CREB is necessary for synaptic maintenance and learning-induced changes of the ampa receptor GluA1 subunit

Hippocampus

Volumn 23, Issue 6, 2013, Pages 488-499

  Middei, Silvia ^a   Houeland, Gry ^b   Cavallucci, Virve ^a   Ammassari Teule, Martine ^a   D'Amelio, Marcello ^a,c   Marie, Hélène ^b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

Glutamatergic receptors; Hippocampus; Memory formation; Synaptic plasticity; Transcription factor

Indexed keywords

AMPA RECEPTOR; AMPA RECEPTOR GLUA1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOXYCYCLINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SYNAPSE;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HIPPOCAMPUS; LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN SUBUNITS; RECEPTORS, AMPA; SYNAPSES;

EID: 84878192270     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22108     Document Type: Article

References (36)

1. Barco A, Marie H. 2011. Genetic approaches to investigate the role of CREB in neuronal plasticity and memory. Mol Neurobiol 44:330-349.
2. Barco A, Alarcon JM, Kandel ER. 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689-703.
3. Bramham CR, Worley PF, Moore MJ, Guzowski JF. 2008. The immediate early gene arc/arg3.1: Regulation, mechanisms, and function. J Neurosci 28:11760-11767.
4. Caldeira MV, Melo CV, Pereira DB, Carvalho R, Correia SS, Backos DS, Carvalho AL, Esteban JA, Duarte CB. 2007. Brain-derived neurotrophic factor regulates the expression and synaptic delivery of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J Biol Chem 282:12619-12628.
5. Carlezon WA, Duman RS, Nestler EJ. 2005. The many faces of CREB. Trends Neurosci 28:436-445.
6. Cingolani LA, Goda Y. 2008. Actin in action: The interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344-356.
7. D'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, Ferri A, Diamantini A, De ZD, Carrara P, Battistini L, Moreno S, Bacci A, Ammassari-Teule M, Marie H, Cecconi F. 2011. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 14:69-76.
8. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC. 2006. CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9:475-477.
9. Han MH, Bolanos CA, Green TA, Olson VG, Neve RL, Liu RJ, Aghajanian GK, Nestler EJ. 2006. Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. J Neurosci 26:4624-4629.
10. Huang YH, Lin Y, Brown TE, Han MH, Saal DB, Neve RL, Zukin RS, Sorg BA, Nestler EJ, Malenka RC, Dong Y. 2008. CREB modulates the functional output of nucleus accumbens neurons: a critical role of N-methyl-D-aspartate glutamate receptor (NMDAR) receptors. J Biol Chem 283:2751-2760.
11. Huang YY, Pittenger C, Kandel ER. 2004. A form of long-lasting, learning-related synaptic plasticity in the hippocampus induced by heterosynaptic low-frequency pairing. Proc Natl Acad Sci USA 101:859-864.
12. Jancic D, Lopez de AM, Valor LM, Olivares R, Barco A. 2009. Inhibition of cAMP response element-binding protein reduces neuronal excitability and plasticity, and triggers neurodegeneration. Cereb. Cortex 19:2535-2547.
13. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J. 2010. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129.
14. Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M, Takemoto-Kimura S, Worley PF, Bito H. 2009. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci USA 106, 316-321.
15. Kida S, Josselyn SA, Pena de OS, Kogan JH, Chevere I, Masushige S, Silva AJ. 2002. CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348-355.
16. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL. 2000. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955-959.
17. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, Petralia RS, Wenthold RJ, Gallagher M, Huganir RL. 2003. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112:631-643.
18. Lopez de Armentia M, Jancic D, Olivares R, Alarcon JM, Kandel ER, Barco A. 2007. cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J Neurosci 27:13909-13918.
19. Lu W, Roche KW. 2012. Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol 22:470-479.
20. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA. 2009. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62:254-268.
21. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
22. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S. 2009. Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402-413.
23. Marchetti C, Tafi E, Marie H. 2011. Viral-mediated expression of a constitutively active form of cAMP response element binding protein in the dentate gyrus increases long term synaptic plasticity. Neuroscience 190:21-26.
24. Marchetti C, Tafi E, Middei S, Rubinacci MA, Restivo L, Ammassari-Teule M, Marie H. 2010. Synaptic adaptations of CA1 pyramidal neurons induced by a highly effective combinational antidepressant therapy. Biol Psychiatry 67:146-154.
25. Marie H, Morishita W, Yu X, Calakos N, Malenka RC. 2005. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741-752.
26. Matsuo N, Reijmers L, Mayford M. 2008. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319:1104-1107.
27. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
28. Middei S, Spalloni A, Longone P, Pittenger C, O'Mara SM, Marie H, Ammassari-Teule M. 2012. CREB selectively controls learning-induced structural remodeling of neurons. Learn Mem 19, 330-336.
29. Newton SS, Thome J, Wallace TL, Shirayama Y, Schlesinger L, Sakai N, Chen J, Neve R, Nestler EJ, Duman RS. 2002. Inhibition of cAMP response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J Neurosci 22:10883-10890.
30. Pittenger C, Huang YY, Paletzki RF, Bourtchouladze R, Scanlin H, Vronskaya S, Kandel ER. 2002. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447-462.
31. Restivo L, Tafi E, Ammassari-Teule M, Marie H. 2009. Viral-mediated expression of a constitutively active form of CREB in hippocampal neurons increases memory. Hippocampus 19:228-234.
32. Rumpel S, LeDoux J, Zador A, Malinow R. 2005. Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83-88.
33. Sekeres MJ, Neve RL, Frankland PW, Josselyn SA. 2010. Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. Learn Mem 17:280-283.
34. Shieh PB, Hu SC, Bobb K, Timmusk T, Ghosh A. 1998. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20:727-740.
35. Viosca J, Lopez de AM, Jancic D, Barco A. 2009. Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. Learn Mem 16:193-197.
36. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ. 2009. CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12:1438-1443.