Mediation of Hippocampal Mossy Fiber Long-Term Potentiation by Cyclic AMP
Abstract
Repetitive activation of hippocampal mossy fibers evokes a long-term potentiation (LTP) of synaptic responses in pyramidal cells in the CA3 region that is independent of N-methyl-D-aspartate receptor activation. Previous results suggest that the site for both the induction and expression of this form of LTP is presynaptic. Experimental elevation of cyclic adenosine 3',5'-monophosphate (cAMP) both mimics and interferes with tetanus-induced mossy fiber LTP, and blockers of the cAMP cascade block mossy fiber LTP. It is proposed that calcium entry into the presynaptic terminal may activate Ca(2+)-calmodulin-sensitive adenylyl cyclase I which, through protein kinase A, causes a persistent enhancement of evoked glutamate release.
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Forskolin, an adenylyl cyclase activator, leads to marked chemical potentiation.
“Similarly, forskolin, an adenylyl cyclase (AC) activator, leads to marked chemical potentiation [29,32,33].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [29]
High-frequency stimulation induces several cAMP-dependent forms of presynaptic plasticity.
“For example, high-frequency stimulation (HFS) induces several cyclic adenosine monophosphate (cAMP)-dependent forms of presynaptic plasticity [21,28–33].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [29]
Forskolin is a widely used adenylyl cyclase activator.
“To maximally activate the cAMP pathway, we applied forskolin, a widely used AC activator [28–31,33,48].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [29]
Because forskolin-induced potentiation occludes with LTP, short-term and long-term plasticity converge on similar pool mechanisms.
“As forskolin-induced potentiation occludes with LTP at this synapse [29], this suggests that both short-term and long-term plasticity converge on similar pool mechanisms.”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [29]
PKA activation is obligatory for the induction and maintenance of mossy fiber LTP.
“Evidence from several laboratories suggests that PKA activation is obligatory for the induction and maintenance of mossy fiber LTP (Y.Y. Huang et al., 1994;Weisskopf et al., 1994).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Weisskopf et al., 1994
Mossy fiber LTP can be induced by forskolin.
“For example, forskolin evokes LTP at the mossy fiber3 CA3 synapse, whereas the inactive forskolin homolog, 1,9-dideoxy-forskolin, does not (Weisskopf et al., 1994), and mutant mice lacking PKA C1 or Ri subunits are defective in mossy fiber LTP (Huang et al., 1995).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Weisskopf et al., 1994
Mossy fiber LTP requires PKA activity.
“Evidence from several laboratories suggests that PKA activation is obligatory for the induction and maintenance of mossy fiber LTP (Y.Y. Huang et al., 1994;Weisskopf et al., 1994).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Weisskopf et al., 1994
Forskolin evokes LTP at the mossy fiber CA3 synapse, whereas the inactive forskolin homolog, 1,9-dideoxy-forskolin, does not.
“For example, forskolin evokes LTP at the mossy fiber3 CA3 synapse, whereas the inactive forskolin homolog, 1,9-dideoxy-forskolin, does not (Weisskopf et al., 1994), and mutant mice lacking PKA C1 or Ri subunits are defective in mossy fiber LTP (Huang et al., 1995).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Weisskopf et al., 1994
The potentiation caused by forskolin is blocked by inhibitors of PKA.
“The potentiation caused by forskolin is blocked by inhibitors of PK A (Y. Y. Huang et al., 1994;Weisskopf et al., 1994).”
From Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation (1998) · cites this paper as Weisskopf et al., 1994
Cites
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218 · see citing works
Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus
Hopkins, W. F., & Johnston, D. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.2.667 · Cited by 310 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Südhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,491 · see citing works
PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity
Esteban, J. A., Shi, S.-H., Wilson, C., Nuriya, M., Huganir, R. L., & Malinow, R. (2003) · Nature Neuroscience · doi:10.1038/nn997 · Cited by 894 · see citing works
Martin, K. C., Michael, D., Rose, J. C., Barad, M., Casadio, A., Zhu, H., & Kandel, E. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80330-x · Cited by 545 · see citing works
Wong, S. T., Athos, J., Figueroa, X. A., Pineda, V. V., Schaefer, M. L., Chavkin, C. C., Muglia, L. J., & Storm, D. R. (1999) · Neuron · doi:10.1016/s0896-6273(01)80036-2 · Cited by 486 · see citing works
Distinct short-term plasticity at two excitatory synapses in the hippocampus
Salin, P. A., Scanziani, M., Malenka, R. C., & Nicoll, R. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.23.13304 · Cited by 438 · see citing works
Self-citationLong-term potentiation and long-term depression: a clinical perspective
Bliss, T. V. P., & Cooke, S. F. (2011) · Clinics · doi:10.1590/s1807-59322011001300002 · Cited by 333 · see citing works
Postsynaptic Induction and PKA-Dependent Expression of LTP in the Lateral Amygdala
Huang, Y.-Y., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80524-3 · Cited by 333 · see citing works
Kamiya, H., Shinozaki, H., & Yamamoto, C. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021395 · Cited by 327 · see citing works
Huang, Y.-Y., Kandel, E. R., Varshavsky, L., Brandont, E. P., Qi, M., Idzerda, R. L., Stanley McKnight, G., & Bourtchouladz, R. (1995) · Cell · doi:10.1016/0092-8674(95)90146-9 · Cited by 267 · see citing works
Munc13 C2B domain is an activity-dependent Ca2+ regulator of synaptic exocytosis
Shin, O.-H., Lu, J., Rhee, J.-S., Tomchick, D. R., Pang, Z. P., Wojcik, S. M., Camacho-Perez, M., Brose, N., Machius, M., Rizo, J., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1758 · Cited by 243 · see citing works
Target-Specific Expression of Presynaptic Mossy Fiber Plasticity
Maccaferri, G., Tóth, K., & McBain, C. J. (1998) · Science · doi:10.1126/science.279.5355.1368 · Cited by 225 · see citing works
Lawrence, J. J., & McBain, C. J. (2003) · Trends in Neurosciences · doi:10.1016/j.tins.2003.09.007 · Cited by 214 · see citing works
Chapter 6 Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase
Abel, T., & Nguyen, P. V. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(07)00006-4 · Cited by 198 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80080-x · Cited by 199 · see citing works
Zhao, M.-G., Ko, S. W., Wu, L.-J., Toyoda, H., Xu, H., Quan, J., Li, J., Jia, Y., Ren, M., Xu, Z. C., et al. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2103-06.2006 · Cited by 197 · see citing works
Type I Adenylyl Cyclase Mutant Mice Have Impaired Mossy Fiber Long-Term Potentiation
Villacres, E. C., Wong, S. T., Chavkin, C., & Storm, D. R. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03186.1998 · Cited by 187 · see citing works
“Isozyme compensation complicates the interpretation of data obtained with the Rib mutant, particularly because the mutant mice show no decrease in total PKA activity.”
BackgroundInfluentialEvers, M. R., Salmen, B., Bukalo, O., Rollenhagen, A., Bösl, M. R., Morellini, F., Bartsch, U., Dityatev, A., & Schachner, M. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07177.2002 · Cited by 172 · see citing works
PTP and LTP at a hippocampal mossy fiber-interneuron synapse
Alle, H., Jonas, P., & Geiger, J. R. P. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.251610898 · Cited by 158 · see citing works
Impaired Cerebellar Long-Term Potentiation in Type I Adenylyl Cyclase Mutant Mice
Storm, D. R., Hansel, C., Hacker, B., Parent, A., & Linden, D. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80500-0 · Cited by 159 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Wang, H., Pineda, V. V., Chan, G. C. K., Wong, S. T., Muglia, L. J., & Storm, D. R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09710.2003 · Cited by 120 · see citing works
Taylor, J. R., Birnbaum, S., Ubriani, R., & Arnsten, A. F. T. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-j0001.1999 · Cited by 120 · see citing works
Hensch, T. K., Gordon, J. A., Brandon, E. P., McKnight, G. S., Idzerda, R. L., & Stryker, M. P. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02108.1998 · Cited by 117 · see citing works
Pelkey, K. A., Topolnik, L., Lacaille, J.-C., & McBain, C. J. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.032 · Cited by 115 · see citing works
Vandael, D., Borges-Merjane, C., Zhang, X., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.013 · Cited by 114 · see citing works
Pelkey, K. A., Topolnik, L., Yuan, X.-Q., Lacaille, J.-C., & McBain, C. J. (2008) · Neuron · doi:10.1016/j.neuron.2008.11.018 · Cited by 69 · see citing works
Adenylate Cyclase 1 as a Key Actor in the Refinement of Retinal Projection Maps
Ravary, A., Muzerelle, A., Hervé, D., Pascoli, V., Ba-Charvet, K. N., Girault, J.-A., Welker, E., & Gaspar, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02228.2003 · Cited by 66 · see citing works
Dopamine selectively potentiates hippocampal mossy fiber to CA3 synaptic transmission
Kobayashi, K., & Suzuki, H. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.08.026 · Cited by 63 · see citing works
Pelkey, K. A., & McBain, C. J. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.148635 · Cited by 58 · see citing works
Plasticity in the Hippocampus, Neurogenesis and Drugs of Abuse
Avchalumov, Y., & Mandyam, C. D. (2021) · Brain Sciences · doi:10.3390/brainsci11030404 · Cited by 49 · see citing works
cAMP-Dependent Synaptic Plasticity at the Hippocampal Mossy Fiber Terminal
Shahoha, M., Cohen, R., Ben-Simon, Y., & Ashery, U. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.861215 · Cited by 46 · see citing works
Structure, biophysics, and circuit function of a “giant” cortical presynaptic terminal
Vandael, D., & Jonas, P. (2024) · Science · doi:10.1126/science.adg6757 · Cited by 45 · see citing works
Fukaya, R., Maglione, M., Sigrist, S. J., & Sakaba, T. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016754118 · Cited by 42 · see citing works
Herry, C., & Garcia, R. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.017 · Cited by 41 · see citing works
Orlando, M., Dvorzhak, A., Bruentgens, F., Maglione, M., Rost, B. R., Sigrist, S. J., Breustedt, J., & Schmitz, D. (2021) · PLOS Biology · doi:10.1371/journal.pbio.3001149 · Cited by 30 · see citing works
Galván, E. J., Cosgrove, K. E., Mauna, J. C., Card, J. P., Thiels, E., Meriney, S. D., & Barrionuevo, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5269-09.2010 · Cited by 28 · see citing works
Synapse-specific compartmentalization of signaling cascades for LTP induction in CA3 interneurons
Galván, E. J., Pérez-Rosello, T., Gómez-Lira, G., Lara, E., Gutiérrez, R., & Barrionuevo, G. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.024 · Cited by 21 · see citing works
Kim, O., Okamoto, Y., Kaufmann, W. A., Brose, N., Shigemoto, R., & Jonas, P. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002879 · Cited by 15 · see citing works
- Authors
- Weisskopf, M. G., Castillo, P. E., Zalutsky, R. A., & Nicoll, R. A.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Science
- Published
- 1994-09-23
- Volume
- 265
- Issue
- 5180
- Pages
- 1878-1882
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2052969380
- Cited by
- 618
- References
- 2
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 18 · 2023: 19 · 2022: 15 · 2021: 10 · 2020: 7 · 2019: 8 · 2018: 4 · 2017: 14 · 2016: 8 · 2015: 13 · 2014: 9 · 2013: 14 · 2012: 14
- FWCI
- 15.38
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- cyclic AMP, hippocampus, CA3 pyramidal cells, protein kinase A, glutamate release, synaptic plasticity
- MeSH terms
- Cyclic AMP, Animals, Calcium, Carbazoles, Colforsin, Glutamates, Guinea Pigs, Hippocampus, Indoles, Isoquinolines, Models, Biological, Nerve Fibers, Synaptic Transmission, Pyrroles, Sulfonamides, Presynaptic Terminals, Long-Term Potentiation, Cyclic AMP-Dependent Protein Kinases, Pyramidal Cells, Glutamic Acid, In Vitro Techniques
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