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Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius.
J Neurosci 2004; 24(20):4709-17JN

Abstract

Vanilloid (VR1) and purinergic (P2X) receptors are found in cranial afferent neurons in nodose ganglia and their central terminations within the solitary tract nucleus (NTS), but little is known about their function. We mechanically dissociated dorsomedial NTS neurons to preserve attached native synapses and tested for VR1 and P2X function primarily in spindle-shaped neurons resembling intact second-order neurons. All neurons (n = 95) exhibited spontaneous glutamate (EPSCs) and GABA (IPSCs)-mediated synaptic currents. VR1 agonist capsaicin (CAP; 100 nm) reversibly increased EPSC frequency, effects blocked by capsazepine. ATP (100 microm) increased EPSC frequency, actions blocked by P2X antagonist pyridoxalphosphate-6-azophenyl-2', 4'-disulfonic acid (PPADS; 20 microm). In all CAP-resistant neurons, P2X agonist alphabeta-methylene-ATP (alphabeta-m-ATP) increased EPSC frequency. Neither CAP nor alphabeta-m-ATP altered EPSC amplitudes, kinetics, or holding currents. Thus, activation of VR1 and P2X receptors selectively facilitated presynaptic glutamate release on different NTS neurons. PPADS and 2',3'-O-(2,4,6-trinitrophenyl)-ATP blocked alphabeta-m-ATP responses, but P2X1-selective antagonist NF023 (8,8'-[carbonylbis (imino-3,1-phenylene carbonylimino)]bis-1,3,5-naphthalenetrisulfonic acid) did not. The pharmacological profile and transient kinetics of ATP responses are consistent with P2X3 homomeric receptors. TTX and Cd(2+) did not eliminate agonist-evoked EPSC frequency increases, suggesting that voltage-gated sodium and calcium channels are not required. In nodose ganglia, CAP but not alphabeta-m-ATP evoked inward currents in slow conducting neurons and the converse pattern in myelinated, rapidly conducting neurons (n = 14). Together, results are consistent with segregation of glutamatergic terminals into either P2X sensitive or VR1 sensitive that correspondingly identify myelinated and unmyelinated afferent pathways at the NTS.

Authors+Show Affiliations

Department of Physiology and Pharmacology, Oregon Health and Science University, Portland, Oregon 97239-3098, USA.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

15152030

Citation

Jin, Young-Ho, et al. "Purinergic and Vanilloid Receptor Activation Releases Glutamate From Separate Cranial Afferent Terminals in Nucleus Tractus Solitarius." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 24, no. 20, 2004, pp. 4709-17.
Jin YH, Bailey TW, Li BY, et al. Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. J Neurosci. 2004;24(20):4709-17.
Jin, Y. H., Bailey, T. W., Li, B. Y., Schild, J. H., & Andresen, M. C. (2004). Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 24(20), pp. 4709-17.
Jin YH, et al. Purinergic and Vanilloid Receptor Activation Releases Glutamate From Separate Cranial Afferent Terminals in Nucleus Tractus Solitarius. J Neurosci. 2004 May 19;24(20):4709-17. PubMed PMID: 15152030.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. AU - Jin,Young-Ho, AU - Bailey,Timothy W, AU - Li,Bai-Yan, AU - Schild,John H, AU - Andresen,Michael C, PY - 2004/5/21/pubmed PY - 2004/9/11/medline PY - 2004/5/21/entrez SP - 4709 EP - 17 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 24 IS - 20 N2 - Vanilloid (VR1) and purinergic (P2X) receptors are found in cranial afferent neurons in nodose ganglia and their central terminations within the solitary tract nucleus (NTS), but little is known about their function. We mechanically dissociated dorsomedial NTS neurons to preserve attached native synapses and tested for VR1 and P2X function primarily in spindle-shaped neurons resembling intact second-order neurons. All neurons (n = 95) exhibited spontaneous glutamate (EPSCs) and GABA (IPSCs)-mediated synaptic currents. VR1 agonist capsaicin (CAP; 100 nm) reversibly increased EPSC frequency, effects blocked by capsazepine. ATP (100 microm) increased EPSC frequency, actions blocked by P2X antagonist pyridoxalphosphate-6-azophenyl-2', 4'-disulfonic acid (PPADS; 20 microm). In all CAP-resistant neurons, P2X agonist alphabeta-methylene-ATP (alphabeta-m-ATP) increased EPSC frequency. Neither CAP nor alphabeta-m-ATP altered EPSC amplitudes, kinetics, or holding currents. Thus, activation of VR1 and P2X receptors selectively facilitated presynaptic glutamate release on different NTS neurons. PPADS and 2',3'-O-(2,4,6-trinitrophenyl)-ATP blocked alphabeta-m-ATP responses, but P2X1-selective antagonist NF023 (8,8'-[carbonylbis (imino-3,1-phenylene carbonylimino)]bis-1,3,5-naphthalenetrisulfonic acid) did not. The pharmacological profile and transient kinetics of ATP responses are consistent with P2X3 homomeric receptors. TTX and Cd(2+) did not eliminate agonist-evoked EPSC frequency increases, suggesting that voltage-gated sodium and calcium channels are not required. In nodose ganglia, CAP but not alphabeta-m-ATP evoked inward currents in slow conducting neurons and the converse pattern in myelinated, rapidly conducting neurons (n = 14). Together, results are consistent with segregation of glutamatergic terminals into either P2X sensitive or VR1 sensitive that correspondingly identify myelinated and unmyelinated afferent pathways at the NTS. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/15152030/Purinergic_and_vanilloid_receptor_activation_releases_glutamate_from_separate_cranial_afferent_terminals_in_nucleus_tractus_solitarius_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=15152030 DB - PRIME DP - Unbound Medicine ER -