Temporal dynamics of a homeostatic pathway controlling neural network activity

Frontiers in Molecular Neuroscience

Volumn 6, Issue SEP, 2013, Pages

  Bateup, Helen S ^a,b   Denefrio, Cassandra L ^a   Johnson, Caroline A ^a   Saulnier, Jessica L ^a   Sabatini, Bernardo L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Activity dependent gene regulation; Arc; ERK signaling; Hippocampus; Homeostatic plasticity; Multi electrode array; Network activity; TSC mTOR

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; DACTINOMYCIN; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ENDOCYTOSIS; GENE REGULATORY NETWORK; HOMEOSTASIS; INTRACELLULAR SIGNALING; LONG TERM DEPRESSION; MOLECULAR DYNAMICS; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; RNA DEGRADATION; RNA SYNTHESIS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

EID: 84885075577     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00028     Document Type: Article

References (55)

1. Antion, M. D., Hou, L., Wong, H., Hoeffer, C. A., and Klann, E. (2008). mGluR-dependent long-term depression is associated with increased phosphorylation of S6 and synthesis of elongation factor 1A but remains expressed in S6K-deficient mice. Mol. Cell. Biol. 28, 2996-3007. doi: 10.1128/MCB.00201-08
2. Banko, J. L., Hou, L., Poulin, F., Sonenberg, N., and Klann, E. (2006). Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26, 2167-2173. doi: 10.1523/JNEUROSCI.5196-05.2006
3. Bateup, H. S., Johnson, C. A., Denefrio, C. L., Saulnier, J. L., Kornacker, K., and Sabatini, B. L. (2013). Excitatory/inhibitory synaptic imbalance leads to hippocampal hyperexcitability in mouse models of tuberous sclerosis. Neuron 78, 510-522. doi: 10.1016/j.neuron.2013.03.017
4. Bateup, H. S., Takasaki, K. T., Saulnier, J. L., Denefrio, C. L., and Sabatini, B. L. (2011). Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excitatory synaptic function. J. Neurosci. 31, 8862-8869. doi: 10.1523/JNEUROSCI.1617-11.2011
5. Beique, J. C., Na, Y., Kuhl, D., Worley, P. F., and Huganir, R. L. (2011). Arc-dependent synapse-specific homeostatic plasticity. Proc. Natl. Acad. Sci. U.S.A. 108, 816-821. doi: 10.1073/pnas.1017914108
6. Bramham, C. R., Alme, M. N., Bittins, M., Kuipers, S. D., Nair, R. R., Pai, B., et al. (2010). The Arc of synaptic memory. Exp. Brain Res. 200, 125-140. doi: 10.1007/s00221-009-1959-2
7. Briz, V., Hsu, Y. T., Li, Y., Lee, E., Bi, X., and Baudry, M. (2013). Calpain-2-mediated PTEN degradation contributes to BDNF-induced stimulation of dendritic protein synthesis. J. Neurosci. 33, 4317-4328. doi: 10.1523/JNEUROSCI.4907-12.2013
8. Chowdhury, S., Shepherd, J. D., Okuno, H., Lyford, G., Petralia, R. S., Plath, N., et al. (2006). Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52, 445-459. doi: 10.1016/j.neuron.2006.08.033
9. Costa-Mattioli, M., Sossin, W. S., Klann, E., and Sonenberg, N. (2009). Translational control of long-lasting synaptic plasticity and memory. Neuron 61, 10-26. doi: 10.1016/j.neuron.2008.10.055
10. Davis, G. W. (2006). Homeostatic control of neural activity: from phenomenology to molecular design. Annu. Rev. Neurosci. 29, 307-323. doi: 10.1146/annurev.neuro.28.061604.135751
11. Fu, A. K., Hung, K. W., Fu, W. Y., Shen, C., Chen, Y., Xia, J., et al. (2011). APC (Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat. Neurosci. 14, 181-189. doi: 10.1038/nn.2715
12. Gallagher, S. M., Daly, C. A., Bear, M. F., and Huber, K. M. (2004). Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J. Neurosci. 24, 4859-4864. doi: 10.1523/JNEUROSCI.5407-03.2004
13. Gelinas, J. N., Banko, J. L., Hou, L., Sonenberg, N., Weeber, E. J., Klann, E., et al. (2007). ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J. Biol. Chem. 282, 27527-27535. doi: 10.1074/jbc.M701077200
14. Giorgi, C., Yeo, G. W., Stone, M. E., Katz, D. B., Burge, C., Turrigiano, G., et al. (2007). The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130, 179-191. doi: 10.1016/j.cell.2007.05.028
15. Goold, C. P., and Nicoll, R. A. (2010). Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron 68, 512-528. doi: 10.1016/j.neuron.2010.09.020
16. Greer, P. L., and Greenberg, M. E. (2008). From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860. doi: 10.1016/j.neuron.2008.09.002
17. Greer, P. L., Hanayama, R., Bloodgood, B. L., Mardinly, A. R., Lipton, D. M., Flavell, S. W., et al. (2010). The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating Arc. Cell 140, 704-716. doi: 10.1016/j.cell.2010.01.026
18. Hou, L., and Klann, E. (2004). Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 24, 6352-6361. doi: 10.1523/JNEUROSCI.0995-04.2004
19. Huber, K. M., Gallagher, S. M., Warren, S. T., and Bear, M. F. (2002). Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. U.S.A. 99, 7746-7750. doi: 10.1073/pnas.122205699
20. Kawashima, T., Okuno, H., Nonaka, M., Adachi-Morishima, A., Kyo, N., Okamura, M., et al. (2009). Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl. Acad. Sci. U.S.A. 106, 316-321. doi: 10.1073/pnas.0806518106
21. Kelleher, R. J. 3rd., Govindarajan, A., Jung, H. Y., Kang, H., and Tonegawa, S. (2004). Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467-479. doi: 10.1016/S0092-8674(04)00115-1
22. Korb, E., Wilkinson, C. L., Delgado, R. N., Lovero, K. L., and Finkbeiner, S. (2013). Arc in the nucleus regulates PML-dependent GluA1 transcription and homeostatic plasticity. Nat. Neurosci. 16, 874-883. doi: 10.1038/nn.3429
23. Kwiatkowski, D. J., Zhang, H., Bandura, J. L., Heiberger, K. M., Glogauer, M., El-Hashemite, N., et al. (2002). A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet. 11, 525-534. doi: 10.1093/hmg/11.5.525
24. Link, W., Konietzko, U., Kauselmann, G., Krug, M., Schwanke, B., Frey, U., et al. (1995). Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. U.S.A. 92, 5734-5738. doi: 10.1073/pnas.92.12.5734
25. Luscher, C., and Huber, K. M. (2010). Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 65, 445-459. doi: 10.1016/j.neuron.2010.01.016
26. Lyford, G. L., Yamagata, K., Kaufmann, W. E., Barnes, C. A., Sanders, L. K., Copeland, N. G., et al. (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. doi: 10.1016/0896-6273(95)90299-6
27. Ma, L., Chen, Z., Erdjument-Bromage, H., Tempst, P., and Pandolfi, P. P. (2005). Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121, 179-193. doi: 10.1016/j.cell.2005.02.031
28. Ma, X. M., and Blenis, J. (2009). Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318. doi: 10.1038/nrm2672
29. Marder, E., and Goaillard, J. M. (2006). Variability, compensation, and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7, 563-574. doi: 10.1038/nrn1949
30. Mendoza, M. C., Er, E. E., and Blenis, J. (2011). The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem. Sci. 36, 320-328. doi: 10.1016/j.tibs.2011.03.006
31. Messaoudi, E., Kanhema, T., Soule, J., Tiron, A., Dagyte, G., Da Silva, B., et al. (2007). Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J. Neurosci. 27, 10445-10455. doi: 10.1523/JNEUROSCI.2883-07.2007
32. Panja, D., Dagyte, G., Bidinosti, M., Wibrand, K., Kristiansen, A. M., Sonenberg, N., et al. (2009). Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J. Biol. Chem. 284, 31498-31511. doi: 10.1074/jbc.M109.056077
33. Park, S., Park, J. M., Kim, S., Kim, J. A., Shepherd, J. D., Smith-Hicks, C. L., et al. (2008). Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59, 70-83. doi: 10.1016/j.neuron.2008.05.023
34. Peebles, C. L., Yoo, J., Thwin, M. T., Palop, J. J., Noebels, J. L., and Finkbeiner, S. (2010). Arc regulates spine morphology and maintains network stability in vivo. Proc. Natl. Acad. Sci. U.S.A. 107, 18173-18178. doi: 10.1073/pnas.1006546107
35. Perkinton, M. S., Sihra, T. S., and Williams, R. J. (1999). Ca(2+)-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J. Neurosci. 19, 5861-5874.
36. Pintchovski, S. A., Peebles, C. L., Kim, H. J., Verdin, E., and Finkbeiner, S. (2009). The serum response factor and a putative novel transcription factor regulate expression of the immediate-early gene Arc/Arg3.1 in neurons. J. Neurosci. 29, 1525-1537. doi: 10.1523/JNEUROSCI.5575-08.2009
37. Pozo, K., and Goda, Y. (2010). Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66, 337-351. doi: 10.1016/j.neuron.2010.04.028
38. Rao, V. R., Pintchovski, S. A., Chin, J., Peebles, C. L., Mitra, S., and Finkbeiner, S. (2006). AMPA receptors regulate transcription of the plasticity-related immediate-early gene Arc. Nat. Neurosci. 9, 887-895. doi: 10.1038/nn1708
39. Rial Verde, E. M., Lee-Osbourne, J., Worley, P. F., Malinow, R., and Cline, H. T. (2006). Increased expression of the immediate-early gene Arc/Arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52, 461-474. doi: 10.1016/j.neuron.2006.09.031
40. Saha, R. N., Wissink, E. M., Bailey, E. R., Zhao, M., Fargo, D. C., Hwang, J. Y., et al. (2011). Rapid activity-induced transcription of Arc and other IEGs relies on poised RNA polymerase II. Nat. Neurosci. 14, 848-856. doi: 10.1038/nn.2839
41. Shepherd, J. D., and Bear, M. F. (2011). New views of Arc, a master regulator of synaptic plasticity. Nat. Neurosci. 14, 279-284. doi: 10.1038/nn.2708
42. Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., et al. (2006). Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52, 475-484. doi: 10.1016/j.neuron.2006.08.034
43. Soule, J., Alme, M., Myrum, C., Schubert, M., Kanhema, T., and Bramham, C. R. (2012). Balancing Arc synthesis, mRNA decay, and proteasomal degradation: maximal protein expression triggered by rapid eye movement sleep-like bursts of muscarinic cholinergic receptor stimulation. J. Biol. Chem. 287, 22354-22366. doi: 10.1074/jbc.M112.376491
44. Takei, N., Inamura, N., Kawamura, M., Namba, H., Hara, K., Yonezawa, K., et al. (2004). Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J. Neurosci. 24, 9760-9769. doi: 10.1523/JNEUROSCI.1427-04.2004
45. Takeuchi, K., Gertner, M. J., Zhou, J., Parada, L. F., Bennett, M. V., and Zukin, R. S. (2013). Dysregulation of synaptic plasticity precedes appearance of morphological defects in a Pten conditional knockout mouse model of autism. Proc. Natl. Acad. Sci. U.S.A. 110, 4738-4743. doi: 10.1073/pnas.1222803110
46. Tian, X., and Feig, L. A. (2006). Age-dependent participation of Ras-GRF proteins in coupling calcium-permeable AMPA glutamate receptors to Ras/Erk signaling in cortical neurons. J. Biol. Chem. 281, 7578-7582. doi: 10.1074/jbc.M512060200
47. Toro, R., Konyukh, M., Delorme, R., Leblond, C., Chaste, P., Fauchereau, F., et al. (2010). Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends Genet. 26, 363-372. doi: 10.1016/j.tig.2010.05.007
48. Turrigiano, G. (2012). Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol. 4:a005736. doi: 10.1101/cshperspect.a005736
49. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., and Nelson, S. B. (1998). Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896. doi: 10.1038/36103
50. Watt, A. J., Van Rossum, M. C., Macleod, K. M., Nelson, S. B., and Turrigiano, G. G. (2000). Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26, 659-670. doi: 10.1016/S0896-6273(00)81202-7
51. Waung, M. W., Pfeiffer, B. E., Nosyreva, E. D., Ronesi, J. A., and Huber, K. M. (2008). Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59, 84-97. doi: 10.1016/j.neuron.2008.05.014
52. Wiegert, J. S., and Bading, H. (2011). 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
53. Ying, S. W., Futter, M., Rosenblum, K., Webber, M. J., Hunt, S. P., Bliss, T. V., et al. (2002). 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.
54. Yuan, L. L., Chen, X., Kunjilwar, K., Pfaffinger, P., and Johnston, D. (2006). Acceleration of K+ channel inactivation by MEK inhibitor U0126. Am. J. Physiol. Cell Physiol. 290, C165-C171. doi: 10.1152/ajpcell.00206.2005
55. Zoghbi, H. Y., and Bear, M. F. (2012). Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4, 1-22. doi: 10.1101/cshperspect.a009886