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Journal of Neuroscience, Vol 15, 5976-5988, Copyright © 1995 by Society for Neuroscience
Ultrastructural immunolabeling shows prominent presynaptic vesicular localization of delta-opioid receptor within both enkephalin- and nonenkephalin-containing axon terminals in the superficial layers of the rat cervical spinal cord
PY Cheng, AL Svingos, H Wang, CL Clarke, S Jenab, IW Beczkowska, CE Inturrisi and VM Pickel
Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021, USA.
Opioid peptides, Met5- and Leu5-enkephalin, are known endogenous ligands
for the delta-opioid receptor (DOR) associated with opioid analgesia at the
spinal level. To determine the cellular sites for DOR- mediated actions, we
examined the ultrastructural localization of DOR and Met5-enkephalin (ME)
in the spinal cord by combining immunoperoxidase and immunogold-silver
labeling for antibodies against DOR and ME, respectively. Antibodies for
DOR localization were raised in guinea pig against peptide 34-47 (p34), an
amino acid sequence within the extracellular N-terminus of the DOR recently
cloned from mouse neuroblastoma glioma (NG-108) cells. Selective
immunoperoxidase labeling for DOR was detected by light microscopy in
NG-108 cells and in the lamina I and II of the dorsal horn of the spinal
cord (C2-C4). Electron microscopy of these spinal laminae revealed that the
majority of the punctate varicosities seen by light microscopy were axon
terminals. delta-opioid receptor-like immunoreactivity (DOR-LI) in axon
terminals was most prominently associated with large dense core vesicles,
and sometimes seen along the membranes of small clear vesicles and segments
of the plasmalemma. A semiquantitative analysis of dually labeled sections
revealed that of the terminals showing DOR- LI, 23/102 (23%) also contained
Met5-enkephalin-like immunoreactivity (ME-LI). Conversely, 23/35 (66%) of
the terminals showing ME-LI also showed DOR-LI. In addition to the
presynaptic localization, selective postsynaptic densities within dendrites
were also occasionally (9%) immunolabeled for the opioid receptor. These
results provide the first ultrastructural evidence that DOR may serve
autoreceptor functions on ME terminals as well as presynaptic modulation of
other transmitters in the dorsal horn of the rat spinal cord. Additionally,
the vesicular localization of DOR-LI in axon terminals suggests the
involvement of these organelles in the transport of the receptors to the
plasma membrane.
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