NF-κB Regulates Spatial Memory Formation and Synaptic Plasticity through Protein Kinase A/CREB Signaling

REFERENCES

• Abel, T., P. V. Nguyen, M. Barad, T. A. Deuel, E. R. Kandel, and R. Bourtchouladze. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615–626.
   PubMed Web of Science ®Google Scholar
• Albensi, B. C., and M. P. Mattson. 2000. Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 35:151–159.
   PubMed Web of Science ®Google Scholar
• Balschun, D., D. P. Wolfer, P. Gass, T. Mantamadiotis, H. Welzl, G. Schutz, J. U. Frey, and H. P. Lipp. 2003. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J. Neurosci. 23:6304–6314.
   PubMedGoogle Scholar
• Barco, A., J. M. Alarcon, and E. R. Kandel. 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689–703.
   PubMed Web of Science ®Google Scholar
• Bhakar, A. L., L. L. Tannis, C. Zeindler, M. P. Russo, C. Jobin, D. S. Park, S. MacPherson, and P. A. Barker. 2002. Constitutive nuclear factor-κB activity is required for central neuron survival. J. Neurosci. 22:8466–8475.
   PubMed Web of Science ®Google Scholar
• Bito, H., K. Deisseroth, and R. W. Tsien. 1996. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203–1214.
   PubMed Web of Science ®Google Scholar
• Bliss, T. V. P., and G. L. Collingridge. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39.
   PubMed Web of Science ®Google Scholar
• Bonizzi, G., and M. Karin. 2004. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25:280–288.
   PubMed Web of Science ®Google Scholar
• Chavez-Noriega, L. E., and C. F. Stevens. 1992. Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin. Brain Res. 574:85–92.
   PubMedGoogle Scholar
• Cruise, L., L. K. Ho, K. Veitch, G. Fuller, and B. J. Morris. 2000. Kainate receptors activate NF-κB via MAP kinase in striatal neurones. Neuroreport 11:395–398.
   PubMedGoogle Scholar
• Dierich, A., M. P. Gaub, J. P. LePennec, D. Astinotti, and P. Chambon. 1987. Cell specificity of the chicken ovalbumin and conalbumin promoters. EMBO J. 6:2305–2312.
   PubMed Web of Science ®Google Scholar
• Duffy, S. N., and P. V. Nguyen. 2003. Postsynaptic application of a peptide inhibitor of cAMP-dependent protein kinase blocks expression of long-lasting synaptic potentiation in hippocampal neurons. J. Neurosci. 23:1142–1150.
   PubMedGoogle Scholar
• Eriksson, P. S., E. Perfilieva, T. Bjork-Eriksson, A. M. Alborn, C. Nordborg, D. A. Peterson, and F. H. Gage. 1998. Neurogenesis in the adult human hippocampus. Nat. Med. 4:1313–1317.
   PubMed Web of Science ®Google Scholar
• Freudenthal, R., M. M. Boccia, G. B. Acosta, M. G. Blake, E. Merlo, C. M. Baratti, and A. Romano. 2005. NF-κB transcription factor is required for inhibitory avoidance long-term memory in mice. Eur. J. Neurosci. 21:2845–2852.
   PubMedGoogle Scholar
• Freudenthal, R., and A. Romano. 2000. Participation of Rel/NF-κB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res. 855:274–281.
   PubMed Web of Science ®Google Scholar
• Freudenthal, R., A. Romano, and A. Routtenberg. 2004. Transcription factor NF-κB activation after in vivo perforant path LTP in mouse hippocampus. Hippocampus 14:677–683.
   PubMedGoogle Scholar
• Fridmacher, V., B. Kaltschmidt, B. Goudeau, D. Ndiaye, F. M. Rossi, J. Pfeiffer, C. Kaltschmidt, A. Israel, and S. Mémet. 2003. Forebrain-specific neuronal inhibition of nuclear factor-κB activity leads to loss of neuroprotection. J. Neurosci. 23:9403–9408.
   PubMed Web of Science ®Google Scholar
• Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109(Suppl.):S81–S96.
   PubMed Web of Science ®Google Scholar
• Goudeau, B., F. Huetz, S. Samson, J. P. Di Santo, A. Cumano, A. Beg, A. Israël, and S. Mémet. 2003. IκBα/IκBε deficiency reveals that a critical NF-κB dosage is required for lymphocyte survival. Proc. Natl. Acad. Sci. USA 100:15800–15805.
   PubMedGoogle Scholar
• Hammond, R. S., L. E. Tull, and R. W. Stackman. 2004. On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol. Learn Mem. 82:26–34.
   PubMed Web of Science ®Google Scholar
• Huber, K. M., M. S. Kayser, and M. F. Bear. 2000. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254–1257.
   PubMed Web of Science ®Google Scholar
• Kaltschmidt, B., M. Uherek, H. Wellmann, B. Volk, and C. Kaltschmidt. 1999. Inhibition of NF-κB potentiates amyloid beta-mediated neuronal apoptosis. Proc. Natl. Acad. Sci. USA 96:9409–9414.
   PubMed Web of Science ®Google Scholar
• Kaltschmidt, C., B. Kaltschmidt, and P. A. Baeuerle. 1993. Brain synapses contain inducible forms of the transcription factor NF-κB. Mech. Dev. 43:135–147.
   PubMedGoogle Scholar
• Kaltschmidt, C., B. Kaltschmidt, and P. A. Baeuerle. 1995. Stimulation of ionotropic glutamate receptors activates transcription factor NF-κB in primary neurons. Proc. Natl. Acad. Sci. USA 92:9618–9622.
   PubMedGoogle Scholar
• Kaltschmidt, C., B. Kaltschmidt, H. Neumann, H. Wekerle, and P. A. Baeuerle. 1994. Constitutive NF-κB activity in neurons. Mol. Cell. Biol. 14:3981–3992.
   PubMed Web of Science ®Google Scholar
• Kandel, E. R. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038.
   PubMed Web of Science ®Google Scholar
• Kassed, C. A., A. E. Willing, S. Garbuzova-Davis, P. R. Sanberg, and K. R. Pennypacker. 2002. Lack of NF-κB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning. Exp. Neurol. 176:277–278.
   PubMed Web of Science ®Google Scholar
• Kemp, N., and Z. I. Bashir. 1997. A role for adenosine in the regulation of long-term depression in the adult rat hippocampus in vitro. Neurosci. Lett. 225:189–192.
   PubMedGoogle Scholar
• Korte, M., P. Carroll, E. Wolf, G. Brems, H. Thoenen, and T. Bonhoeffer. 1995. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92:8856–8860.
   PubMed Web of Science ®Google Scholar
• Levenson, J. M., S. Choi, S. Y. Lee, Y. A. Cao, H. J. Ahn, K. C. Worley, M. Pizzi, H. C. Liou, and J. D. Sweatt. 2004. A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-Rel. J. Neurosci. 24:3933–3943.
   PubMedGoogle Scholar
• Li, Q., and I. M. Verma. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2:725–734.
   PubMed Web of Science ®Google Scholar
• Lilienbaum, A., and A. Israël. 2003. From calcium to NF-κB signaling pathways in neurons. Mol. Cell. Biol. 23:2680–2698.
   PubMed Web of Science ®Google Scholar
• Liu, L., T. P. Wong, M. F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y. P. Auberson, and Y. T. Wang. 2004. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:973–974.
   PubMedGoogle Scholar
• Mantamadiotis, T., T. Lemberger, S. C. Bleckmann, H. Kern, O. Kretz, A. Martin Villalba, F. Tronche, C. Kellendonk, D. Gau, J. Kapfhammer, C. Otto, W. Schmid, and G. Schutz. 2002. Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31:47–54.
   PubMed Web of Science ®Google Scholar
• Martin, S. J., P. D. Grimwood, and R. G. M. Morris. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23:649–711.
   PubMed Web of Science ®Google Scholar
• Mattson, M. P., and S. Camandola. 2001. NF-κB in neuronal plasticity and neurodegenerative disorders. J. Clin. Investig. 107:247–254.
   PubMed Web of Science ®Google Scholar
• Mattson, M. P., Y. Goodman, H. Luo, W. Fu, and K. Furukawa. 1997. Activation of NF-κB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49:681–697.
   PubMed Web of Science ®Google Scholar
• Matynia, A., S. A. Kushner, and A. J. Silva. 2002. Genetic approaches to molecular and cellular cognition: a focus on LTP and learning and memory. Annu. Rev. Genet. 36:687–720.
   PubMedGoogle Scholar
• Mayford, M., M. E. Bach, Y. Y. Huang, L. Wang, R. D. Hawkins, and E. R. Kandel. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678–1683.
   PubMed Web of Science ®Google Scholar
• Mayford, M., and E. R. Kandel. 1999. Genetic approaches to memory storage. Trends Genet. 15:463–470.
   PubMed Web of Science ®Google Scholar
• Meberg, P. J., W. R. Kinney, E. G. Valcourt, and A. Routtenberg. 1996. Gene expression of the transcription factor NF-κB in hippocampus: regulation by synaptic activity. Mol. Brain Res. 38:179–190.
   PubMedGoogle Scholar
• Meffert, M. K., and D. Baltimore. 2005. Physiological functions for brain NF-κB. Trends Neurosci. 28:37–43.
   PubMed Web of Science ®Google Scholar
• Meffert, M. K., J. M. Chang, B. J. Wiltgen, M. S. Fanselow, and D. Baltimore. 2003. NF-κB functions in synaptic signaling and behavior. Nat. Neurosci. 6:1072–1078.
   PubMed Web of Science ®Google Scholar
• Mémet, S., D. Laouini, J.-C. Epinat, S. T. Whiteside, B. Goudeau, D. Philpott, S. Kayal, P. J. Sansonetti, P. Berche, J. Kanellopoulos, and A. Israël. 1999. IκBε-deficient mice: reduction of one T cell precursor sub-species, and enhanced Ig isotype switching and cytokine synthesis. J. Immunol. 163:5994–6005.
   PubMed Web of Science ®Google Scholar
• Merlo, E., R. Freudenthal, H. Maldonado, and A. Romano. 2005. Activation of the transcription factor NF-κB by retrieval is required for long-term memory reconsolidation. Learn Mem. 12:23–29.
   PubMedGoogle Scholar
• Minichiello, L., A. M. Calella, D. L. Medina, T. Bonhoeffer, R. Klein, and M. Korte. 2002. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36:121–137.
   PubMed Web of Science ®Google Scholar
• Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:5322.
   PubMed Web of Science ®Google Scholar
• O'Neill, L. A., and C. Kaltschmidt. 1997. NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20:252–258.
   PubMed Web of Science ®Google Scholar
• Pittenger, C., Y. Y. Huang, R. F. Paletzki, R. Bourtchouladze, H. Scanlin, S. Vronskaya, and E. R. Kandel. 2002. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34:447–462.
   PubMed Web of Science ®Google Scholar
• Saura, C. A., S. Y. Choi, V. Beglopoulos, S. Malkani, D. Zhang, B. S. Shankaranarayana Rao, S. Chattarji, R. J. Kelleher III, E. R. Kandel, K. Duff, A. Kirkwood, and J. Shen. 2004. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42:23–36.
   PubMed Web of Science ®Google Scholar
• Schmidt-Ullrich, R., S. Mémet, A. Lilienbaum, J. Feuillard, M. Raphael, and A. Israël. 1996. NF-κB activity in transgenic mice: developmental regulation and tissue specificity. Development 122:2117–2128.
   PubMedGoogle Scholar
• Schwamborn, J., A. Lindecke, M. Elvers, V. Horejschi, M. Kerick, M. Rafigh, J. Pfeiffer, M. Prullage, B. Kaltschmidt, and C. Kaltschmidt. 2003. Microarray analysis of tumor necrosis factor alpha induced gene expression in U373 human glioblastoma cells. BMC Genomics 4:46.
   PubMedGoogle Scholar
• Silva, A. J., J. H. Kogan, P. W. Frankland, and S. Kida. 1998. CREB and memory. Annu. Rev. Neurosci. 21:127–148.
   PubMed Web of Science ®Google Scholar
• Thierry, F., G. Spyrou, M. Yaniv, and P. Howley. 1992. Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J. Virol. 66:3740–3748.
   PubMedGoogle Scholar
• Vincent, S., L. Marty, and P. Fort. 1993. S26 ribosomal protein RNA: an invariant control for gene regulation experiments in eucaryotic cells and tissues. Nucleic Acids Res. 21:1498.
   PubMedGoogle Scholar
• Wellmann, H., B. Kaltschmidt, and C. Kaltschmidt. 2001. Retrograde transport of transcription factor NF-κB in living neurons. J. Biol. Chem. 276:11821–11829.
   PubMedGoogle Scholar
• West, A. E., E. C. Griffith, and M. E. Greenberg. 2002. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3:921–931.
   PubMed Web of Science ®Google Scholar
• Yeh, S. H., C. H. Lin, and P. W. Gean. 2004. Acetylation of nuclear factor-κB in rat amygdala improves long-term but not short-term retention of fear memory. Mol. Pharmacol. 65:1286–1292.
   PubMed Web of Science ®Google Scholar
• Yeh, S. H., C. H. Lin, C. F. Lee, and P. W. Gean. 2002. A requirement of nuclear factor-κB activation in fear-potentiated startle. J. Biol. Chem. 277:46720–46729.
   PubMedGoogle Scholar
• Zhong, H. H., H. Suyang, H. Erdjument Bromage, P. Tempst, and S. Ghosh. 1997. The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell 89:413–424.
   PubMed Web of Science ®Google Scholar
• Zhong, H. H., R. E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1:661–671.
   PubMed Web of Science ®Google Scholar
• Zucker, R. S. 1989. Short-term synaptic plasticity. Annu. Rev. Neurosci. 12:13–31.
   PubMed Web of Science ®Google Scholar