Profiling the MAPK/ERK dependent and independent activity regulated transcriptional programs in the murine hippocampus in vivo

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Blüthgen, Nils ^a   Van Bentum, Mirjam ^a   Merz, Barbara ^b   Kuhl, DIetmar ^b   Hermey, Guido ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE INHIBITOR; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ANIMAL; DENTATE GYRUS; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MAPK SIGNALING; METABOLISM; MOUSE; NERVE CELL; PATHOPHYSIOLOGY; PHOSPHORYLATION; SEIZURE; TRANSCRIPTION INITIATION;

ALTERNATIVE SPLICING; ANIMALS; DENTATE GYRUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RNA, LONG NONCODING; SEIZURES; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME;

EID: 85016617711     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep45101     Document Type: Article

References (59)

1. Ebert, D. H., Greenberg, M. E. Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493, 327-337, doi: 10. 1038/nature11860 (2013).
2. Kauer, J. A., Malenka, R. C. Synaptic plasticity and addiction. Nat Rev Neurosci 8, 844-858, doi: 10. 1038/nrn2234 (2007).
3. Bading, H. Nuclear calcium signalling in the regulation of brain function. Nat Rev Neurosci 14, 593-608, doi: 10. 1038/nrn3531 (2013).
4. Jordan, B. A., Kreutz, M. R. Nucleocytoplasmic protein shuttling: The direct route in synapse-to-nucleus signaling. Trends Neurosci 32, 392-401, doi: 10. 1016/j.tins. 2009. 04.001 (2009).
5. Benito, E., Barco, A. The neuronal activity-driven transcriptome. Mol Neurobiol 51, 1071-1088, doi: 10. 1007/s12035-014-8772-z (2015).
6. Thomas, G. M., Huganir, R. L. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5, 173-183, doi: 10. 1038/nrn1346 (2004).
7. Bluthgen, N., Legewie, S. Systems analysis of MAPK signal transduction. Essays Biochem 45, 95-107, doi: 10. 1042/BSE0450095 (2008).
8. Impey, S., Obrietan, K., Storm, D. R. Making new connections: Role of ERK/MAP kinase signaling in neuronal plasticity. Neuron 23, 11-14 (1999).
9. Wiegert, J. S., Bading, H. Activity-dependent calcium signaling and ERK-MAP kinases in neurons: A link to structural plasticity of the nucleus and gene transcription regulation. Cell Calcium 49, 296-305, doi: 10. 1016/j.ceca.2010.11.009 (2011).
10. Sweatt, J. D. The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76, 1-10 (2001).
11. Lavaur, J., et al. A TAT-DEF-Elk-1 peptide regulates the cytonuclear trafficking of Elk-1 and controls cytoskeleton dynamics. J Neurosci 27, 14448-14458, doi: 10. 1523/JNEUROSCI. 2279-07. 2007 (2007).
12. Davis, S., Laroche, S. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: A review. Genes Brain Behav 5 Suppl 2, 61-72, doi: 10. 1111/j.1601-183X. 2006.00230. x (2006).
13. English, J. D., Sweatt, J. D. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271, 24329-24332 (1996).
14. Davis, S., Vanhoutte, P., Pages, C., Caboche, J., Laroche, S. 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 (2000).
15. Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., Sweatt, J. D. The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1, 602-609, doi: 10. 1038/2836 (1998).
16. Berman, D. E., Hazvi, S., Rosenblum, K., Seger, R., Dudai, Y. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J Neurosci 18, 10037-10044 (1998).
17. Blum, S., Moore, A. N., Adams, F., Dash, P. K. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J Neurosci 19, 3535-3544 (1999).
18. Rosenblum, K., Futter, M., Jones, M., Hulme, E. C., Bliss, T. V. ERKI/II regulation by the muscarinic acetylcholine receptors in neurons. J Neurosci 20, 977-985 (2000).
19. Schafe, G. E., et al. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20, 8177-8187 (2000).
20. Selcher, J. C., Atkins, C. M., Trzaskos, J. M., Paylor, R., Sweatt, J. D. A necessity for MAP kinase activation in mammalian spatial learning. Learn Mem 6, 478-490 (1999).
21. Kelly, A., Laroche, S., Davis, S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23, 5354-5360 (2003).
22. Thiels, E., Kanterewicz, B. I., Norman, E. D., Trzaskos, J. M., Klann, E. Long-term depression in the adult hippocampus in vivo involves activation of extracellular signal-regulated kinase and phosphorylation of Elk-1. J Neurosci 22, 2054-2062 (2002).
23. Yufune, S., et al. Transient Blockade of ERK Phosphorylation in the Critical Period Causes Autistic Phenotypes as an Adult in Mice. Sci Rep 5, 10252, doi: 10. 1038/srep10252 (2015).
24. Chotiner, J. K., et al. Assessment of the role of MAP kinase in mediating activity-dependent transcriptional activation of the immediate early gene Arc/Arg3. 1 in the dentate gyrus in vivo. Learn Mem 17, 117-129, doi: 10. 1101/lm. 1585910 (2010).
25. Waltereit, R., et al. Arg3. 1/Arc mRNA induction by Ca2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J Neurosci 21, 5484-5493 (2001).
26. Ying, S. W., 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. J Neurosci 22, 1532-1540 (2002).
27. Gangarossa, G., Sakkaki, S., Lory, P., Valjent, E. Mouse hippocampal phosphorylation footprint induced by generalized seizures: Focus on ERK, mTORC1 and Akt/GSK-3 pathways. Neuroscience 311, 474-483, doi: 10. 1016/j.neuroscience.2015.10. 051 (2015).
28. Favata, M. F., et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273, 18623-18632 (1998).
29. Klinger, B., et al. Network quantification of EGFR signaling unveils potential for targeted combination therapy. Mol Syst Biol 9, 673, doi: 10. 1038/msb. 2013. 29 (2013).
30. Clemson, C. M., et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33, 717-726, doi: 10. 1016/j.molcel. 2009. 01. 026 (2009).
31. Naganuma, T., et al. Alternative 3-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J 31, 4020-4034, doi: 10. 1038/emboj. 2012. 251 (2012).
32. Karpova, A., et al. Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus. Cell 152, 1119-1133, doi: 10. 1016/j.cell. 2013. 02.002 (2013).
33. Lanahan, A., Worley, P. Immediate-early genes and synaptic function. Neurobiol Learn Mem 70, 37-43, doi: 10. 1006/nlme. 1998. 3836 (1998).
34. Loebrich, S., Nedivi, E. The function of activity-regulated genes in the nervous system. Physiol Rev 89, 1079-1103, doi: 10. 1152/physrev.00013. 2009 (2009).
35. Crosio, C., Heitz, E., Allis, C. D., Borrelli, E., Sassone-Corsi, P. Chromatin remodeling and neuronal response: Multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J Cell Sci 116, 4905-4914, doi: 10. 1242/jcs.00804 (2003).
36. Scherle, P. A., Ma, W., Lim, H., Dey, S. K., Trzaskos, J. M. Regulation of cyclooxygenase-2 induction in the mouse uterus during decidualization. An event of early pregnancy. J Biol Chem 275, 37086-37092, doi: 10. 1074/jbc. M006168200 (2000).
37. Sato, M., Suzuki, K., Nakanishi, S. NMDA receptor stimulation and brain-derived neurotrophic factor upregulate homer 1a mRNA via the mitogen-activated protein kinase cascade in cultured cerebellar granule cells. J Neurosci 21, 3797-3805 (2001).
38. Choy, M. S., et al. Structural and Functional Analysis of the GADD34:PP1 eIF2alpha Phosphatase. Cell Rep 11, 1885-1891, doi: 10. 1016/j.celrep.2015.05. 043 (2015).
39. Munton, R. P., Vizi, S., Mansuy, I. M. The role of protein phosphatase-1 in the modulation of synaptic and structural plasticity. FEBS Lett 567, 121-128, doi: 10. 1016/j.febslet. 2004. 03. 121 (2004).
40. Pascoli, V., Cahill, E., Bellivier, F., Caboche, J., Vanhoutte, P. Extracellular signal-regulated protein kinases 1 and 2 activation by addictive drugs: A signal toward pathological adaptation. Biol Psychiatry 76, 917-926, doi: 10. 1016/j.biopsych. 2014. 04.005 (2014).
41. Benito, E., Valor, L. M., Jimenez-Minchan, M., Huber, W., Barco, A. cAMP response element-binding protein is a primary hub of activity-driven neuronal gene expression. J Neurosci 31, 18237-18250, doi: 10. 1523/JNEUROSCI. 4554-11. 2011 (2011).
42. Cahill, E., Salery, M., Vanhoutte, P., Caboche, J. Convergence of dopamine and glutamate signaling onto striatal ERK activation in response to drugs of abuse. Front Pharmacol 4, 172, doi: 10. 3389/fphar. 2013.00172 (2014).
43. Wittmann, M., et al. Synaptic activity induces dramatic changes in the geometry of the cell nucleus: Interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J Neurosci 29, 14687-14700, doi: 10. 1523/JNEUROSCI. 1160-09. 2009 (2009).
44. Brami-Cherrier, K., Roze, E., Girault, J. A., Betuing, S., Caboche, J. Role of the ERK/MSK1 signalling pathway in chromatin remodelling and brain responses to drugs of abuse. J Neurochem 108, 1323-1335, doi: 10. 1111/j.1471-4159. 2009. 05879. x (2009).
45. Ciccarelli, A., Giustetto, M. Role of ERK signaling in activity-dependent modifications of histone proteins. Neuropharmacology 80, 34-44, doi: 10. 1016/j.neuropharm. 2014. 01. 039 (2014).
46. Maag, J. L., et al. Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity. Front Neurosci 9, 351, doi: 10. 3389/fnins. 2015.00351 (2015).
47. Bergmann, J. H., Spector, D. L. Long non-coding RNAs: Modulators of nuclear structure and function. Curr Opin Cell Biol 26, 10-18, doi: 10. 1016/j.ceb. 2013. 08.005 (2014).
48. Sauvageau, M., et al. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife 2, e01749, doi: 10. 7554/eLife. 01749 (2013).
49. Marin-Bejar, O., et al. Pint lincRNA connects the p53 pathway with epigenetic silencing by the Polycomb repressive complex 2. Genome Biol 14, R104, doi: 10. 1186/gb-2013-14-9-r104 (2013).
50. Sasaki, Y. T., Ideue, T., Sano, M., Mituyama, T., Hirose, T. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci USA 106, 2525-2530, doi: 10. 1073/pnas. 0807899106 (2009).
51. Lipovich, L., et al. Activity-dependent human brain coding/noncoding gene regulatory networks. Genetics 192, 1133-1148, doi: 10. 1534/genetics. 112. 145128 (2012).
52. Fox, A. H., et al. Paraspeckles: A novel nuclear domain. Curr Biol 12, 13-25 (2002).
53. Hall, M. H., et al. Localization and regulation of PML bodies in the adult mouse brain. Brain Struct Funct 221, 2511-2525, doi: 10. 1007/s00429-015-1053-4 (2016).
54. Chen, L. L., Carmichael, G. G. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Mol Cell 35, 467-478, doi: 10. 1016/j.molcel. 2009. 06. 027 (2009).
55. Hirose, T., et al. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol Biol Cell 25, 169-183, doi: 10. 1091/mbc. E13-09-0558 (2014).
56. Nakagawa, S., Naganuma, T., Shioi, G., Hirose, T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J Cell Biol 193, 31-39, doi: 10. 1083/jcb. 201011110 (2011).
57. Hermey, G., et al. Genome-wide profiling of the activity-dependent hippocampal transcriptome. PLoS One 8, e76903, doi: 10. 1371/journal. pone.0076903 (2013).
58. Plath, N., et al. Arc/Arg3. 1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52, 437-444, doi: 10. 1016/j.neuron. 2006. 08. 024 (2006).
59. Oetjen, S., Mahlke, C., Hermans-Borgmeyer, I., Hermey, G. Spatiotemporal expression analysis of the growth factor receptor SorCS3. J Comp Neurol 522, 3386-3402, doi: 10. 1002/cne. 23606 (2014).