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Volume 16, Number 24, Issue of December 15, 1996 pp. 7950-7964
Copyright ©1996 Society for Neuroscience

Endocytosis of Activated TrkA: Evidence that Nerve Growth Factor Induces Formation of Signaling Endosomes

Received July 9, 1996; revised Sept. 16, 1996; accepted Oct. 4, 1996.

Mark L. Grimes¹, Jie Zhou^2, , Eric C. Beattie^6, , Eric C. Yuen², Deborah E. Hall², Janice S. Valletta², Kimberly S. Topp^{3, 5}, Jennifer H. LaVail^{3, 4}, Nigel W. Bunnett⁶, and William C. Mobley^{2, 3}

¹ Department of Biochemistry, Massey University, Palmerston North, New Zealand, and ² Department of Neurology, ³ Department of Anatomy, ⁴ The Neuroscience Program, ⁵ The Graduate Program in Physical Therapy, and ⁶ Department of Physiology, University of California, San Francisco, San Francisco, California 94143

The survival, differentiation, and maintenance of responsive neurons are regulated by nerve growth factor (NGF), which is secreted by the target and interacts with receptors on the axon tip. It is uncertain how the NGF signal is communicated retrogradely from distal axons to neuron cell bodies. Retrograde transport of activated receptors in endocytic vesicles could convey the signal. However, little is known about endocytosis of NGF receptors, and there is no evidence that NGF receptors continue to signal after endocytosis. We have examined early events in the membrane traffic of NGF and its receptor, gp140^TrkA (TrkA), in PC12 cells. NGF induced rapid and extensive endocytosis of TrkA in these cells, and the receptor subsequently moved into small organelles located near the plasma membrane. Some of these organelles contained clathrin and -adaptin, which implies that TrkA is internalized by clathrin-mediated endocytosis. Using mechanical permeabilization and fractionation, intracellular organelles derived from endocytosis were separated from the plasma membrane. After NGF treatment, NGF was bound to TrkA in endocytic organelles, and TrkA was tyrosine-phosphorylated and bound to PLC-1, suggesting that these receptors were competent to initiate signal transduction. These studies raise the possibility that NGF induces formation of signaling endosomes containing activated TrkA. They are an important first step in elucidating the molecular mechanism of NGF retrograde signaling.

Key words: NGF; TrkA; signaling; endosome; clathrin; PLC-1

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