 |
Previous Article | Next Article 
The Journal of Neuroscience, September 15, 1999, 19(18):7834-7845
Lamina-Specific Synaptic Activation Causes Domain-Specific
Alterations in Dendritic Immunostaining for MAP2 and CAM Kinase
II
Oswald
Steward1 and
Shelley
Halpain2
1 Department of Neuroscience, University of Virginia,
Charlottesville, Virginia 22908, and 2 Department of Cell
Biology, The Scripps Research Institute, La Jolla, California 92037
Polyribosomal complexes are selectively localized beneath
postsynaptic sites on neuronal dendrites; this localization suggests that the translation of the mRNAs that are present in dendrites may be
regulated by synaptic activity. The present study tests this hypothesis
by evaluating whether synaptic activation alters the immunostaining
pattern for two proteins whose mRNAs are present in dendrites: the
dendrite-specific cytoskeletal protein MAP2 and the -subunit of
CAMKII. High-frequency stimulation of the perforant path projections to
the dentate gyrus, which terminate in a discrete band on the dendrites
of dentate granule cells, produced a two-stage alteration in
immunostaining for MAP2 in the dendritic laminae. Five minutes of
stimulation (30 trains) caused a decrease in MAP2 immunostaining in the
lamina in which the activated synapses terminate. After more prolonged
periods of stimulation (1-2 hr), there was an increase in
immunostaining in the sideband laminae just proximal and distal to the
activated band of synapses. The same stimulation paradigm produced a
modest increase in immunostaining for -CAMKII in the activated
laminae, with no detectable changes in the sideband laminae. The
alterations in immunostaining for MAP2 were diminished, but not
eliminated, by inhibiting protein synthesis; the increases in CAMKII
were not. These findings reveal that patterned synaptic activity can produce domain-specific alterations in the molecular composition of
dendrites; these alterations may be caused in part by local protein
synthesis and in part by other mechanisms.
Key words:
dendritic mRNA; MAP2; calcium-calmodulin-dependent
protein kinase II; synapse; protein synthesis; protein synthesis
inhibitors; LTP
Copyright © 1999 Society for Neuroscience 0270-6474/99/19187834-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
E. Messaoudi, T. Kanhema, J. Soule, A. Tiron, G. Dagyte, B. da Silva, and C. R. Bramham
Sustained Arc/Arg3.1 Synthesis Controls Long-Term Potentiation Consolidation through Regulation of Local Actin Polymerization in the Dentate Gyrus In Vivo
J. Neurosci.,
September 26, 2007;
27(39):
10445 - 10455.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. E. Willis, E. A. van Niekerk, Y. Sasaki, M. Mesngon, T. T. Merianda, G. G. Williams, M. Kendall, D. S. Smith, G. J. Bassell, and J. L. Twiss
Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs
J. Cell Biol.,
September 7, 2007;
178(6):
965 - 980.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Huang, J. K. Chotiner, and O. Steward
Actin Polymerization and ERK Phosphorylation Are Required for Arc/Arg3.1 mRNA Targeting to Activated Synaptic Sites on Dendrites
J. Neurosci.,
August 22, 2007;
27(34):
9054 - 9067.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Sajikumar, S. Navakkode, and J. U. Frey
Identification of Compartment- and Process-Specific Molecules Required for "Synaptic Tagging" during Long-Term Potentiation and Long-Term Depression in Hippocampal CA1
J. Neurosci.,
May 9, 2007;
27(19):
5068 - 5080.
[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]
|
 |
|

|
 |

|
 |
 
J. M. Alarcon, A. Barco, and E. R. Kandel
Capture of the Late Phase of Long-Term Potentiation within and across the Apical and Basilar Dendritic Compartments of CA1 Pyramidal Neurons: Synaptic Tagging Is Compartment Restricted
J. Neurosci.,
January 4, 2006;
26(1):
256 - 264.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Jaworski, S. Spangler, D. P. Seeburg, C. C. Hoogenraad, and M. Sheng
Control of Dendritic Arborization by the Phosphoinositide-3'-Kinase-Akt-Mammalian Target of Rapamycin Pathway
J. Neurosci.,
December 7, 2005;
25(49):
11300 - 11312.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Iijima, T. Imai, Y. Kimura, A. Bernstein, H. J. Okano, M. Yuzaki, and H. Okano
Hzf protein regulates dendritic localization and BDNF-induced translation of type 1 inositol 1,4,5-trisphosphate receptor mRNA
PNAS,
November 22, 2005;
102(47):
17190 - 17195.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Huang, J. K. Chotiner, and O. Steward
The mRNA for Elongation Factor 1{alpha} Is Localized in Dendrites and Translated in Response to Treatments That Induce Long-Term Depression
J. Neurosci.,
August 3, 2005;
25(31):
7199 - 7209.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Tongiorgi, M. Armellin, P. G. Giulianini, G. Bregola, S. Zucchini, B. Paradiso, O. Steward, A. Cattaneo, and M. Simonato
Brain-Derived Neurotrophic Factor mRNA and Protein Are Targeted to Discrete Dendritic Laminas by Events That Trigger Epileptogenesis
J. Neurosci.,
July 28, 2004;
24(30):
6842 - 6852.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Moccia, D. Chen, V. Lyles, E. Kapuya, Y. E, S. Kalachikov, C. M. T. Spahn, J. Frank, E. R. Kandel, M. Barad, et al.
An Unbiased cDNA Library Prepared from Isolated Aplysia Sensory Neuron Processes Is Enriched for Cytoskeletal and Translational mRNAs
J. Neurosci.,
October 15, 2003;
23(28):
9409 - 9417.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Shan, T. P. Munro, E. Barbarese, J. H. Carson, and R. Smith
A Molecular Mechanism for mRNA Trafficking in Neuronal Dendrites
J. Neurosci.,
October 1, 2003;
23(26):
8859 - 8866.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Wang, A. Iacoangeli, S. Popp, I. A. Muslimov, H. Imataka, N. Sonenberg, I. B. Lomakin, and H. Tiedge
Dendritic BC1 RNA: Functional Role in Regulation of Translation Initiation
J. Neurosci.,
December 1, 2002;
22(23):
10232 - 10241.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-Q. Zheng, T. K. Kelly, B. Chang, S. Ryazantsev, A. K. Rajasekaran, K. C. Martin, and J. L. Twiss
A Functional Role for Intra-Axonal Protein Synthesis during Axonal Regeneration from Adult Sensory Neurons
J. Neurosci.,
December 1, 2001;
21(23):
9291 - 9303.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-p. Yu, S. McKinney, H. A. Lester, and N. Davidson
gamma -Aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses
PNAS,
April 5, 2001;
(2001)
91093998.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
I. S. Moon, I. S. Park, L. T. Schenker, M. B. Kennedy, J.-I. Moon, and I. Jin
Presence of both Constitutive and Inducible Forms of Heat Shock Protein 70 in the Cerebral Cortex and Hippocampal Synapses
Cereb Cortex,
March 1, 2001;
11(3):
238 - 248.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. K. Pinkstaff, S. A. Chappell, V. P. Mauro, G. M. Edelman, and L. A. Krushel
Internal initiation of translation of five dendritically localized neuronal mRNAs
PNAS,
February 15, 2001;
(2001)
51623398.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
M. Kneussel and H. Betz
Receptors, gephyrin and gephyrin-associated proteins: novel insights into the assembly of inhibitory postsynaptic membrane specializations
J. Physiol.,
May 15, 2000;
525(1):
1 - 9.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Righi, E. Tongiorgi, and A. Cattaneo
Brain-Derived Neurotrophic Factor (BDNF) Induces Dendritic Targeting of BDNF and Tyrosine Kinase B mRNAs in Hippocampal Neurons through a Phosphatidylinositol-3 Kinase-Dependent Pathway
J. Neurosci.,
May 1, 2000;
20(9):
3165 - 3174.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Ouyang, A. Rosenstein, G. Kreiman, E. M. Schuman, and M. B. Kennedy
Tetanic Stimulation Leads to Increased Accumulation of Ca2+/Calmodulin-Dependent Protein Kinase II via Dendritic Protein Synthesis in Hippocampal Neurons
J. Neurosci.,
September 15, 1999;
19(18):
7823 - 7833.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. K. Pinkstaff, S. A. Chappell, V. P. Mauro, G. M. Edelman, and L. A. Krushel
Internal initiation of translation of five dendritically localized neuronal mRNAs
PNAS,
February 27, 2001;
98(5):
2770 - 2775.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T.-p. Yu, S. McKinney, H. A. Lester, and N. Davidson
gamma -Aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses
PNAS,
April 24, 2001;
98(9):
5264 - 5269.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|