushart TM, Gordon T. 2000a. Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci 12: 4381-4390.
5. Al-Majed AA, Neumann CM, Brushart TM, Gordon T. 2000b. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 20: 2602-2608.
6. Andrews T, Zhang P, Bhat NR. 1998. TNFalpha potentiates IFNgamma-induced cell death in oligodendrocyte progenitors. J Neurosci Res 54: 574-583.
7. Balkowiec A, Katz DM. 2000. Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J Neurosci 20: 7417-7423.
8. Balkowiec A, Katz DM. 2002. Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22: 10399-10407.
9. Barres BA, Raff MC. 1993. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361: 258-260.
10. Barres BA, Jacobson MD, Schmid R, Sendtner M, Raff MC. 1993a. Does oligodendrocyte survival depend on axons? Curr Biol 3: 489-497.
11. Barres BA, Schmid R, Sendnter M, Raff MC. 1993b. Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118: 283-295.
12. Becker D, Gary DS, Rosenzweig ES, Grill WM, McDonald JW. 2010. Functional electrical stimulation helps replenish progenitor cells in the injured spinal cord of adult rats. Exp Neurol 222: 211-218.
13. Belanger M, Stein RB, Wheeler GD, Gordon T, Leduc B. 2000. Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil 81: 1090-1098.
14. Belegu V, Oudega M, Gary DS, McDonald JW. 2007. Restoring function after spinal cord injury: promoting spontaneous regeneration with stem cells and activity-based therapies. Neurosurg Clin North Am 18: 143-168, xi.
15. Brus-Ramer M, Carmel JB, Chakrabarty S, Martin JH. 2007. Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. J Neurosci 27: 13793-13801.
16. Buttery PC, ffrench-Constant C. 1999. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol Cell Neurosci 14: 199-212.
17. Chen S, Lee JM, Zeng C, Chen H, Hsu CY, Xu J. 2006. Amyloid beta peptide increases DP5 expression via activation of neutral sphingomyelinase and JNK in oligodendrocytes. J Neurochem 97: 631-640.
18. Chen Y, Balasubramaniyan V, Peng J, Hurlock EC, Tallquist M, Li J, Lu QR. 2007. Isolation and culture of rat and mouse oligodendrocyte precursor cells. Nat Protoc 2: 1044-1051.
19. Courtine G, Gerasimenko Y, van den Brand R, Yew A, Musienko P, Zhong H, Song B, Ao Y, Ichiyama RM, Lavrov I, Roy RR, Sofroniew MV, Edgerton VR. 2009. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12: 1333-1342.
20. Daly JJ, Marsolais EB, Mendell LM, Rymer WZ, Stefanovska A, Wolpaw JR, Kantor C. 1996. Therapeutic neural effects of electrical stimulation. IEEE Trans Rehabil Eng 4: 218-230.
21. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C. 1996. Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci U S A 93: 9887-9892.
22. Domercq M, Etxebarria E, Perez-Samartin A, Matute C. 2005. Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 52: 36-46.
23. Domercq M, Perez-Samartin A, Aparicio D, Alberdi E, Pampliega O, Matute C. 2010. P2X7 receptors mediate ischemic damage to oligodendrocytes. Glia 58: 730-740.
24. Dong H, Fazzaro A, Xiang C, Korsmeyer SJ, Jacquin MF, McDonald JW. 2003. Enhanced oligodendrocyte survival after spinal cord injury in Bax-deficient mice and mice with delayed Wallerian degeneration. J Neurosci 23: 8682-8691.
25. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW, Bethea J, Levi AD. 1998. Apoptosis after traumatic human spinal cord injury. J Neurosurg 89: 911-920.
26. Faghri PD, Glaser RM, Figoni SF. 1992. Functional electrical stimulation leg cycle ergometer exercise: training effects on cardiorespiratory responses of spinal cord injured subjects at rest and during submaximal exercise. Arch Phys Med Rehabil 73: 1085-1093.
27. 2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci 17: 7252-7266.
28. Fu Y, Sun W, Shi Y, Shi R, Cheng JX. 2009. Glutamate excitotoxicity inflicts paranodal myelin splitting and retraction. PLoS One 4: e6705.
29. Gary DS, Mattson MP. 2001. Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. JNeurochem 76: 1485-1496.
30. Gary DS, Milhavet O, Camandola S, Mattson MP. 2003. Essential role for integrin linked kinase in Akt-mediated integrin survival signaling in hippocampal neurons. J Neurochem 84: 878-890.
31. Gerasimenko Y, Musienko P, Bogacheva I, Moshonkina T, Savochin A, Lavrov I, Roy RR, Edgerton VR. 2009. Propriospinal bypass of the serotonergic system that can facilitate stepping. J Neurosci 29: 5681-5689.
32. Geremia NM, Gordon T, Brushart TM, Al-Majed AA, Verge VM. 2007. Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Exp Neurol 205: 347-359.
33. s mutant mouse. J Physiol 534: 627-639.
34. Gottlieb M, Domercq M, Matute C. 2000. Altered expression of the glutamate transporter EAAC1 in neurons and immature oligodendrocytes after transient forebrain ischemia. J Cereb Blood Flow Metab 20: 678-687.
35. Gyllensten L, Malmfors T. 1963. Myelinization of the optic nerve and its dependence on visual function-a quantitative investigation in mice. JEmbryol Exp Morphol 11: 255-266.
36. Hisahara S, Shoji S, Okano H, Miura M. 1997. ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J Neurochem 69: 10-20.
37. Hooker SP, Figoni SF, Rodgers MM, Glaser RM, Mathews T, Suryaprasad AG, Gupta SC. 1992a. Metabolic and hemodynamic responses to concurrent voluntary arm crank and electrical stimulation leg cycle exercise in quadriplegics. J Rehabil Res Dev 29: 1-11.
38. Hooker SP, Figoni SF, Rodgers MM, Glaser RM, Mathews T, Suryaprasad AG, Gupta SC. 1992b. Physiologic effects of electrical stimulation leg cycle exercise training in spinal cord injured persons. Arch Phys Med Rehabil 73: 470-476.
39. Hooker SP, Scremin AM, Mutton DL, Kunkel CF, Cagle G. 1995. Peak and submaximal physiologic responses following electrical stimulation leg cycle ergometer training. J Rehabil Res Dev 32: 361-366.
40. Horiuchi M, Maezawa I, Itoh A, Wakayama K, Jin LW, Itoh T, Decarli C. 2010. Amyloid beta1-42 oligomer inhibits myelin sheet formation in vitro. Neurobiol Aging (in press).
41. Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, Frommer F, von Hoch L, Kramer D, Minichiello L, Kollias G, Lassmann H, Waisman A. 2005. Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol 175: 5875-5884.
42. Hu QD, Ang BT, Karsak M, Hu WP, Cui XY, Duka T, Takeda Y, Chia W, Sankar N, Ng YK, Ling EA, Maciag T, Small D, Trifonova R, Kopan R, Okano H, Nakafuku M, Chiba S, Hirai H, Aster JC, Schachner M, Pallen CJ, Watanabe K, Xiao ZC. 2003. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell 115: 163-175.
43. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD. 2006. Astrocytes promote myelination in response to electrical impulses. Neuron 49: 823-832.
44. Itoh K, Stevens B, Schachner M, Fields RD. 1995. Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 270: 1369-1372.
45. Jeon JY, Weiss CB, Steadward RD, Ryan E, Burnham RS, Bell G, Chilibeck P, Wheeler GD. 2002. Improved glucose tolerance and insulin sensitivity after electrical stimulation-assisted cycling in people with spinal cord injury. Spinal Cord 40: 110-117.
46. Kolodziejczyk K, Hamilton NB, Wade A, Karadottir R, Attwell D. 2009. The effect of N-acetyl-aspartyl-glutamate and N-acetyl-aspartate on white matter oligodendrocytes. Brain 132: 1496-1508.
47. Lavrov I, Courtine G, Dy CJ, van den Brand R, Fong AJ, Gerasimenko Y, Zhong H, Roy RR, Edgerton VR. 2008. Facilitation of stepping with epidural stimulation in spinal rats: role of sensory input. J Neurosci 28: 7774-7780.
48. Li J, Ramenaden ER, Peng J, Koito H, Volpe JJ, Rosenberg PA. 2008. Tumor necrosis factor alpha mediates lipopolysaccharide-induced microglial toxicity to developing oligodendrocytes when astrocytes are present. J Neurosci 28: 5321-5330.
49. Li Q, Brus-Ramer M, Martin JH, McDonald JW. 2010. Electrical stimulation of the medullary pyramid promotes proliferation and differentiation of oligodendrocyte progenitor cells in the corticospinal tract of the adult rat. Neurosci Lett 479: 128-133.
50. Li S, Stys PK. 2000. Mechanisms of ionotropic glutamate receptor-mediated excitotoxicity in isolated spinal cord white matter. J Neurosci 20: 1190-1198.
51. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW. 1997. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17: 5395-5406.
52. Matute C, Domercq M, Sanchez-Gomez MV. 2006. Glutamate-mediated glial injury: mechanisms and clinical importance. Glia 53: 212-224.
53. Matute C, Alberdi E, Domercq M, Sanchez-Gomez MV, Perez-Samartin A, Rodriguez-Antiguedad A, Perez-Cerda F. 2007. Excitotoxic damage to white matter. J Anat 210: 693-702.
54. McDonald JW, Belegu V. 2006. Demyelination and remyelination after spinal cord injury. J Neurotrauma 23: 345-359.
55. McDonald JW, Sadowsky C. 2002. Spinal-cord injury. Lancet 359: 417-425.
56. McIver SR, Muccigrosso M, Gonzales ER, Lee JM, Roberts MS, Sands MS, Goldberg MP. 2010. Oligodendrocyte degeneration and recovery after focal cerebral ischemia. Neuroscience (in press).
57. Minagar A, Toledo EG, Alexander JS, Kelley RE. 2004. Pathogenesis of brain and spinal cord atrophy in multiple sclerosis. J Neuroimaging 14( Suppl 3): 5S-10S.
58. Mohr T, Andersen JL, Biering-Sorensen F, Galbo H, Bangsbo J, Wagner A, Kjaer M. 1997a. Long-term adaptation to electrically induced cycle training in severe spinal cord injured individuals. Spinal Cord 35: 1-16.
59. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. 1997b. Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int 61: 22-25.
60. Mutton DL, Scremin AM, Barstow TJ, Scott MD, Kunkel CF, Cagle TG. 1997. Physiologic responses during functional electrical stimulation leg cycling and hybrid exercise in spinal cord injured subjects. Arch Phys Med Rehabil 78: 712-718.
61. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, She H, Michaud N, Hafezi-Moghadam A, Miller JW, Benowitz LI. 2006. Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 26: 12633-12641.
62. Omlin FX. 1997. Optic disc and optic nerve of the blind cape mole-rat (Georychus capensis): a proposed model for naturally occurring reactive gliosis. Brain Res Bull 44: 627-632.
63. Park E, Velumian AA, Fehlings MG. 2004. The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration. J Neurotrauma 21: 754-774.
64. Ragnarsson KT. 1988. Physiologic effects of functional electrical stimulation-induced exercises in spinal cord-injured individuals. Clin Orthop Relat Res: 53-63.
65. Relvas JB, Setzu A, Baron W, Buttery PC, LaFlamme SE, Franklin RJ, ffrench-Constant C. 2001. Expression of dominant-negative and chimeric subunits reveals an essential role for beta1 integrin during myelination. Curr Biol 11: 1039-1043.
66. Schulz R, Vogel T, Mashima T, Tsuruo T, Krieglstein K. 2009. Involvement of Fractin in TGF-beta-induced apoptosis in oligodendroglial progenitor cells. Glia 57: 1619-1629.
67. Schuster N, Bender H, Philippi A, Subramaniam S, Strelau J, Wang Z, Krieglstein K. 2002. TGF-beta induces cell death in the oligodendroglial cell line OLI-neu. Glia 40: 95-108.
68. Scremin AM, Kurta L, Gentili A, Wiseman B, Perell K, Kunkel C, Scremin OU. 1999. Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program. Arch Phys Med Rehabil 80: 1531-1536.
69. Scurlock B, Dawson G. 1999. Differential responses of oligodendrocytes to tumor necrosis factor and other pro-apoptotic agents: role of ceramide in apoptosis. J Neurosci Res 55: 514-522.
70. Stevens B, Fields RD. 2000. Response of Schwann cells to action potentials in development. Science 287: 2267-2271.
71. Stevens B, Tanner S, Fields RD. 1998. Control of myelination by specific patterns of neural impulses. J Neurosci 18: 9303-9311.
72. Stevens B, Porta S, Haak LL, Gallo V, Fields RD. 2002. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36: 855-868.
73. Stevens B, Ishibashi T, Chen JF, Fields RD. 2004. Adenosine: an activity-dependent axonal signal regulating MAP kinase and proliferation in developing Schwann cells. Neuron Glia Biol 1: 23-34.
74. Tauber H, Waehneldt TV, Neuhoff V. 1980. Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16: 235-238.
75. Udina E, Furey M, Busch S, Silver J, Gordon T, Fouad K. 2008. Electrical stimulation of intact peripheral sensory axons in rats promotes outgrowth of their central projections. Exp Neurol 210: 238-247.
76. Wang Y, Ren Z, Tao D, Tilwalli S, Goswami R, Balabanov R. 2010. STAT1/IRF-1 signaling pathway mediates the injurious effect of interferon-gamma on oligodendrocyte progenitor cells. Glia 58: 195-208.
77. Warden P, Bamber NI, Li H, Esposito A, Ahmad KA, Hsu CY, Xu XM. 2001. Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats. Exp Neurol 168: 213-224.
78. Wu B, Ren X. 2009. Promoting axonal myelination for improving neurological recovery in spinal cord injury. J Neurotrauma 26: 1847-1856.
79. Xu J, Chen S, Ahmed SH, Chen H, Ku G, Goldberg MP, Hsu CY. 2001. Amyloid-beta peptides are cytotoxic to oligodendrocytes. J Neurosci 21: RC118.