Abstract
Small GTPases of the Rho family play key roles in the formation of neuronal axons and dendrites by transducing signals from guidance cues, such as neurotrophins, to the actin cytoskeleton. However, there is little insight into the mechanism by which neurotrophins regulate Rho GTPases. Here, we show the crucial role of the ubiquitous Rac1-specific guanine nucleotide exchange factor, Tiam1 (T lymphoma invasion and metastasis 1), in transducing a neurotrophin-mediated change in cell shape. We demonstrate that BDNF, acting through TrkB, directly binds and specifically activates Tiam1 by phosphorylating Tyr-829, leading to Rac1 activation and lamellipodia formation in Cos-7 cells and increased neurite outgrowth from cortical neurons. A point mutation in Tiam1, Tyr-829 to Phe-829, blocked these BDNF-induced changes in cellular morphology. The findings are evidence of a previously uncharacterized mechanism for the activation of Tiam1 and of a role for this effector in neurotrophin-mediated signal transduction leading to changes in cellular morphology.
MeSH Terms
Animals
Brain-Derived Neurotrophic Factor/pharmacology
Cell Membrane/drug effects,metabolism
Cell Shape
Cells, Cultured
Chlorocebus aethiops
Guanine Nucleotide Exchange Factors/genetics,metabolism
Neoplasm Proteins/genetics,metabolism
Neurites/drug effects,metabolism
Neurons/cytology,drug effects,metabolism
Phosphotyrosine/metabolism
Protein Binding
Pseudopodia/drug effects,metabolism
Rats
Rats, Sprague-Dawley
Receptor, trkB/metabolism
T-Lymphoma Invasion and Metastasis-inducing Protein 1
rac1 GTP-Binding Protein/genetics,metabolism
Chemicals
Brain-Derived Neurotrophic Factor
Guanine Nucleotide Exchange Factors
Neoplasm Proteins
T-Lymphoma Invasion and Metastasis-inducing Protein 1
Tiam1 protein, rat
Phosphotyrosine
Receptor, trkB
rac1 GTP-Binding Protein
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Miyamoto Yuki
Departments of *Neurology and Neurological Sciences and yukim@nch.go.jp. | Department of Pharmacology, National Research Institute for Child Health and Development, Setagaya, Tokyo 157-8535, Japan.
Yamauchi Junji
Department of Pharmacology, National Research Institute for Child Health and Development, Setagaya, Tokyo 157-8535, Japan. | Neurobiology, Stanford University School of Medicine, Stanford, CA 94305; and.
Tanoue Akito
Department of Pharmacology, National Research Institute for Child Health and Development, Setagaya, Tokyo 157-8535, Japan.
Wu Chengbiao
Departments of *Neurology and Neurological Sciences and.
Mobley William C
Departments of *Neurology and Neurological Sciences and.
References (28)
28 references, click to expand
-
Regulation of Tiam1-Rac signalling.
FEBS Lett. 2003 Jul 3;546(1):11-6
PMID: 12829230
-
A novel role for p75NTR in subplate growth cone complexity and visual thalamocortical innervation.
J Neurosci. 2002 May 1;22(9):3580-93
PMID: 11978834
-
Trk receptors: roles in neuronal signal transduction.
Annu Rev Biochem. 2003;72:609-42
PMID: 12676795
-
Nerve growth factor, brain-derived neurotrophic factor, and neurotrophin-3 are sorted to dense-core vesicles and released via the regulated pathway in primary rat cortical neurons.
J Neurosci Res. 2004 Mar 15;75(6):825-34
PMID: 14994343
-
The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions.
J Biol Chem. 2004 Jul 16;279(29):30092-8
PMID: 15138270
-
Studies on ras proteins. Catalytic properties of normal and activated ras proteins purified in the absence of protein denaturants.
Biochim Biophys Acta. 1988 Jan 25;949(1):97-109
PMID: 3275466
-
Identification of an invasion-inducing gene, Tiam-1, that encodes a protein with homology to GDP-GTP exchangers for Rho-like proteins.
Cell. 1994 May 20;77(4):537-49
PMID: 7999144
-
Sequence of the human invasion-inducing TIAM1 gene, its conservation in evolution and its expression in tumor cell lines of different tissue origin.
Oncogene. 1995 Apr 6;10(7):1371-6
PMID: 7731688
-
The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho.
J Cell Biol. 1997 Nov 3;139(3):797-807
PMID: 9348295
-
Targeting of Tiam1 to the plasma membrane requires the cooperative function of the N-terminal pleckstrin homology domain and an adjacent protein interaction domain.
J Biol Chem. 1997 Nov 7;272(45):28447-54
PMID: 9353304
-
Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases.
J Biol Chem. 1999 May 7;274(19):13198-204
PMID: 10224076
-
EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP.
Nat Neurosci. 2002 Nov;5(11):1117-8
PMID: 12389031
-
XPLN, a guanine nucleotide exchange factor for RhoA and RhoB, but not RhoC.
J Biol Chem. 2002 Nov 8;277(45):42964-72
PMID: 12221096
-
Rho GTPases in cell biology.
Nature. 2002 Dec 12;420(6916):629-35
PMID: 12478284
-
Cytoskeletal dynamics underlying collateral membrane protrusions induced by neurotrophins in cultured Xenopus embryonic neurons.
J Neurobiol. 2003 Feb 5;54(2):393-405
PMID: 12500314
-
Signalling and crosstalk of Rho GTPases in mediating axon guidance.
Nat Cell Biol. 2003 Jan;5(1):38-45
PMID: 12510192
-
Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin.
Neuron. 2003 Jan 23;37(2):263-74
PMID: 12546821
-
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
-
The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines.
Neuron. 2005 Feb 17;45(4):525-38
PMID: 15721239
-
The neurotrophin-3 receptor TrkC directly phosphorylates and activates the nucleotide exchange factor Dbs to enhance Schwann cell migration.
Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5198-203
PMID: 15758069
-
Ras activation of a Rac1 exchange factor, Tiam1, mediates neurotrophin-3-induced Schwann cell migration.
Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14889-94
PMID: 16203995
-
Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells.
Annu Rev Biochem. 1999;68:459-86
PMID: 10872457
-
Rho GTPases in neuronal morphogenesis.
Nat Rev Neurosci. 2000 Dec;1(3):173-80
PMID: 11257905
-
Evidence for the involvement of Tiam1 in axon formation.
J Neurosci. 2001 Apr 1;21(7):2361-72
PMID: 11264310
-
Nerve growth factor signaling, neuroprotection, and neural repair.
Annu Rev Neurosci. 2001;24:1217-81
PMID: 11520933
-
Regulation of neurotrophin-induced axonal responses via Rho GTPases.
J Comp Neurol. 2001 Oct 1;438(4):377-87
PMID: 11559894
-
Characterization of STEF, a guanine nucleotide exchange factor for Rac1, required for neurite growth.
J Biol Chem. 2002 Jan 25;277(4):2860-8
PMID: 11707441
-
Src kinase regulates the activation of a novel FGD-1-related Cdc42 guanine nucleotide exchange factor in the signaling pathway from the endothelin A receptor to JNK.
J Biol Chem. 2003 Aug 8;278(32):29890-900
PMID: 12771149