NMDA receptor couples Rac1-GEF Tiam1 to direct oligodendrocyte precursor cell migration

GLIA

Volumn 61, Issue 12, 2013, Pages 2078-2099

  Xiao, Lin ^a   Hu, Chun ^a   Yang, Wenjing ^a   Guo, Dazhi ^a   Li, Cui ^a   Shen, Weiran ^a   Liu, Xiuyun ^a   Aijun, Huang ^a   Dan, Wang ^a   He, Cheng ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

ERK; Migration; NMDA receptors; Oligodendrocyte precursor cells; Tiam1

Indexed keywords

GLUTAMIC ACID; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN TIAM1; RAC1 PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SLICE; CELL LINEAGE; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CHEMOKINESIS; CHEMOTAXIS; CONTROLLED STUDY; EXPLANT; HUMAN; HUMAN CELL; MYELINATION; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROCYTE PRECURSOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; REMYELINIZATION; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; WHITE MATTER;

ERK; MIGRATION; NMDA RECEPTORS; OLIGODENDROCYTE PRECURSOR CELLS; TIAM1;

ANIMALS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CEREBRAL CORTEX; GUANINE NUCLEOTIDE EXCHANGE FACTORS; N-METHYLASPARTATE; NEOPLASM PROTEINS; NEURAL STEM CELLS; NEURONS; OLIGODENDROGLIA; RAC1 GTP-BINDING PROTEIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84886639989     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22578     Document Type: Article

References (111)

1. Armstrong R, Friedrich VL Jr, Holmes KV, Dubois-Dalcq M. 1990a. In vitro analysis of the oligodendrocyte lineage in mice during demyelination and remyelination. J Cell Biol 111:1183-1195.
2. Armstrong RC, Harvath L, Dubois-Dalcq ME. 1990b. Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules. J Neurosci Res 27:400-407.
3. Baer AS, Syed YA, Kang SU, Mitteregger D, Vig R, Ffrench-Constant C, Franklin RJ, Altmann F, Lubec G, Kotter MR. 2009. Myelin-mediated inhibition of oligodendrocyte precursor differentiation can be overcome by pharmacological modulation of Fyn-RhoA and protein kinase C signalling. Brain 132:465-481.
4. Bakiri Y, Hamilton NB, Karadottir R, Attwell D. 2008. Testing NMDA receptor block as a therapeutic strategy for reducing ischaemic damage to CNS white matter. Glia 56:233-240.
5. Baumann N, Pham-Dinh D. 2001. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871-927.
6. Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL. 1999. Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449-4461.
7. Belousov AB, van den Pol AN. 1997. Local synaptic release of glutamate from neurons in the rat hypothalamic arcuate nucleus. J Physiol 499 (Pt 3):747-761.
8. Berger T, Walz W, Schnitzer J, Kettenmann H. 1992. GABA- and glutamate-activated currents in glial cells of the mouse corpus callosum slice. J Neurosci Res 31:21-27.
9. Calver AR, Hall AC, Yu WP, Walsh FS, Heath JK, Betsholtz C, Richardson WD. 1998. Oligodendrocyte population dynamics and the role of PDGF in vivo. Neuron 20:869-882.
10. Chung CY, Funamoto S, Firtel RA. 2001. Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem Sci 26:557-566.
11. Cull-Candy S, Brickley S, Farrant M. 2001. NMDA receptor subunits: Diversity, development and disease. Curr Opin Neurobiol 11:327-335.
12. Curtis R, Cohen J, Fok-Seang J, Hanley MR, Gregson NA, Reynolds R, Wilkin GP. 1988. Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J Neurocytol 17:43-54.
13. de Biase LM, Kang SH, Baxi EG, Fukaya M, Pucak ML, Mishina M, Calabresi PA, Bergles DE. 2011. NMDA receptor signaling in oligodendrocyte progenitors is not required for oligodendrogenesis and myelination. J Neurosci 31:12650-12662.
14. de Castro F, Bribian A. 2005. The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res Brain Res Rev 49:227-241.
15. Ehler E, van Leeuwen F, Collard JG, Salinas PC. 1997. Expression of Tiam-1 in the developing brain suggests a role for the Tiam-1-Rac signaling pathway in cell migration and neurite outgrowth. Mol Cell Neurosci 9:1-12.
16. 2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274:12753-12758.
17. Frost EE, Zhou Z, Krasnesky K, Armstrong RC. 2009. Initiation of oligodendrocyte progenitor cell migration by a PDGF-A activated extracellular regulated kinase (ERK) signaling pathway. Neurochem Res 34:169-181.
18. Fukata M, Nakagawa M, Kaibuchi K. 2003. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr Opin Cell Biol 15:590-597.
19. Funamoto S, Meili R, Lee S, Parry L, Firtel RA. 2002. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109:611-623.
20. Gage FH, Ray J, Fisher LJ. 1995. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18:159-192.
21. Gallo V, Ghiani CA. 2000. Glutamate receptors in glia: New cells, new inputs and new functions. Trends Pharmacol Sci 21:252-258.
22. Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC. 1996. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 16:2659-2670.
23. Garcion E, Faissner A, ffrench-Constant C. 2001. Knockout mice reveal a contribution of the extracellular matrix molecule tenascin-C to neural precursor proliferation and migration. Development 128:2485-2496.
24. Garraway SM, Xu Q, Inturrisi CE. 2009. siRNA-mediated knockdown of the NR1 subunit gene of the NMDA receptor attenuates formalin-induced pain behaviors in adult rats. J Pain 10:380-390.
25. Ge WP, Zhou W, Luo Q, Jan LY, Jan YN. 2009. Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proc Natl Acad Sci USA 106:328-333.
26. Gudz TI, Komuro H, Macklin WB. 2006. Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J Neurosci 26:2458-2466.
27. Guo F, Maeda Y, Ko EM, Delgado M, Horiuchi M, Soulika A, Miers L, Burns T, Itoh T, Shen H, et al. 2012. Disruption of NMDA receptors in oligodendroglial lineage cells does not alter their susceptibility to experimental autoimmune encephalomyelitis or their normal development. J Neurosci 32:639-645.
28. Habets GG, Scholtes EH, Zuydgeest D, van der Kammen RA, Stam JC, Berns A, Collard JG. 1994. Identification of an invasion-inducing gene, Tiam-1, that encodes a protein with homology to GDP-GTP exchangers for Rho-like proteins. Cell 77:537-549.
29. Hamelers IH, Olivo C, Mertens AE, Pegtel DM, van der Kammen RA, Sonnenberg A, Collard JG. 2005. The Rac activator Tiam1 is required for (alpha)3(beta)1-mediated laminin-5 deposition, cell spreading, and cell migration. J Cell Biol 171:871-881.
30. Hatten ME, Mason CA. 1990. Mechanisms of glial-guided neuronal migration in vitro and in vivo. Experientia 46:907-916.
31. Haydar TF, Bambrick LL, Krueger BK, Rakic P. 1999. Organotypic slice cultures for analysis of proliferation, cell death, and migration in the embryonic neocortex. Brain Res Brain Res Protoc 4:425-437.
32. Hoey SE, Williams RJ, Perkinton MS. 2009. Synaptic NMDA receptor activation stimulates alpha-secretase amyloid precursor protein processing and inhibits amyloid-beta production. J Neurosci 29:4442-4460.
33. Huang C, Jacobson K, Schaller MD. 2004. MAP kinases and cell migration. J Cell Sci 117:4619-4628.
34. Huang ZH, Wang Y, Cao L, Su ZD, Zhu YL, Chen YZ, Yuan XB, He C. 2008. Migratory properties of cultured olfactory ensheathing cells by single-cell migration assay. Cell Res 18:479-490.
35. 2+-dependent cofilin activation and RhoA inhibition. J Cell Sci 124:186-197.
36. Hunter SF, Bottenstein JE. 1989. Bipotential glial progenitors are targets of neuronal cell line-derived growth factors. Brain Res Dev Brain Res 49:33-49.
37. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW. 1999. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283:70-74.
38. Itoh T, Beesley J, Itoh A, Cohen AS, Kavanaugh B, Coulter DA, Grinspan JB, Pleasure D. 2002. AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 81:390-402.
39. Jarjour AA, Kennedy TE. 2004. Oligodendrocyte precursors on the move: Mechanisms directing migration. Neuroscientist 10:99-105.
40. Johnson JL. 1978. The excitant amino acids glutamic and aspartic acid as transmitter candidates in the vertebrate central nervous system. Prog Neurobiol 10:155-202.
41. Karadottir R, Cavelier P, Bergersen LH, Attwell D. 2005. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162-1166.
42. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M. 2003. The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 22:4190-4201.
43. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. 2006. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179.
44. Kiernan BW, Gotz B, Faissner A, ffrench-Constant C. 1996. Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms. Mol Cell Neurosci 7:322-335.
45. Kim MJ, Dunah AW, Wang YT, Sheng M. 2005. Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46:745-760.
46. Kolodziejczyk K, Saab AS, Nave KA, Attwell D. 2010. Why do oligodendrocyte lineage cells express glutamate receptors? F1000 Biol Rep 2:57.
47. Komuro H, Rakic P. 1993. Modulation of neuronal migration by NMDA receptors. Science 260:95-97.
48. 2+ fluctuations. J Neurobiol 37:110-130.
49. Leeuwen FN, Kain HE, Kammen RA, Michiels F, Kranenburg OW, Collard JG. 1997. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J Cell Biol 139:797-807.
50. Lerma J, Herranz AS, Herreras O, Abraira V, Martin del Rio R. 1986. In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145-155.
51. LeVine SM, Goldman JE. 1988. Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci 8:3992-4006.
52. Levison SW, Goldman JE. 1993. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201-212.
53. Li C, Xiao L, Liu X, Yang W, Shen W, Hu C, Yang G, He C. 2013. A functional role of NMDA receptor in regulating the differentiation of oligodendrocyte precursor cells and remyelination. Glia 61:732-749.
54. Lisman J, Schulman H, Cline H. 2002. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
55. Liu HN, Almazan G. 1995. Glutamate induces c-fos proto-oncogene expression and inhibits proliferation in oligodendrocyte progenitors: Receptor characterization. Eur J Neurosci 7:2355-2363.
56. Liu X, Hashimoto-Torii K, Torii M, Haydar TF, Rakic P. 2008. The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc Natl Acad Sci USA 105:11802-11807.
57. Lohof AM, Quillan M, Dan Y, Poo MM. 1992. Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 12:1253-1261.
58. Malenka RC, Bear MF. 2004. LTP and LTD: An embarrassment of riches. Neuron 44:5-21.
59. Manent JB, Beguin S, Ganay T, Represa A. 2011. Cell-autonomous and cell-to-cell signalling events in normal and altered neuronal migration. Eur J Neurosci 34:1595-1608.
60. Manning SM, Talos DM, Zhou C, Selip DB, Park HK, Park CJ, Volpe JJ, Jensen FE. 2008. NMDA receptor blockade with memantine attenuates white matter injury in a rat model of periventricular leukomalacia. J Neurosci 28:6670-6678.
61. Matute C, Sanchez-Gomez MV, Martinez-Millan L, Miledi R. 1997. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci USA 94:8830-8835.
62. McCarthy KD, de Vellis J. 1980. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
63. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907-7918.
64. Mertens AE, Roovers RC, Collard JG. 2003. Regulation of Tiam1-Rac signalling. FEBS Lett 546:11-16.
65. Michiels F, Collard JG. 1999. Rho-like GTPases: Their role in cell adhesion and invasion. Biochem Soc Symp 65:125-146.
66. Michiels F, Habets GG, Stam JC, van der Kammen RA, Collard JG. 1995. A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature 375:338-340.
67. Micu I, Jiang Q, Coderre E, Ridsdale A, Zhang L, Woulfe J, Yin X, Trapp BD, McRory JE, Rehak R, et al. 2006. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 439:988-992.
68. Miller RH. 2002. Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67:451-467.
69. Miller RH, Payne J, Milner L, Zhang H, Orentas DM. 1997. Spinal cord oligodendrocytes develop from a limited number of migratory highly proliferative precursors. J Neurosci Res 50:157-168.
70. Milner R, Anderson HJ, Rippon RF, McKay JS, Franklin RJ, Marchionni MA, Reynolds R, Ffrench-Constant C. 1997. Contrasting effects of mitogenic growth factors on oligodendrocyte precursor cell migration. Glia 19:85-90.
71. Milner R, Edwards G, Streuli C, Ffrench-Constant C. 1996. A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J Neurosci 16:7240-7252.
72. Milner R, Ffrench-Constant C. 1994. A developmental analysis of oligodendroglial integrins in primary cells: Changes in alpha v-associated beta subunits during differentiation. Development 120:3497-3506.
73. Nacher J, McEwen BS. 2006. The role of N-methyl-d-asparate receptors in neurogenesis. Hippocampus 16:267-270.
74. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Baron-Van Evercooren A. 2008. The role of SVZ-derived neural precursors in demyelinating diseases: From animal models to multiple sclerosis. J Neurol Sci 265:26-31.
75. O'Toole TE, Bialkowska K, Li X, Fox JE. 2011. Tiam1 is recruited to beta1-integrin complexes by 14-3-3zeta where it mediates integrin-induced Rac1 activation and motility. J Cell Physiol 226:2965-2978.
76. Ortega MC, Bribian A, Peregrin S, Gil MT, Marin O, de Castro F. 2012. Neuregulin-1/ErbB4 signaling controls the migration of oligodendrocyte precursor cells during development. Exp Neurol 235:610-620.
77. Ozawa S, Kamiya H, Tsuzuki K. 1998. Glutamate receptors in the mammalian central nervous system. Prog Neurobiol 54:581-618.
78. Paoletti P, Neyton J. 2007. NMDA receptor subunits: Function and pharmacology. Curr Opin Pharmacol 7:39-47.
79. Patneau DK, Wright PW, Winters C, Mayer ML, Gallo V. 1994. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 12:357-371.
80. Payne HR, Lemmon V. 1993. Glial cells of the O-2A lineage bind preferentially to N-cadherin and develop distinct morphologies. Dev Biol 159:595-607.
81. Perez Villegas EM, Olivier C, Spassky N, Poncet C, Cochard P, Zalc B, Thomas JL, Martinez S. 1999. Early specification of oligodendrocytes in the chick embryonic brain. Dev Biol 216:98-113.
82. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-83.
83. Rakic P. 1990. Principles of neural cell migration. Experientia 46:882-891.
84. Richardson WD, Kessaris N, Pringle N. 2006. Oligodendrocyte wars. Nat Rev Neurosci 7:11-18.
85. Richardson WD, Smith HK, Sun T, Pringle NP, Hall A, Woodruff R. 2000. Oligodendrocyte lineage and the motor neuron connection. Glia 29:136-142.
86. Rossman KL, Der CJ, Sondek J. 2005. GEF means go: Turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6:167-180.
87. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT, et al. 2003. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 33:401-406.
88. Salter MG, Fern R. 2005. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438:1167-1171.
89. Sander EE, van Delft S, ten Klooster JP, Reid T, van der Kammen RA, Michiels F, Collard JG. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J Cell Biol 143:1385-1398.
90. Simpson PB, Armstrong RC. 1999. Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration. Glia 26:22-35.
91. Skoff RP. 1990. Gliogenesis in rat optic nerve: Astrocytes are generated in a single wave before oligodendrocytes. Dev Biol 139:149-168.
92. Spassky N, Goujet-Zalc C, Parmantier E, Olivier C, Martinez S, Ivanova A, Ikenaka K, Macklin W, Cerruti I, Zalc B, et al. 1998. Multiple restricted origin of oligodendrocytes. J Neurosci 18:8331-8343.
93. Suetsugu S, Takenawa T. 2003. Regulation of cortical actin networks in cell migration. Int Rev Cytol 229:245-286.
94. Szele FG, Cepko CL. 1998. The dispersion of clonally related cells in the developing chick telencephalon. Dev Biol 195:100-113.
95. Terawaki S, Kitano K, Mori T, Zhai Y, Higuchi Y, Itoh N, Watanabe T, Kaibuchi K, Hakoshima T. 2010. The PHCCEx domain of Tiam1/2 is a novel protein- and membrane-binding module. EMBO J 29:236-250.
96. Tiwari-Woodruff SK, Buznikov AG, Vu TQ, Micevych PE, Chen K, Kornblum HI, Bronstein JM. 2001. OSP/claudin-11 forms a complex with a novel member of the tetraspanin super family and beta1 integrin and regulates proliferation and migration of oligodendrocytes. J Cell Biol 153:295-305.
97. Tolias KF, Bikoff JB, Burette A, Paradis S, Harrar D, Tavazoie S, Weinberg RJ, Greenberg ME. 2005. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45:525-538.
98. Tong XP, Li XY, Zhou B, Shen W, Zhang ZJ, Xu TL, Duan S. 2009. Ca(2+) signaling evoked by activation of Na(+) channels and Na(+)/Ca(2+) exchangers is required for GABA-induced NG2 cell migration. J Cell Biol 186:113-128.
99. Tsai HH, Frost E, To V, Robinson S, Ffrench-Constant C, Geertman R, Ransohoff RM, Miller RH. 2002. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 110:373-383.
100. Ueda H, Levine JM, Miller RH, Trapp BD. 1999. Rat optic nerve oligodendrocytes develop in the absence of viable retinal ganglion cell axons. J Cell Biol 146:1365-1374.
101. Wang C, Rougon G, Kiss JZ. 1994. Requirement of polysialic acid for the migration of the O-2A glial progenitor cell from neurohypophyseal explants. J Neurosci 14:4446-4457.
102. Wang S, Watanabe T, Matsuzawa K, Katsumi A, Kakeno M, Matsui T, Ye F, Sato K, Murase K, Sugiyama I, et al. 2012. Tiam1 interaction with the PAR complex promotes talin-mediated Rac1 activation during polarized cell migration. J Cell Biol 199:331-345.
103. Wu JJ, Chen JX, Rothman TP, Gershon MD. 1999. Inhibition of in vitro enteric neuronal development by endothelin-3: Mediation by endothelin B receptors. Development 126:1161-1173.
104. Xiao L, Feng C, Chen Y. 2010. Glucocorticoid rapidly enhances NMDA-evoked neurotoxicity by attenuating the NR2A-containing NMDA receptor-mediated ERK1/2 activation. Mol Endocrinol 24:497-510.
105. Xiao L, Guo D, Hu C, Shen W, Shan L, Li C, Liu X, Yang W, Zhang W, He C. 2012. Diosgenin promotes oligodendrocyte progenitor cell differentiation through estrogen receptor-mediated ERK1/2 activation to accelerate remyelination. Glia 60:1037-1052.
106. Xiao L, Hu C, Feng C, Chen Y. 2011. Switching of N-methyl-d-aspartate (NMDA) receptor-favorite intracellular signal pathways from ERK1/2 protein to p38 mitogen-activated protein kinase leads to developmental changes in NMDA neurotoxicity. J Biol Chem 286:20175-20193.
107. Xiao L, Qi A, Chen Y. 2005. Cultured embryonic hippocampal neurons deficient in glucocorticoid (GC) receptor: A novel model for studying nongenomic effects of GC in the neural system. Endocrinology 146:4036-4041.
108. Yamauchi J, Miyamoto Y, Tanoue A, Shooter EM, Chan JR. 2005. Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration. Proc Natl Acad Sci USA 102:14889-14894.
109. Yuan X, Eisen AM, McBain CJ, Gallo V. 1998. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901-2914.
110. Zhang Y, Zhao JH, Zhang XY, Guo HB, Liu F, Chen HL. 2004. Relations of the type and branch of surface N-glycans to cell adhesion, migration and integrin expressions. Mol Cell Biochem 260:137-146.
111. Zheng MH, Fan Y, Wysocki SJ, Lau AT, Robertson T, Beilharz M, Wood DJ, Papadimitriou JM. 1994. Gene expression of transforming growth factor-beta 1 and its type II receptor in giant cell tumors of bone. Possible involvement in osteoclast-like cell migration. Am J Pathol 145:1095-104.