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Volume 16, Number 21, Issue of November 1, 1996 pp. 6878-6885
Copyright ©1996 Society for Neuroscience

Changes in the Regulatory Effects of Cell-Cell Interactions on Neuronal AChR Subunit Transcript Levels after Synapse Formation

Received May 30, 1996; revised July 31, 1996; accepted Aug. 9, 1996.

Marjory S. Levey and Michele H. Jacob

Worcester Foundation for Biomedical Research, Shrewsbury, Massachusetts 01545

Nicotinic acetylcholine receptors (AChRs) mediate excitatory synaptic transmission in the chick ciliary ganglion. AChR protein and mRNA levels are increased by both innervation and retrograde signals from target tissues during synapse formation. We now show that AChR 3, 4, and 5 subunit transcript levels stop increasing after synaptogenesis. Moreover, maintenance of these mRNA levels requires the continued presence of regulatory signals from both pre- and postganglionic tissues. Unilateral preganglionic denervation or postganglionic axotomy causes declines in 3, 4, and 5 transcript levels, ranging from twofold to 3.5-fold, relative to contralateral control neuron values in newly hatched chicks. The reductions are not merely an injury response; c4-tubulin mRNA levels are not affected by either axotomy or denervation. Further, similar decreases in AChR mRNA levels are observed after local application of colchicine to the postganglionic nerves, which blocks fast transport without disturbing axonal integrity. These results also demonstrate a developmental change in the regulatory effects of target tissues. Reductions in 5 mRNA levels caused by axotomy or colchicine treatment after peripheral synapse formation contrast with the lack of an effect on 5 when synapse formation with the target tissue is prevented. The ability of the target tissue to regulate 5 mRNA levels after synaptogenesis is interesting, because this subunit may be necessary for the formation of high-conductance AChRs. The specific regulatory effects of target tissues and inputs at different developmental stages demonstrate that neurons continually depend on signals from their pre- and postsynaptic tissues to accomplish mature levels of AChR subunit expression and optimal functioning of that neuronal circuit.

Key words: nicotinic acetylcholine receptors (AChRs); parasympathetic ciliary ganglion neurons; development; synapse formation and maturation; denervation; axotomy; regulation of gene expression; mRNA

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