Abstract
Transcription and translation are required for consolidation of long-lasting changes in synaptic function and are required for learning and memory. The targets of activity-dependent transcription in neurons have been of great interest. Despite this, the ultimate consequences of an activity-dependent change in programs of gene expression with respect to neural function have been surprisingly elusive. For example, experimental data have not clearly established how gene expression is required for memory-associated events, such as synapse-specific strengthening or changes in the input-output function of the neuron. Many activity-regulated genes are transcriptional factors which themselves modify programs of downstream gene expression, and the short- and long-term consequences of these changes in gene expression remain largely unknown. Although there have been many complementary approaches to experimentally and computationally define the plasticity transcriptome, the specific gene targets that have been identified using different experimental approaches show surprisingly little overlap. The purpose of this review is three-fold: 1) to discuss what is known about activity-dependent transcription during learning, 2) to review efforts to identify genes in the plasticity transcriptome, and 3) to develop a hypothesis about how transcription might be required for information coding at the synaptic and cellular level.
Keywords
- Monocular Deprivation
- Dependent Gene Expression
- Silent Synapse
- CREB Binding Site
- CREB Target Gene
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Babity, J. M., Armstrong, J. N., Plumier, J. C., Currie, R. W., and Robertson, H. A. (1997) A novel seizure-induced synaptotagmin gene identified by differential display. Proc. Natl. Acad. Sci. USA 94, 2638–2641.
Banerjee, P. K., Tillakaratne, N. J., Brailowsky, S., Olsen, R. W., Tobin, A. J., and Snead, O. C., 3rd (1998) Alterations in GABAA receptor alpha 1 and alpha 4 subunit mRNA levels in thalamic relay nuclei following absence-like seizures in rats. Exp. Neurol. 154, 213–223.
Barco, A., Alarcon, J. M., and Kandel, E. R. (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108, 689–703.
Barco, A., Patterson, S., Alarcon, J. M., Gromova, P., Mata-Roig, M., Morozov, A., and Kandel, E. R. (2005) Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48, 123–137.
Barondes, S. H., and Jarvik, M. E. (1964) The Influence Of Actinomycin-D On Brain Rna Synthesis And On Memory. J. Neurochem. 11, 187–195.
Barth, A. L., Gerkin, R. C., and Dean, K. L. (2004) Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J. Neurosci. 24, 6466–6475.
Barzilai, A., Kennedy, T. E., Sweatt, J. D., and Kandel, E. R. (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2, 1577–1586.
Bender, R. A., Soleymani, S. V., Brewster, A. L., Nguyen, S. T., Beck, H., Mathern, G. W., and Baram, T. Z. (2003) Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J. Neurosci. 23, 6826–6836.
Bernard, C., Anderson, A., Becker, A., Poolos, N. P., Beck, H., and Johnston, D. (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532–535.
Berry, F. B., and Brown, I. R. (1996) CaM I mRNA is localized to apical dendrites during postnatal development of neurons in the rat brain. J. Neurosci. Res. 43, 565–575.
Bito, H., Deisseroth, K., and Tsien, R. W. (1996) CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203–1214.
Bloch, B., Guitteny, A. F., Normand, E., and Chouham, S. (1990) Presence of neuropeptide messenger RNAs in neuronal processes. Neurosci. Lett. 109, 259–264.
Burgin, K. E., Waxham, M. N., Rickling, S., Westgate, S. A., Mobley, W. C., and Kelly, P. T. (1990) In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 10, 1788–1798.
Cha-Molstad, H., Keller, D. M., Yochum, G. S., Impey, S., and Goodman, R. H. (2004) Cell-type-specific binding of the transcription factor CREB to the cAMP-response element. Proc. Natl. Acad. Sci. USA 101, 13572–13577.
Chicurel, M. E., Terrian, D. M., and Potter, H. (1993) mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J. Neurosci. 13, 4054–4063.
Cochran, B. H., Reffel, A. C., and Stiles, C. D. (1983) Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell 33, 939–947.
Corriveau, R. A., Shatz, C. J., and Nedivi, E. (1999) Dynamic regulation of cpg15 during activity-dependent synaptic development in the mammalian visual system. J. Neurosci. 19, 7999–8008.
Cottrell, J. R., Borok, E., Horvath, T. L., and Nedivi, E. (2004) CPG2: a brain- and synapse-specific protein that regulates the endocytosis of glutamate receptors. Neuron 44, 677–690.
Crino, P., Khodakhah, K., Becker, K., Ginsberg, S., Hemby, S., and Eberwine, J. (1998) Presence and phosphorylation of transcription factors in developing dendrites. Proc. Natl. Acad. Sci. USA 95, 2313–2318.
Crino, P. B., and Eberwine, J. (1996) Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron 17, 1173–1187.
Dash, P. K., Hochner, B., and Kandel, E. R. (1990) Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature 345, 718–721.
Davis, S., Vanhoutte, P., Pages, C., Caboche, J., and Laroche, S. (2000) The MAPK/ERK cascade targets both Elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci. 20, 4563–4572.
Desai, N. S., Rutherford, L. C., and Turrigiano, G. G. (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat. Neurosci. 2, 515–520.
Dumas, S., Javoy-Agid, F., Hirsch, E., Agid, Y., and Mallet, J. (1990) Tyrosine hydroxylase gene expression in human ventral mesencephalon: detection of tyrosine hydroxylase messenger RNA in neurites. J. Neurosci. Res. 25, 569–575.
Eberwine, J., Miyashiro, K., Kacharmina, J. E., and Job, C. (2001) Local translation of classes of mRNAs that are targeted to neuronal dendrites. Proc. Natl. Acad. Sci. USA 98, 7080–7085.
Elliott, R. C., Miles, M. F., and Lowenstein, D. H. (2003) Overlapping microarray profiles of dentate gyrus gene expression during development- and epilepsy-associated neurogenesis and axon outgrowth. J. Neurosci. 23, 2218–2227.
Euskirchen, G., Royce, T. E., Bertone, P., Martone, R., Rinn, J. L., Nelson, F. K., Sayward, F., Luscombe, N. M., Miller, P., Gerstein, M., et al., (2004) CREB binds to multiple loci on human chromosome 22. Mol. Cell Biol. 24, 3804–3814.
Flavell, S. W., Cowan, C. W., Kim, T. K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., and Greenberg, M. E. (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008–1012.
Flexner, J. B., Flexner, L. B., and Stellar, E. (1963) Memory in mice as affected by intracerebral puromycin. Science 141, 57–59.
Foulkes, N. S., Borrelli, E., and Sassone-Corsi, P. (1991) CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 64, 739–749.
Furuichi, T., Simon-Chazottes, D., Fujino, I., Yamada, N., Hasegawa, M., Miyawaki, A., Yoshikawa, S., Guenet, J. L., and Mikoshiba, K. (1993) Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. Receptors Channels 1, 11–24.
Garner, C. C., Tucker, R. P., and Matus, A. (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336, 674–677.
Glazewski, S., Barth, A. L., Wallace, H., McKenna, M., Silva, A., and Fox, K. (1999) Impaired experience-dependent plasticity in barrel cortex of mice lacking the alpha and delta isoforms of CREB. Cereb. Cortex 9, 249–256.
Goelet, P., Castellucci, V. F., Schacher, S., and Kandel, E. R. (1986) The long and the short of long-term memory–a molecular framework. Nature 322, 419–422.
Grooms, S. Y., Noh, K. M., Regis, R., Bassell, G. J., Bryan, M. K., Carroll, R. C., and Zukin, R. S. (2006) Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J. Neurosci. 26, 8339–8351.
Guan, Z., Saraswati, S., Adolfsen, B., and Littleton, J. T. (2005) Genome-wide transcriptional changes associated with enhanced activity in the Drosophila nervous system. Neuron 48, 91–107.
Guzowski, J. F., Miyashita, T., Chawla, M. K., Sanderson, J., Maes, L. I., Houston, F. P., Lipa, P., McNaughton, B. L., Worley, P. F., and Barnes, C. A. (2006) Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. USA 103, 1077–1082.
Impey, S., McCorkle, S. R., Cha-Molstad, H., Dwyer, J. M., Yochum, G. S., Boss, J. M., McWeeney, S., Dunn, J. J., Mandel, G., and Goodman, R. H. (2004) Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119, 1041–1054.
Ingi, T., Krumins, A. M., Chidiac, P., Brothers, G. M., Chung, S., Snow, B. E., Barnes, C. A., Lanahan, A. A., Siderovski, D. P., Ross, E. M., et al., (1998) Dynamic regulation of RGS2 suggests a novel mechanism in G-protein signaling and neuronal plasticity. J. Neurosci. 18, 7178–7188.
Ishimoto, T., Fujimori, K., Kasai, M., and Taguchi, T. (2000) Dendritic translocation of the rat ferritin H chain mRNA. Biochem. Biophys. Res. Commun. 272, 789–793.
James, A. B., Conway, A. M., and Morris, B. J. (2005) Genomic profiling of the neuronal target genes of the plasticity-related transcription factor – Zif268. J. Neurochem. 95, 796–810.
James, A. B., Conway, A. M., and Morris, B. J. (2006) Regulation of the neuronal proteasome by Zif268 (Egr1) J. Neurosci. 26, 1624–1634.
Job, C., and Eberwine, J. (2001) Localization and translation of mRNA in dendrites and axons. Nat. Rev. Neurosci. 2, 889–898.
Josselyn, S. A., Kida, S., and Silva, A. J. (2004) Inducible repression of CREB function disrupts amygdala-dependent memory. Neurobiol. Learn. Mem. 82, 159–163.
Kaminska, B., Kaczmarek, L., and Chaudhuri, A. (1996) Visual stimulation regulates the expression of transcription factors and modulates the composition of AP-1 in visual cortex. J. Neurosci. 16, 3968–3978.
Kamphuis, W., De Rijk, T. C., and Lopes da Silva, F. H. (1995) Expression of GABAA receptor subunit mRNAs in hippocampal pyramidal and granular neurons in the kindling model of epileptogenesis: an in situ hybridization study. Brain Res. Mol. Brain Res. 31, 33–47.
Kida, S., Josselyn, S. A., de Ortiz, S. P., Kogan, J. H., Chevere, I., Masushige, S., and Silva, A. J. (2002) CREB required for the stability of new and reactivated fear memories. Nat. Neurosci. 5, 348–355.
Kleiman, R., Banker, G., and Steward, O. (1994) Development of subcellular mRNA compartmentation in hippocampal neurons in culture. J. Neurosci. 14, 1130–1140.
Kohrmann, M., Luo, M., Kaether, C., DesGroseillers, L., Dotti, C. G., and Kiebler, M. A. (1999) Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10, 2945–2953.
Kosik, K. S., Crandall, J. E., Mufson, E. J., and Neve, R. L. (1989) Tau in situ hybridization in normal and Alzheimer brain: localization in the somatodendritic compartment. Ann. Neurol. 26, 352–361.
Landry, C. F., Watson, J. B., Kashima, T., and Campagnoni, A. T. (1994) Cellular influences on RNA sorting in neurons and glia: an in situ hybridization histochemical study. Brain Res. Mol. Brain Res. 27, 1–11.
Laurent-Demir, C., Decorte, L., Jaffard, R., and Mons, N. (2000) Differential regulation of Ca(2+)-calmodulin stimulated and Ca(2+)-insensitive adenylyl cyclase messenger RNA in intact and denervated mouse hippocampus. Neuroscience 96, 267–274.
Lauterborn, J. C., Rivera, S., Stinis, C. T., Hayes, V. Y., Isackson, P. J., and Gall, C. M. (1996) Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J. Neurosci. 16, 7428–7436.
Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U., and Kuhl, D. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA 92, 5734–5738.
Lukasiuk, K., Kontula, L., and Pitkanen, A. (2003) cDNA profiling of epileptogenesis in the rat brain. Eur. J. Neurosci. 17, 271–279.
Lukasiuk, K., and Pitkanen, A. (2004) Large-scale analysis of gene expression in epilepsy research: is synthesis already possible? Neurochem. Res. 29, 1169–1178.
Lyford, G. L., Yamagata, K., Kaufmann, W. E., Barnes, C. A., Sanders, L. K., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Lanahan, A. A., and Worley, P. F. (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14, 433–445.
Majdan, M., and Shatz, C. J. (2006) Effects of visual experience on activity-dependent gene regulation in cortex. Nat. Neurosci. 9, 650–659.
Marie, H., Morishita, W., Yu, X., Calakos, N., and Malenka, R. C. (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 741–752.
Meshorer, E., Erb, C., Gazit, R., Pavlovsky, L., Kaufer, D., Friedman, A., Glick, D., Ben-Arie, N., and Soreq, H. (2002) Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science 295, 508–512.
Miranti, C. K., Ginty, D. D., Huang, G., Chatila, T., and Greenberg, M. E. (1995) Calcium activates serum response factor-dependent transcription by a Ras- and Elk-1-independent mechanism that involves a Ca2+/calmodulin-dependent kinase. Mol. Cell Biol. 15, 3672–3684.
Miyashiro, K., Dichter, M., and Eberwine, J. (1994) On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. Natl. Acad. Sci. USA 91, 10800–10804.
Mohr, E., Meyerhof, W., and Richter, D. (1995) Vasopressin and oxytocin: molecular biology and evolution of the peptide hormones and their receptors. Vitam. Horm. 51, 235–266.
Morgan, J. I., Cohen, D. R., Hempstead, J. L., and Curran, T. (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237, 192–197.
Moriya, M., and Tanaka, S. (1994) Prominent expression of protein kinase C (gamma) mRNA in the dendrite-rich neuropil of mice cerebellum at the critical period for synaptogenesis. Neuroreport 5, 929–932.
Nedivi, E., Hevroni, D., Naot, D., Israeli, D., and Citri, Y. (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363, 718–722.
Nedivi, E., Wu, G. Y., and Cline, H. T. (1998) Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. Science 281, 1863–1866.
Pfenning, A. R., Schwartz, R., and Barth, A. L. (2007) A comparative genomics approach to identifying the plasticity transcriptome. BMC Neurosci. 13(8), 20.
Qian, Z., Gilbert, M., and Kandel, E. R. (1994) Temporal and spatial regulation of the expression of BAD2, a MAP kinase phosphatase, during seizure, kindling, and long-term potentiation. Learn. Mem. 1, 180–188.
Qian, Z., Gilbert, M. E., Colicos, M. A., Kandel, E. R., and Kuhl, D. (1993) Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361, 453–457.
Racca, C., Gardiol, A., and Triller, A. (1997) Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs. J. Neurosci. 17, 1691–1700.
Saffen, D. W., Cole, A. J., Worley, P. F., Christy, B. A., Ryder, K., and Baraban, J. M. (1988) Convulsant-induced increase in transcription factor messenger RNAs in rat brain. Proc. Natl. Acad. Sci. USA 85, 7795–7799.
Shah, M. M., Anderson, A. E., Leung, V., Lin, X., and Johnston, D. (2004) Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495–508.
Shaywitz, A. J., and Greenberg, M. E. (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821–861.
Sheng, M., and Greenberg, M. E. (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4, 477–485.
Sonnenberg, J. L., Rauscher, F. J., 3rd, Morgan, J. I., and Curran, T. (1989) Regulation of proenkephalin by Fos and Jun. Science 246, 1622–1625.
Sperk, G., Schwarzer, C., Tsunashima, K., and Kandlhofer, S. (1998) Expression of GABA(A) receptor subunits in the hippocampus of the rat after kainic acid-induced seizures. Epilepsy Res. 32, 129–139.
Steward, O., Wallace, C. S., Lyford, G. L., and Worley, P. F. (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21, 741–751.
Strong, M. J., Svedmyr, A., Gajdusek, D. C., and Garruto, R. M. (1990) The temporal expression of amyloid precursor protein mRNA in vitro in dissociated hippocampal neuron cultures. Exp. Neurol. 109, 171–179.
Surges, R., Brewster, A. L., Bender, R. A., Beck, H., Feuerstein, T. J., and Baram, T. Z. (2006) Regulated expression of HCN channels and cAMP levels shape the properties of the h current in developing rat hippocampus. Eur. J. Neurosci. 24, 94–104.
Swirnoff, A. H., Apel, E. D., Svaren, J., Sevetson, B. R., Zimonjic, D. B., Popescu, N. C., and Milbrandt, J. (1998) Nab1, a corepressor of NGFI-A (Egr-1), contains an active transcriptional repression domain. Mol. Cell Biol. 18, 512–524.
Tang, Y., Lu, A., Aronow, B. J., Wagner, K. R., and Sharp, F. R. (2002) Genomic responses of the brain to ischemic stroke, intracerebral haemorrhage, kainate seizures, hypoglycemia, and hypoxia. Eur. J. Neurosci. 15, 1937–1952.
Tongiorgi, E., Righi, M., and Cattaneo, A. (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17, 9492–9505.
Tropea, D., Kreiman, G., Lyckman, A., Mukherjee, S., Yu, H., Horng, S., and Sur, M. (2006) Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci. 9, 660–668.
West, A. E., Griffith, E. C., and Greenberg, M. E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3, 921–931.
Worley, P. F., Bhat, R. V., Baraban, J. M., Erickson, C. A., McNaughton, B. L., and Barnes, C. A. (1993) Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J. Neurosci. 13, 4776–4786.
Xiao, B., Tu, J. C., Petralia, R. S., Yuan, J. P., Doan, A., Breder, C. D., Ruggiero, A., Lanahan, A. A., Wenthold, R. J., and Worley, P. F. (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 21, 707–716.
Yamagata, K., Andreasson, K. I., Kaufmann, W. E., Barnes, C. A., and Worley, P. F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11, 371–386.
Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., and Tully, T. (1994) Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49–58.
Zhang, X., Odom, D. T., Koo, S. H., Conkright, M. D., Canettieri, G., Best, J., Chen, H., Jenner, R., Herbolsheimer, E., Jacobsen, E., et al., (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl. Acad. Sci. USA 102, 4459–4464.
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Barth, A.L., Yassin, L. (2008). Activity-dependent Gene Transcription in Neurons: Defining the Plasticity Transcriptome. In: Dudek, S.M. (eds) Transcriptional Regulation by Neuronal Activity. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-73609-9_15
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