Home LiteratureArticle Details
PMID: 18701695 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Cdk5 phosphorylation of WAVE2 regulates oligodendrocyte precursor cell migration through nonreceptor tyrosine kinase Fyn.

Miyamoto Y, Yamauchi J, Tanoue A

Abstract

Myelin formation of the CNS is a complex and dynamic process. Before the onset of myelination, oligodendrocytes (OLs), the myelin-forming glia of the CNS, proliferate and migrate along axons. Little is known about the molecular mechanisms underlying the early myelination processes. Here, we show that platelet-derived growth factor (PDGF), the crucial physiological ligand in early OL development, controls the migration of oligodendrocyte precursor cells (OPCs) through cyclin-dependent kinase 5 (Cdk5). PDGF stimulates Cdk5 activity in a time-dependent manner, whereas suppression of Cdk5 by the specific inhibitor roscovitine or by the retrovirus encoding short-hairpin RNA for Cdk5 impairs PDGF-dependent OPC migration. The activation of Cdk5 by PDGF is mediated by the phosphorylation of the nonreceptor tyrosine kinase, Fyn, whose inhibition reduces PDGF-dependent OPC migration. Furthermore, Cdk5 regulates PDGF-dependent OPC migration through the direct phosphorylation of WASP (Wiskott-Aldrich syndrome protein)-family verprolin-homologous protein 2 (WAVE2). Cdk5 phosphorylates WAVE2 at Ser-137 in vitro. Infection of the WAVE2 construct harboring the Ser-137-to-Ala reduces PDGF-dependent migration. Together, PDGF regulates OPC migration through an as-yet-unidentified signaling cascade coupling Fyn kinase to Cdk5 phosphorylation of WAVE2. These results provide new insights into both the role of Cdk5 in glial cells and the molecular mechanisms controlling the early developmental stage of OLs.

MeSH Terms
Animals Cell Movement/physiology Cells, Cultured Cyclin-Dependent Kinase 5/genetics,metabolism Humans Mice Oligodendroglia/cytology,enzymology,physiology Phosphorylation Proto-Oncogene Proteins c-fyn/genetics,metabolism,physiology Rats Rats, Sprague-Dawley Stem Cells/cytology,enzymology,physiology Wiskott-Aldrich Syndrome Protein Family/genetics,metabolism,physiology
Chemicals
Wiskott-Aldrich Syndrome Protein Family Proto-Oncogene Proteins c-fyn Cyclin-Dependent Kinase 5
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Miyamoto Yuki
Department of Pharmacology, National Research Institute for Child Health and Development, Okura, Setagaya, Tokyo 157-8535, Japan.
Yamauchi Junji
Tanoue Akito
References (46)
46 references, click to expand
  1. Cdk5 regulates differentiation of oligodendrocyte precursor cells through the direct phosphorylation of paxillin.
    J Cell Sci. 2007 Dec 15;120(Pt 24):4355-66 PMID: 18042622
  2. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology.
    Nature. 2006 Aug 17;442(7104):814-7 PMID: 16862120
  3. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11173-8 PMID: 8855328
  4. Platelet-derived growth factor: three isoforms and two receptor types.
    Trends Genet. 1989 Apr;5(4):108-11 PMID: 2543106
  5. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors.
    Nat Rev Mol Cell Biol. 2005 Feb;6(2):167-80 PMID: 15688002
  6. The origin of remyelinating cells in the central nervous system.
    J Neuroimmunol. 1999 Jul 1;98(1):69-76 PMID: 10426364
  7. An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator.
    J Biol Chem. 1995 Nov 10;270(45):26897-903 PMID: 7592934
  8. Rho kinase regulates schwann cell myelination and formation of associated axonal domains.
    J Neurosci. 2004 Apr 21;24(16):3953-63 PMID: 15102911
  9. WAVE1 is required for oligodendrocyte morphogenesis and normal CNS myelination.
    J Neurosci. 2006 May 24;26(21):5849-59 PMID: 16723544
  10. Regulation of oligodendrocyte development in the vertebrate CNS.
    Prog Neurobiol. 2002 Aug;67(6):451-67 PMID: 12385864
  11. Gliogenesis in the central nervous system.
    Glia. 2000 Apr;30(2):105-21 PMID: 10719353
  12. Evidence for neuronal regulation of oligodendrocyte development: cellular localization of platelet-derived growth factor alpha receptor and A-chain mRNA during cerebral cortex development in the rat.
    J Neurosci Res. 1996 Jul 01;45(1):28-39 PMID: 8811510
  13. A unique role for Fyn in CNS myelination.
    J Neurosci. 2001 Mar 15;21(6):2039-47 PMID: 11245687
  14. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase.
    J Cell Biol. 1999 Jun 14;145(6):1209-18 PMID: 10366594
  15. Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules.
    J Neurosci Res. 1990 Nov;27(3):400-7 PMID: 2097382
  16. Cellular functions regulated by Src family kinases.
    Annu Rev Cell Dev Biol. 1997;13:513-609 PMID: 9442882
  17. Cyclin-dependent kinase-5 in neurodegeneration.
    J Neurochem. 2004 Mar;88(6):1313-26 PMID: 15009631
  18. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice.
    Development. 1999 Feb;126(3):457-67 PMID: 9876175
  19. Adult brain retains the potential to generate oligodendroglial progenitors with extensive myelination capacity.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4089-94 PMID: 10097168
  20. p250GAP, a neural RhoGAP protein, is associated with and phosphorylated by Fyn.
    Biochem Biophys Res Commun. 2003 Jun 20;306(1):151-5 PMID: 12788081
  21. Neurotrophins regulate Schwann cell migration by activating divergent signaling pathways dependent on Rho GTPases.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8774-9 PMID: 15161978
  22. Molecular organization of axo-glial junctions.
    Curr Opin Neurobiol. 2003 Oct;13(5):552-9 PMID: 14630217
  23. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality.
    Neuron. 1997 Jan;18(1):29-42 PMID: 9010203
  24. Characterization of the WAVE1 knock-out mouse: implications for CNS development.
    J Neurosci. 2003 Apr 15;23(8):3343-52 PMID: 12716942
  25. PDGF A chain homodimers drive proliferation of bipotential (O-2A) glial progenitor cells in the developing rat optic nerve.
    EMBO J. 1989 Apr;8(4):1049-56 PMID: 2545439
  26. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth.
    Neuron. 2000 Jun;26(3):633-46 PMID: 10896159
  27. TrkB binds and tyrosine-phosphorylates Tiam1, leading to activation of Rac1 and induction of changes in cellular morphology.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10444-10449 PMID: 16801538
  28. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell.
    Nature. 1988 Jun 9;333(6173):560-2 PMID: 3287176
  29. PDGF A-chain gene is expressed by mammalian neurons during development and in maturity.
    Cell. 1991 Jan 11;64(1):209-16 PMID: 1986867
  30. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system.
    Cell. 1988 Apr 22;53(2):309-19 PMID: 2834067
  31. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac.
    EMBO J. 1998 Dec 1;17(23):6932-41 PMID: 9843499
  32. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5.
    Nature. 1994 Sep 29;371(6496):419-23 PMID: 8090221
  33. Activation of C-jun N-terminal kinase/stress-activated protein kinase in primary glial cultures.
    J Neurosci Res. 1996 Oct 01;46(1):114-21 PMID: 8892112
  34. Initial events of myelination involve Fyn tyrosine kinase signalling.
    Nature. 1994 Feb 10;367(6463):572-6 PMID: 7509042
  35. Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex.
    Neuron. 2002 Aug 29;35(5):907-20 PMID: 12372285
  36. Phosphorylation of WAVE2 by MAP kinases regulates persistent cell migration and polarity.
    J Cell Sci. 2007 Dec 1;120(Pt 23):4144-54 PMID: 18032787
  37. Axonal control of oligodendrocyte development.
    J Cell Biol. 1999 Dec 13;147(6):1123-8 PMID: 10601327
  38. PDGF and its receptors in the developing rodent retina and optic nerve.
    Development. 1993 Jun;118(2):539-52 PMID: 8223278
  39. Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension.
    J Neurochem. 1997 Mar;68(3):945-53 PMID: 9048739
  40. Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation.
    J Neurobiol. 2001 Oct;49(1):62-78 PMID: 11536198
  41. FGF modulates the PDGF-driven pathway of oligodendrocyte development.
    Neuron. 1990 Nov;5(5):603-14 PMID: 2171589
  42. Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau.
    J Neurosci. 2002 Feb 1;22(3):698-707 PMID: 11826099
  43. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement.
    J Cell Sci. 2001 May;114(Pt 10):1801-9 PMID: 11329366
  44. WAVE2 is required for directed cell migration and cardiovascular development.
    Nature. 2003 Jul 24;424(6947):452-6 PMID: 12879075
  45. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization.
    Cell. 1996 Mar 8;84(5):723-34 PMID: 8625410
  46. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment.
    J Neurosci. 2001 Sep 1;21(17):6758-71 PMID: 11517264
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2008-08-13
Pages
8326-37
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6670578
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com