Neuronal activity promotes myelination via a cAMP pathway

GLIA

Volumn 61, Issue 6, 2013, Pages 843-854

  Malone, Misti ^a,b   Gary, Devin ^a,b   Yang, In Hong ^a,c   Miglioretti, Anna ^b   Houdayer, Thierry ^b   Thakor, Nitish ^a,c   Mcdonald, John ^a,b  

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

^b Hugo Moser Kennedy Krieger Research Institute   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Electrical stimulation; Frequency; Microfluidic chamber; Myelin; Oligodendrocyte

Indexed keywords

CYCLIC AMP; FORSKOLIN; MYELIN; ROLIPRAM;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ELECTROSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MIXED CELL CULTURE; MYELIN SHEATH; MYELINATION; NERVE CONDUCTION; NERVE FIBER GROWTH; NERVE STIMULATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

ACTION POTENTIALS; ANIMALS; AXONS; CELLS, CULTURED; CYCLIC AMP; ELECTRIC STIMULATION; GANGLIA, SPINAL; MYELIN SHEATH; NEURONS; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84876475744     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22476     Document Type: Article

References (84)

1. Afshari FS, Chu AK, Sato-Bigbee C. Effect of cyclic AMP on the expression of myelin basic protein species and myelin proteolipid protein in committed oligodendrocytes: Differential involvement of the transcription factor CREB. J Neurosci Res 2001:66:37-45.
2. Anderson S, Miskimins R. Involvement of protein kinase C in cAMP regulation of myelin basic protein gene expression. J Neurosci Res 1994;37:604-611.
3. Bakiri Y, Attwell D, Karadottir R. Electrical signalling properties of oligodendrocyte precursor cells. Neuron Glia Biol 2009;5:3-11.
4. Baron W, Colognato H, Ffrench-Constant C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 2005;49:467-479.
5. Barres BA, Raff MC. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 1993;361:258-260.
6. Becker D, Gary DS, Rosenzweig ES, Grill WM, McDonald JW. Functional electrical stimulation helps replenish progenitor cells in the injured spinal cord of adult rats. Exp Neurol 2010;222:211-218.
7. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 2001;30:385-397.
8. Brushart TM, Hoffman PN, Royall RM, Murinson BB, Witzel C, Gordon T. Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci 2002;22:6631-6638.
9. Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL. GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 1996;17:229-243.
10. Charles P, Tait S, Faivre-Sarrailh C, Barbin G, Gunn-Moore F, Denisenko-Nehrbass N, Guennoc AM, Girault JA, Brophy PJ, Lubetzki C. Neurofascin is a glial receptor for the paranodin/Caspr-contactin axonal complex at the axoglial junction. Curr Biol 2002;12:217-220.
11. Clark RE Jr., Miskimins WK, Miskimins R. Cyclic AMP inducibility of the myelin basic protein gene promoter requires the NF1 site. Int J Dev Neurosci 2002;20:103-111.
12. Colognato H, Baron W, Avellana-Adalid V, Relvas JB, Baron-Van Evercooren A, Georges-Labouesse E, Ffrench-Constant C. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat Cell Biol 2002;4:833-841.
13. Colognato H, Ramachandrappa S, Olsen IM, Ffrench-Constant C. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 2004;167:365-375.
14. De Angelis F, Bernardo A, Magnaghi V, Minghetti L, Tata AM. Muscarinic receptor subtypes as potential targets to modulate oligodendrocyte progenitor survival, proliferation, and differentiation. Dev Neurobiol 2012;72:713-728.
15. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C. Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 1996;93:9887-9892.
16. Eyermann C, Czaplinski K, Colognato H. Dystroglycan promotes filopodial formation and process branching in differentiating oligodendroglia. J Neurochem 2012;120:928-947.
17. Fernandez PA, Tang DG, Cheng L, Prochiantz A, Mudge AW, Raff MC. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 2000;28:81-90.
18. Fields RD. Myelination: An overlooked mechanism of synaptic plasticity. Neuroscientist 2005;11:528-531.
19. Fields RD, Eshete F, Stevens B, Itoh K. Action potential-dependent regulation of gene expression: Temporal specificity in Ca2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci 1997;17:7252-7266.
20. Fields RD, Neale EA, Nelson PG. Effects of patterned electrical activity on neurite outgrowth from mouse sensory neurons. J Neurosci 1990;10:2950-2964.
21. Fitzgerald M. Spontaneous and evoked activity of fetal primary afferents in vivo. Nature 1987;326:603-605.
22. Fouad K, Pedersen V, Schwab ME, Brosamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 2001;11:1766-1770.
23. Fricker FR, Zhu N, Tsantoulas C, Abrahamsen B, Nassar MA, Thakur M, Garratt AN, Birchmeier C, McMahon SB, Wood JN. Sensory axon-derived neuregulin-1 is required for axoglial signaling and normal sensory function but not for long-term axon maintenance. J Neurosci 2009;29:7667-7678.
24. Friessen AJ, Miskimins WK, Miskimins R. Cyclin-dependent kinase inhibitor p27kip1 is expressed at high levels in cells that express a myelinating phenotype. J Neurosci Res 1997;50:373-382.
25. Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 1996;16:2659-2670.
26. Garcia C, Paez P, Davio C, Soto EF, Pasquini JM. Apotransferrin induces cAMP/CREB pathway and cell cycle exit in immature oligodendroglial cells. J Neurosci Res 2004;78:338-346.
27. Gary DS, Malone M, Capestany P, Houdayer T, McDonald JW. Electrical stimulation promotes the survival of oligodendrocytes in mixed cortical cultures. J Neurosci Res 2012;90:72-83.
28. Geremia NM, Gordon T, Brushart TM, Al-Majed AA, Verge VM. Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Exp Neurol 2007;205:347-359.
29. Gollan L, Sabanay H, Poliak S, Berglund EO, Ranscht B, Peles E. Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J Cell Biol 2002;157:1247-1256.
30. Gordon T, Udina E, Verge VM, de Chaves EI. Brief electrical stimulation accelerates axon regeneration in the peripheral nervous system and promotes sensory axon regeneration in the central nervous system. Motor Control 2009;13:412-441.
31. Gudz TI, Komuro H, Macklin WB. Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J Neurosci 2006;26:2458-2466.
32. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 2000;20:3993-4001.
33. Hu QD, Ang BT, Karsak M, Hu WP, Cui XY, Duka T, Takeda Y, Chia W, Sankar N, Ng YK. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell 2003;115:163-175.
34. Hughes P, Dragunow M. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 1995;47:133-178.
35. Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD. Astrocytes promote myelination in response to electrical impulses. Neuron 2006;49:823-832.
36. Itoh K, Ozaki M, Stevens B, Fields RD. Activity-dependent regulation of N-cadherin in DRG neurons: Differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials. J Neurobiol 1997;33:735-748.
37. Itoh K, Stevens B, Schachner M, Fields RD. Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 1995;270:1369-1372.
38. Karadottir R, Hamilton NB, Bakiri Y, Attwell D. Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nat Neurosci 2008;11:450-456.
39. Kimura K, Yanagida Y, Haruyama T, Kobatake E, Aizawa M. Gene expression in the electrically stimulated differentiation of PC12 cells. J Biotechnol 1998;63:55-65.
40. Lee X, Yang Z, Shao Z, Rosenberg SS, Levesque M, Pepinsky RB, Qiu M, Miller RH, Chan JR, Mi S. NGF regulates the expression of axonal LINGO-1 to inhibit oligodendrocyte differentiation and myelination. J Neurosci 2007;27:220-225.
41. Li H, Wang C. Post-transcriptional regulation of PDGF alpha-receptor in O-2A progenitor cells. Int J Clin Exp Med 2011;4:241-251.
42. Li Q, Brus-Ramer M, Martin JH, McDonald JW. Electrical stimulation of the medullary pyramid promotes proliferation and differentiation of oligodendrocyte progenitor cells in the corticospinal tract of the adult rat. Neurosci Lett 2010;479:128-133.
43. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 2004;24:6402-6409.
44. Marmur R, Kessler JA, Zhu G, Gokhan S, Mehler MF. Differentiation of oligodendroglial progenitors derived from cortical multipotent cells requires extrinsic signals including activation of gp130/LIFbeta receptors. J Neurosci 1998;18:9800-9811.
45. Marta CB, Paez P, Lopez M, Pellegrino de Iraldi A, Soto EF, Pasquini JM. Morphological changes of myelin sheaths in rats intracranially injected with apotransferrin. Neurochem Res 2003;28:101-110.
46. McMorris FA. Cyclic AMP induction of the myelin enzyme 2', 3'-cyclic nucleotide 3'-phosphohydrolase in rat oligodendrocytes. J Neurochem 1983;41:506-515.
47. Ming GL, Song HJ, Berninger B, Holt CE, Tessier-Lavigne M, Poo MM. cAMP-dependent growth cone guidance by netrin-1. Neuron 1997;19:1225-1235.
48. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 2002;34:885-893.
49. Neumann S, Woolf CJ. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 1999;23:83-91.
50. Noble M, Murray K, Stroobant P, Waterfield MD, Riddle P. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature 1988;333:560-562.
51. Ozaki M, Itoh K, Miyakawa Y, Kishida H, Hashikawa T. Protein processing and release of neuregulin-1 are regulated in an activity-dependent manner. J Neurochem 2004;91:176-188.
52. Paez PM, Garcia CI, Davio C, Campagnoni AT, Soto EF, Pasquini JM. Apotransferrin promotes the differentiation of two oligodendroglial cell lines. Glia 2004;46:207-217.
53. Park SK, Solomon D, Vartanian T. Growth factor control of CNS myelination. Dev Neurosci 2001;23:327-337.
54. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 2002;34:895-903.
55. Raible DW, McMorris FA. Cyclic AMP regulates the rate of differentiation of oligodendrocytes without changing the lineage commitment of their progenitors. Dev Biol 1989;133:437-446.
56. Raible DW, McMorris FA. Oligodendrocyte differentiation and progenitor cell proliferation are independently regulated by cyclic AMP. J Neurosci Res 1993;34:287-294.
57. Relucio J, Tzvetanova ID, Ao W, Lindquist S, Colognato H. Laminin alters fyn regulatory mechanisms and promotes oligodendrocyte development. J Neurosci 2009;29:11794-11806.
58. Richardson PM, Issa VM. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 1984;309:791-793.
59. Rush AM, Craner MJ, Kageyama T, Dib-Hajj SD, Waxman SG, Ranscht B. Contactin regulates the current density and axonal expression of tetrodotoxin-resistant but not tetrodotoxin-sensitive sodium channels in DRG neurons. Eur J Neurosci 2005;22:39-49.
60. Sadowsky CL, McDonald JW. Activity-based restorative therapies: Concepts and applications in spinal cord injury-related neurorehabilitation. Dev Disabil Res Rev 2009;15:112-116.
61. Sheng HZ, Fields RD, Nelson PG. Specific regulation of immediate early genes by patterned neuronal activity. J Neurosci Res 1993;35:459-467.
62. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 1998;281:1515-1518.
63. Song HJ, Ming GL, Poo MM. cAMP-induced switching in turning direction of nerve growth cones. Nature 1997;388:275-279.
64. Sontheimer H, Black JA, Waxman SG. Voltage-gated Na+ channels in glia: Properties and possible functions. Trends Neurosci 1996;19:325-331.
65. Stevens B, Porta S, Haak LL, Gallo V, Fields RD. Adenosine: A neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 2002;36:855-868.
66. Stevens B, Tanner S, Fields RD. Control of myelination by specific patterns of neural impulses. J Neurosci 1998;18:9303-9311.
67. Sun X, Liu Y, Liu B, Xiao Z, Zhang L. Rolipram promotes remyelination possibly via MEK-ERK signal pathway in cuprizone-induced demyelination mouse. Exp Neurol 2012;237:304-311.
68. Taveggia C, Thaker P, Petrylak A, Caporaso GL, Toews A, Falls DL, Einheber S, Salzer JL. Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 2008;56:284-293.
69. Tao F, Li Q, Siu S, Wu H, Skinner J, Hurtado A, Belegu V, Furmanski O, Yang Y, McDonald JW, Johns RA. Role of neuregulin-1/ErbB signaling in stem cell therapy for spinal cord injury-induced chronic neuropathic pain. Stem Cells 2012;31:83-91.
70. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M. Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 2006;172:937-948.
71. Trifunovski A, Josephson A, Ringman A, Brene S, Spenger C, Olson L. Neuronal activity-induced regulation of Lingo-1. Neuroreport 2004;15:2397-2400.
72. Udina E, Furey M, Busch S, Silver J, Gordon T, Fouad K. Electrical stimulation of intact peripheral sensory axons in rats promotes outgrowth of their central projections. Exp Neurol 2008;210:238-247.
73. Udina E, Ladak A, Furey M, Brushart T, Tyreman N, Gordon T. Rolipram-induced elevation of cAMP or chondroitinase ABC breakdown of inhibitory proteoglycans in the extracellular matrix promotes peripheral nerve regeneration. Exp Neurol 2010;223:143-152.
74. Verkhratsky A, Steinhauser C. Ion channels in glial cells. Brain Res Brain Res Rev 2000;32:380-412.
75. Wake H, Lee PR, Fields RD. Control of local protein synthesis and initial events in myelination by action potentials. Science 2011;333:1647-1651.
76. Wan L, Xia R, Ding W. Short-term low-frequency electrical stimulation enhanced remyelination of injured peripheral nerves by inducing the promyelination effect of brain-derived neurotrophic factor on Schwann cell polarization. J Neurosci Res 2010;88:2578-2587.
77. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 1998;21:63-75.
78. Wang Z, Colognato H, Ffrench-Constant C. Contrasting effects of mitogenic growth factors on myelination in neuron-oligodendrocyte co-cultures. Glia 2007;55:537-545.
79. Xiao J, Wong AW, Willingham MM, van den Buuse M, Kilpatrick TJ, Murray SS. Brain-derived neurotrophic factor promotes central nervous system myelination via a direct effect upon oligodendrocytes. Neurosignals 2010;18:186-202.
80. Yamada H, Komiyama A, Suzuki K. Schwann cell responses to forskolin and cyclic AMP analogues: Comparative study of mouse and rat Schwann cells. Brain Res 1995;681:97-104.
81. Yang IH, Gary D, Malone M, Dria S, Houdayer T, Belegu V, McDonald JW, Thakor N. Axon myelination and electrical stimulation in a microfluidic, compartmentalized cell culture platform. Neuromolecular Med 2012;14:112-118.
82. Yang IH, Siddique R, Hosmane S, Thakor N, Hoke A. Compartmentalized microfluidic culture platform to study mechanism of paclitaxel-induced axonal degeneration. Exp Neurol 2009;218:124-128.
83. Zonouzi M, Renzi M, Farrant M, Cull-Candy SG. Bidirectional plasticity of calcium-permeable AMPA receptors in oligodendrocyte lineage cells. Nat Neurosci 2011;14:1430-1438.
84. Zonta B, Tait S, Melrose S, Anderson H, Harroch S, Higginson J, Sherman DL, Brophy PJ. Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system. J Cell Biol 2008;181:1169-1177.