Different Rho GTPase–dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation
Open accessAbstract
The releasable factor adenosine blocks the formation of long-term potentiation (LTP). These experiments used this observation to uncover the synaptic processes that stabilize the potentiation effect. Brief adenosine infusion blocked stimulation-induced actin polymerization within dendritic spines along with LTP itself in control rat hippocampal slices but not in those pretreated with the actin filament stabilizer jasplakinolide. Adenosine also blocked activity-driven phosphorylation of synaptic cofilin but not of synaptic p21-activated kinase (PAK). A search for the upstream origins of these effects showed that adenosine suppressed RhoA activity but only modestly affected Rac and Cdc42. A RhoA kinase (ROCK) inhibitor reproduced adenosine's effects on cofilin phosphorylation, spine actin polymerization, and LTP, whereas a Rac inhibitor did not. However, inhibitors of Rac or PAK did prolong LTP's vulnerability to reversal by latrunculin, a toxin which blocks actin filament assembly. Thus, LTP induction initiates two synaptic signaling cascades: one (RhoA-ROCK-cofilin) leads to actin polymerization, whereas the other (Rac-PAK) stabilizes the newly formed filaments.
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Each theta-burst stimulus led to actin filament polymerization in spines, which is important for stabilization of LTP.
“Each theta-burst stimulus led to actin filament polymerization in spines, which is known to be important for the stabilization of LTP49.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [49]
The mechanism underlying this phenomenon involves local spreading of signaling cascades from the activated spine to its neighbors, and some of these spreading signals are potent drivers of F-actin dynamics.
“The mechanism underlying this phenomenon involves local spreading of signaling cascades from the activated spine to its neighbors, and some of these spreading signals are potent drivers of F-actin dynamics (24–26).”
From Synaptic evidence for the efficacy of spaced learning (2012) · cites this paper as [26]
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Cites
Rational design and characterization of a Rac GTPase-specific small molecule inhibitor
Gao, Y., Dickerson, J. B., Guo, F., Zheng, J., & Zheng, Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307512101 · Cited by 1,091 · see citing works
Biology of the p21-Activated Kinases
Bokoch, G. (2003) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.72.121801.161742 · Cited by 1,080 · see citing works
The Biochemistry of Memory: A New and Specific Hypothesis
LYNCH, G. S., & Baudry, M. (1984) · Science · doi:10.1126/science.6144182 · Cited by 1,045 · see citing works
Self-citationHuber, A. B., Kolodkin, A. L., Ginty, D. D., & Cloutier, J. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.010302.081139 · Cited by 720 · see citing works
Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., & Inokuchi, K. (2003) · Neuron · doi:10.1016/s0896-6273(03)00206-x · Cited by 695 · see citing works
Niwa, R., Nagata-Ohashi, K., Takeichi, M., Mizuno, K., & Uemura, T. (2002) · Cell · doi:10.1016/s0092-8674(01)00638-9 · Cited by 694 · see citing works
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
Messaoudi, E., Kanhema, T., Soule, J. D., Tiron, A., Dagytė, G., da Silva, B., & Bramham, C. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2883-07.2007 · Cited by 452 · see citing works
Tashiro, A. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.927 · Cited by 416 · see citing works
High actin concentrations in brain dendritic spines and postsynaptic densities.
Matus, A., Ackermann, M., Pehling, G., Byers, H. R., & Fujiwara, K. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.23.7590 · Cited by 401 · see citing works
A Role of Actin Filament in Synaptic Transmission and Long-Term Potentiation
Kim, C.-H., & Lisman, J. E. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04314.1999 · Cited by 386 · see citing works
Reid, T., Furuyashiki, T., Ishizaki, T., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.23.13556 · Cited by 375 · see citing works
Krucker, T., Siggins, G. R., & Halpain, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.100139797 · Cited by 374 · see citing works
Deacon, S. W., Beeser, A., Fukui, J. A., Rennefahrt, U. E. E., Myers, C., Chernoff, J., & Peterson, J. R. (2008) · Chemistry & Biology · doi:10.1016/j.chembiol.2008.03.005 · Cited by 366 · see citing works
Rex, C. S., Lin, C.-Y., Kramár, E. A., Chen, L. Y., Gall, C. M., & Lynch, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4037-06.2007 · Cited by 324 · see citing works
Self-citationChanges in Synaptic Morphology Accompany Actin Signaling during LTP
Chen, L. Y., Rex, C. S., Casale, M. S., Gall, C. M., & Lynch, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0164-07.2007 · Cited by 296 · see citing works
Self-citationInhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice
Hayashi, M. L., Rao, B. S. S., Seo, J.-S., Choi, H.-S., Dolan, B. M., Choi, S.-Y., Chattarji, S., & Tonegawa, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705003104 · Cited by 281 · see citing works
Hayashi, M. L., Choi, S.-Y., Rao, B. S. S., Jung, H.-Y., Lee, H.-K., Zhang, D., Chattarji, S., Kirkwood, A., & Tonegawa, S. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.003 · Cited by 280 · see citing works
The Mechanism of PAK Activation
Chong, C., Tan, L. H.-P., Lim, L., & Manser, E. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009316200 · Cited by 260 · see citing works
How long will long-term potentiation last?
Abraham, W. C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1222 · Cited by 258 · see citing works
Sasaki, Y., Suzuki, M., & Hidaka, H. (2002) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(02)00191-2 · Cited by 234 · see citing works
Contribution of cytoskeleton to the internalization of AMPA receptors
Zhou, Q., Xiao, M., & Nicoll, R. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.3.1261 · Cited by 229 · see citing works
New Insights into Mechanism and Regulation of Actin Capping Protein
Cooper, J. A., & Sept, D. (2008) · International review of cytology · doi:10.1016/s1937-6448(08)00604-7 · Cited by 227 · see citing works
Integrin-driven actin polymerization consolidates long-term potentiation
Kramár, E. A., Lin, B., Rex, C. S., Gall, C. M., & Lynch, G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601354103 · Cited by 221 · see citing works
Self-citationA WAVE-1 and WRP Signaling Complex Regulates Spine Density, Synaptic Plasticity, and Memory
Soderling, S. H., Guire, E. S., Kaech, S., White, J., Zhang, F., Schutz, K., Langeberg, L. K., Banker, G., Raber, J., & Scott, J. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3209-06.2006 · Cited by 217 · see citing works
Wang, H., Lu, F.-M., Jin, I., Udo, H., Kandel, E. R., de Vente, J., Walter, U., Lohmann, S. M., Hawkins, R. D., & Antonova, I. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.011 · Cited by 216 · see citing works
LTP consolidation: Substrates, explanatory power, and functional significance
Lynch, G., Rex, C. S., & Gall, C. M. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.027 · Cited by 214 · see citing works
Self-citationChapter 2 PKMζ, LTP maintenance, and the dynamic molecular biology of memory storage
Sacktor, T. C. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(07)00002-7 · Cited by 208 · see citing works
Meng, J., Meng, Y., Hanna, A., Janus, C., & Jia, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0028-05.2005 · Cited by 192 · see citing works
The Mental Retardation Protein PAK3 Contributes to Synapse Formation and Plasticity in Hippocampus
Boda, B., Alberi, S., Nikonenko, I., Nodé-Langlois, R., Jourdain, P., Moosmayer, M., Jourdain, L., & Müller, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2931-04.2004 · Cited by 183 · see citing works
Theta Stimulation Polymerizes Actin in Dendritic Spines of Hippocampus
Lin, B., Kramár, E. A., Bi, X., Brücher, F., Gall, C. M., & LYNCH, G. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4283-04.2005 · Cited by 180 · see citing works
Self-citationReversal of LTP by theta frequency stimulation
Larson, J., Xiao, P., & LYNCH, G. S. (1993) · Brain Research · doi:10.1016/0006-8993(93)90406-d · Cited by 145 · see citing works
Self-citationRegulation of Growth Cone Actin Dynamics by ADF/Cofilin
Gungabissoon, R. A., & Bamburg, J. R. (2003) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540305100402 · Cited by 142 · see citing works
Diverse Roles of Rho Family GTPases in Neuronal Development, Survival, and Death
Linseman, D. (2008) · Frontiers in Bioscience · doi:10.2741/2710 · Cited by 134 · see citing works
Gehler, S., Gallo, G., Veien, E. S., & Letourneau, P. C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0404-04.2004 · Cited by 132 · see citing works
SynGAP Regulates Steady-State and Activity-Dependent Phosphorylation of Cofilin
Carlisle, H. J., Manzerra, P., Marcora, E., & Kennedy, M. B. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4695-08.2008 · Cited by 128 · see citing works
Huang, F., Chotiner, J. K., & Steward, O. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2410-07.2007 · Cited by 125 · see citing works
Spatial organization of cofilin in dendritic spines
Rácz, B., & Weinberg, R. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.11.025 · Cited by 121 · see citing works
Rho mediates calcium-dependent activation of p38α and subsequent excitotoxic cell death
Semenova, M. M., Mäki-Hokkonen, A. M. J., Cao, J., et al. (2007) · Nature Neuroscience · doi:10.1038/nn1869 · Cited by 115 · see citing works
Smart, F. M., Edelman, G., & Vanderklish, P. (2003) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2436349100 · Cited by 105 · see citing works
Anoxia reveals a vulnerable period in the development of long-term potentiation
Arai, A., Larson, J., & LYNCH, G. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)90184-d · Cited by 93 · see citing works
Self-citationAuto‐inhibition of rat parallel fibre–Purkinje cell synapses by activity‐dependent adenosine release
Wall, M. J., & Dale, N. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.126417 · Cited by 93 · see citing works
Phosphorylation of cortactin by p21-activated kinase
Webb, B. A., Zhou, S., Eves, R. L., Shen, L., Jia, L., & Mak, A. S. (2006) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2006.06.011 · Cited by 86 · see citing works
Rho proteins, mental retardation and the neurobiological basis of intelligence
van Galen, E., & Ramakers, G. J. A. (2004) · Progress in brain research · doi:10.1016/s0079-6123(04)47022-8 · Cited by 84 · see citing works
Thirone, A. C. P., Speight, P., Zulys, M., Rotstein, O. D., Szászi, K., Pedersen, S. F., & Kapùs, A. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00467.2008 · Cited by 67 · see citing works
Ireland, D. R., & Abraham, W. C. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90643.2008 · Cited by 53 · see citing works
Takahashi, K., & Suzuki, K. (2009) · Cellular Signalling · doi:10.1016/j.cellsig.2009.01.007 · Cited by 49 · see citing works
Homeostatic shutdown of long-term potentiation in the adult hippocampus
Roth-Alpermann, C., Morris, R., Körte, M., & Bonhoeffer, T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600894103 · Cited by 46 · see citing works
O'Kane, E. M., Stone, T. W., & MORRIS, B. J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.11.020 · Cited by 46 · see citing works
Thaxton, C., Lopera, J., Bott, M., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.11.003 · Cited by 27 · see citing works
Pituicyte Stellation is Prevented by RhoA-or Cdc42-Dependent Actin Polymerization
Rosso, L., Pierson, P. M., Golfier, C., et al. (2007) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-007-9176-7 · Cited by 14 · see citing works
The receptor tyrosine phosphatase CRYP? affects growth cone morphology
Mueller, B. K., Ledig, M. M., & Wahl, S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(200008)44:2 · Cited by 12 · see citing works
Epi-fluorescent image modeling for viral infection analysis
Rout, S., Lam, V., Bell, A., et al. (2005) · 2018 52nd Asilomar Conference on Signals, Systems, and Computers · doi:10.1109/acssc.2004.1399483 · Cited by 1 · see citing works
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- Authors
- Rex, C. S., Chen, L. Y., Sharma, A., Liu, J., Babayan, A. H., Gall, C. M., & Lynch, G.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- Rex, Christopher S.
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2009-07-13
- Volume
- 186
- Issue
- 1
- Pages
- 85-97
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2712993
- OpenAlex
- W2151843908
- Cited by
- 293
- References
- 53
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 16 · 2023: 17 · 2022: 12 · 2021: 14 · 2020: 11 · 2019: 13 · 2018: 11 · 2017: 19 · 2016: 19 · 2015: 20 · 2014: 37 · 2013: 30 · 2012: 24
- FWCI
- 9.40
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institute of Mental Health (MH083396, F31MH083396)
- National Institute of Neurological Disorders and Stroke (P01NS045260, NS 37799, NS-45260, NS 045540, R01NS037799, T32NS045540)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- long-term potentiation, adenosine, RhoA, Rho kinase, cofilin phosphorylation, Rac, p21-activated kinase, actin polymerization, dendritic spines, hippocampus, actin filament stabilization, latrunculin, jasplakinolide
- MeSH terms
- Actins, Adenosine, Animals, Fluorescent Antibody Technique, Male, Actin Cytoskeleton, Models, Biological, Phosphorylation, Time Factors, Signal Transduction, Rats, Sprague-Dawley, Long-Term Potentiation, rho GTP-Binding Proteins, rhoA GTP-Binding Protein, rac1 GTP-Binding Protein, Dendritic Spines, Actin Depolymerizing Factors, Rats, p21-Activated Kinases
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