Transient cell–cell interactions in neural circuit formation

Chao, Daniel L.; Ma, Le; Shen, Kang

doi:10.1038/nrn2594

Cited by 83 publications

(82 citation statements)

References 77 publications

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“…How is this change regulated? A plausible mechanism, supported by observations in other neural systems (for review, see Chao et al, 2009), is that signals along the mesoprefrontal trajectory trigger changes in axon responsiveness to Sema3F. Interestingly, the change in Sema3F responses of mesoprefrontal axons coincides with their arrival in the SP, a well known intermediate target (Allendoerfer and Shatz, 1994;Ló pezBendito and Molnár, 2003).…”

Section: Npn-2 Controls Mpfc Innervation Through the External Capsulementioning

confidence: 65%

Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting

Kolk¹,

Gunput²,

Tran³

et al. 2009

J. Neurosci.

104

138

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Dopaminergic neurons in the mesodiencephalon (mdDA neurons) make precise synaptic connections with targets in the forebrain via the mesostriatal, mesolimbic, and mesoprefrontal pathways. Because of the functional importance of these remarkably complex ascending axon pathways and their implication in human disease, the mechanisms underlying the development of these connections are of considerable interest. Despite extensive in vitro studies, the molecular determinants that ensure the perfect formation of these pathways in vivo remain mostly unknown. Here, we determine the embryonic origin and ontogeny of the mouse mesoprefrontal pathway and use these data to reveal an unexpected requirement for semaphorin 3F (Sema3F) and its receptor neuropilin-2 (Npn-2) during mdDA pathway development using tissue culture approaches and analysis of sema3F Ϫ / Ϫ , npn-2 Ϫ / Ϫ , and npn-2 Ϫ / Ϫ ;TH-Cre mice. We show that Sema3F is a bifunctional guidance cue for mdDA axons, some of which have the remarkable ability to regulate their responsiveness to Sema3F as they develop. During early developmental stages, Sema3F chemorepulsion controls previously uncharacterized aspects of mdDA pathway development through both Npn-2-dependent (axon fasciculation and channeling) and Npn-2-independent (rostral growth) mechanisms. Later on, chemoattraction mediated by Sema3F and Npn-2 is required to orient mdDA axon projections in the cortical plate of the medial prefrontal cortex. This latter finding demonstrates that regulation of axon orientation in the target field occurs by chemoattractive mechanisms, and this is likely to also apply to other neural systems. In all, this study provides a framework for additional dissection of the molecular basis of mdDA pathway development and disease.

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Section: Npn-2 Controls Mpfc Innervation Through the External Capsulementioning

confidence: 65%

Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting

Kolk¹,

Gunput²,

Tran³

et al. 2009

J. Neurosci.

104

138

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show abstract

“…This effect requires DCC signaling within dopamine neurons. DCC-mediated synaptic decrease is in line with the fact that, in addition to their role in axonal guidance, DCC receptors continue to organize neuronal connectivity beyond axonal pathfinding (Dickson, 2002;Chao et al, 2009;Poon et al, 2013). DCC receptors function in a shortrange capacity to dictate axonal target recognition, axon and dendrite arborization, and synaptogenesis (Deiner et al, * Figure 5 Amphetamine exposure in adolescence, but not in adulthood, leads to augmented salience attribution and requires dcc in dopamine neurons.…”

Section: Dcc-mediated Effects Of Amphetamine On the Sculpting Of Mpfcmentioning

confidence: 79%

Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner

Reynolds

Makowski

Yogendran

et al. 2014

Neuropsychopharmacol

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Initiation of drug use during adolescence is a strong predictor of both the incidence and severity of addiction throughout the lifetime. Intriguingly, adolescence is a period of dynamic refinement in the organization of neuronal connectivity, in particular medial prefrontal cortex (mPFC) dopamine circuitry. The guidance cue receptor, DCC (deleted in colorectal cancer), is highly expressed by dopamine neurons and orchestrates their innervation to the mPFC during adolescence. Furthermore, we have shown that amphetamine in adolescence regulates DCC expression in dopamine neurons. Drugs in adolescence may therefore induce their enduring behavioral effects via DCC-mediated disruption in mPFC dopamine development. In this study, we investigated the impact of repeated exposure to amphetamine during adolescence on both the development of mPFC dopamine connectivity and on salience attribution to drug context in adulthood. We compare these effects to those induced by adult exposure to an identical amphetamine regimen. Finally, we determine whether DCC signaling within dopamine neurons is necessary for these events. Exposure to amphetamine in adolescence, but not in adulthood, leads to an increase in the span of dopamine innervation to the mPFC, but a reduction of presynaptic sites present on these axons. Amphetamine treatment in adolescence, but not in adulthood, also produces an increase in salience attribution to a previously drug-paired context in adulthood. Remarkably, DCC signaling within dopamine neurons is required for both of these effects. Drugs of abuse in adolescence may therefore induce their detrimental behavioral consequences by disrupting mesocortical dopamine development through alterations in the DCC signaling cascade.

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“…Our model implies that, on contact with differing extracellular adhesive environments, growth cones change their turning responses to guidance cues by modulating the efficiency of RyR-mediated CICR via the two counteractive pathways. Such mechanisms may operate in vivo, for example, when a growth cone is migrating through an intermediate target that secretes a guidance cue (Chao et al, 2009). CAMs present in the intermediate target could modulate cyclic nucleotide and Ca 2ϩ signaling in the growth cone, thereby switching its response to the guidance cue from attraction to repulsion.…”

Section: Discussionmentioning

confidence: 99%

The Nitric Oxide-cGMP Pathway Controls the Directional Polarity of Growth Cone Guidance via Modulating Cytosolic Ca2+ Signals

Tojima

Itofusa²,

Kamiguchi³

2009

Journal of Neuroscience

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Transient cell–cell interactions in neural circuit formation

Cited by 83 publications

References 77 publications

Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting

Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting

Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner

The Nitric Oxide-cGMP Pathway Controls the Directional Polarity of Growth Cone Guidance via Modulating Cytosolic Ca2+ Signals

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