Home LiteratureArticle Details
PMID: 15703388 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A truncated tropomyosin-related kinase B receptor, T1, regulates glial cell morphology via Rho GDP dissociation inhibitor 1.

Ohira K, Kumanogoh H, Sahara Y, Homma KJ, Hirai H, Nakamura S, Hayashi M

Abstract

Through tropomyosin-related kinase B (TrkB) receptors, brain-derived neurotrophic factor (BDNF) performs many biological functions such as neural survival, differentiation, and plasticity. T1, an isoform of TrkB receptors that lacks a tyrosine kinase, predominates in the adult mammalian CNS, yet its role remains controversial. In this study, to examine whether T1 transduces a signal and to determine its function, we first performed an affinity purification of T1-binding protein with the T1-specific C-terminal peptide and identified Rho GDP dissociation inhibitor 1 (GDI1), a GDP dissociation inhibitor of Rho small G-proteins, as a signaling protein directly associated with T1. The binding of BDNF to T1 caused Rho GDI1 to dissociate from the C-terminal tail of T1. Astrocytes cultured for 30 d expressed only endogenous T1 among the BDNF receptors. In 30 d cultured astrocytes, Rho GDI1, when dissociated in a BDNF-dependent manner, controlled the activities of the Rho GTPases, which resulted in rapid changes in astrocytic morphology. Furthermore, using 2 d cultured astrocytes that were transfected with T1, a T1 deletion mutant, or cyan fluorescent protein fusion protein of the T1-specific C-terminal sequence, we demonstrated that T1-Rho GDI1 signaling was indispensable for regulating the activities of Rho GTPases and for the subsequent morphological changes among astrocytes. Therefore, these findings indicate that the T1 signaling cascade can alter astrocytic morphology via regulation of Rho GTPase activity.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Animals Astrocytes/drug effects,metabolism,ultrastructure Bacterial Toxins/pharmacology Brain/metabolism Brain-Derived Neurotrophic Factor/pharmacology,physiology Cell Shape/drug effects Cells, Cultured/drug effects,metabolism,ultrastructure Cytoskeleton/ultrastructure Guanine Nucleotide Dissociation Inhibitors/physiology Hippocampus/cytology Humans Kidney Molecular Sequence Data Nerve Tissue Proteins/physiology Protein Binding Protein Interaction Mapping Protein Isoforms/chemistry,physiology Protein Structure, Tertiary Rats Rats, Sprague-Dawley Rats, Wistar Receptor, trkB/chemistry,genetics,physiology Recombinant Fusion Proteins/physiology Signal Transduction Transfection rho GTP-Binding Proteins/antagonists & inhibitors,physiology
Chemicals
Bacterial Toxins Brain-Derived Neurotrophic Factor GDP dissociation inhibitor 1 Guanine Nucleotide Dissociation Inhibitors Nerve Tissue Proteins Protein Isoforms Recombinant Fusion Proteins Receptor, trkB rho GTP-Binding Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ohira Koji
Department of Biochemistry and Cellular Biology, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo 187-8502, Japan.
Kumanogoh Haruko
Sahara Yoshinori
Homma Koichi J
Hirai Hirohisa
Nakamura Shun
Hayashi Motoharu
References (48)
48 references, click to expand
  1. Tripartite synapses: glia, the unacknowledged partner.
    Trends Neurosci. 1999 May;22(5):208-15 PMID: 10322493
  2. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase.
    Science. 1999 Aug 6;285(5429):895-8 PMID: 10436159
  3. Activity-dependent activation of TrkB neurotrophin receptors in the adult CNS.
    Learn Mem. 1999 May-Jun;6(3):216-31 PMID: 10492004
  4. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth.
    Neuron. 1999 Nov;24(3):585-93 PMID: 10595511
  5. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth.
    Nat Neurosci. 2000 Apr;3(4):342-9 PMID: 10725923
  6. Neurotrophin signal transduction in the nervous system.
    Curr Opin Neurobiol. 2000 Jun;10(3):381-91 PMID: 10851172
  7. Neurotrophins and activity-dependent plasticity.
    Prog Brain Res. 2000;128:183-91 PMID: 11105678
  8. Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system.
    Genes Dev. 2000 Dec 1;14(23):2919-37 PMID: 11114882
  9. Small GTP-binding proteins.
    Physiol Rev. 2001 Jan;81(1):153-208 PMID: 11152757
  10. TTIP is a novel protein that interacts with the truncated T1 TrkB neurotrophin receptor.
    Biochem Biophys Res Commun. 2000 Dec 29;279(3):925-30 PMID: 11162451
  11. Truncated trkB.T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival.
    Biochem Biophys Res Commun. 2001 Feb 9;280(5):1352-8 PMID: 11162678
  12. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons.
    Science. 2001 Mar 23;291(5512):2419-23 PMID: 11264540
  13. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons.
    Science. 2001 May 4;292(5518):923-6 PMID: 11340204
  14. Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia.
    Science. 2001 May 4;292(5518):926-9 PMID: 11340205
  15. TrkB dimerization during development of the prefrontal cortex of the macaque.
    J Neurosci Res. 2001 Sep 1;65(5):463-9 PMID: 11536331
  16. Rho GTPases and cell migration.
    J Cell Sci. 2001 Aug;114(Pt 15):2713-22 PMID: 11683406
  17. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses.
    EMBO J. 2001 Nov 1;20(21):5887-97 PMID: 11689429
  18. BDNF binding to truncated trkB.T1 does not affect gene expression.
    Neuroreport. 2002 Jul 2;13(9):1189-93 PMID: 12151767
  19. Rho GTPases in cell biology.
    Nature. 2002 Dec 12;420(6916):629-35 PMID: 12478284
  20. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI.
    Nat Neurosci. 2003 May;6(5):461-7 PMID: 12692556
  21. Expression of TrkB subtypes in the adult monkey cerebellar cortex.
    J Chem Neuroanat. 2003 Mar;25(3):175-83 PMID: 12706205
  22. RhoA interaction with inositol 1,4,5-trisphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. Role in signaling increased endothelial permeability.
    J Biol Chem. 2003 Aug 29;278(35):33492-500 PMID: 12766172
  23. Rho-dependent kinase is involved in agonist-activated calcium entry in rat arteries.
    J Physiol. 2003 Sep 15;551(Pt 3):855-67 PMID: 12853654
  24. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells.
    Nature. 2003 Nov 6;426(6962):74-8 PMID: 14603320
  25. Astroglial processes show spontaneous motility at active synaptic terminals in situ.
    Eur J Neurosci. 2004 Oct;20(8):2235-9 PMID: 15450103
  26. Neurotrophin action on a rapid timescale.
    Curr Opin Neurobiol. 2004 Oct;14(5):558-63 PMID: 15464888
  27. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors.
    Mol Cell Biol. 1991 Jan;11(1):143-53 PMID: 1846020
  28. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain.
    Cell. 1990 May 18;61(4):647-56 PMID: 2160854
  29. Determination of amino acid compositions and NH2-terminal sequences of peptides electroblotted onto PVDF membranes from tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis: application to peptide mapping of human complement component C3.
    Anal Biochem. 1989 Aug 15;181(1):33-9 PMID: 2817381
  30. Truncated and catalytic isoforms of trkB are co-expressed in neurons of rat and mouse CNS.
    Eur J Neurosci. 1995 Jun 1;7(6):1403-9 PMID: 7582115
  31. Selective binding and internalisation by truncated receptors restrict the availability of BDNF during development.
    Development. 1995 Aug;121(8):2461-70 PMID: 7671810
  32. Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins.
    J Neurosci. 1995 Jan;15(1 Pt 2):477-91 PMID: 7823156
  33. The Trk family of neurotrophin receptors.
    J Neurobiol. 1994 Nov;25(11):1386-403 PMID: 7852993
  34. The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile.
    J Clin Invest. 1995 Mar;95(3):1026-31 PMID: 7883950
  35. Regulated neurotrophin receptor responsiveness during neuronal migrationand early differentiation.
    J Neurosci. 1994 Mar;14(3 Pt 2):1542-54 PMID: 8126554
  36. Regulation of neurotrophin receptors during the maturation of the mammalian visual system.
    J Neurosci. 1994 Mar;14(3 Pt 2):1795-811 PMID: 8126572
  37. Characterization of glial trkB receptors: differential response to injury in the central and peripheral nervous systems.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):4971-5 PMID: 8389459
  38. Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons.
    J Neurosci. 1993 Jul;13(7):3041-50 PMID: 8392538
  39. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling.
    J Neurosci. 1996 May 15;16(10):3123-9 PMID: 8627351
  40. Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain.
    J Comp Neurol. 1996 Oct 07;374(1):21-40 PMID: 8891944
  41. Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2.
    J Neurosci. 1997 Apr 15;17(8):2683-90 PMID: 9092589
  42. Signalling through the neurotrophin receptor p75NTR.
    Curr Opin Neurobiol. 1997 Jun;7(3):413-8 PMID: 9232808
  43. Rho GTPases and the actin cytoskeleton.
    Science. 1998 Jan 23;279(5350):509-14 PMID: 9438836
  44. Functional evidence that BDNF is an anterograde neuronal trophic factor in the CNS.
    J Neurosci. 1998 Apr 15;18(8):2808-21 PMID: 9525998
  45. The Rho small G protein family-Rho GDI system as a temporal and spatial determinant for cytoskeletal control.
    Biochem Biophys Res Commun. 1998 Apr 28;245(3):641-5 PMID: 9588168
  46. Stimulation of phospholipase C-beta2 by the Rho GTPases Cdc42Hs and Rac1.
    EMBO J. 1998 Nov 2;17(21):6241-9 PMID: 9799233
  47. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton.
    EMBO J. 1999 Feb 1;18(3):578-85 PMID: 9927417
  48. Change of expression of full-length and truncated TrkBs in the developing monkey central nervous system.
    Brain Res Dev Brain Res. 1999 Jan 11;112(1):21-9 PMID: 9974156
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2005-02-09
Pages
1343-53
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6725989
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: [email protected]