ATP P2X Receptor-Mediated Enhancement of Glutamate Release and Evoked EPSCs in Dorsal Horn Neurons of the Rat Spinal Cord

Nakatsuka, Terumasa; Gu, Jianguo G.

doi:10.1523/jneurosci.21-17-06522.2001

Cited by 174 publications

(144 citation statements)

References 43 publications

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“…As the present and other studies have shown, the primary afferent neurons express both P2X 2 and P2X 3 receptors. In vitro studies in the spinal dorsal horn have show that the P2X receptor agonist α ,β-meATP causes an increase in glutamatergic (Nakatsuka and Gu, 2001;Nakatsuka et al, 2002;Nakatsuka et al, 2003;Tsuzuki et al, 2003). We have reported analogous results in the medullary dorsal horn (Jennings et al, 2006).…”

Section: Functional Roles Of P2x Receptors In Nociceptive Signallingsupporting

confidence: 71%

“…In the spinal somatosensory system, all P2X receptor subtypes with the exception of P2X 7 are expressed in the spinal dorsal horn, the dorsal root ganglion (DRG), and the central terminals of primary afferent neurons (Burnstock, 2000;Khakh, 2001;North, 2002). In vivo and in vitro electrophysiological recordings from single dorsal horn neurons have implicated P2X receptors on primary afferent terminals in spinal nociceptive transmission (Nakatsuka and Gu, 2001;Nakatsuka et al, 2002;Nakatsuka et al, 2003; Correspondence details: Dr. Ernest Jennings Dept. Anatomy & Cell Biology The University of Melbourne Parkville, Victoria, 3010, Australia Tel: +61 3 8344 5802 Fax: +61 3 9347 9619 Email: e.jennings@unimelb.edu.au.…”

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confidence: 99%

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Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons

et al. 2007

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Purine receptors have been implicated in central neurotransmission from nociceptive primary afferent neurons, and adenosine 5'tri-phosphate (ATP)-mediated currents in sensory neurons have been shown to be mediated by both P2X 3 and P2X 2/3 receptors. The aim of the present study was to quantitatively examine the distribution of P2X 2 and P2X 3 receptors in primary afferent cell bodies in the rat trigeminal ganglion, including those innervating the dura. In order to determine the classes of neurons that express these receptor subtypes, purine receptor immunoreactivity was examined for colocalisation with markers of myelinated (neurofilament 200; NF200) or mostly unmyelinated, nonpeptidergic fibres (Bandeiraea simplicifolia isolectin B4; IB4). 40 % of P2X 2 and 64 % of P2X 3 receptor-expressing cells were IB4 positive, and 33 % of P2X 2 and 31 % of P2X 3 receptor-expressing cells were NF200 positive. Approximately 40 % of cells expressing P2X 2 receptors also expressed P2X 3 receptors and vice versa. Trigeminal ganglion neurons innervating the dura mater were retrogradely labelled and 52 % of these neurons expressed either P2X 2 or P2X 3 or both receptors. These results are consistent with electrophysiological findings that P2X receptors exist on the central terminals of trigeminal afferent neurons, and provide evidence that afferents supplying the dura express both receptors. In addition, the data suggest specific differences exist in P2X receptor expression between the spinal and trigeminal nociceptive systems. Keywords purine receptors; trigeminal ganglia; sensory neuron; migraine; pain Purine receptors have been widely implicated in nociceptive processing (Burnstock, 2000;Khakh, 2001;Liu and Salter, 2005). The receptors are of two types: ionotropic (P2X) and metabotropic (P2Y), both of which are stimulated by adenosine 5'tri-phosphate (ATP). Seven P2X receptor subtypes have been cloned, and some occur as heteromultimers (e.g. P2X 2/3 , P2X 1/5 and P2X 4/6 receptors). In the spinal somatosensory system, all P2X receptor subtypes with the exception of P2X 7 are expressed in the spinal dorsal horn, the dorsal root ganglion (DRG), and the central terminals of primary afferent neurons (Burnstock, 2000;Khakh, 2001;North, 2002). In vivo and in vitro electrophysiological recordings from single dorsal horn neurons have implicated P2X receptors on primary afferent terminals in spinal nociceptive transmission (Nakatsuka and Gu, 2001;Nakatsuka et al., 2002;Nakatsuka et al., 2003; Correspondence details: Dr. Ernest Jennings Dept. Anatomy & Cell Biology The University of Melbourne Parkville, Victoria, 3010, Australia Tel: +61 3 8344 5802 Fax: +61 3 9347 9619 Email: e.jennings@unimelb.edu.au. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form...

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Section: Functional Roles Of P2x Receptors In Nociceptive Signallingsupporting

confidence: 71%

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confidence: 99%

Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons

et al. 2007

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“…Previous studies suggest that P2X receptors modulate glutamatergic and GABAergic synaptic transmission in the CNS, namely spinal cord, the nucleus tractus solitarius, medial habenula, locus coeruleus, hippocampus, and somatosensory cortex (Bardoni et al, 1997;Evans et al, 1992;Gu and MacDermott, 1997;Hugel and Schlichter, 2000;Jin et al, 2004;Mori et al, 2001;Nakatsuka and Gu, 2001;Nieber et al, 1997;Pankratov et al, 1998). For example, activation of P2X receptors has been shown to presynaptically alter the release of glutamate, GABA, glycine and vasopressin (Jin et al, 2004;Khakh and Henderson, 2000;Nakatsuka and Gu, 2001;Rhee et al, 2000;Troadec et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Purinergic P2X receptors presynaptically increase glutamatergic synaptic transmission in dorsolateral periaqueductal gray

Xing¹,

Lu²,

Li³

2008

Brain Research

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Purinergic P2X receptors have been reported to present in regions of the midbrain periaqueductal gray (PAG). The purpose of this study was to determine the role of presynaptic P2X receptors in modulating excitatory and inhibitory synaptic inputs to the dorsolateral PAG (dl-PAG), which has abundant neuronal connections. First, whole cell voltage-clamp recording was performed to obtain excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) of the dl-PAG neurons. Our data show that α, β-methylene ATP (a P2X receptors agonist), in the concentration of 50 µM, significantly increased the frequency of miniature EPSCs without altering the amplitude of miniature EPSCs in eight tested neurons. The effects were attenuated by PPADS, an antagonist to P2X receptors. Furthermore, α, β-methylene ATP increased the amplitude of evoked EPSCs, and decreased the paired-pulse ratio of eEPSCs in ten neurons. In contrast, activation of P2X had no distinct effect on IPSCs. In addition, immunofluoresent methods demonstrate that P2X labeling was co-localized with a presynaptic marker, synaptophysin, in the dl-PAG. The results of the current study provide the first evidence indicating that P2X receptors facilitate glutamatergic synaptic transmission in the dl-PAG via presynaptic mechanisms. SectionNeurophysiology, Neuropharmacology and other forms of Intercellular Communication

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“…Although a slight potentiation of the sEPSC amplitude (a measure of postsynaptic sensitivity) occurred in some of the experiments, the facilitation of the sEPSC frequency (a measure of spontaneous transmitter release) was a much more pronounced phenomenon. The enhancement of spontaneous glutamatergic transmission by ATP has been reported originally for the nociceptive afferent pathways to lamina V [22] and I [23] in the spinal cord dorsal horn. In this case, the general P2 receptor agonist ATP and the P2X1,3 selective agonist α,β-meATP had comparable activities, indicating the involvement of pain-relevant, presynaptic P2X3 receptors [24].…”

Section: Discussionmentioning

confidence: 67%

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

Khakpay

Polster

Köles

et al. 2010

Purinergic Signalling

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Locus coeruleus (LC) neurons in a rat brain slice preparation were superfused with a Mg 2+ -free and bicuculline-containing external medium. Under these conditions, glutamatergic spontaneous excitatory postsynaptic currents (sEPSCs) were recorded by means of the whole-cell patch-clamp method. ATP, as well as its structural analogue 2-methylthio ATP (2-MeSATP), both caused transient inward currents, which were outlasted by an increase in the frequency but not the amplitude of the sEPSCs. PPADS, but not suramin or reactive blue 2 counteracted both effects of 2-MeSATP. By contrast, α,β-methylene ATP (α,β-meATP), UTP and BzATP did not cause an inward current response. Of these latter agonists, only BzATP slightly facilitated the sEPSC amplitude and strongly potentiated its frequency. PPADS and Brilliant Blue G, as well as fluorocitric acid and aminoadipic acid prevented the activity of BzATP. Furthermore, BzATP caused a similar facilitation of the miniature (m)EPSC (recorded in the presence of tetrodotoxin) and sEPSC frequencies (recorded in its absence). Eventually, capsaicin augmented the frequency of the sEPSCs in a capsazepine-, but not PPADS-antagonizable, manner. In conclusion, the stimulation of astrocytic P2X7 receptors appears to lead to the outflow of a signalling molecule, which presynaptically increases the spontaneous release of glutamate onto LC neurons from their afferent fibre tracts. It is suggested, that the two algogenic compounds ATP and capsaicin utilise separate receptor systems to potentiate the release of glutamate and in consequence to increase the excitability of LC neurons.

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ATP P2X Receptor-Mediated Enhancement of Glutamate Release and Evoked EPSCs in Dorsal Horn Neurons of the Rat Spinal Cord

Cited by 174 publications

References 43 publications

Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons

Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons

Purinergic P2X receptors presynaptically increase glutamatergic synaptic transmission in dorsolateral periaqueductal gray

Potentiation of the glutamatergic synaptic input to rat locus coeruleus neurons by P2X7 receptors

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