Chronic Fluoxetine Treatment Induces Brain Region-Specific Upregulation of Genes Associated with BDNF-Induced Long-Term Potentiation

Alme, Maria Nordheim; Wibrand, Karin; Dagestad, Grethe; Bramham, Clive R.

doi:https://doi.org/10.1155/2007/26496

Neural Plasticity

On this page

Abstract References Copyright Related Articles

Research Article | Open Access

Volume 2007 | Article ID 026496 | https://doi.org/10.1155/2007/26496

Chronic Fluoxetine Treatment Induces Brain Region-Specific Upregulation of Genes Associated with BDNF-Induced Long-Term Potentiation

Maria Nordheim Alme,¹Karin Wibrand,¹Grethe Dagestad,¹and Clive R. Bramham¹

Academic Editor: Monica Di Luca

Received23 Mar 2007

Accepted27 Jul 2007

Published17 Sept 2007

Abstract

Several lines of evidence implicate BDNF in the pathogenesis of stress-induced depression and the delayed efficacy of antidepressant drugs. Antidepressant-induced upregulation of BDNF signaling is thought to promote adaptive neuronal plasticity through effects on gene expression, but the effector genes downstream of BDNF has not been identified. Local infusion of BDNF into the dentate gyrus induces a long-term potentiation (BDNF-LTP) of synaptic transmission that requires upregulation of the immediate early gene Arc. Recently, we identified five genes (neuritin, Narp, TIEG1, Carp, and Arl4d) that are coupregulated with Arc during BDNF-LTP. Here, we examined the expression of these genes in the dentate gyrus, hippocampus proper, and prefrontal cortex after antidepressant treatment. We show that chronic, but not acute, fluoxetine administration leads to upregulation of these BDNF-LTP-associated genes in a brain region-specific pattern. These findings link chronic effects of antidepressant treatment to molecular mechanisms underlying BDNF-induced synaptic plasticity.

References

T. Bliss, G. Collingridge, and R. Morris, “Synaptic plasticity in the hippocampus,” in The Hippocampus Book, P. Andersen, R. Morris, D. Amaral, T. Bliss, and J. O'Keefe, Eds., pp. 343–474, Oxford University Press, New York, NY, USA, 2007.
View at: Google Scholar
R. Blum and A. Konnerth, “Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions,” Physiology, vol. 20, no. 1, pp. 70–78, 2005.
View at: Publisher Site | Google Scholar
C. R. Bramham and E. Messaoudi, “BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis,” Progress in Neurobiology, vol. 76, no. 2, pp. 99–125, 2005.
View at: Publisher Site | Google Scholar
C. T. Drake, T. A. Milner, and S. L. Patterson, “Ultastructural localization of full-length trkB immunoreactivity in rat hippocampus suggests multiple roles in modulating activity-dependent synaptic plasticity,” The Journal of Neuroscience, vol. 19, no. 18, pp. 8009–8026, 1999.
View at: Google Scholar
S. Santi, S. Cappello, M. Riccio et al., “Hippocampal neurons recycle BDNF for activity-dependent secretion and LTP maintenance,” EMBO Journal, vol. 25, no. 18, pp. 4372–4380, 2006.
View at: Publisher Site | Google Scholar
M. Hartmann, R. Heumann, and V. Lessmann, “Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses,” EMBO Journal, vol. 20, no. 21, pp. 5887–5897, 2001.
View at: Publisher Site | Google Scholar
A. Balkowiec and D. M. Katz, “Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons,” The Journal of Neuroscience, vol. 22, no. 23, pp. 10399–10407, 2002.
View at: Google Scholar
H. Kang, A. A. Welcher, D. Shelton, and E. M. Schuman, “Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation,” Neuron, vol. 19, no. 3, pp. 653–664, 1997.
View at: Publisher Site | Google Scholar
E. Messaoudi, S.-W. Ying, T. Kanhema, S. D. Croll, and C. R. Bramham, “Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo,” The Journal of Neuroscience, vol. 22, no. 17, pp. 7453–7461, 2002.
View at: Google Scholar
S.-W. Ying, M. Futter, K. Rosenblum et al., “Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis,” The Journal of Neuroscience, vol. 22, no. 5, pp. 1532–1540, 2002.
View at: Google Scholar
E. Messaoudi, T. Kanhema, J. Soule et al., “Sustained Arc synthesis controls LTP consolidation through regulation of local actin polymerization in the dentate gyrus in vivo,” to appear in The Journal of Neuroscience.
View at: Google Scholar
C. R. Bramham and D. G. Wells, “Dendritic mRNA: transport, translation, and function,” to appear in Nature Reviews Neuroscience.
View at: Google Scholar
O. Berton and E. J. Nestler, “New approaches to antidepressant drug discovery: beyond monoamines,” Nature Reviews Neuroscience, vol. 7, no. 2, pp. 137–151, 2006.
View at: Publisher Site | Google Scholar
S. D. Kuipers and C. R. Bramham, “Brain-derived neurotrophic factor mechanisms and function in adult synaptic plasticity: new insights and implications for therapy,” Current Opinion in Drug Discovery and Development, vol. 9, no. 5, pp. 580–586, 2006.
View at: Google Scholar
E. Castrén, V. Võikar, and T. Rantamäki, “Role of neurotrophic factors in depression,” Current Opinion in Pharmacology, vol. 7, no. 1, pp. 18–21, 2007.
View at: Publisher Site | Google Scholar
R. S. Duman and L. M. Monteggia, “A neurotrophic model for stress-related mood disorders,” Biological Psychiatry, vol. 59, no. 12, pp. 1116–1127, 2006.
View at: Publisher Site | Google Scholar
L. M. Monteggia, M. Barrot, C. M. Powell et al., “Essential role of brain-derived neurotrophic factor in adult hippocampal function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 29, pp. 10827–10832, 2004.
View at: Publisher Site | Google Scholar
J. Grønli, C. R. Bramham, R. Murison et al., “Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper,” Pharmacology Biochemistry and Behavior, vol. 85, no. 4, pp. 842–849, 2006.
View at: Publisher Site | Google Scholar
L. M. Monteggia, B. Luikart, M. Barrot et al., “Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors,” Biological Psychiatry, vol. 61, no. 2, pp. 187–197, 2007.
View at: Publisher Site | Google Scholar
T. Saarelainen, P. Hendolin, G. Lucas et al., “Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects,” The Journal of Neuroscience, vol. 23, no. 1, pp. 349–357, 2003.
View at: Google Scholar
E. Castrén, “Is mood chemistry?” Nature Reviews Neuroscience, vol. 6, no. 3, pp. 241–246, 2005.
View at: Publisher Site | Google Scholar
K. Wibrand, E. Messaoudi, B. Håvik et al., “Identification of genes co-upregulated with Arc during BDNF-induced long-term potentiation in adult rat dentate gyrus in vivo,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1501–1511, 2006.
View at: Publisher Site | Google Scholar
E. Nedivi, S. Fieldust, L. E. Theill, and D. Hevroni, “A set of genes expressed in response to light in the adult cerebral cortex and regulated during development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 5, pp. 2048–2053, 1996.
View at: Publisher Site | Google Scholar
E. Nedivi, G.-Y. Wu, and H. T. Cline, “Promotion of dendritic growth by CPG15, an activity-induced signaling molecule,” Science, vol. 281, no. 5384, pp. 1863–1866, 1998.
View at: Publisher Site | Google Scholar
D. Xu, C. Hopf, R. Reddy et al., “Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity,” Neuron, vol. 39, no. 3, pp. 513–528, 2003.
View at: Publisher Site | Google Scholar
M. Subramaniam, S. A. Harris, M. J. Oursler, K. Rasmussen, B. L. Riggs, and T. C. Spelsberg, “Identification of a novel TGF- $β$ -regulated gene encoding a putative zinc finger protein in human osteoblasts,” Nucleic Acids Research, vol. 23, no. 23, pp. 4907–4912, 1995.
View at: Publisher Site | Google Scholar
G. Suske, E. Bruford, and S. Philipsen, “Mammalian SP/KLF transcription factors: bring in the family,” Genomics, vol. 85, no. 5, pp. 551–556, 2005.
View at: Publisher Site | Google Scholar
S. A. Johnsen, M. Subramaniam, T. Katagiri, R. Janknecht, and T. C. Spelsberg, “Transcriptional regulation of Smad2 is required for enhancement of TGF $β$ /Smad signaling by TGF $β$ inducible early gene,” Journal of Cellular Biochemistry, vol. 87, no. 2, pp. 233–241, 2002.
View at: Publisher Site | Google Scholar
J. D. Berke, R. F. Paletzki, G. J. Aronson, S. E. Hyman, and C. R. Gerfen, “A complex program of striatal gene expression induced by dopaminergic stimulation,” The Journal of Neuroscience, vol. 18, no. 14, pp. 5301–5310, 1998.
View at: Google Scholar
E. Vreugdenhil, N. Datson, B. Engels et al., “Kainate-elicited seizures induce mRNA encoding a CaMK-related peptide: a putative modulator of kinase activity in rat hippocampus,” Journal of Neurobiology, vol. 39, no. 1, pp. 41–50, 1999.
View at: Publisher Site | Google Scholar
S. Pasqualato, L. Renault, and J. Cherfils, “Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for ‘front-back’ communication,” EMBO Reports, vol. 3, no. 11, pp. 1035–1041, 2002.
View at: Publisher Site | Google Scholar
C. G. Burd, T. I. Strochlic, and S. R. Gangi Setty, “Arf-like GTPases: not so Arf-like after all,” Trends in Cell Biology, vol. 14, no. 12, pp. 687–694, 2004.
View at: Publisher Site | Google Scholar
R. A. Kahn, J. Cherfils, M. Elias, R. C. Lovering, S. Munro, and A. Schurmann, “Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins,” Journal of Cell Biology, vol. 172, no. 5, pp. 645–650, 2006.
View at: Publisher Site | Google Scholar
G. Dagestad, S. D. Kuipers, E. Messaoudi, and C. R. Bramham, “Chronic fluoxetine induces region-specific changes in translation factor eIF4E and eEF2 activity in the rat brain,” European Journal of Neuroscience, vol. 23, no. 10, pp. 2814–2818, 2006.
View at: Publisher Site | Google Scholar
J. Vandesompele, K. De Preter, F. Pattyn et al., “Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes,” Genome Biology, vol. 3, no. 7, pp. research0034.1–research0034.11, 2002.
View at: Publisher Site | Google Scholar
X. Tao, A. E. West, W. G. Chen, G. Corfas, and M. E. Greenberg, “A calcium-responsive transcription factor, CaRF, that regulates neuronal activity-dependent expression of BDNF,” Neuron, vol. 33, no. 3, pp. 383–395, 2002.
View at: Publisher Site | Google Scholar
J. C. Lauterborn, S. Rivera, C. T. Stinis, V. Y. Hayes, P. J. Isackson, and C. M. Gall, “Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters,” The Journal of Neuroscience, vol. 16, no. 23, pp. 7428–7436, 1996.
View at: Google Scholar
A. L. Dow, D. S. Russell, and R. S. Duman, “Regulation of activin mRNA and Smad2 phosphorylation by antidepressant treatment in the rat brain: effects in behavioral models,” The Journal of Neuroscience, vol. 25, no. 20, pp. 4908–4916, 2005.
View at: Publisher Site | Google Scholar
T. Cook, B. Gebelein, M. Belal, K. Mesa, and R. Urrutia, “Three conserved transcriptional repressor domains are a defining feature of the TIEG subfamily of Sp1-like zinc finger proteins,” Journal of Biological Chemistry, vol. 274, no. 41, pp. 29500–29504, 1999.
View at: Publisher Site | Google Scholar
G. Suske, “The Sp-family of transcription factors,” Gene, vol. 238, no. 2, pp. 291–300, 1999.
View at: Publisher Site | Google Scholar
S. A. Johnsen, M. Subramaniam, R. Janknecht, and T. C. Spelsberg, “TGF $β$ inducible early gene enhances TGF $β$ /Smad-dependent transcriptional responses,” Oncogene, vol. 21, no. 37, pp. 5783–5790, 2002.
View at: Publisher Site | Google Scholar
J. Chin, R.-Y. Liu, L. J. Cleary, A. Eskin, and J. H. Byrne, “TGF- $β$ 1-induced long-term changes in neuronal excitability in Aplysia sensory neurons depend on MAPK,” Journal of Neurophysiology, vol. 95, no. 5, pp. 3286–3290, 2006.
View at: Publisher Site | Google Scholar
C. C. Tsui, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, C. Barnes, and P. F. Worley, “Narp, a novel member of the pentraxin family, promotes neurite outgrowth and is dynamically regulated by neuronal activity,” The Journal of Neuroscience, vol. 16, no. 8, pp. 2463–2478, 1996.
View at: Google Scholar
R. J. O'Brien, D. Xu, R. S. Petralia, O. Steward, R. L. Huganir, and P. Worley, “Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp,” Neuron, vol. 23, no. 2, pp. 309–323, 1999.
View at: Publisher Site | Google Scholar
R. O'Brien, D. Xu, R. Mi, X. Tang, C. Hopf, and P. Worley, “Synaptically targeted Narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons,” The Journal of Neuroscience, vol. 22, no. 11, pp. 4487–4498, 2002.
View at: Google Scholar
G. S. Naeve, M. Ramakrishnan, R. Kramer, D. Hevroni, Y. Citri, and L. E. Theill, “Neuritin: a gene induced by neural activity and neurotrophins that promotes neuritogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 6, pp. 2648–2653, 1997.
View at: Publisher Site | Google Scholar
S. Di Giovanni, A. I. Faden, A. Yakovlev et al., “Neuronal plasticity after spinal cord injury: identification of a gene cluster driving neurite outgrowth,” FASEB Journal, vol. 19, no. 1, pp. 153–154, 2005.
View at: Publisher Site | Google Scholar
T. Fujino, W.-C. Lee, and E. Nedivi, “Regulation of cpg15 by signaling pathways that mediate synaptic plasticity,” Molecular and Cellular Neuroscience, vol. 24, no. 3, pp. 538–554, 2003.
View at: Publisher Site | Google Scholar
C. Harwell, B. Burbach, K. Svoboda, and E. Nedivi, “Regulation of cpg15 expression during single whisker experience in the barrel cortex of adult mice,” Journal of Neurobiology, vol. 65, no. 1, pp. 85–96, 2005.
View at: Publisher Site | Google Scholar
J. Krebs, “Calmodulin-dependent protein kinase IV: regulation of function and expression,” Biochimica et Biophysica Acta, vol. 1448, no. 2, pp. 183–189, 1998.
View at: Publisher Site | Google Scholar
E. Vreugdenhil, B. Engels, R. Middelburg et al., “Multiple transcripts generated by the DCAMKL gene are expressed in the rat hippocampus,” Molecular Brain Research, vol. 94, no. 1-2, pp. 67–74, 2001.
View at: Publisher Site | Google Scholar
S. Jacobs, C. Schilf, and F. Fliegert, “ADP-ribosylation factor (ARF)-like 4, 6, and 7 represent a subgroup of the ARF family characterization by rapid nucleotide exchange and a nuclear localization signal,” FEBS Letters, vol. 456, no. 3, pp. 384–388, 1999.
View at: Publisher Site | Google Scholar
T. Katayama, K. Imaizumi, M. Tsuda, Y. Mori, T. Takagi, and M. Tohyama, “Expression of an ADP-ribosylation factor like gene, ARF4L, is induced after transient forebrain ischemia in the gerbil,” Molecular Brain Research, vol. 56, no. 1-2, pp. 66–75, 1998.
View at: Publisher Site | Google Scholar
T. Katayama, K. Imaizumi, T. Yoneda et al., “Role of ARF4L in recycling between endosomes and the plasma membrane,” Cellular and Molecular Neurobiology, vol. 24, no. 1, pp. 137–147, 2004.
View at: Publisher Site | Google Scholar
Q. Pei, T. S. Zetterström, M. Sprakes, R. Tordera, and T. Sharp, “Antidepressant drug treatment induces Arc gene expression in the rat brain,” Neuroscience, vol. 121, no. 4, pp. 975–982, 2003.
View at: Publisher Site | Google Scholar
M. H. Larsen, H. Rosenbrock, F. Sams-Dodd, and J. D. Mikkelsen, “Expression of brain derived neurotrophic factor, activity-regulated cytoskeleton protein mRNA, and enhancement of adult hippocampal neurogenesis in rats after sub-chronic and chronic treatment with the triple monoamine re-uptake inhibitor tesofensine,” European Journal of Pharmacology, vol. 555, no. 2-3, pp. 115–121, 2007.
View at: Publisher Site | Google Scholar
Y. Dwivedi, H. S. Rizavi, and G. N. Pandey, “Antidepressants reverse corticosterone-mediated decrease in brain-derived neurotrophic factor expression: differential regulation of specific exons by antidepressants and corticosterone,” Neuroscience, vol. 139, no. 3, pp. 1017–1029, 2006.
View at: Publisher Site | Google Scholar
A. A. Khundakar and T. S. Zetterström, “Biphasic change in BDNF gene expression following antidepressant drug treatment explained by differential transcript regulation,” Brain Research, vol. 1106, no. 1, pp. 12–20, 2006.
View at: Publisher Site | Google Scholar
M. Gooney, E. Messaoudi, F. O. Maher, C. R. Bramham, and M. A. Lynch, “BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events,” Neurobiology of Aging, vol. 25, no. 10, pp. 1323–1331, 2004.
View at: Publisher Site | Google Scholar
S.-W. Ying, M. Futter, K. Rosenblum et al., “Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis,” The Journal of Neuroscience, vol. 22, no. 5, pp. 1532–1540, 2002.
View at: Google Scholar
J. Thome, N. Sakai, K.-H. Shin et al., “cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment,” The Journal of Neuroscience, vol. 20, no. 11, pp. 4030–4036, 2000.
View at: Google Scholar
T. Kanhema, G. Dagestad, D. Panja et al., “Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control,” Journal of Neurochemistry, vol. 99, no. 5, pp. 1328–1337, 2006.
View at: Publisher Site | Google Scholar
Y. Shirayama, A. C.-H. Chen, S. Nakagawa, D. S. Russell, and R. S. Duman, “Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression,” The Journal of Neuroscience, vol. 22, no. 8, pp. 3251–3261, 2002.
View at: Google Scholar

Copyright

Copyright © 2007 Maria Nordheim Alme et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

849

Downloads

1494

Citations