 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, February 1, 2000, 20(3):969-976
Metabotropic Glutamate Receptors Trigger Homosynaptic Protein Synthesis to Prolong Long-Term Potentiation
Clarke R. Raymond1, 3, Vida L. Thompson2, 3, Warren P. Tate2, 3, and Wickliffe C. Abraham1, 3 Departments of 1 Psychology and 2 Biochemistry and the 3 Neuroscience Research Centre, University of Otago, Dunedin, New Zealand
We investigated the mechanisms by which previous "priming" activation of group I metabotropic glutamate receptors (mGluRs) facilitates the persistence of long-term potentiation (LTP) in area CA1 of rat hippocampal slices. Priming of LTP was elicited by either pharmacological or synaptic activation of mGluRs before a weak tetanic stimulus that normally produced only a rapidly decaying phase of LTP that did not involve protein synthesis or mGluRs. Pharmacological priming of LTP persistence by a selective group I mGluR agonist was blocked by an inhibitor of group I mGluRs and by inhibitors of translation, but not by a transcriptional inhibitor. The same mGluR agonist increased 35S-methionine incorporation into slice proteins. LTP could also be facilitated using a synaptic stimulation priming protocol, and this effect was similarly blocked by group I mGluR and protein synthesis inhibitors. Furthermore, using a two-pathway protocol, the synaptic priming of LTP was found to be input-specific. To test for the contribution of group I mGluRs and protein synthesis to LTP in nonprimed slices, a longer duration control tetanization protocol was used to elicit a more slowly decaying form of LTP than did the weak tetanus used in the previous experiments. The persistence of the LTP induced by this stronger tetanus was dependent on mGluR activation and protein synthesis but not on transcription. Together, these results suggest that mGluRs couple to nearby protein synthesis machinery to homosynaptically regulate an intermediate phase of LTP dependent on new proteins made from pre-existing mRNA.
Key words: LTP; mGluRs; metaplasticity; protein synthesis; synaptic plasticity; hippocampus
Copyright © 2000 Society for Neuroscience 0270-6474/00/203969-08$05.00/0
This article has been cited by other articles:
B. E. Pfeiffer and K. M. Huber
The State of Synapses in Fragile X Syndrome
Neuroscientist, October 1, 2009; 15(5): 549 - 567.
[Abstract] [PDF]
J. W. Rudy and P. Matus-Amat
DHPG activation of group 1 mGluRs in BLA enhances fear conditioning
Learn. Mem., June 24, 2009; 16(7): 421 - 425.
[Abstract] [Full Text] [PDF]
S. Sajikumar, Q. Li, W. C. Abraham, and Z. C. Xiao
Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1
Learn. Mem., February 17, 2009; 16(3): 178 - 186.
[Abstract] [Full Text] [PDF]
M. D. Antion, L. Hou, H. Wong, C. A. Hoeffer, and E. Klann
mGluR-Dependent Long-Term Depression Is Associated with Increased Phosphorylation of S6 and Synthesis of Elongation Factor 1A but Remains Expressed in S6K-Deficient Mice
Mol. Cell. Biol., May 1, 2008; 28(9): 2996 - 3007.
[Abstract] [Full Text] [PDF]
G. Dolen and M. F. Bear
Role for metabotropic glutamate receptor 5 (mGluR5) in the pathogenesis of fragile X syndrome
J. Physiol., March 15, 2008; 586(6): 1503 - 1508.
[Abstract] [Full Text] [PDF]
S. R. Young, R. Bianchi, and R. K. S. Wong
Signaling Mechanisms Underlying Group I mGluR-Induced Persistent AHP Suppression in CA3 Hippocampal Neurons
J Neurophysiol, March 1, 2008; 99(3): 1105 - 1118.
[Abstract] [Full Text] [PDF]
U. Narayanan, V. Nalavadi, M. Nakamoto, D. C. Pallas, S. Ceman, G. J. Bassell, and S. T. Warren
FMRP Phosphorylation Reveals an Immediate-Early Signaling Pathway Triggered by Group I mGluR and Mediated by PP2A
J. Neurosci., December 26, 2007; 27(52): 14349 - 14357.
[Abstract] [Full Text] [PDF]
M. I. Boulware, H. Kordasiewicz, and P. G. Mermelstein
Caveolin Proteins Are Essential for Distinct Effects of Membrane Estrogen Receptors in Neurons
J. Neurosci., September 12, 2007; 27(37): 9941 - 9950.
[Abstract] [Full Text] [PDF]
B. G. Mockett, D. Guevremont, J. M. Williams, and W. C. Abraham
Dopamine D1/D5 Receptor Activation Reverses NMDA Receptor-Dependent Long-Term Depression in Rat Hippocampus
J. Neurosci., March 14, 2007; 27(11): 2918 - 2926.
[Abstract] [Full Text] [PDF]
N. S. Desai, T. M. Casimiro, S. M. Gruber, and P. W. Vanderklish
Early Postnatal Plasticity in Neocortex of Fmr1 Knockout Mice
J Neurophysiol, October 1, 2006; 96(4): 1734 - 1745.
[Abstract] [Full Text] [PDF]
S. Y. Grooms, K.-M. Noh, R. Regis, G. J. Bassell, M. K. Bryan, R. C. Carroll, and R. S. Zukin
Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons.
J. Neurosci., August 9, 2006; 26(32): 8339 - 8351.
[Abstract] [Full Text] [PDF]
R. Gong, C. S. Park, N. R. Abbassi, and S.-J. Tang
Roles of Glutamate Receptors and the Mammalian Target of Rapamycin (mTOR) Signaling Pathway in Activity-dependent Dendritic Protein Synthesis in Hippocampal Neurons
J. Biol. Chem., July 7, 2006; 281(27): 18802 - 18815.
[Abstract] [Full Text] [PDF]
B. E. Pfeiffer and K. M. Huber
Current advances in local protein synthesis and synaptic plasticity.
J. Neurosci., July 5, 2006; 26(27): 7147 - 7150.
[Abstract] [Full Text] [PDF]
B. Capron, C. Sindic, E. Godaux, and L. Ris
The characteristics of LTP induced in hippocampal slices are dependent on slice-recovery conditions
Learn. Mem., May 1, 2006; 13(3): 271 - 277.
[Abstract] [Full Text] [PDF]
C. R. Raymond and S. J. Redman
Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus
J. Physiol., January 1, 2006; 570(1): 97 - 111.
[Abstract] [Full Text] [PDF]
D. Manahan-Vaughan and K.-H. Braunewell
The Metabotropic Glutamate Receptor, mGluR5, is a Key Determinant of Good and Bad Spatial Learning Performance and Hippocampal Synaptic Plasticity
Cereb Cortex, November 1, 2005; 15(11): 1703 - 1713.
[Abstract] [Full Text] [PDF]
M. D. Antion
A TOP at the Synapse
J. Neurosci., October 26, 2005; 25(43): 9823 - 9824.
[Full Text] [PDF]
S.-C. Chuang, W. Zhao, R. Bauchwitz, Q. Yan, R. Bianchi, and R. K. S. Wong
Prolonged Epileptiform Discharges Induced by Altered Group I Metabotropic Glutamate Receptor-Mediated Synaptic Responses in Hippocampal Slices of a Fragile X Mouse Model
J. Neurosci., August 31, 2005; 25(35): 8048 - 8055.
[Abstract] [Full Text] [PDF]
F. Angenstein, A. M. Evans, S.-C. Ling, R. E. Settlage, S. Ficarro, F. A. Carrero-Martinez, J. Shabanowitz, D. F. Hunt, and W. T. Greenough
Proteomic Characterization of Messenger Ribonucleoprotein Complexes Bound to Nontranslated or Translated Poly(A) mRNAs in the Rat Cerebral Cortex
J. Biol. Chem., February 25, 2005; 280(8): 6496 - 6503.
[Abstract] [Full Text] [PDF]
P. Serrano, Y. Yao, and T. C. Sacktor
Persistent Phosphorylation by Protein Kinase M{zeta} Maintains Late-Phase Long-Term Potentiation
J. Neurosci., February 23, 2005; 25(8): 1979 - 1984.
[Abstract] [Full Text] [PDF]
A. Aschrafi, B. A. Cunningham, G. M. Edelman, and P. W. Vanderklish
The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain
PNAS, February 8, 2005; 102(6): 2180 - 2185.
[Abstract] [Full Text] [PDF]
B. Hu, S. Karnup, L. Zhou, and A. Stelzer
Reversal of Hippocampal LTP by Spontaneous Seizure-Like Activity: Role of Group I mGluR and Cell Depolarization
J Neurophysiol, January 1, 2005; 93(1): 316 - 336.
[Abstract] [Full Text] [PDF]
D. J. Froc and R. J. Racine
Interactions Between LTP- and LTD-Inducing Stimulation in the Sensorimotor Cortex of the Awake Freely Moving Rat
J Neurophysiol, January 1, 2005; 93(1): 548 - 556.
[Abstract] [Full Text] [PDF]
M. Wu, T. Hajszan, C. Xu, C. Leranth, and M. Alreja
Group I Metabotropic Glutamate Receptor Activation Produces a Direct Excitation of Identified Septohippocampal Cholinergic Neurons
J Neurophysiol, August 1, 2004; 92(2): 1216 - 1225.
[Abstract] [Full Text] [PDF]
L. A. Schrader, S. P. Perrett, L. Ye, and M. J. Friedlander
Substrates for Coincidence Detection and Calcium Signaling for Induction of Synaptic Potentiation in the Neonatal Visual Cortex
J Neurophysiol, June 1, 2004; 91(6): 2747 - 2764.
[Abstract] [Full Text] [PDF]
S. M. Gallagher, C. A. Daly, M. F. Bear, and K. M. Huber
Extracellular Signal-Regulated Protein Kinase Activation Is Required for Metabotropic Glutamate Receptor-Dependent Long-Term Depression in Hippocampal Area CA1
J. Neurosci., May 19, 2004; 24(20): 4859 - 4864.
[Abstract] [Full Text] [PDF]
T. A. Fiacco and K. D. McCarthy
Intracellular Astrocyte Calcium Waves In Situ Increase the Frequency of Spontaneous AMPA Receptor Currents in CA1 Pyramidal Neurons
J. Neurosci., January 21, 2004; 24(3): 722 - 732.
[Abstract] [Full Text] [PDF]
W. Zhao, R. Bianchi, M. Wang, and R. K. S. Wong
Extracellular Signal-Regulated Kinase 1/2 Is Required for the Induction of Group I Metabotropic Glutamate Receptor-Mediated Epileptiform Discharges
J. Neurosci., January 7, 2004; 24(1): 76 - 84.
[Abstract] [Full Text] [PDF]
W. C. Abraham and J. M. Williams
Properties and Mechanisms of LTP Maintenance
Neuroscientist, December 1, 2003; 9(6): 463 - 474.
[Abstract] [PDF]
M. Cammalleri, R. Lutjens, F. Berton, A. R. King, C. Simpson, W. Francesconi, and P. P. Sanna
Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1
PNAS, November 25, 2003; 100(24): 14368 - 14373.
[Abstract] [Full Text] [PDF]
P. K. Todd, K. J. Mack, and J. S. Malter
The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95
PNAS, November 25, 2003; 100(24): 14374 - 14378.
[Abstract] [Full Text] [PDF]
F. Angenstein, A. M. Evans, R. E. Settlage, S. T. Moran, S.-C. Ling, A. Y. Klintsova, J. Shabanowitz, D. F. Hunt, and W. T. Greenough
A Receptor for Activated C Kinase Is Part of Messenger Ribonucleoprotein Complexes Associated with PolyA-mRNAs in Neurons
J. Neurosci., October 15, 2002; 22(20): 8827 - 8837.
[Abstract] [Full Text] [PDF]
W.-M. Zho, J.-L. You, C.-C. Huang, and K.-S. Hsu
The Group I Metabotropic Glutamate Receptor Agonist (S)-3,5-Dihydroxyphenylglycine Induces a Novel Form of Depotentiation in the CA1 Region of the Hippocampus
J. Neurosci., October 15, 2002; 22(20): 8838 - 8849.
[Abstract] [Full Text] [PDF]
D. R. Ireland and W. C. Abraham
Group I mGluRs Increase Excitability of Hippocampal CA1 Pyramidal Neurons by a PLC-Independent Mechanism
J Neurophysiol, July 1, 2002; 88(1): 107 - 116.
[Abstract] [Full Text] [PDF]
C. R. Raymond and S. J. Redman
Different Calcium Sources Are Narrowly Tuned to the Induction of Different Forms of LTP
J Neurophysiol, July 1, 2002; 88(1): 249 - 255.
[Abstract] [Full Text] [PDF]
K. M. Huber, S. M. Gallagher, S. T. Warren, and M. F. Bear
Altered synaptic plasticity in a mouse model of fragile X mental retardation
PNAS, May 28, 2002; 99(11): 7746 - 7750.
[Abstract] [Full Text] [PDF]
T. Blank, I. Nijholt, K. Eckart, and J. Spiess
Priming of Long-Term Potentiation in Mouse Hippocampus by Corticotropin-Releasing Factor and Acute Stress: Implications for Hippocampus-Dependent Learning
J. Neurosci., May 1, 2002; 22(9): 3788 - 3794.
[Abstract] [Full Text] [PDF]
N. Lezcano and C. Bergson
D1/D5 Dopamine Receptors Stimulate Intracellular Calcium Release in Primary Cultures of Neocortical and Hippocampal Neurons
J Neurophysiol, April 1, 2002; 87(4): 2167 - 2175.
[Abstract] [Full Text] [PDF]
P. W. Vanderklish and G. M. Edelman
Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons
PNAS, January 24, 2002; (2002) 32681099.
[Abstract] [Full Text] [PDF]
K.-S. Hsu, W.-C. Ho, C.-C. Huang, and J.-J. Tsai
Transient Removal of Extracellular Mg2+ Elicits Persistent Suppression of LTP at Hippocampal CA1 Synapses Via PKC Activation
J Neurophysiol, September 1, 2000; 84(3): 1279 - 1288.
[Abstract] [Full Text] [PDF]
K. M. Huber, M. S. Kayser, and M. F. Bear
Role for Rapid Dendritic Protein Synthesis in Hippocampal mGluR-Dependent Long-Term Depression
Science, May 19, 2000; 288(5469): 1254 - 1256.
[Abstract] [Full Text]
P. W. Vanderklish and G. M. Edelman
Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons
PNAS, February 5, 2002; 99(3): 1639 - 1644.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|