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The Journal of Neuroscience logoLink to The Journal of Neuroscience
. 1994 Jun 1;14(6):3881–3897. doi: 10.1523/JNEUROSCI.14-06-03881.1994

Willardiines differentiate agonist binding sites for kainate- versus AMPA-preferring glutamate receptors in DRG and hippocampal neurons

LA Wong 1, ML Mayer 1, DE Jane 1, JC Watkins 1
PMCID: PMC6576952  PMID: 7515954

Abstract

Concentration jump responses to 5-substituted (S)-willardiines were recorded from dorsal root ganglion (DRG) and hippocampal neurons under voltage clamp. After block of desensitization by concanavalin-A, dose- response analysis for activation of kainate-preferring receptors in DRG neurons gave the potency sequence trifluoromethyl > iodo > bromo approximately chloro > nitro approximately cyano > kainate > methyl > fluoro > (R,S)-AMPA >> willardiine; EC50 values for the most and least potent willardiine derivatives, 5-trifluoromethyl (70 nM) and 5-fluoro (69 microM), differed 1000-fold. The potency sequence for equilibrium responses at AMPA-preferring receptors in hippocampal neurons was strikingly different from that obtained in DRG neurons: fluoro > cyano approximately trifluoromethyl approximately nitro > chloro approximately bromo > (R,S)-AMPA > iodo > willardiine > kainate > methyl. In hippocampal neurons EC50 values for the most and least potent willardiine derivatives, 5-fluoro (1.5 microM) and 5-methyl (251 microM), differed only 170-fold. Consistent with equilibrium potency measurements, in DRG neurons the kinetics of deactivation for willardiines, recorded following a return to agonist-free solution, were rapid for 5-fluoro (tau off = 43 msec) but slow for 5-iodo (tau off = 4.2 sec), while the opposite sequence was observed for hippocampal neurons, slow for 5-fluoro (tau off = 2.1 sec) and rapid for 5-iodo (tau off = 188 msec). The kinetics of recovery from desensitization showed comparable agonist- and cell-dependent differences. Structure-activity analysis for agonist responses recorded from DRG and hippocampal neurons suggests that for both kainate- preferring and AMPA-preferring receptors the binding of willardiines involves interactions with polar groups such that potency is related to ionization of the uracil ring, and hence the electron-withdrawing ability of the 5-position substituent. However, kainate-preferring receptors differ from AMPA-preferring receptors in possessing a lipophilic pocket that further enhances agonist potency by hydrophobic bonding of the 5-substituent. In contrast, AMPA-preferring receptors lack such a lipophilic site, and for 5-position substituents of the same electron-withdrawing ability, potency decreases with increase in size.


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