Hippocampal dynamics of synaptic NF-kappa B during inhibitory avoidance long-term memory consolidation in mice

Neuroscience

Volumn 291, Issue , 2015, Pages 70-80

  Salles, A ^a   Boccia, M ^b   Blake, M ^b   Corbi, N ^c   Passananti, C ^c   Baratti, C M ^b   Romano, A ^a   Freudenthal, R ^a  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

I kappa B alpha; Memory consolidation; NF kappa B; Synapse

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNAPTIC MEMBRANE; SYNAPTOPLASM; ANIMAL; CELL NUCLEUS; DENDRITE; ELECTRIC SHOCK; FLUORESCENT ANTIBODY TECHNIQUE; FOOT; METABOLISM; OUTBRED STRAIN; PHYSIOLOGY; SYNAPSE; SYNAPTOSOME; WESTERN BLOTTING;

ANIMALS; ANIMALS, OUTBRED STRAINS; AVOIDANCE LEARNING; BLOTTING, WESTERN; CELL NUCLEUS; DENDRITES; ELECTROSHOCK; FLUORESCENT ANTIBODY TECHNIQUE; FOOT; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MICE; NF-KAPPA B; SYNAPSES; SYNAPTOSOMES; TRANSCRIPTION FACTOR RELA;

EID: 84939433766     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.01.063     Document Type: Article

References (43)

1. Agranoff B.W., Davis R.E., Brink J.J. Chemical studies on memory fixation in goldfish. Brain Res 1966, 1:303-309.
2. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 2009, 89:1.
3. Baeuerle P.A., Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell 1988, 53:211-217.
4. Boccia M., Freudenthal R., Blake M., de la Fuente V., Acosta G., Baratti C., Romano A. Activation of hippocampal nuclear factor-kappa B by retrieval is required for memory reconsolidation. J Neurosci 2007, 27:13436-13445. 10.1523/JNEUROSCI.4430-07.2007.
5. Boccia M.M., Acosta G.B., Blake M.G., Baratti C.M. Memory consolidation and reconsolidation of an inhibitory avoidance response in mice: effects of i.c.v. injections of hemicholinium-3. Neuroscience 2004, 124:735-741. 10.1016/j.neuroscience.2004.01.001.
6. Boersma M.C.H., Dresselhaus E.C., De Biase L.M., Mihalas A.B., Bergles D.E., Meffert M.K. A requirement for nuclear factor-kappaB in developmental and plasticity-associated synaptogenesis. J Neurosci 2011, 31:5414-5425. 10.1523/JNEUROSCI.2456-10.2011.
7. Davis H.P., Squire L.R. Protein synthesis and memory: a review. Psychol Bull 1984, 96:518-559.
8. Freudenthal R., Boccia M.M., Acosta G.B., Blake M.G., Merlo E., Baratti C.M., Romano A. NF-kappaB transcription factor is required for inhibitory avoidance long-term memory in mice. Eur J Neurosci 2005, 21:2845-2852. 10.1111/j.1460-9568.2005.04126.x.
9. Freudenthal R., Romano A. Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res. 2000, 855:274-281.
10. Freudenthal R., Romano A., Routtenberg A. Transcription factor NF-kappaB activation after in vivo perforant path LTP in mouse hippocampus. Hippocampus 2004, 14:677-683. 10.1002/hipo.20020.
11. Glowinski J., Iversen L. Regional studies of catecholamines in the rat brain. 3. Subcellullar distribution of endogenous and exogenous catecholamines in various brain regions. Biochem Pharmacol 1966, 15:977-987.
12. Heckscher E.S., Fetter R.D., Marek K.W., Albin S.D., Davis G.W. NF-kappaB, IkappaB, and IRAK control glutamate receptor density at the Drosophila NMJ. Neuron 2007, 55:859-873. 10.1016/j.neuron.2007.08.005.
13. Huxford T., Huang D.B., Malek S., Ghosh G. The crystal structure of the IkappaBalpha/NF-kappaB complex reveals mechanisms of NF-kappaB inactivation. Cell 1998, 95(6):759-770.
14. Kaltschmidt B., Kaltschmidt C. Constitutive NF-kappa B activity is modulated via neuron-astroglia interaction. Exp Brain Res 2000, 130:100-104.
15. Kaltschmidt B., Kaltschmidt C. DNA array analysis of the developing rat cerebellum: transforming growth factor-beta2 inhibits constitutively activated NF-kappaB in granule neurons. Mech Dev 2001, 101:11-19.
16. Kaltschmidt B., Kaltschmidt C. NF-kappaB in the nervous system. Cold Spring Harb Perspect Biol 2009, 1:a001271. 10.1101/cshperspect.a001271.
17. Kaltschmidt C., Kaltschmidt B., Baeuerle P.A. Brain synapses contain inducible forms of the transcription factor NF-kappa B. Mech Dev 1993, 43:135-147.
18. Kaltschmidt C., Kaltschmidt B., Neumann H., Wekerle H., Baeuerle P.A. Constitutive NF-kappa B activity in neurons. Mol Cell Biol 1994, 14:3981-3992.
19. Landeira-Fernandez J., DeCola J.P., Kim J.J., Fanselow M.S. Immediate shock deficit in fear conditioning: effects of shock manipulations. Behav Neurosci 2006, 120:873-879. 10.1037/0735-7044.120.4.873.
20. Malek S., Huxford T., Ghosh G. Ikappa B alpha functions through direct contacts with the nuclear localization signals and the DNA binding sequences of NF-kappaB. J Biol Chem 1998, 273(39):25427-25435.
21. Meberg P.J., Kinney W.R., Valcourt E.G., Routtenberg A. Gene expression of the transcription factor NF-kappa B in hippocampus: regulation by synaptic activity. Brain Res Mol Brain Res 1996, 38:179-190.
22. Meffert M.K., Baltimore D. Physiological functions for brain NF-kappaB. Trends Neurosci 2005, 28:37-43. 10.1016/j.tins.2004.11.002.
23. Meffert M.K., Chang J.M., Wiltgen B.J., Fanselow M.S., Baltimore D. NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci 2003, 6:1072-1078. 10.1038/nn1110.
24. Merlo E., Freudenthal R., Romano A. The IkappaB kinase inhibitor sulfasalazine impairs long-term memory in the crab Chasmagnathus. Neuroscience 2002, 112:161-172.
25. Mindorff E.N., O'Keefe D.D., LabbÈ A., Yang J.P., Ou Y., Yoshikawa S., van Meyel D.J. A gain-of-function screen for genes that influence axon guidance identifies the NF-kappaB protein dorsal and reveals a requirement for the kinase Pelle in Drosophila photoreceptor axon targeting. Genetics 2007, 176:2247-2263. 10.1534/genetics.107.072819.
26. Murata S., Usuda N., Okano A., Kobayashi S., Suzuki T. Occurrence of a transcription factor, signal transducer and activators of transcription 3 (Stat3), in the postsynaptic density of the rat brain. Brain Res Mol Brain Res 2000, 78:80-90.
27. Nagy A., Delgado-Escueta A.V. Rapid preparation of synaptosomes from mammalian brain using nontoxic isoosmotic gradient material (Percoll). J Neurochem 1984, 43:1114-1123.
28. O'Sullivan N.C., McGettigan P.A., Sheridan G.K., Pickering M., Conboy L., O'Connor J.J., Moynagh P.N., Higgins D.G., Regan C.M., Murphy K.J. Temporal change in gene expression in the rat dentate gyrus following passive avoidance learning. J Neurochem 2007, 101:1085-1098. 10.1111/j.1471-4159.2006.04418.x.
29. Ohkawa N., Sugisaki S., Tokunaga E., Fujitani K., Hayasaka T., Setou M., Inokuchi K. N-acetyltransferase ARD1-NAT1 regulates neuronal dendritic development. Genes Cells Devoted Mol Cell Mech 2008, 13:1171-1183. 10.1111/j.1365-2443.2008.01235.x.
30. Oikawa K., Odero G.L., Platt E., Neuendorff M., Hatherell A., Bernstein M.J., Albensi B.C. NF-κB p50 subunit knockout impairs late LTP and alters long term memory in the mouse hippocampus. BMC Neurosci 2012, 13:45. 10.1186/1471-2202-13-45.
31. Rodrigues R.J., Alfaro T.M., Rebola N., Oliveira C.R., Cunha R.A. Co-localization and functional interaction between adenosine A(2A) and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum. J Neurochem 2005, 92:433-441. 10.1111/j.1471-4159.2004.02887.x.
32. Romano A., Freudenthal R., Merlo E., Routtenberg A. Evolutionarily-conserved role of the NF-kappaB transcription factor in neural plasticity and memory. Eur J Neurosci 2006, 24:1507-1516. 10.1111/j.1460-9568.2006.05022.x.
33. Russo S.J., Wilkinson M.B., Mazei-Robison M.S., Dietz D.M., Maze I., Krishnan V., Renthal W., Graham A., Birnbaum S.G., Green T.A., Robison B., Lesselyong A., Perrotti L.I., BolaÒos C.A., Kumar A., Clark M.S., Neumaier J.F., Neve R.L., Bhakar A.L., Barker P.A., Nestler E.J. Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J Neurosci 2009, 29:3529-3537. 10.1523/JNEUROSCI.6173-08.2009.
34. Ryan M.M., Ryan B., Kyrke-Smith M., Logan B., Tate W.P., Abraham W.C., Williams J.M. Temporal profiling of gene networks associated with the late phase of long-term potentiation in vivo. PloS One 2012, 7:e40538. 10.1371/journal.pone.0040538.
35. Schmeisser M.J., Baumann B., Johannsen S., Vindedal G.F., Jensen V., Hvalby O.C., Sprengel R., Seither J., Maqbool A., Magnutzki A., Lattke M., Oswald F., Boeckers T.M., Wirth T. IκB kinase/nuclear factor κB-dependent insulin-like growth factor 2 (Igf2) expression regulates synapse formation and spine maturation via Igf2 receptor signaling. J Neurosci 2012, 32:5688-5703. 10.1523/JNEUROSCI.0111-12.2012.
36. Sgambato V., Vanhoutte P., PagËs C., Rogard M., Hipskind R., Besson M.J., Caboche J. In vivo expression and regulation of Elk-1, a target of the extracellular-regulated kinase signaling pathway, in the adult rat brain. J Neurosci 1998, 18:214-226.
37. Sulejczak D., Skup M. Axoplasmic localisation of the NF kappa B p65 subunit in the rat brain. Acta Neurobiol Exp (Warsz) 2000, 60:217.
38. Suzuki T., Mitake S., Okumura-Noji K., Yang J.P., Fujii T., Okamoto T. Presence of NF-kappaB-like and IkappaB-like immunoreactivities in postsynaptic densities. Neuroreport 1997, 8:2931-2935.
39. Suzuki T., Usuda N., Ishiguro H., Mitake S., Nagatsu T., Okumura-Noji K. Occurrence of a transcription factor, cAMP response element-binding protein (CREB), in the postsynaptic sites of the brain. Mol Brain Res 1998, 61:69-77. 10.1016/S0169-328X(98)00199-5.
40. Tomita S., Fujita T., Kirino Y., Suzuki T. PDZ domain-dependent suppression of NF-kappaB/p65-induced Abeta42 production by a neuron-specific X11-like protein. J Biol Chem 2000, 275:13056-13060.
41. Wellmann H., Kaltschmidt B., Kaltschmidt C. Retrograde transport of transcription factor NF-kappa B in living neurons. J Biol Chem 2001, 276:11821-11829. 10.1074/jbc.M009253200.
42. Xu H., Jiang B., Meng L., Ren T., Zeng Y., Wu J., Qu L., Shou C. N-α-acetyltransferase 10 protein inhibits apoptosis through RelA/p65-regulated MCL1 expression. Carcinogenesis 2012, 33:1193-1202. 10.1093/carcin/bgs144.
43. Zhong H., Voll R.E., Ghosh S. Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1998, 1:661-671.