The roles of extracellular related-kinases 1 and 2 signaling in CNS myelination

Neuropharmacology

Volumn 110, Issue , 2016, Pages 586-593

  Gonsalvez, David ^a   Ferner, Anita H ^a   Peckham, Haley ^a   Murray, Simon S ^a   Xiao, Junhua ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Akt; BDNF; Erk; Fyn; Myelin; Oligodendrocyte

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLYCOGEN SYNTHASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR YY1;

CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; ENZYME ACTIVITY; HUMAN; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REMYELINIZATION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ENZYMOLOGY; METABOLISM; MYELIN SHEATH; PHYSIOLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYELIN SHEATH; OLIGODENDROGLIA; SIGNAL TRANSDUCTION;

EID: 84929603320     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.04.024     Document Type: Review

References (86)

1. Aksamitiene, E., Kiyatkin, A., Kholodenko, B.N., Cross-talk between mitogenic Ras/MAPK and survival PI3K/Akt pathways: a fine balance. Biochem. Soc. Trans. 40:1 (2012), 139–146.
2. Azim, K., Butt, A.M., GSK3beta negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 59:4 (2011), 540–553.
3. Bansal, R., Magge, S., Winkler, S., Specific inhibitor of FGF receptor signaling: FGF-2-mediated effects on proliferation, differentiation, and MAPK activation are inhibited by PD173074 in oligodendrocyte-lineage cells. J. Neurosci. Res. 74:4 (2003), 486–493.
4. Baron, W., et al. PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol. Cell. Neurosci. 15:3 (2000), 314–329.
5. Bhat, N.R., Zhang, P., Activation of mitogen-activated protein kinases in oligodendrocytes. J. Neurochem. 66:5 (1996), 1986–1994.
6. Boulton, T.G., et al. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:4 (1991), 663–675.
7. Carracedo, A., et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J. Clin. Invest 118:9 (2008), 3065–3074.
8. Cheng, P., Alberts, I., Li, X., The role of ERK1/2 in the regulation of proliferation and differentiation of astrocytes in developing brain. Int. J. Dev. Neurosci. 31:8 (2013), 783–789.
9. Chew, L.-J., et al. Mechanisms of regulation of oligodendrocyte development by p38 mitogen-activated protein kinase. J. Neurosci. 30:33 (2010), 11011–11027.
10. Cleghon, V., Morrison, D.K., Raf-1 interacts with Fyn and Src in a non-phosphotyrosine-dependent manner. J. Biol. Chem. 269:26 (1994), 17749–17755.
11. Colognato, H., et al. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell. Biol. 4:11 (2002), 833–841.
12. Cui, Q.-L., Almazan, G., IGF-I-induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src-like tyrosine kinases. J. Neurochem. 100:6 (2007), 1480–1493.
13. Cui, Q.-L., et al. Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J. biological Chem. 280:10 (2005), 8918–8928.
14. Czopka, T., Ffrench-Constant, C., Lyons, D.A., Individual oligodendrocytes have only a few hours in which to generate new myelin sheaths in vivo. Dev. Cell. 25:6 (2013), 599–609.
15. Dai, Z.M., et al. Stage-specific regulation of oligodendrocyte development by Wnt/beta-catenin signaling. J. Neurosci. 34:25 (2014), 8467–8473.
16. Dai, J., Bercury, K.K., Macklin, W.B., Interaction of mTOR and Erk1/2 signaling to regulate oligodendrocyte differentiation. Glia 62:12 (2014), 2096–2109.
17. Ding, Q., et al. Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol. Cell. 19:2 (2005), 159–170.
18. Domercq, M., et al. Dual-specific phosphatase-6 (Dusp6) and ERK mediate AMPA receptor-induced oligodendrocyte death. J. biological Chem. 286:13 (2011), 11825–11836.
19. Emery, B., Transcriptional and post-transcriptional control of CNS myelination. Curr. Opin. Neurobiol. 20:5 (2010), 601–607.
20. Emery, B., Regulation of oligodendrocyte differentiation and myelination. Science 330:6005 (2010), 779–782.
21. Fancy, S.P., et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes. Dev. 23:13 (2009), 1571–1585.
22. Fancy, S.P., et al. Myelin regeneration: a recapitulation of development?. Annu Rev. Neurosci. 34 (2011), 21–43.
23. Fancy, S.P., et al. Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14:8 (2011), 1009–1016.
24. Feigenson, K., et al. Canonical Wnt signalling requires the BMP pathway to inhibit oligodendrocyte maturation. ASN Neuro, 3(3), 2011, e00061.
25. Flores, A.I., et al. Constitutively active Akt induces enhanced myelination in the CNS. J. Neurosci. 28:28 (2008), 7174–7183.
26. Franklin, R.J., et al. Neuroprotection and repair in multiple sclerosis. Nat. Rev. Neurol. 8:11 (2012), 624–634.
27. Frederick, T.J., et al. Synergistic induction of cyclin D1 in oligodendrocyte progenitor cells by IGF-I and FGF-2 requires differential stimulation of multiple signaling pathways. Glia 55:10 (2007), 1011–1022.
28. Furusho, M., et al. Fibroblast growth factor signaling is required for the generation of oligodendrocyte progenitors from the embryonic forebrain. J. Neurosci. 31:13 (2011), 5055–5066.
29. Fyffe-Maricich, S.L., et al. The ERK2 mitogen-activated protein kinase regulates the timing of oligodendrocyte differentiation. J. Neurosci. 31:3 (2011), 843–850.
30. Fyffe-Maricich, S.L., et al. Signaling through ERK1/2 controls myelin thickness during myelin repair in the adult central nervous system. J. Neurosci. 33:47 (2013), 18402–18408.
31. Galabova-Kovacs, G., et al. Essential role of B-Raf in oligodendrocyte maturation and myelination during postnatal central nervous system development. J. Cell. Biol. 180:5 (2008), 947–955.
32. Gehart, H., et al. MAPK signalling in cellular metabolism: stress or wellness?. EMBO Rep. 11:11 (2010), 834–840.
33. Guardiola-Diaz, H.M., Ishii, A., Bansal, R., Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation. Glia 60:3 (2012), 476–486.
34. Hazzalin, C.A., Mahadevan, L.C., MAPK-regulated transcription: a continuously variable gene switch?. Nat. Rev. Mol. Cell. Biol. 3:1 (2002), 30–40.
35. He, Y., et al. Yy1 as a molecular link between neuregulin and transcriptional modulation of peripheral myelination. Nat. Neurosci. 13:12 (2010), 1472–1480.
36. Huser, M., et al. MEK kinase activity is not necessary for Raf-1 function. EMBO J. 20:8 (2001), 1940–1951.
37. Ishii, A., et al. ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. J. Neurosci. 32:26 (2012), 8855–8864.
38. Ishii, A., Furusho, M., Bansal, R., Sustained activation of ERK1/2 MAPK in oligodendrocytes and schwann cells enhances myelin growth and stimulates oligodendrocyte progenitor expansion. J. Neurosci. 33:1 (2013), 175–186.
39. Ivanova, T., Karolczak, M., Beyer, C., Estrogen stimulates the mitogen-activated protein kinase pathway in midbrain astroglia. Brain Res. 889:1–2 (2001), 264–269.
40. Jacobs, D., et al. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes. Dev. 13:2 (1999), 163–175.
41. Kim, S.D., et al. Inhibition of GSK-3beta mediates expression of MMP-9 through ERK1/2 activation and translocation of NF-kappaB in rat primary astrocyte. Brain Res. 1186 (2007), 12–20.
42. Kramer, E.M., et al. Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J. Biol. Chem. 274:41 (1999), 29042–29049.
43. Kumar, S., et al. NT-3-mediated TrkC receptor activation promotes proliferation and cell survival of rodent progenitor oligodendrocyte cells in vitro and in vivo. J. Neurosci. Res. 54:6 (1998), 754–765.
44. Lang, J., et al. Adenomatous polyposis coli regulates oligodendroglial development. J. Neurosci. 33:7 (2013), 3113–3130.
45. Lee, T., et al. Docking motif interactions in MAP kinases revealed by hydrogen exchange mass spectrometry. Mol. Cell. 14:1 (2004), 43–55.
46. Lee, J.Y., Oh, T.H., Yune, T.Y., Ghrelin inhibits hydrogen peroxide-induced apoptotic cell death of oligodendrocytes via ERK and p38MAPK signaling. Endocrinology 152:6 (2011), 2377–2386.
47. Li, H., et al. Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 69:5 (2011), 918–929.
48. Liang, X., et al. The N-terminal SH4 region of the Src family kinase Fyn is modified by methylation and heterogeneous fatty acylation: role in membrane targeting, cell adhesion, and spreading. J. Biol. Chem. 279:9 (2004), 8133–8139.
49. Liang, X., Draghi, N.A., Resh, M.D., Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J. Neurosci. 24:32 (2004), 7140–7149.
50. Liu, N., et al. ATM deficiency induces oxidative stress and endoplasmic reticulum stress in astrocytes. Lab. Invest 85:12 (2005), 1471–1480.
51. Lundgaard, I., et al. Neuregulin and BDNF induce a switch to NMDA receptor-dependent myelination by oligodendrocytes. PLoS Biol., 11(12), 2013, e1001743.
52. McCubrey, J.A., et al. GSK-3 as potential target for therapeutic intervention in cancer. Oncotarget 5:10 (2014), 2881–2911.
53. McCubrey, J.A., et al. Multifaceted roles of GSK-3 and Wnt/beta-catenin in hematopoiesis and leukemogenesis: opportunities for therapeutic intervention. Leukemia 28:1 (2014), 15–33.
54. Narayanan, S.P., et al. Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J. Neurosci. 29:21 (2009), 6860–6870.
55. Nave, K.A., Trapp, B.D., Axon-glial signaling and the glial support of axon function. Annu Rev. Neurosci. 31 (2008), 535–561.
56. Nave, K.A., Werner, H.B., Myelination of the nervous system: mechanisms and functions. Annu Rev. Cell. Dev. Biol. 30 (2014), 503–533.
57. Newbern, J.M., et al. Specific functions for ERK/MAPK signaling during PNS development. Neuron 69:1 (2011), 91–105.
58. Niu, J., et al. Phosphorylated olig1 localizes to the cytosol of oligodendrocytes and promotes membrane expansion and maturation. Glia 60:9 (2012), 1427–1436.
59. Osterhout, D.J., et al. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J. Cell. Biol. 145:6 (1999), 1209–1218.
60. Pages, G., et al. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 286:5443 (1999), 1374–1377.
61. Pereira, D.B., Chao, M.V., The tyrosine kinase Fyn determines the localization of TrkB receptors in lipid rafts. J. Neurosci. 27:18 (2007), 4859–4869.
62. Raman, M., Chen, W., Cobb, M.H., Differential regulation and properties of MAPKs. Oncogene 26:22 (2007), 3100–3112.
63. Richardson, W.D., et al. Oligodendrocyte lineage and the motor neuron connection. Glia 29:2 (2000), 136–142.
64. Roskoski, R. Jr., ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol. Res. 66:2 (2012), 105–143.
65. Sato, I., et al. Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J. Cell. Sci. 122:Pt 7 (2009), 965–975.
66. Selcher, J.C., et al. Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn Mem. 8:1 (2001), 11–19.
67. Shin, S., et al. Glycogen synthase kinase (GSK)-3 promotes p70 ribosomal protein S6 kinase (p70S6K) activity and cell proliferation. Proc. Natl. Acad. Sci. U. S. A. 108:47 (2011), E1204–E1213.
68. Sperber, B.R., et al. A unique role for Fyn in CNS myelination. J. Neurosci. 21:6 (2001), 2039–2047.
69. Stariha, R.L., et al. Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension. J. Neurochem. 68:3 (1997), 945–953.
70. Sun, Y., et al. Phosphorylation state of Olig2 regulates proliferation of neural progenitors. Neuron 69:5 (2011), 906–917.
71. Sun, X., et al. Rolipram promotes remyelination possibly via MEK-ERK signal pathway in cuprizone-induced demyelination mouse. Exp. Neurol. 237:2 (2012), 304–311.
72. Tanoue, T., et al. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell. Biol. 2:2 (2000), 110–116.
73. Tyler, W.A., et al. Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J. Neurosci. 29:19 (2009), 6367–6378.
74. Wahl, S.E., et al. Mammalian target of rapamycin promotes oligodendrocyte differentiation, initiation and extent of CNS myelination. J. Neurosci. 34:13 (2014), 4453–4465.
75. Watkins, T.A., et al. Distinct stages of myelination regulated by gamma-secretase and astrocytes in a rapidly myelinating CNS coculture system. Neuron 60:4 (2008), 555–569.
76. Wong, A.W., et al. Oligodendroglial expression of TrkB independently regulates myelination and progenitor cell proliferation. J. Neurosci. 33:11 (2013), 4947–4957.
77. Wood, T.L., et al. mTOR: a link from the extracellular milieu to transcriptional regulation of oligodendrocyte development. ASN Neuro, 5(1), 2013, e00108.
78. Xiao, J., et al. Extracellular signal-regulated kinase 1/2 signaling promotes oligodendrocyte myelination in vitro. J. Neurochem. 122:6 (2012), 1167–1180.
79. Xiao, J., Kilpatrick, T.J., Murray, S.S., The role of neurotrophins in the regulation of myelin development. Neurosignals 17:4 (2009), 265–276.
80. Yao, Y., et al. Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proc. Natl. Acad. Sci. U. S. A. 100:22 (2003), 12759–12764.
81. Ye, F., et al. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat. Neurosci. 12:7 (2009), 829–838.
82. Younes-Rapozo, V., et al. A role for the MAPK/ERK pathway in oligodendroglial differentiation in vitro: stage specific effects on cell branching. Int. J. Dev. Neurosci. 27:8 (2009), 757–768.
83. Zassadowski, F., et al. Regulation of the transcriptional activity of nuclear receptors by the MEK/ERK1/2 pathway. Cell. Signal 24:12 (2012), 2369–2377.
84. Zhang, J., et al. A bipartite mechanism for ERK2 recognition by its cognate regulators and substrates. J. Biol. Chem. 278:32 (2003), 29901–29912.
85. Zhang, S.Q., et al. Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol. Cell. 13:3 (2004), 341–355.
86. Zhao, L., Brinton, R.D., Vasopressin-induced cytoplasmic and nuclear calcium signaling in embryonic cortical astrocytes: dynamics of calcium and calcium-dependent kinase translocation. J. Neurosci. 23:10 (2003), 4228–4239.