Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5525-5535

  Krucker, Thomas ^a   Siggins, George R ^a   McNamara, Robert K ^b   Lindsley, Kristen A ^a   Dao, Alan ^a   Allison, David W ^a   De Lecea, Luis ^a   Lovenberg, Timothy W ^a   Sutcliffe, J Gregor ^a   Gerendasy, Dan D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Calcium; CaMKII; Dendrite; Dendritic spine; Depotentiation; Frequency response; LTD; LTP; Metaplasticity; mGluR; Molecular switch; Neurogranin; Neuroplasticity; PKC ; Postsynaptic; Priming

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; CALMODULIN; CALMODULIN BINDING PROTEIN; CALMODULIN DEPENDENT PROTEIN KINASE II; GLUTAMATE RECEPTOR AGONIST; METABOTROPIC RECEPTOR AGONIST; NEUROGRANIN; PROTEIN KINASE C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPRESSION; ENZYME BINDING; ENZYME MECHANISM; ENZYME SUBSTRATE; GENE DISRUPTION; GENE MUTATION; GENE TARGETING; GENETIC RECOMBINATION; HIPPOCAMPUS; IMMUNOREACTIVITY; KNOCKOUT MOUSE; LONG TERM POTENTIATION; METAPLASIA; MOUSE; NEUROANATOMY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPTIC MEMBRANE; WILD TYPE;

EID: 0036662781     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05525.2002     Document Type: Article

References (30)

1. Abraham WC, Bear MF (1996) Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
2. Abraham WC, Tate WP (1997) Metaplasticity: A new vista across the field of synaptic plasticity. Prog Neurobiol 52:303-323.
3. Artola A, Brocher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69-72.
4. Bear MF, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev Neurosci 19:437-462.
5. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48.
6. Dudek SM, Bear MF (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13:2910-2918.
7. 2+ signal transduction by members of the calpacitin protein family. J Neurosci Res 58:107-119.
8. Gerendasy DD, Sutcliffe JG (1997) RC3/neurogranin, a postsynaptic calpacitin for setting the response threshold to calcium influxes. Mol Neurobiol 15:131-163.
9. Gerendasy DD, Herron SR, Watson JB, Sutcliffe JG (1994a) Mutational and biophysical studies suggest RC3/neurogranin regulates calmodulin availability. J Biol Chem 269:22420-22426.
10. Gerendasy DD, Herron SR, Wong KK, Watson JB, Sutcliffe JG (1994b) Rapid purification, site-directed mutagenesis, and initial characterization of recombinant RC3/neurogranin. J Mol Neurosci 5:133-148.
11. 2+ is absent. J Biol Chem 270:6741-6750.
12. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP, learning. Science 279:870-873.
13. Hogan B, Beddington R, Constantini F, Lacy E (1994) Manipulating the Mouse Embryo: A Laboratory Manual. Plainview, NY: Cold Spring Harbor Laboratory.
14. Holland LL, Wagner JJ (1998) Primed facilitation of homosynaptic long-term depression and depotentiation in rat hippocampus. J Neurosci 18:887-894.
15. Huang KP, Huang FL, Chen HC (1993) Characterization of a 7.5-kDa protein kinase C substrate (RC3 protein, neurogranin) from rat brain. Arch Biochem Biophys 305:570-580.
16. Joyner AL (1993) Gene Targeting: A Practical Approach. Oxford: IRL.
17. Krucker T, Toggas SM, Mucke L, Siggins GR (1998) Transgenic mice with cerebral expression of human immunodeficiency virus type-1 coat protein gp120 show divergent changes in short- and long-term potentiation in CA1. Neuroscience 83:691-700.
18. Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97:6856-6861.
19. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
20. Mayford M, Wang J, Kandel ER, O'Dell TJ (1995) CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD, LTP. Cell 81:891-904.
21. McNamara RK, Lenox RH (1997) Comparative distribution of myristoylated alanine-rich C kinase substrate (MARCKS) and F1/GAP-43 gene expression in the adult rat brain. J Comp Neurol 379:48-71.
22. McNamara RK, Namgung U, Routtenberg A (1996) Distinctions between hippocampus of mouse and rat: Protein F1/GAP-43 gene expression, promoter activity, and spatial memory. Brain Res Mol Brain Res 40:177-187.
23. Meyer T, Hanson PI, Stryer L, Schulman H (1992) Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256:1199-1202.
24. Pak JH, Huang FL, Li J, Balschun D, Reymann KG, Chiang C, Westphal H, Huang KP (2000) Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: A study with knockout mice. Proc Natl Acad Sci USA 97:11232-11237.
25. Ramakers GM, Gerendasy DD, De Graan PN (1999) Substrate phosphorylation in the protein kinase Cγ knockout mouse. J Biol Chem 274:1873-1874.
26. Schnabel R, Palmer MJ, Kilpatrick IC, Collingridge GL (1999) A CaMKII inhibitor, KN-62, facilitates DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 38:605-608.
27. Silva AJ, Stevens CF, Tonegawa S, Wang Y (1992) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257:201-206.
28. Wagner JJ, Alger BE (1996) Homosynaptic LTD, depotentiation: Do they differ in name only? Hippocampus 6:24-29.
29. Watson JB, Battenberg EF, Wong KK, Bloom FE, Sutcliffe JG (1990) Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein. J Neurosci Res 26:397-408.
30. Zhuo M, Zhang W, Son H, Mansuy I, Sobel RA, Seidman J, Kandel ER (1999) A selective role of calcineurin Aα in synaptic depotentiation in hippocampus. Proc Natl Acad Sci USA 96:4650-4655.