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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Nielander, H.B. et al. J. Neurochem. 65, 1712–1720 (1995).
Fujita, Y. et al. J. Biol. Chem. 271, 7265–7268 (1996).
Shimazaki, Y. et al. J. Biol. Chem. 271, 14548–14553 (1996).
Malenka, R.C., Madison, D.V. & Nicoll, R.A. Nature 321, 175–177 (1986).
Capogna, M., Gähwiler, B.H. & Thompson, S.M. J. Neurosci. 15, 1249–1260 (1995).
Wu, X.S. & Wu, L.G. J. Neurosci. 21, 7928–7936 (2001).
Magleby, K.L. & Zengel, J.E. J. Physiol. 245, 163–182 (1975).
Delaney, K.R., Zucker, R.S. & Tank, D.W. J. Neurosci. 9, 3558–3567 (1989).
Regehr, W.G., Delaney, K.R. & Tank, D.W. J. Neurosci. 14, 523–537 (1994).
Salin, P., Scanziani, M., Malenka, R.C. & Nicoll, R.A. Proc. Natl. Acad. Sci. USA 93, 13304–13309 (1996).
Brager, D.H., Capogna, M. & Thompson, S.M. J. Physiol. 541, 545–559 (2002).
Capogna, M., Fankhauser, C., Gagliardini, V., Gähwiler, B.H. & Thompson, S.M. Eur. J. Neurosci. 11, 433–440 (1999).
Akers, R.F. & Routtenberg, A. J. Neurosci, 7, 3976–3983 (1987).
Thompson, S.M., Capogna, M. & Scanziani, M. Trends Neurosci. 16, 222–227 (1993).
Yawo, H. J. Physiol. 515, 169–180 (1999).
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
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 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)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1067
This article is cited by
-
Reduced presynaptic vesicle stores mediate cellular and network plasticity defects in an early-stage mouse model of Alzheimer’s disease
Molecular Neurodegeneration (2019)
-
SNAP-25 phosphorylation at Ser187 regulates synaptic facilitation and short-term plasticity in an age-dependent manner
Scientific Reports (2017)
-
PKC epsilon facilitates recovery of exocytosis after an exhausting stimulation
Pflügers Archiv - European Journal of Physiology (2009)