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Volume 17, Number 1, Issue of January 1, 1997 pp. 140-151
Copyright ©1997 Society for NeuroscienceTrafficking of Cell-Surface
-Amyloid Precursor Protein: Evidence that a Sorting Intermediate Participates in Synaptic Vesicle Recycling
Received Aug. 2, 1996; revised Oct. 15, 1996; accepted Oct. 22, 1996.
Numa R. Marquez-Sterling1, Amy C. Y. Lo2, Sangram S. Sisodia2, and Edward H. Koo3 1 Department of Pathology, Northwestern University Medical School, Chicago, Illinois 60611, 2 Department of Pathology and the Neuropathology Laboratory, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, and 3 Departments of Neurology and Pathology, Harvard Medical School, Boston, Massachusetts 02115
We recently demonstrated that the Alzheimer's
-amyloid precursor protein (APP) is internalized from the axonal cell surface. In this study, we use biochemical and cell biological methods to characterize endocytotic compartments that participate in trafficking of APP in central neurons. APP is present in presynaptic clathrin-coated vesicles purified from bovine brain, together with the recycling synaptic vesicle integral membrane proteins synaptophysin, synaptotagmin, and SV2. In contrast, APP is largely excluded from synaptic vesicles purified from rat brain. In primary cerebellar macroneurons, cell-surface APP is internalized with recycling synaptic vesicle integral membrane proteins but is subsequently sorted away from synaptic vesicles and transported retrogradely to the neuronal soma. Internalized APP partially co-localizes with rab5a-containing compartments in axons and with V-ATPase-containing compartments in both axons and neuronal soma. These results provide direct biochemical evidence that an obligate sorting compartment participates in the regeneration of synaptic vesicles during exo/endocytotic recycling at nerve terminals but do not preclude concurrent "kiss-and-run" recycling. Moreover, APP is now, to our knowledge, the first demonstrated example of an axonal cell-surface protein that is internalized with recycling synaptic vesicle membrane proteins but is subsequently sorted away from synaptic vesicles.
Key words: Alzheimer's disease; amyloid precursor; axons; cell surface; cerebellar macroneurons; clathrin-coated vesicles; endocytosis; protein trafficking; synaptic vesicle recycling
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