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Volume 17, Number 23, Issue of December 1, 1997 pp. 9026-9034

Dendroaxonal Transcytosis of Transferrin in Cultured Hippocampal and Sympathetic Neurons

Received April 11, 1997; revised Sept. 15, 1997; accepted Sept. 18, 1997.

Agnès Hémar1, 4, Jean-Christophe Olivo2, Edward Williamson1, Rainer Saffrich3, and Carlos G. Dotti1

1 Cell Biology Programme, 2 Cell Biophysics Programme, and 3 Biochemical Instrumentation Programme, European Molecular Biology Laboratory, 69117 Heidelberg, Germany, and 4 Unité de Biologie des Interactions Cellulaires, Unité de Recherche Associée Centre National de la Recherche Scientifique 1960, Institut Pasteur, 75724 Paris, France

Previous studies using overexpressed polymeric immunoglobulin receptor in cultured neurons have suggested that these cells may use a dendroaxonal transcytotic pathway (; ). By using a combination of semiquantitative light microscopy, video microscopy, and a biochemical assay, we show that this pathway is used by the endogenous ligand transferrin (Tf) and its receptor. Labeled Tf added to fully mature hippocampal neurons changes the intracellular distribution of its receptor from preferentially dendritic shortly after addition to dendritic and axonal at longer times. Incubation of living neurons with (caged)FITC-Tf followed by uncaging in the dendrites results in the later appearance of fluorescence in the axon of the same cell. In "chambered" sympathetic neurons in culture, 125I-Tf or iron as 55Fe-Tf added to the cell body/dendrite chamber is recovered in the axonal chamber, showing that internalized ligand from the cell body-dendrite area is released at the axonal end. Finally, we show that excitatory neurotransmitters increase Tf receptor transcytosis, whereas inhibitory neurotransmitters reduce it. The dendritic uptake, transcytotic transport, and axonal release of physiologically active Tf demonstrated here could be envisioned for other trophic factors and therefore have important consequences for neuronal anterograde target maturation. Moreover, the changes in transcytosis after neurotransmitter addition may be important in the cellular responses that follow electrical activation.

Key words: transferrin; receptor; L-glutamate; hippocampal neurons; sympathetic neurons; transcytosis




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