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Evidence that glutamate mediates Axon‐to‐Schwann cell signaling in the squid
Author(s) -
Lieberman Edward M.,
Abbott N. Joan,
Hassan Sami
Publication year - 1989
Publication title -
glia
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.954
H-Index - 164
eISSN - 1098-1136
pISSN - 0894-1491
DOI - 10.1002/glia.440020205
Subject(s) - hyperpolarization (physics) , biology , glutamate receptor , axon , kainate receptor , neuroscience , stimulation , biophysics , schwann cell , ampa receptor , kainic acid , microbiology and biotechnology , biochemistry , receptor , chemistry , stereochemistry , nuclear magnetic resonance spectroscopy
High‐frequency stimulation (100 Hz) of isolated giant axons of the small squid Alloteuthis subulata and the large squid Loligo forbesi caused the periaxonal Schwann cell resting potential (E m = ‐40 mV) to hyperpolarize up to 11 mV in direct proportion to train duration and action potential amplitude. In both species, the Schwann cell also hyperpolarized up to 17 m V with the application of L‐glutamate (10 −9 to 10 −6 M), in a dose‐dependent manner. By contrast, in the presence of 10 −8 M d‐tubocurarine (d‐TC) to block the cholinergic component of the Schwann cell response, Schwann cells depolarized 8–9 mV during electrical stimulation of the axon or application of L‐glutamate. In the presence of 10 −5 M 2‐amino‐4‐phosphonobutyrate (2‐APB), the hyperpolarization to glutamate and to axon stimulation was blocked, whereas the cholinergic (carbacholinduced) hyperpolarization was unaffected. In experiments with Alloteuthis , L‐aspartate (10 −7 M) also caused a Schwann cell hyperpolarization, but this was not blocked by 2‐APB. In tests with glutamate receptor agonists and antagonists, quisqualate (10 −5 M) produced a hyperpolarization blocked by 10 −4 M L‐glutamic acid diethylester (GDEE), which also blocked the response to axonal stimulation. Kainic acid (10 −4 M) also caused a hyperpolarization, but n‐methyl‐D‐aspartate (NMDA; 10 −4 M), ibotenate (10 −5 M), α‐amino‐3 hydroxy‐5‐methyl‐isoxazole proprionate (AMPA; 10 −4 M), and isethionate (10 −5 M) had no effect. The results suggest that glutamate is a mediator of communication between the active axon and its surrounding Schwann cells and, by acting on quisqualate/kainate (i.e., non‐NMDA) glutamate receptors, causes depolarization of the Schwann cell membrane. This depolarization in turn appears to activate cholinergic mechanisms in the Schwann cell that result in a secondary, long‐lasting Schwann cell hyperpolarization. The function of the hyperpolarization is presently not well understood, but a contribution to regulation of the [K + ] in the periaxonal microenvironment is proposed.