Excitation of single sensory neurones in the rat caudal trigeminal nucleus by iontophoretically applied adenosine 5′-triphosphate

doi:10.1016/0304-3940(83)90526-8

Neuroscience Letters

Volume 35, Issue 1, 31 January 1983, Pages 53-57

https://doi.org/10.1016/0304-3940(83)90526-8 Get rights and content

Abstract

ATP can be released from the peripheral endings of sensory nerves, and thus may be a neurotransmitter of primary afferent fibres [12]. We have found that ATP is excitatory when applied to single sensory neurones in the rat caudal trigeminal nucleus, and this action is consistent with a neurotransmitter role. However, adenosine monophosphate and pyrophosphate, two metabolites of ATP, were respectively found to be inhibitory and excitatory, and thus it remains unclear whether the actions of ATP are direct or are due to actions of its metabolites.

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Investigations show the paratrigeminal nucleus (Pa5) as an input site for sensory information from the sciatic nerve field. Functional or physical disruption of the Pa5 alters behavioral and somatosensory responses to nociceptive hindpaw stimulation or sciatic nerve electrostimulation (SNS), both contralateral to the affected structure. The nucleus, an input site for cranial and spinal nerves, known for orofacial nociceptive sensory processing, has efferent connections to structures associated with nociception and cardiorespiratory functions. This study aimed at determining the afferent sciatic pathway to dorsal lateral medulla by means of a neuronal tract-tracer (biocytin) injected in the iliac segment of the sciatic nerve. Spinal cord samples revealed bilateral labeling in the gracile and pyramidal or cuneate tracts from survival day 2 (lumbar L1/L2) to day 8 (cervical C2/C3 segments) following biocytin application. From day 10 to day 20 medulla samples showed labeling of the contralateral Pa5 to the injection site. The ipsilateral paratrigeminal nucleus showed labeling on day 10 only. The lateral reticular nucleus (LRt) showed fluorescent labeled terminal fibers on day 12 and 14, after tracer injection to contralateral sciatic nerve. Neurotracer injection into the LRt of sciatic nerve-biocytin-treated rats produced retrograde labeled neurons soma in the Pa5 in the vicinity of biocytin labeled nerve terminals. Therefore, Pa5 may be considered one of the first sites in the brain for sensory/nociceptive inputs from the sciatic nerve. Also, the findings include Pa5 and LRt in the neural pathway of the somatosympathetic pressor response to SNS and nocifensive responses to hindpaw stimulation.
Cellular distribution and functions of P2 receptor subtypes in different systems
2004, International Review of Cytology
Citation Excerpt :
In the first study of the effects of ATP on neurons receiving direct synaptic input from primary afferents, neurons of the cuneate nucleus of the corticospinal tract were excited (Galindo et al., 1967; Stone and Perkins, 1981; Stone and Taylor, 1978). Later studies showed ATP actions on cerebral cortical neurons (Phillis et al., 1974, 1979), area postrema (Borison et al., 1975), hippocampus (Di Cori and Henry, 1984; Inoue et al., 1991, 1992; Lee et al., 1981; Wieraszko and Seyfried, 1989a), trigeminal nucleus caudalis of the dorsal horn of the spinal cord (Salt and Hill, 1983), the spinal dorsal horn (Fyffe and Perl, 1984; Salter and Henry, 1985), lateral and medial vestibular nuclei (Mori et al., 1985), mesenchephalic trigeminal neurons (Regenold et al., 1988), medium eminence (Barnea et al., 1991), and locus coeruleus (Harms et al., 1992; Shen and North, 1993; Tschopl et al., 1992). ATP depolarized terminals of primary afferent fibers within toad spinal cord (Phillis and Kirkpatrick, 1978).
This review is aimed at providing readers with a comprehensive reference article about the distribution and function of P2 receptors in all the organs, tissues, and cells in the body. Each section provides an account of the early history of purinergic signaling in the organ⧸cell up to 1994, then summarizes subsequent evidence for the presence of P2X and P2Y receptor subtype mRNA and proteins as well as functional data, all fully referenced. A section is included describing the plasticity of expression of P2 receptors during development and aging as well as in various pathophysiological conditions. Finally, there is some discussion of possible future developments in the purinergic signaling field.
Purinergic Receptors in the Nervous System
2003, Current Topics in Membranes
Citation Excerpt :
Although the MNV is located in the CNS, it contains cell bodies of primary afferent neurons that relay proprioceptive information exclusively (Liem et al., 1991). An early paper reported excitation of single sensory neurons in the rat caudal trigeminal nucleus by iontophoretically applied ATP (Salt and Hill, 1983). The MNV is known to contain mRNA for P2X2, P2X4, P2X5, and P2X6 subtypes (Collo et al., 1996; Kanjhan et al., 1999).
This chapter focuses on the localization and roles of purinergic receptor subtypes in the central nervous system (CNS), as comprehensive reviews of purinergic signaling in the peripheral nervous system. The concept of purinergic neurotransmission is the existence of postjunctional purinergic receptors. A basis for distinguishing two types of purinoceptor, identiﬁed as P1 and P2 [for adenosine and adenosine triphosphate (ATP)/adenosine diphosphate (ADP), respectively], was proposed by Burnstock in 1978, but it was not until 1985 that a basis for distinguishing two types of P2 receptor(P2X and P2Y) was suggested, largely on the basis of pharmacological criteria. Pamela Holton provided the ﬁrst hint of a transmitter role for adenosine triphosphate (ATP) in the nervous system by demonstrating the release of ATP during antidromic stimulation of sensory nerves . Then, in 1970, it was proposed that nonadrenergic, noncholinergic (NANC) nerves supplying smooth muscle of the gut and bladder utilized ATP as a neurotransmitter. The experimental evidence included the mimicry of the NANC nerve-mediated response by ATP; the measurement of the release of ATP during the stimulation of NANC nerves with luciferin-luciferase luminometry; histochemical labeling of the subpopulations of neurons in the gut and the bladder with quinacrine—a ﬂuorescent dye known to selectively label high levels of ATP bound to peptides; and the demonstration that the slowly degradable analogue of ATP—αβ-methylene ATP, which produces selective desensitization of the ATP receptor—blocks the responses to NANC nerve stimulation.
Effect on urinary bladder function and arterial blood pressure of the activation of putative purine receptors in brainstem areas
2001, Autonomic Neuroscience: Basic and Clinical
The effect on bladder function and arterial blood pressure of adenosine-5′-triphosphate (ATP) and its synthetic analogue, α,β-methylene ATP (α,β-meATP) applied by microinjection to brainstem areas was assessed in the anaesthetised, paralysed and artificially ventilated female rat. Recordings of bladder pressure, changes in the pelvic nerve activity, arterial blood pressure and heart rate were evaluated. The purinergic drugs were microinjected into two brainstem areas – the periaqueductal grey matter (PAG) and the area of the Barrington nucleus/locus coeruleus (LC) – only after electrical stimulation (50 Hz, 1 ms, 30–50 μA; n_(PAG)=17; n_(LC)=18) and the microinjection of glutamate (2 mM, pH 7.4±0.1; n_(PAG)=16; n_(LC)=16) had shown increases of bladder pressure and/or rate of bladder contractions and/or pelvic nerve activity at specific sites. Electrical and glutamate activation of PAG evoked an increase of arterial blood pressure. Microinjections of ATP (20 mM, pH 7.4±0.1; n_(PAG)=11; n_(LC)=11) and α,β-meATP (2 mM, pH 7.4±0.1; n_(PAG)=10; n_(LC)=9) both evoked consistent increases of bladder pressure and/or pelvic nerve activity. Stimulation with ATP elicited a biphasic change of arterial blood pressure characterised by an increase followed by a decrease which was accompanied by a rise of heart rate. Microinjection of α,β-meATP into PAG did not elicit a consistent response: a decrease of arterial blood pressure was evoked in five rats, while in two other rats an increase occurred. Electrical stimulation and glutamate activation of Barrington’s nucleus/LC evoked an increase of arterial blood pressure, but a decrease was observed after microinjection of both ATP and α,β-meATP. At some sites (n=8) the effect of α,β-meATP after a pre-injection at the same site of the P2 purino receptor antagonist, suramin (20 mM, pH 7.4±0.1) was smaller than the control. At three sites within PAG and two within LC located more medially to sites where an excitatory response had been observed, electrical stimulation evoked a small decrease or no change in bladder pressure. Following the stimulus, a rise in bladder pressure was preceded by an increase of pelvic nerve activity. A similar effect of glutamate was observed in one case. These data suggest that activation of P2 purine receptors in both PAG and Barrington’s nucleus/LC is implicated in the neuronal mechanisms that generate patterns of activity in the parasympathetic innervation of the bladder and that purines also act at this level to modify sympathetic outflow to the cardiovascular system.
ATP as a presynaptic modulator
2000, Life Sciences
There is considerable evidence that ATP acts as a fast transmitter or co-transmitter in autonomic and sensory nerves mostly through activation of ionotropic P2X receptors but also through metabotropic P2Y receptors. By analogy, the observations that ATP is released from stimulated central nervous system (CNS) nerve terminals and that responses to exogenously added ATP can be recorded in central neurons, lead to the proposal that ATP might also be a fast transmitter in the CNS. However, in spite of the robust expression of P2 receptor mRNA and binding to P2 receptors in the CNS, the demonstration of central purinergic transmission has mostly remained elusive. We now review evidence to suggest that ATP may also act presynaptically rather than solely postsynaptically in the nervous system.
P2X receptors mediate ATP-induced primary nociceptive neurone activation
2000, Journal of the Autonomic Nervous System
ATP-gated P2X ion-channel receptors are localised throughout the mammalian nervous system and have been identified on neurones which participate in conduction of nociceptive information from the periphery to, and within, the CNS. This article briefly reviews recently published research describing the role that ATP and P2X receptors may play in pain perception, highlighting the importance of the P2X₃ receptor in this process. The P2X₃ receptor subunit is almost exclusively expressed on a subset of small and medium diameter sensory neurones innervating cutaneous and visceral tissue. Activation of P2X receptors present on the peripheral terminals of primary afferents results in neuronal depolarisation and, in conscious animals, leads to the manifestation of acute nociceptive behaviour. Recent animal studies have also shown that P2X₃ receptor expression is increased in sensory ganglia following acute neuronal injury, hinting that similar plasticity in the expression of this receptor subtype could underlie the mechanisms involved in a range of conditions characterised by sensory hypersensitivity in man. It is apparent from the evidence available that functional antagonists at specific P2X receptor subtypes could represent an important class of novel analgesic agents.

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^∗: Present address: Department of Physiology, University College, Cardiff CF1 1XL, U.K.

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Excitation of single sensory neurones in the rat caudal trigeminal nucleus by iontophoretically applied adenosine 5′-triphosphate

Abstract

Biochim. biophys. Acta

Gen. Pharmacol.

Progr. Neurobiol.

Brain Res.

Neuropeptides

Brain Res.

Formation constants for the complexes of adenosine di-or tri-phosphate with magnesium or calcium ions

Biochem. J.

Aktivitätsschwankungen der sauren Phosphatase im Rückenmark und den Spinalganglien der Ratte nach Durchschneidung des Nervus ischiadicus

Arch. Psychiat. Nervkrankh.

The excitation of spinal neurones by the iontophoretic application of agents which chelate calcium

J. Neurochem.

Cholinergic and non-cholinergic transmission in the mammalian spinal cord

J. Physiol. (Lond.)

Pharmacology and nerve-endings