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Re-evaluation of phorbol ester-induced potentiation of transmitter release from mossy fibre terminals of the mouse hippocampus

Izumi Honda*†, Haruyuki Kamiya‡§ and Hiromu Yawo*§

1. To investigate the mechanisms by which phorbol esters potentiate transmitter release from mossy fibre terminals we used fura dextran to measure the intraterminal Ca²⁺ concentration in mouse hippocampal slices.

2. A phorbol ester, phorbol 12,13-diacetate (PDAc), potentiated the field excitatory postsynaptic potential (fEPSP) slope. PDAc also enhanced the stimulation-dependent increase of [Ca²⁺]_i in the mossy fibre terminal ([Ca²⁺]_pre). The magnitude of the PDAc-induced fEPSP potentiation (463 ± 57 % at 10 µM) was larger than that expected from the enhancement of [Ca²⁺]_pre (153 ± 5 %).

3. The [Ca²⁺]_pre was suppressed by -agatoxin IVA (-AgTx_IVA, 200 nM), a P/Q-type Ca²⁺ channel-specific blocker, by 31 %. The effect of PDAc did not select between -AgTx_IVA-sensitive and -resistant components.

4. The PDAc-induced potentiation of the fEPSP slope was partially antagonized by the protein kinase C (PKC) inhibitor bisindolylmaleimide I (BIS-I, 10 µM), whereas the [Ca²⁺]_pre was completely blocked by BIS-I. Although the BIS-I-sensitive fEPSP potentiation was accompanied by a reduction of the paired-pulse ratio (PPR), the BIS-I-resistant component was not.

5. Whole-cell patch clamp recording from a CA3 pyramidal neuron in a BIS-I-treated slice demonstrated that PDAc (10 µM) increased the frequency of miniature excitatory postsynaptic currents (mEPSCs, 259 ± 33 % of control) without a noticeable change in their amplitude (102 ± 5 % of control).

6. These results suggest that PKC potentiates transmitter release by at least two distinct mechanisms, one [Ca²⁺]_pre dependent and the other [Ca²⁺]_pre independent. In addition, some phorbol ester-mediated potentiation of synaptic transmission appears to occur without activating PKC.

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