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The Journal of Neuroscience, January 1, 1999, 19(1):21-33
The Mammalian Brain High-Affinity L-Proline
Transporter Is Enriched Preferentially in Synaptic Vesicles in a
Subpopulation of Excitatory Nerve Terminals in Rat Forebrain
Stephani E.
Renick1,
Dan T.
Kleven1,
June
Chan3,
Katinka
Stenius4,
Teresa A.
Milner3,
Virginia M.
Pickel3, and
Robert T.
Fremeau Jr1, 2
Departments of 1 Pharmacology and Cancer Biology and
2 Neurobiology, Duke University Medical Center, Durham,
North Carolina 27710, 3 Department of Neurology and
Neuroscience, Cornell University Medical College, New York, New York
10021, and 4 Department of Cell Biology, Yale University
School of Medicine, New Haven, Connecticut 06510
The expression of a brain-specific high-affinity
Na+-dependent (and
Cl -dependent) L-proline transporter
(PROT) in subpopulations of putative glutamatergic neurons in mammalian
brain suggests a physiological role for this carrier in excitatory
neurotransmission (). To gain insights into
potential sites where PROT may function, we used a C-terminal domain
antipeptide antibody to determine the regional distribution and
subcellular localization of PROT in rat forebrain. PROT
immunoreactivity was seen in processes having a regional light
microscopic distribution comparable to that of known glutamatergic
projections within the cortex, caudate putamen nucleus (CPN),
hippocampal formation, and other forebrain regions. In all regions
examined by electron microscopy (cortex, CPN, and the stratum oriens of
CA1), PROT labeling was observed primarily within subpopulations
of axon terminals forming asymmetric excitatory-type synapses.
Immunogold labeling for PROT was detected in close contact with
membranes of small synaptic vesicles (SSVs) and more rarely with the
plasma membrane in these axon terminals. Subcellular fractionation
studies confirmed the preferential distribution of PROT to synaptic
vesicles. The topology of PROT in synaptic vesicles was found to be
inverted with respect to the plasma membrane, suggesting that
PROT-containing vesicles are generated by a process involving
endocytosis from the plasma membrane. Because PROT lacks any of the
known characteristics of other vesicular transporters, these results
suggest that certain excitatory terminals have a reserve pool of PROT
associated with SSVs. The delivery of PROT to the plasma membrane by
exocytosis could play a critical role in the plasticity of certain
glutamatergic pathways.
Key words:
neurotransmitter transporter; excitatory
neurotransmission; L-proline; synapse; electron microscopy; presynaptic nerve terminal; excitatory amino acids
Copyright © 1999 Society for Neuroscience 0270-6474/99/19121-13$05.00/0
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