Kainate receptors and RNA editing in cholinergic neurons.
Parasympathetic ganglia are considered simple relay systems that have cholinergic input and output, with modulation occurring centrally. Greater complexity is suggested, however, by our showing here that avian ciliary ganglion (CG) neurons also express a different excitatory receptor type--ionotropic glutamate receptors of the kainate subtype (KARs). This is the first report of glutamate receptor expression in the CG and KAR expression in any cholinergic neuron. We show that KARs form functional channels on CG neurons. KARs localize to CG neuron axons and somata as well as axons and terminals of pre-synaptic inputs to the CG. Glutamate transporters are expressed on Schwann cells that surround synapses on neuronal somata, and may provide a local source of glutamate. CG neurons express multiple KAR subunit mRNAs (GluR5, GluR7, and KA1), and their relative levels change dramatically during axon outgrowth and synaptic differentiation. The developmental role for KARs may depend upon their calcium permeability, a property regulated by mRNA editing. We show GluR5 editing increases predominantly at the time CG axons contact peripheral targets. Our data suggest that glutamatergic signaling may function as a local circuit mechanism to modulate excitability and calcium signaling during synapse formation and maturation in the CG in vivo.
Olsen
Douglas P
DP
Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, Massachusetts 02111, USA.
Dunlap
Kathleen
K
Jacob
Michele H
MH
D000109:Acetylcholine / Q000378:metabolism*; D027322:Amino Acid Transport System X-AG / Q000502:physiology; D000818:Animals; D020013:Calcium Signaling / Q000502:physiology; D002462:Cell Membrane / Q000378:metabolism / Q000648:ultrastructure; D002645:Chickens; D002799:Cholinergic Fibers / Q000378:metabolism*; D005726:Ganglia, Parasympathetic / Q000187:drug effects / Q000378:metabolism*; D018698:Glutamic Acid / Q000378:metabolism; D020439:Growth Cones / Q000378:metabolism / Q000648:ultrastructure; D006801:Humans; D051379:Mice; D009474:Neurons / Q000378:metabolism*; D021122:Protein Subunits / Q000235:genetics; D017393:RNA Editing / Q000502:physiology*; D012333:RNA, Messenger / Q000378:metabolism; D064529:Receptor, Metabotropic Glutamate 5; D018092:Kainic Acid Receptors / Q000235:genetics*; D018094:Receptors, Metabotropic Glutamate / Q000235:genetics; D012583:Schwann Cells / Q000378:metabolism; D013569:Synapses / Q000378:metabolism / Q000648:ultrastructure; D009435:Synaptic Transmission / Q000502:physiology
D000109:Acetylcholine; D027322:Amino Acid Transport System X-AG; D018698:Glutamic Acid; D021122:Protein Subunits; D012333:RNA, Messenger; D064529:Receptor, Metabotropic Glutamate 5; D018092:Kainic Acid Receptors; D018094:Receptors, Metabotropic Glutamate