Frequent coexpression of the vesicular glutamate transporter 1 and 2 genes, as well as coexpression with genes for choline acetyltransferase or glutamic acid decarboxylase in neurons of rat brain

Danik, Marc; Cassoly, Estelle; Manseau, Frédéric; Sotty, Florence; Mouginot, Didier; Williams, Sylvain

doi:10.1002/jnr.20500

Cited by 57 publications

(50 citation statements)

References 62 publications

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“…This has been demonstrated in rat and squirrel monkey mesopontine tegmentum (Clarke et al 1997;Lavoie and Parent 1994); rat cerebellum, striatum, and septum (Boulland et al 2004;Danik et al 2005); rat and mouse motor neurons (Koyuncuoglu et al 1998;Nishimaru et al 2005;Waerhaug and Ottersen 1993); and Xenopus spinal cord . Developmental switches in neurotransmitter phenotypes have also been documented.…”

Section: Functional Implicationsmentioning

confidence: 92%

Regulation of Cholinergic Phenotype in Developing Neurons

Liu

Popescu²,

Denisova³

et al. 2008

Journal of Neurophysiology

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Liu X, Popescu IR, Denisova JV, Neve RL, Corriveau RA, Belousov AB. Regulation of cholinergic phenotype in developing neurons. J Neurophysiol 99: 2443-2455, 2008. First published March 5, 2008 doi:10.1152/jn.00762.2007. Specification of neurotransmitter phenotype is critical for neural circuit development and is influenced by intrinsic and extrinsic factors. Recent findings in rat hypothalamus in vitro suggest the role of neurotransmitter glutamate in the regulation of cholinergic phenotype. Here we extended our previous studies on the mechanisms of glutamate-dependent regulation of cholinergic phenotypic properties in hypothalamic neurons. Using immunocytochemistry, electrophysiology, and calcium imaging, we demonstrate that hypothalamic expression of choline acetyltransferase (the cholinergic marker) and responsiveness of neurons to acetylcholine (ACh) receptor agonists increase during chronic administration of an Nmethyl-D-aspartate receptor (NMDAR) blocker, MK-801, in developing rats in vivo and genetic and pharmacological inactivation of NMDARs in mouse and rat developing neuronal cultures. In hypothalamic cultures, an inactivation of NMDA receptors also induces ACh-dependent synaptic activity, as do inactivations of PKA, ERK/ MAPK, CREB, and NF-B, which are known to be regulated by NMDA receptors. Interestingly, the increase in cholinergic properties in developing neurons that is induced by NMDAR blockade is prevented by the blockade of ACh receptors, suggesting that function of ACh receptor is required for the cholinergic up-regulation. Using dual recording of monosynaptic excitatory postsynaptic currents, we further demonstrate that chronic inactivation of ionotropic glutamate receptors induces the cholinergic phenotype in a subset of glutamatergic neurons. The phenotypic switch is partial as ACh and glutamate are coreleased. The results suggest that developing neurons may not only coexpress multiple transmitter phenotypes, but can also change the phenotypes following changes in signaling in neuronal circuits.

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Section: Functional Implicationsmentioning

confidence: 92%

Regulation of Cholinergic Phenotype in Developing Neurons

Liu

Popescu²,

Denisova³

et al. 2008

Journal of Neurophysiology

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“…Note that the number of cycles was augmented in the bottom to 39 instead of 27 as in the top. MS, Whole mesencephalon plus striatum, used as positive control (Danik et al, 2003(Danik et al, , 2005; m, muscle, negative control (Aihara et al, 2000). The presence of TH mRNA was first verified to ascertain their dopaminergic phenotype, whereas the presence of ␤-actin mRNA was used to confirm the presence of intact mRNA and to test for genomic DNA contamination (top).…”

Section: Dopamine Neurons Express Vglut2 But Not Vglut1 Nor Vglut3mentioning

confidence: 99%

Developmental and Target-Dependent Regulation of Vesicular Glutamate Transporter Expression by Dopamine Neurons

Mendez

Bourque²,

Bo³

et al. 2008

Journal of Neuroscience

116

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Mesencephalic dopamine (DA) neurons have been suggested to use glutamate as a cotransmitter. Here, we suggest a mechanism for this form of cotransmission by showing that a subset of DA neurons both in vitro and in vivo expresses vesicular glutamate transporter 2 (VGluT2). Expression of VGluT2 decreases with age. Moreover, when DA neurons are grown in isolation using a microculture system, there is a marked upregulation of VGluT2 expression. We provide evidence that expression of this transporter is normally repressed through a contact-dependent interaction with GABA and other DA neurons, thus providing a partial explanation for the highly restricted expression of VGluT2 in DA neurons in vivo. Our results demonstrate that the neurotransmitter phenotype of DA neurons is both developmentally and dynamically regulated. These findings may have implications for a better understanding of the fast synaptic action of DA neurons as well as basal ganglia circuitry.

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“…Recently, using vesicular glutamate transporter 2 (VGLUT2) as a marker, a third population of neurons has been found in the MS-DBB that uses glutamate as a neurotransmitter (Lin et al, 2003;Sotty et al, 2003;Hajszan et al, 2004;Danik et al, 2005). This population is estimated to constitute 25% of the MS-DBB population (Colom et al, 2005) and to provide 4 -23% of the septohippocampal projection (Colom et al, 2005;Henderson et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…To address these questions, we used transgenic mice in which the expression of the VGLUT2 gene is linked with that of the enhanced green fluorescent protein (eGFP). VGLUT2 is considered a specific marker for glutamatergic neurons (Fremeau et al, 2001), and it is highly expressed in the rodent MS-DBB (Sotty et al, 2003;Danik et al, 2005). Second, we used an in vitro septohippocampal preparation where the fornix-fimbria fibers are kept intact to probe whether hippocampal cells receive glutamatergic synaptic input from MS-DBB neurons.…”

Section: Introductionmentioning

confidence: 99%

Glutamatergic Neurons of the Mouse Medial Septum and Diagonal Band of Broca Synaptically Drive Hippocampal Pyramidal Cells: Relevance for Hippocampal Theta Rhythm

Huh¹,

Goutagny²,

Williams³

2010

J. Neurosci.

134

125

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Neurons of the medial septum and diagonal band of Broca (MS-DBB) provide an important input to the hippocampus and are critically involved in learning and memory. Although cholinergic and GABAergic MS-DBB neurons are known to modulate hippocampal activity, the role of recently described glutamatergic MS-DBB neurons is unknown. Here, we examined the electrophysiological properties of glutamatergic MS-DBB neurons and tested whether they provide a functional synaptic input to the hippocampus. To visualize the glutamatergic neurons, we used MS-DBB slices from transgenic mice in which the green fluorescent protein is expressed specifically by vesicular glutamate transporter 2-positive neurons and characterized their properties using whole-cell patch-clamp technique. For assessing the function of the glutamatergic projection, we used an in vitro septohippocampal preparation, electrically stimulated the fornix or chemically activated the MS-DBB using NMDA microinfusions and recorded postsynaptic responses in CA3 pyramidal cells. We found that glutamatergic MS-DBB neurons as a population display a highly heterogeneous set of firing patterns including fast-, cluster-, burst-, and slow-firing. Remarkably, a significant proportion exhibited fast-firing properties, prominent I h , and rhythmic spontaneous firing at theta frequencies similar to those found in GABAergic MS-DBB neurons. Activation of the MS-DBB led to fast, AMPA receptormediated glutamatergic responses in CA3 pyramidal cells. These results describe for the first time the electrophysiological signatures of glutamatergic MS-DBB neurons, their rhythmic firing properties, and their capacity to drive hippocampal principal neurons. Our findings suggest that the glutamatergic septohippocampal pathway may play an important role in hippocampal theta oscillations and relevant cognitive functions.

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Frequent coexpression of the vesicular glutamate transporter 1 and 2 genes, as well as coexpression with genes for choline acetyltransferase or glutamic acid decarboxylase in neurons of rat brain

Cited by 57 publications

References 62 publications

Regulation of Cholinergic Phenotype in Developing Neurons

Regulation of Cholinergic Phenotype in Developing Neurons

Developmental and Target-Dependent Regulation of Vesicular Glutamate Transporter Expression by Dopamine Neurons

Glutamatergic Neurons of the Mouse Medial Septum and Diagonal Band of Broca Synaptically Drive Hippocampal Pyramidal Cells: Relevance for Hippocampal Theta Rhythm

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