Rapid Dendritic Remodeling in the Developing Retina: Dependence on Neurotransmission and Reciprocal Regulation by Rac and Rho

Wong, Wai T; Faulkner-Jones, Beverly E.; Sanes, Joshua R.; Wong, Rachel

doi:10.1523/jneurosci.20-13-05024.2000

Cited by 227 publications

(185 citation statements)

References 72 publications

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“…Accordingly, human hemizygosity of LIM-domain-containing protein kinase (LIMK), which is activated by p21-activated kinase (PAK), an effector of Rac GTPase, has been associated with MR (23). On the other hand, Rho activation has been shown to cause neurite retraction (39,40) by means of formation of stress fibers in the growth cone (41) and to reduce growth cone mobility and dendrite branching (42,43). The meaning of these latter actions in the physiology of learning is unclear.…”

Section: Discussionmentioning

confidence: 99%

Enhancement of learning and memory after activation of cerebral Rho GTPases

Diana

Valentini

Travaglione

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

119

115

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The mechanism whereby the morphology and connectivity of the dendritic tree is regulated depends on an actin dynamics that, in turn, is controlled by Rho GTPases, a family of small GTP-binding proteins encompassing Rho, Rac, and Cdc42 subfamilies. Cytotoxic necrotizing factor 1 (CNF1), a protein toxin from Escherichia coli, constitutively activates Rho GTPases, thus leading to remodeling of the actin cytoskeleton in intact cells. Here, we show that the modulation of cerebral RhoA and Rac1 activity induced by CNF1 in mice leads to (i) rearrangement of cerebral actin cytoskeleton, (ii) enhanced neurotransmission and synaptic plasticity, and (iii) improved learning and memory in various behavioral tasks. The effects persist for weeks and are not observed in mice treated with a recombinant CNF1, in which the enzymatic activity was abolished by substituting serine to cysteine at position 866. The results suggest that learning ability can be improved through pharmacological manipulation of neural connectivity.cytotoxic necrotizing factor 1 ͉ brain ͉ bacterial toxins ͉ dendritic spines ͉ drug therapy

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Section: Discussionmentioning

confidence: 99%

Enhancement of learning and memory after activation of cerebral Rho GTPases

Diana

Valentini

Travaglione

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

119

115

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“…In Xenopus tectal neurons and in retinal neurons, active Rac and Cdc42 are essential for branch addition (10,56,57). In our hippocampal neurons, dendritogenesis was indeed no longer inducible when they expressed dnRac1 or dnCdc42, suggesting that both GTPases were necessary.…”

Section: Discussionmentioning

confidence: 99%

Vasoactive Intestinal Peptide and PACAP38 Control N-Methyl-D-aspartic Acid-induced Dendrite Motility by Modifying the Activities of Rho GTPases and Phosphatidylinositol 3-Kinases

Henle

Fischer

Meyer

et al. 2006

Journal of Biological Chemistry

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Dendrite morphogenesis is highly dynamic and characterized by the addition and elongation of processes and also by their selective maintenance, retraction, and elimination. Glutamate can influence these events via N-methyl-D-aspartic acid (NMDA) receptors. The neuropeptides vasoactive intestinal peptide and pituitary adenylyl cyclase-activating polypeptide-38 (PACAP38) affect neurogenesis and differentiation in the developing nervous system. We report here that the peptides and NMDA acted synergistically on dendrite and branch formation. In stage III hippocampal neurons, NMDA increased not only the addition but also the elimination of new dendrites and branches by activating Rac and Cdc42 and phosphatidylinositol 3-kinases, respectively. When applied alone, the neuropeptides did not influence dendrite or branch formation. However, they reduced the elimination of newly formed dendrites and branches caused by NMDA by preventing the NMDA-induced activation of phosphatidylinositol 3-kinases. This led to the formation of persistent dendrites and branches. Additional timelapse studies on the dynamics of dendrite elongation showed alternating periods of elongation and retraction. Phosphatidylinositol 3-kinases increased the velocities of dendrite elongation and retraction, whereas the neuropeptides prolonged the periods of elongation. By modifying NMDA-induced activation of Rho GTPases and phosphatidylinositol 3-kinases, vasoactive intestinal peptide and PACAP38 could play an important role in the control of dendrite growth and branching during development and in response to neuronal activity.To integrate synaptic input, neurons develop a specific dendritic branching pattern that determines their function (1). Neuronal activity modifies the formation and stabilization of dendritic processes (2, 3). Dendrites are motile structures that contain high concentrations of filamentous actin. By controlling the stability and assembly of the actin cytoskeleton, members of the Rho family of small GTPases regulate neuronal morphogenesis (4). Rac and Cdc42 facilitate the outgrowth of dendrites, dendritic branches, filopodia, and spines, whereas RhoA and Rho kinase (ROCK) 3 attenuate it (5-9). In Xenopus optic tectal neurons, the neurotransmitter glutamate changes the activity of Rho GTPases by acting on ionotropic NMDA (NMDAR) and L-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors. It facilitates dendrite formation by inhibiting RhoA and activating Rac (10). Because calcium signaling plays an important role in dendrite formation (11,12), mainly the effects of NMDAR stimulation seem to be important. In hippocampal neurons, the guanine exchange factor Tiam1 couples NMDARs to the activity-dependent development by activating Rac1 and inhibiting RhoA (13,14).In vitro, class I phosphatidylinositol 3-kinases (PI3Ks) support neurite formation by producing membrane-bound phosphatidylinositol 3,4-bisphosphate and phosphatidylinositol 3,4,5-trisphosphate (15-17). PI3Ks stimulate dendrite and branch outgrowth by inhibiting the RhoA/...

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“…Neurotransmitters have been proposed to act as an activity-dependent signal during synaptic development and neuronal plasticity in the retina (Redburn & Rowe-Rendleman, 1996). In particular, glutamate has been shown to play a role in synaptic motility (Engert & Bonhoeffer, 1999;Maletic-Savatic et al, 1999;Wong et al, 2000;Wong & Wong, 2001) and in the growth and maintenance of dendritic spines (Passafaro et al, 2003). Glutamate may also cell-autonomously affect presynaptic development using local feedback loops through presynaptic α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA)/kainate-type receptors (Chang & De Camilli, 2001).…”

Section: Role Of the α 1f Subunit Of The Vdcc In Synaptic Developmentmentioning

confidence: 99%

Thenob2mouse, a null mutation inCacna1f: Anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses

et al. 2006

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Glutamate release from photoreceptor terminals is controlled by voltage-dependent calcium channels (VDCCs). In humans, mutations in the Cacna1f gene, encoding the α 1F subunit of VDCCs, underlie the incomplete form of X-linked congenital stationary night blindness (CSNB2). These mutations impair synaptic transmission from rod and cone photoreceptors to bipolar cells. Here, we report anatomical and functional characterizations of the retina in the nob2 (no b-wave 2) mouse, a naturally occurring mutant caused by a null mutation in Cacna1f. Not surprisingly, the b-waves of both the light-and dark-adapted electroretinogram are abnormal in nob2 mice. The outer plexiform layer (OPL) is disorganized, with extension of ectopic neurites through the outer nuclear layer that originate from rod bipolar and horizontal cells, but not from hyperpolarizing bipolar cells. These ectopic neurites continue to express mGluR6, which is frequently associated with profiles that label with the

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Rapid Dendritic Remodeling in the Developing Retina: Dependence on Neurotransmission and Reciprocal Regulation by Rac and Rho

Cited by 227 publications

References 72 publications

Enhancement of learning and memory after activation of cerebral Rho GTPases

Enhancement of learning and memory after activation of cerebral Rho GTPases

Vasoactive Intestinal Peptide and PACAP38 Control N-Methyl-D-aspartic Acid-induced Dendrite Motility by Modifying the Activities of Rho GTPases and Phosphatidylinositol 3-Kinases

Thenob2mouse, a null mutation inCacna1f: Anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses

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