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Science 6 December 1996:
Vol. 274. no. 5293, pp. 1678 - 1683
DOI: 10.1126/science.274.5293.1678
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Research Articles

Control of Memory Formation Through Regulated Expression of a CaMKII Transgene

Mark Mayford, Mary Elizabeth Bach, Yan-You Huang, Lei Wang, Robert D. Hawkins, Eric R. Kandel *

One of the major limitations in the use of genetically modified mice for studying cognitive functions is the lack of regional and temporal control of gene function. To overcome these limitations, a forebrain-specific promoter was combined with the tetracycline transactivator system to achieve both regional and temporal control of transgene expression. Expression of an activated calcium-independent form of calcium-calmodulin-dependent kinase II (CaMKII) resulted in a loss of hippocampal long-term potentiation in response to 10-hertz stimulation and a deficit in spatial memory, a form of explicit memory. Suppression of transgene expression reversed both the physiological and the memory deficit. When the transgene was expressed at high levels in the lateral amygdala and the striatum but not other forebrain structures, there was a deficit in fear conditioning, an implicit memory task, that also was reversible. Thus, the CaMKII signaling pathway is critical for both explicit and implicit memory storage, in a manner that is independent of its potential role in development.

The authors are at the Center for Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, and Howard Hughes Medical Institute, 722 West 168 Street, New York, NY 10032, USA.
*   To whom correspondence should be addressed.

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Pavlovian Fear Conditioning Regulates Thr286 Autophosphorylation of Ca2+/Calmodulin-Dependent Protein Kinase II at Lateral Amygdala Synapses.
S. M. Rodrigues, C. R. Farb, E. P. Bauer, J. E. LeDoux, and G. E. Schafe (2004)
J. Neurosci. 24, 3281-3288
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Regulation of the Development of Mesencephalic Dopaminergic Systems by the Selective Expression of Glial Cell Line-Derived Neurotrophic Factor in Their Targets.
N. Kholodilov, O. Yarygina, T. F. Oo, H. Zhang, D. Sulzer, W. Dauer, and R. E. Burke (2004)
J. Neurosci. 24, 3136-3146
   Abstract »    Full Text »    PDF »
Long-term effects of culture of preimplantation mouse embryos on behavior.
D. J. Ecker, P. Stein, Z. Xu, C. J. Williams, G. S. Kopf, W. B. Bilker, T. Abel, and R. M. Schultz (2004)
PNAS 101, 1595-1600
   Abstract »    Full Text »    PDF »
Long-Term Potentiation and Memory.
M. A. LYNCH (2004)
Physiol Rev 84, 87-136
   Abstract »    Full Text »    PDF »
Harnessing Apoptosis for Improved Anticancer Gene Therapy.
D. J. Waxman and P. S. Schwartz (2003)
Cancer Res. 63, 8563-8572
   Abstract »    Full Text »    PDF »
Forebrain-Specific Neuronal Inhibition of Nuclear Factor-{kappa}B Activity Leads to Loss of Neuroprotection.
V. Fridmacher, B. Kaltschmidt, B. Goudeau, D. Ndiaye, F. M. Rossi, J. Pfeiffer, C. Kaltschmidt, A. Israel, and S. Memet (2003)
J. Neurosci. 23, 9403-9408
   Abstract »    Full Text »    PDF »
Differential Pattern of cAMP Response Element-Binding Protein Activation in the Rat Brain after Conditioned Aversion as a Function of the Associative Process Engaged: Taste versus Context Association.
A. Desmedt, S. Hazvi, and Y. Dudai (2003)
J. Neurosci. 23, 6102-6110
   Abstract »    Full Text »    PDF »
Ca2+-dependent Phosphorylation of Syntaxin-1A by the Death-associated Protein (DAP) Kinase Regulates Its Interaction with Munc18.
J.-H. Tian, S. Das, and Z.-H. Sheng (2003)
J. Biol. Chem. 278, 26265-26274
   Abstract »    Full Text »    PDF »
Neuropathologies in Transgenic Mice Expressing Human Immunodeficiency Virus Type 1 Tat Protein under the Regulation of the Astrocyte-Specific Glial Fibrillary Acidic Protein Promoter and Doxycycline.
B. O. Kim, Y. Liu, Y. Ruan, Z. C. Xu, L. Schantz, and J. J. He (2003)
Am. J. Pathol. 162, 1693-1707
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Microarray Technology: A Review of New Strategies to Discover Candidate Vulnerability Genes in Psychiatric Disorders.
W. E. Bunney, B. G. Bunney, M. P. Vawter, H. Tomita, J. Li, S. J. Evans, P. V. Choudary, R. M. Myers, E. G. Jones, S. J. Watson, et al. (2003)
Am J Psychiatry 160, 657-666
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Pharmacologically Regulated Induction of Silent Mutations (PRISM): Combined Pharmacological and Genetic Approaches for Learning and Memory.
P. W. Frankland, M. Ohno, E. Takahashi, A. P. Chen, R. M. Costa, S. A. Kushner, and A. J. Silva (2003)
Neuroscientist 9, 104-109
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Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain.
H. Wang, E. Shimizu, Y.-P. Tang, M. Cho, M. Kyin, W. Zuo, D. A. Robinson, P. J. Alaimo, C. Zhang, H. Morimoto, et al. (2003)
PNAS 100, 4287-4292
   Abstract »    Full Text »    PDF »
One Hundred Years of Mouse Genetics: An Intellectual History. II. The Molecular Revolution (1981-2002).
K. Paigen (2003)
Genetics 163, 1227-1235
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An In Vivo Doxycycline-Controlled Expression System for Functional Studies of the Retina.
B. Angeletti, J. Loster, A. Auricchio, F. Gekeler, K. Shinoda, A. Ballabio, J. Graw, and V. Marigo (2003)
Invest. Ophthalmol. Vis. Sci. 44, 755-760
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Memory-specific temporal profiles of gene expression in the hippocampus.
S. Cavallaro, V. D'Agata, P. Manickam, F. Dufour, and D. L. Alkon (2002)
PNAS 99, 16279-16284
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Stringent doxycycline dependent control of CRE recombinase in vivo.
K. Schonig, F. Schwenk, K. Rajewsky, and H. Bujard (2002)
Nucleic Acids Res. 30, e134
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Analysis of Transcriptional Regulatory Sequences of the N-Methyl-D-aspartate Receptor 2A Subunit Gene in Cultured Cortical Neurons and Transgenic Mice.
A. Desai, D. Turetsky, K. Vasudevan, and A. Buonanno (2002)
J. Biol. Chem. 277, 46374-46384
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Overexpression of motor protein KIF17 enhances spatial and working memory in transgenic mice.
R. W.-C. Wong, M. Setou, J. Teng, Y. Takei, and N. Hirokawa (2002)
PNAS 99, 14500-14505
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