Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor.

Abstract Neurons from the superior cervical ganglia of newborn rats were plated into the center compartments of three-compartment culture dishes and maintained, for 3–11 days, with 1 μg/ml 7S nerve growth factor (NGF) in all three compartments. During this period neurites elongating from the cell bodies in the center compartments penetrated silicone grease barriers and entered the separate fluid environments of the left and right compartments. Neurites in the right compartments of some cultures were then subjected to local withdrawal of NGF, while the cell bodies and neurites in the center compartments as well as the neurites in the left compartments had continuous access to NGF at 1 μg/ml. Local NGF withdrawal caused the neurites to cease elongating, and after about 7 days a precipitous, retrograde degeneration occurred, lasting about 10 days. The degeneration was not complete; residual neurites remained in the right compartments as long as a month after NGF withdrawal. Some of them appeared to loop back into the NGF-supplied center compartments, and this may have been responsible for their survival. Neurites continued to elongate in the left compartments provided with NGF, and cell counts carried out in a low-density culture showed that neurons did not die during the period of degeneration of the NGF-deprived neurites. NGF was withdrawn from all three compartments in some cultures and resulted in a more rapid degeneration of neurites and the death of the neurons. Evidence from these experiments and from preceding work indicates that survival of neurite segments is promoted either by direct exposure to extracellular NGF or by an anatomically proximal relationship to segments directly exposed; i.e., neurites survive if they connect the cell body to an NGF supply. This provides a possible mechanism for eliminating collaterals during development by local NGF withdrawal, and thereby sculpting an excessive and/or imperfectly distributed axonal tree to the adult configuration.

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