Cooperativity between extracellular adenosine 5′-triphosphate and activation of N-methyl-D-aspartate receptors in long-term potentiation induction in hippocampal CA1 neurons
Section snippets
Slice preparation
The animals used were maintained and handled following the guidelines of the Animal Care and Use Committee of the Yamagata University School of Medicine. Adult male Hartley guinea-pigs (250–300 g, Funabashi Farm Co., Tokyo, Japan) were killed by decapitation, then the hippocampi were quickly removed and cut into 500-μm-thick transverse slices using a rotary slicer (Dosaka DK-7700, Kyoto, Japan). Slices were pre-incubated for a minimum of 1 h at 30–32°C in a 95% O2/5% CO2 atmosphere in standard
ATP-induced LTP in hippocampal CA1 neurons
Perfusion for 10 min with 1–10 μM ATP caused a transient reduction in the response, which, after removal of ATP, was followed by a gradual increase to a potentiated plateau, which was maintained for at least 30 min (ATP-induced LTP). Figure 1A, B, which, respectively, show sample wave forms (upper traces) and the summarized results (main figure) for the S-EPSP and A-PS, clearly show that a robust LTP was induced in slices perfused with 10 μM ATP, but not to any significant level in those
Discussion
The results of the present study indicate that ATP-induced LTP in CA1 neurons is not due to decreased activity of inhibitory inter-neurons or to increased excitatory transmitter release from pre-synaptic terminals (Fig. 2), but is due to the activation of NMDA receptors/channels (Fig. 3). Thus, the formation of ATP-induced LTP occurs at a post-synaptic site at hippocampal CA1 synapses and involves NMDA receptors/channels. Previous studies on the rat nucleus accumbens (Harvey and Lacey, 1997)
References (48)
- et al.
Protein kinase C modulation of NMDA currents: an important link for LTP induction
Trends Neurosci.
(1992) - et al.
Characterization of LTP induced by the activation of glutamate metabotropic receptors in area CA1 of the hippocampus
Neuropharmacology
(1993) - et al.
Synaptic transmission is required for initiation of long-lasting potentiation
Brain Res.
(1978) - et al.
Extracellular phosphorylation of membrane protein modifies theta burst-induced long-term potentiation in CA1 neurons of guinea-pig hippocampal slices
Neurosci. Lett.
(1995) - et al.
The mechanism of ATP-induced long-term potentiation involves extracellular phosphorylation of membrane proteins in guinea-pig hippocampal CA1 neurons
Neurosci. Lett.
(1995) - et al.
Extracellular adenosine 5′-triphosphate plus activation of glutamatergic receptors induces long-term potentiation in CA1 neurons of guinea-pig hippocampal slices
Neurosci. Lett.
(1999) - et al.
LTP induction: a synaptic catch mechanism released by extracellular phosphorylation
Neuroscience
(2000) - et al.
Extracellular adenosine 5′-triphosphate-evoked glutamate release in culture hippocampal neurons
Neurosci. Lett.
(1992) - et al.
Voltage-gated Ca2+ channel blockers, ′-Aga IV and Ni2+, suppress the induction of θ-burst induced long-term potentiation in guinea-pig hippocampal CA1 neurons
Neurosci. Lett.
(1995) - et al.
Requirement of extracellular Ca2+ after tetanus for induction of long-term potentiation in guinea-pig hippocampal slices
Neurosci. Lett.
(1987)
K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide dependent protein kinases
Biochem. Biophys. Res. Commun.
Evidence that changes in presynaptic calcium currents are not responsible for long-term potentiation in hippocampus
Brain Res.
A substrate of ecto-protein kinase is microtubule-associated protein 1B in cortical cell cultures undergoing synaptogenesis
Biochem. Biophys. Res. Commun.
Inhibition of nerve growth factor-induced neurite outgrowth of PC12 cells by a protein kinase inhibitor which does not permeate the cell membrane
FEBS Lett.
Nucleotide receptors
Curr. Opin. Neurobiol.
Characterization of ATP-induced facilitation of transmission in rat hippocampus
Eur. J. Pharmacol.
ATP receptor-mediated synaptic transmission in the hippocampus
Prog. Brain Res.
Glutamate receptor channels: novel properties and new clones
Trends Pharmacol. Sci.
Stimulation-dependent release of adenosine triphosphate from hippocampal slices
Brain Res.
ATP-induced synaptic potentiation in hippocampal slices
Brain Res.
Ceramide-induced sustained depression of synaptic currents mediated by ionotropic glutamate receptors in the hippocampus: an essential role of postsynaptic protein phosphatases
Neuroscience
Effect of P2 purinoceptor antagonists on kainate-induced currents in rat cultured neurons
Brain Res.
Nucleotide receptors in the nervous system. An abundant component using diverse transduction mechanisms
Mol. Neurobiol.
Long-term synaptic depression
Annu. Rev. Neurosci.
Cited by (34)
Differential regulation of STP, LTP and LTD by structurally diverse NMDA receptor subunit-specific positive allosteric modulators
2022, NeuropharmacologyCitation Excerpt :Both histamine (Burban et al., 2010; Williams, 1994a) and spermine (Williams, 1994b) are GluN2B preferring PAMs, with unknown effects on STP and LTD. Application of ATP (10–70 μM) to hippocampal slices causes a transient depression of responses, followed by a slowly developing LTP (Fujii et al., 1999; Wieraszko and Seyfried, 1989), which is [Ca2+]o-dependent and is blocked by AP5 (Fujii et al., 1999, 2002). Higher concentrations of ATP (e.g. 250 μM) produce an LTD like effect, which can be reversed by 3,4-diaminopyridine (Wieraszko and Seyfried, 1989).
Modulation of the neuronal network activity by P2X receptors and their involvement in neurological disorders
2015, Pharmacological ResearchCitation Excerpt :The use of ATP as a fast neurotransmitter seems to be restricted to the PNS [41], however in certain CNS zones it has been described the use of ATP for inter-neuronal communication, for example in lamina I of dorsal root of spine [42], and even in rat hippocampus CA3 pyramidal neurons [43]; nonetheless this function could be exceptional in CNS, being the principal role of ATP neuromodulation [44], and neuron–glia communication [45]. An example of the involvement of ATP in neuromodulation is given by the observation made by diverse groups at the beginning of the present millennium, when using pharmacological and genetic approaches was possible to establish the involvement of P2X receptors in the formation of LTP in rat hippocampus [46–48]; for instance, in P2X4-KO mice was detected an impairment in LTP formation in hippocampus [49,50], this modification could be due to a reduction in synaptic [Ca2+] [50] and related to that, a lower incorporation of NR2B subunits at the post-synapse [49]. Another interesting aspect to P2X receptors is the capability of interact with other types of receptors, such as nicotinic α4β2 which interacts with P2X2 [41], this provokes a cross-inhibition of both.
Purinergic signalling: From normal behaviour to pathological brain function
2011, Progress in NeurobiologyCitation Excerpt :Low levels of adenosine will preferentially activate adenosine A1 receptors, whereas higher concentrations will also activate adenosine A2A receptors (Almeida et al., 2003; de Mendonca and Ribeiro, 2001). Though less information on the behavioural responses mediated by P2 receptors on learning and memory tasks is available, it is quite clear that ATP, similar to adenosine, profoundly influences synaptic strength and other molecular mechanisms involved in learning and memory processes (Fujii et al., 2002; Mori et al., 2001). The original in vitro evidence dates back to the mid-1990s, when ATP was shown to reproduce the enhancement of synaptic strength, which is the basis of LTP, typically induced by a specific pattern of high frequency stimulation (HFS) in the hippocampus (reviewed by Wieraszko, 1996).
Role of Purinergic Receptors in CNS Function and Neuroprotection
2011, Advances in PharmacologyCitation Excerpt :However, a consensus opinion regarding the role of P2X receptors in long-term potentiation and long-term depression has not yet been gained. Obtaining a better understanding of the role of P2X receptors in synaptic plasticity, it would require consideration of complex factors around the synapse (i.e., purinergic regulation of release of both excitatory and inhibitory neurotransmitters), extracellular purinergic metabolism, receptor phosphorylation by modulation of ecto-kinase activity (Fujii et al., 2002), and purinergic effects on perisynaptic glia (also known as the tripartite synapse) (Araque et al., 1999). In hippocampal slices, administration of ATP or its metabolically stable ATP-analog ATPγS exerts an inhibitory action on fast excitatory postsynaptic currents and population spikes (Coppi et al., 2007; Pedata et al., 2007) under normoxic conditions.
P2X receptors and synaptic plasticity
2009, NeuroscienceCitation Excerpt :Although significant bidirectional changes in the field excitatory synaptic potentials (fEPSPs) have been reported following administration of P2X agonists, conclusions about the role of P2X receptors in these effects are controversial (Yamazaki et al., 2003; Fujii, 2004). In addition, the role of exogenous ATP is obscured by the effect of phosphorylation of glutamate receptors ectodomains (Fujii et al., 2002). Moreover, ATP applied to brain slices may also act through astroglia, and indeed recent data indicate the involvement of glial P2X receptors in synaptic plasticity in the spinal cord (Ikeda et al., 2007).