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Activity-dependent activation of presynaptic protein kinase C mediates post-tetanic potentiation

Abstract

Vesicle exocytosis is mediated by the complex interaction between synaptic vesicle and plasma membrane proteins, many of which are substrates for protein kinases1,2,3. Exogenous protein kinase activators increase release probability at several mammalian CNS synapses4,5,6, but the physiological conditions under which presynaptic protein kinases become activated are not known. We report here that calcium/phospholipid-dependent protein kinase C (PKC) is activated by high-frequency stimulation and mediates post-tetanic potentiation (PTP) in the rat hippocampus.

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Figure 1: PTP of CA3–CA1 cell EPSCs and intraterminal Ca2+.
Figure 2: Antagonists of protein kinase C block PTP.

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Acknowledgements

We thank B.E. Alger, J. Kim and J.P.Y. Kao for advice and comments. Supported by US National Institutes of Health grants R01 MH65488 and R01 NS40338 to S.M.T.

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Correspondence to Scott M Thompson.

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Supplementary information

Supplementary Methods (PDF 17 kb)

Supplementary Fig. 1.

Antagonists of protein kinase C blocked PTP of spontaneous EPSCs. (a), Spontaneous EPSCs recorded from individual cells 15 s before and 15 s after tetanic stimulation (100 Hz, 4.5 s) from untreated, STR-, and BIS-treated cultures (Scale: 25 pA, 500 ms). (b) Cumulative probability plots from 4 trials from a cell in an untreated culture demonstrating a significant increase in sEPSC frequency (P < 0.005, K-S test) with no significant change in amplitude. (c) Summary data showing the PTP of sEPSC frequency in untreated cultures () but not in STR- (□ ) and BIS- ( ) treated cultures. The increase in sEPSC frequency was significant in all four untreated cells (P < 0.005, K-S test), but not in any of the STR- or BIS-treated cells. The increase in sEPSC frequency was small, presumably because a large number of synapses contribute to baseline sEPSC frequency, but only a fraction of these experience the tetanic stimulation. (GIF 11 kb)

Supplementary Table 1 (PDF 9 kb)

Supplementary Table 2 (PDF 9 kb)

Supplementary Video.

Time lapse image sequence of Fluo-4 fluorescence in a single CA3 cell axon in str. radiatum of area CA1 before, during, and after eliciting a high frequency train of action potentials (HFS, 100 Hz for 4.5 s) with the recording electrode at the cell body. Same axon as Fig. 1c,d. Images acquired every 2 s. No background subtraction has been applied. (AVI 1689 kb)

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Brager, D., Cai, X. & Thompson, S. Activity-dependent activation of presynaptic protein kinase C mediates post-tetanic potentiation. Nat Neurosci 6, 551–552 (2003). https://doi.org/10.1038/nn1067

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