Activity-dependent Gene Transcription in Neurons: Defining the Plasticity Transcriptome

  • Alison L. Barth
  • Lina Yassin


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.


Monocular Deprivation Dependent Gene Expression Silent Synapse CREB Binding Site CREB Target Gene 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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.Google Scholar
  2. 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.PubMedCrossRefGoogle Scholar
  3. 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.Google Scholar
  4. 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.Google Scholar
  5. 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.Google Scholar
  6. 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.Google Scholar
  7. 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.Google Scholar
  8. 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.Google Scholar
  9. 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.Google Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. 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.Google Scholar
  12. Bloch, B., Guitteny, A. F., Normand, E., and Chouham, S. (1990) Presence of neuropeptide messenger RNAs in neuronal processes. Neurosci. Lett. 109, 259–264.Google Scholar
  13. 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.Google Scholar
  14. 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.Google Scholar
  15. 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.Google Scholar
  16. 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.Google Scholar
  17. 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.Google Scholar
  18. 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.Google Scholar
  19. 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.Google Scholar
  20. 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.Google Scholar
  21. 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.Google Scholar
  22. 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.Google Scholar
  23. 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.Google Scholar
  24. 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.Google Scholar
  25. 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.Google Scholar
  26. 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.Google Scholar
  27. 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.Google Scholar
  28. 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.Google Scholar
  29. Flexner, J. B., Flexner, L. B., and Stellar, E. (1963) Memory in mice as affected by intracerebral puromycin. Science 141, 57–59.Google Scholar
  30. 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.Google Scholar
  31. 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.Google Scholar
  32. 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.Google Scholar
  33. 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.Google Scholar
  34. 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.Google Scholar
  35. 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.Google Scholar
  36. 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.Google Scholar
  37. 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.Google Scholar
  38. 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.Google Scholar
  39. 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.Google Scholar
  40. 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.Google Scholar
  41. 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.Google Scholar
  42. James, A. B., Conway, A. M., and Morris, B. J. (2006) Regulation of the neuronal proteasome by Zif268 (Egr1) J. Neurosci. 26, 1624–1634.Google Scholar
  43. Job, C., and Eberwine, J. (2001) Localization and translation of mRNA in dendrites and axons. Nat. Rev. Neurosci. 2, 889–898.Google Scholar
  44. 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.Google Scholar
  45. 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.Google Scholar
  46. 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.Google Scholar
  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.Google Scholar
  48. Kleiman, R., Banker, G., and Steward, O. (1994) Development of subcellular mRNA compartmentation in hippocampal neurons in culture. J. Neurosci. 14, 1130–1140.Google Scholar
  49. 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.Google Scholar
  50. 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.Google Scholar
  51. 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.Google Scholar
  52. 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.Google Scholar
  53. 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.PubMedGoogle Scholar
  54. 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.Google Scholar
  55. Lukasiuk, K., Kontula, L., and Pitkanen, A. (2003) cDNA profiling of epileptogenesis in the rat brain. Eur. J. Neurosci. 17, 271–279.Google Scholar
  56. Lukasiuk, K., and Pitkanen, A. (2004) Large-scale analysis of gene expression in epilepsy research: is synthesis already possible? Neurochem. Res. 29, 1169–1178.Google Scholar
  57. 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.Google Scholar
  58. Majdan, M., and Shatz, C. J. (2006) Effects of visual experience on activity-dependent gene regulation in cortex. Nat. Neurosci. 9, 650–659.Google Scholar
  59. 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.Google Scholar
  60. 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.Google Scholar
  61. 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.Google Scholar
  62. 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.Google Scholar
  63. 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.Google Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 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.Google Scholar
  66. 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.Google Scholar
  67. 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.Google Scholar
  68. Pfenning, A. R., Schwartz, R., and Barth, A. L. (2007) A comparative genomics approach to identifying the plasticity transcriptome. BMC Neurosci. 13(8), 20.Google Scholar
  69. 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.Google Scholar
  70. 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.Google Scholar
  71. Racca, C., Gardiol, A., and Triller, A. (1997) Dendritic and postsynaptic localizations of glycine receptor alpha subunit mRNAs. J. Neurosci. 17, 1691–1700.Google Scholar
  72. 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.Google Scholar
  73. 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.Google Scholar
  74. 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.Google Scholar
  75. 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.Google Scholar
  76. 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.Google Scholar
  77. 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.Google Scholar
  78. 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.Google Scholar
  79. 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.Google Scholar
  80. 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.Google Scholar
  81. 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.Google Scholar
  82. 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.Google Scholar
  83. 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.PubMedGoogle Scholar
  84. 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.Google Scholar
  85. West, A. E., Griffith, E. C., and Greenberg, M. E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3, 921–931.Google Scholar
  86. 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.Google Scholar
  87. 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.Google Scholar
  88. 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.Google Scholar
  89. 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.Google Scholar
  90. 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.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Alison L. Barth
  • Lina Yassin

There are no affiliations available

Personalised recommendations