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Volume 16, Number 23, Issue of December 1, 1996 pp. 7428-7436
Copyright ©1996 Society for Neuroscience

Differential Effects of Protein Synthesis Inhibition on the Activity-Dependent Expression of BDNF Transcripts: Evidence for Immediate-Early Gene Responses from Specific Promoters

Received March 8, 1996; revised Aug. 1, 1996; accepted Sept. 5, 1996.

Julie C. Lauterborn^{1, 2}, Santiago Rivera¹, Curtiss T. Stinis¹, Valerie Y. Hayes³, Paul J. Isackson^{3, 4}, and Christine M. Gall^{1, 2}

Departments of ¹ Anatomy and Neurobiology and ² Psychobiology, University of California, Irvine, California 92697-1275, and Departments of ³ Molecular Neuroscience and ⁴ Biochemistry and Molecular Biology, Mayo Clinic, Jacksonville, Florida 32224

In the adult rat forebrain, brain-derived neurotrophic factor (BDNF) expression is very rapidly induced by neuronal activity, suggesting that this might occur without intervening protein synthesis. The rat BDNF gene has four differentially regulated promoter regions; each gives rise to an mRNA containing a unique 5 exon (I-IV) and a common 3 exon (V) that codes for mature BDNF protein. The present study used exon-specific in situ hybridization and both in vivo and in vitro preparations to determine whether activity induces BDNF as an "immediate-early gene" (IEG) from specific promoter regions and to compare the regulation of BDNF and nerve growth factor (NGF). In cultured hippocampal slices, kainic acid markedly increased pan-BDNF (exon V) and NGF mRNA content; cycloheximide attenuated the effect of kainic acid on both. In vivo stimulation of a paroxysmal afterdischarge increased both pan-BDNF and NGF mRNA levels in the dentate gyrus granule cells; pretreatment with anisomycin modestly attenuated the paroxysmal afterdischarge-induced increase of both transcripts. To determine whether partial drug effects on BDNF expression reflect the differential regulation of transcript species, levels of mRNAs containing exons I-IV were evaluated. A single afterdischarge increased exon I-IV-containing mRNA levels; anisomycin significantly attenuated the increase in exon I- and II-containing mRNAs but had no effect on the increase in exon III- and IV-containing mRNAs. These data show that for mature forebrain neurons, activity induces the expression of BDNF exon III- and IV-containing transcripts as IEG responses.

Key words: brain-derived neurotrophic factor; hippocampus; nerve growth factor; cycloheximide; immediate-early gene; gene regulation

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