Most peptide-containing sensory neurons lack proteins for exocytotic release and vesicular transport of glutamate.
We used multiple-labeling immunohistochemistry and confocal microscopy to examine co-expression of immunoreactivity for vesicular glutamate transporters (VGluTs), synaptic vesicle proteins, and soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins in peptide-containing sensory neurons of guinea pigs, mice, and toads. Axon terminals in the superficial layers of the dorsal horn of the spinal cord with immunoreactivity (IR) for both substance P (SP) and calcitonin gene-related peptide (CGRP) lacked IR for synaptosome-associated protein of 25 kDa (SNAP-25), syntaxin, synaptotagmin, synaptophysin, and synapsin, although adjacent varicosities without neuropeptides had IR for these synaptic proteins. Similarly, peptide-containing axon terminals in the superficial dorsal horn lacked IR for VGluT1 and VGluT2, despite the presence of VGluT2-IR in nearby nonpeptide varicosities. VGluT3-IR was sparse in the dorsal horn of the mouse spinal cord and was not present in peptide-containing axons. Most peripheral terminals of sensory neurons with both SP-IR and CGRP-IR in the skin, viscera, and autonomic ganglia of guinea pigs and mice also lacked IR for synaptic vesicle proteins, SNARE proteins, VGluT1, and VGluT2. In dorsal root ganglia from guinea pigs and mice, most small neurons with IR for both SP and CGRP lacked IR for SNAP-25, VGluT1, and VGluT2. Thus, proteins considered essential for vesicular uptake and exocytotic release of glutamate are not expressed at detectable levels by most sensory neurons containing SP and CGRP in rodents and toads. These data raise the possibility that most peptide-containing sensory neurons may not normally release glutamate as a transmitter.
Morris
Judy L
JL
Centre for Neuroscience, Flinders University, Adelaide, South Australia 5001, Australia. Judy.Morris@flinders.edu.au
König
Peter
P
Shimizu
Toshihiko
T
Jobling
Phillip
P
Gibbins
Ian L
IL
D026922:Amino Acid Transport Systems, Acidic / Q000378:metabolism; D000818:Animals; D002024:Bufo marinus; D015740:Calcitonin Gene-Related Peptide / Q000378:metabolism; D005089:Exocytosis / Q000502:physiology*; D018698:Glutamic Acid / Q000378:metabolism*; D006168:Guinea Pigs; D007150:Immunohistochemistry; D008565:Membrane Proteins / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000378:metabolism*; D051379:Mice; D009419:Nerve Tissue Proteins / Q000378:metabolism*; D009475:Neurons, Afferent / Q000378:metabolism*; D020671:Posterior Horn Cells / Q000378:metabolism; D017729:Presynaptic Terminals / Q000378:metabolism*; D050600:SNARE Proteins; D013045:Species Specificity; D013116:Spinal Cord / Q000166:cytology / Q000378:metabolism; D013373:Substance P / Q000378:metabolism; D013572:Synaptic Vesicles / Q000378:metabolism*; D014018:Tissue Distribution; D050598:Vesicular Glutamate Transport Protein 1; D050599:Vesicular Glutamate Transport Protein 2; D050496:Vesicular Glutamate Transport Proteins; D033921:Vesicular Transport Proteins / Q000378:metabolism*
D026922:Amino Acid Transport Systems, Acidic; D008565:Membrane Proteins; D026901:Membrane Transport Proteins; D009419:Nerve Tissue Proteins; C460879:SLC17A8 protein, human; D050600:SNARE Proteins; C493477:Slc17a6 protein, mouse; C493465:Slc17a7 protein, mouse; D050598:Vesicular Glutamate Transport Protein 1; D050599:Vesicular Glutamate Transport Protein 2; D050496:Vesicular Glutamate Transport Proteins; D033921:Vesicular Transport Proteins; D013373:Substance P; D018698:Glutamic Acid; D015740:Calcitonin Gene-Related Peptide