The nuclear calcium signaling target, activating transcription factor 3 (ATF3), protects against dendrotoxicity and facilitates the recovery of synaptic transmission after an excitotoxic insult

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9970-9982

  Ahlgren, Hanna ^a   Bas Orth, Carlos ^a   Freitag, H Eckehard ^a   Hellwig, Andrea ^a   Ottersen, Ole Petter ^b   Bading, Hilmar ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; GENES; MICROELECTRODES; NEURONS; SIGNAL ENCODING; TRANSCRIPTION; TRANSCRIPTION FACTORS;

ACTIVATING TRANSCRIPTION FACTOR; CALCIUM SIGNALING; EXCITOTOXIC INJURY; HIPPOCAMPAL NEURONS; MICROELECTRODE ARRAY; NEURONAL NETWORKS; PATHOLOGICAL CONDITIONS; SYNAPTIC TRANSMISSION;

NEURAL NETWORKS;

ACTIVATING TRANSCRIPTION FACTOR 3; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DENDRITE; EXCITOTOXICITY; GENE SILENCING; HIPPOCAMPUS; MOUSE; NERVE CELL NECROSIS; NERVE CELL NETWORK; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION;

CALCIUM SIGNALING; CELL SIGNALING; GENE EXPRESSION; GLUTAMATE RECEPTORS IONOTROPIC (AMPA, NMDA); NEUROBIOLOGY; NEURODEGENERATION; NEUROPROTECTION; NEUROTRANSMITTERS; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; BRAIN ISCHEMIA; CALCIUM SIGNALING; CELL DEATH; DENDRITES; EXCITATORY AMINO ACID AGONISTS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; MICE; N-METHYLASPARTATE; NERVE NET; NERVE TISSUE PROTEINS; SYNAPTIC TRANSMISSION; TRANSCRIPTION, GENETIC;

EID: 84898064607     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.502914     Document Type: Article

References (67)

1. Lipton, S. A., and Rosenberg, P. A. (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622
2. Katsura, K., Kristián, T., and Siesjö, B. K. (1994) Energy metabolism, ion homeostasis, and cell damage in the brain. Biochem. Soc. Trans. 22, 991-996
3. Olney, J. W. (1969) Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164, 719-721
4. Dirnagl, U., Iadecola, C., and Moskowitz, M. A. (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397
5. Hardingham, G. E., Fukunaga, Y., and Bading, H. (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414
6. Hardingham, G. E., and Bading, H. (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696
7. Olney, J. W., Fuller, T., and de Gubareff, T. (1979) Acute dendrotoxic changes in the hippocampus of kainate-treated rats. Brain Res. 176, 91-100
8. Hori, N., and Carpenter, D. O. (1994) Functional and morphological changes induced by transient in vivo ischemia. Exp. Neurol. 129, 279-289
9. von Lubitz, D. K., and Diemer, N. H. (1983) Cerebral ischemia in the rat: ultrastructural and morphometric analysis of synapses in stratum radia-tum of the hippocampal CA-1 region. Acta Neuropathol. 61, 52-60
10. Risher, W. C, Ard, D., Yuan, J., and Kirov, S. A. (2010) Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J. Neurosci. 30, 9859-9868
11. Risher, W. C, Lee, M. R., Fomitcheva, I. V., Hess, D. C, and Kirov, S. A. (2011) Dibucaine mitigates spreading depolarization in human neocorti-cal slices and prevents acute dendritic injury in the ischemic rodent neocortex. PLoS One 6, e22351
12. Enright, L. E., Zhang, S., and Murphy, T. H. (2007) Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J. Cereb. Blood Flow Metab. 27, 1185-1200
13. Murphy, T. H, Li, P., Betts, K., and Liu, R. (2008) Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J. Neurosci. 28, 1756-1772
14. Sigler, A., and Murphy, T. H. (2010) In vivo 2-photon imaging of fine structure in the rodent brain: before, during, and after stroke. Stroke 41, S117-S123
15. Zhang, S., Boyd, J., Delaney, K., and Murphy, T. H. (2005) Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J. Neurosci. 25, 5333-5338
16. 2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J. Neurosci. 25, 4279-4287
17. Zhang, S. J., Zou, M., Lu, L., Lau, D., Ditzel, D. A., Delucinge-Vivier, C, Aso, Y., Descombes, P., and Bading, H. (2009) Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet. 5, e1000604
18. Lee, B., Butcher, G. Q., Hoyt, K. R., Impey, S., and Obrietan, K. (2005) Activity-dependent neuroprotection and cAMP response element-binding protein (CREB): Kinase coupling, stimulus intensity, and temporal regulation of CREB phosphorylation at serine 133. J. Neurosci. 25, 1137-1148
19. Zhang, S. J., Steijaert, M. N, Lau, D., Schütz, G., Delucinge-Vivier, C, Descombes, P., and Bading, H. (2007) Decoding NMDA receptor signaling: Identification of genomic programs specifying neuronal survival and death. Neuron 53, 549-562
20. Zhang, S. J., Buchthal, B., Lau, D., Hayer, S., Dick, O., Schwaninger, M., Veltkamp, R., Zou, M., Weiss, U., and Bading, H. (2011) A signaling cascade of nuclear calcium-CREB-ATF3 activated by synaptic NMDA receptors defines a gene repression module that protects against extrasynaptic NMDA receptor-induced neuronal cell death and ischemic brain damage. J. Neurosci. 31, 4978-4990
21. Bading, H., and Greenberg, M. E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912-914
22. Soriano, F. X., Papadia, S., Hofmann, F., Hardingham, N. R., Bading, H, and Hardingham, G. E. (2006) Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J. Neurosci. 26, 4509-4518
23. Arnold, F. J., Hofmann, F., Bengtson, C. P., Wittmann, M., Vanhoutte, P., and Bading, H. (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity. J. Physiol. 564, 3-19
24. Bading, H., Ginty, D. D., and Greenberg, M. E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260, 181-186
25. Wiegert, J. S., Bengtson, C. P., and Bading, H. (2007) Diffusion and not active transport underlies and limits ERK1/2 synapse-to-nucleus signaling in hippocampal neurons. J. Biol. Chem. 282, 29621-29633
26. Lau, D., and Bading, H. (2009) Synaptic activity-mediated suppression of p53 and induction of nuclear calcium-regulated neuroprotective genes promote survival through inhibition of mitochondrial permeability transition. J. Neurosci. 29, 4420-4429
27. Klugmann, M., Symes, C. W., Leichtlein, C. B., Klaussner, B. K., Dunning, J., Fong, D., Young, D., and During, M. J. (2005) AAV-mediated hip-pocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol. Cell. Neurosci. 28, 347-360
28. Tauskela, J. S., Comas, T., Hewitt, K., Monette, R., Paris, J., Hogan, M., and Morley, P. (2001) Cross-tolerance to otherwise lethal N-methyl-D-aspar-tate and oxygen-glucose deprivation in preconditioned cortical cultures. Neuroscience 107, 571-584
29. Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212
30. Faddis, B.T., Hasbani, M. J., and Goldberg, M. P. (1997) Calpain activation contributes to dendritic remodeling after brief excitotoxic injury in vitro. J. Neurosci. 17, 951-959
31. Ikegaya, Y., Kim, J. A., Baba, M., Iwatsubo, T., Nishiyama, N., and Matsuki, N. (2001) Rapid and reversible changes in dendrite morphology and syn-aptic efficacy following NMDA receptor activation: implication for a cellular defense against excitotoxicity. J. Cell Sci. 114, 4083-4093
32. Hasbani, M. J., Hyrc, K. L., Faddis, B. T., Romano, C., and Goldberg, M. P. (1998) Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp. Neurol. 154, 241-258
33. Hasbani, M. J., Schlief, M. L., Fisher, D. A., and Goldberg, M. P. (2001) Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J. Neurosci. 21, 2393-2403
34. Park, J. S., Bateman, M. C., and Goldberg, M. P. (1996) Rapid alterations in dendrite morphology during sublethal hypoxia or glutamate receptor activation. Neurobiol. Dis. 3, 215-227
35. Brewer, L. D., Thibault, O., Staton, J., Thibault, V., Rogers, J. T., Garcia-Ramos, G., Kraner, S., Landfield, P. W., and Porter, N. M. (2007) Increased vulnerability of hippocampal neurons with age in culture: temporal association with increases in NMDA receptor current, NR2A subunit expression, and recruitment of L-type calcium channels. Brain Res. 1151, 20-31
36. Rintoul, G. L., Filiano, A. J., Brocard, J. B., Kress, G. J., and Reynolds, I. J. (2003) Glutamate decreases mitochondrial size and movement in primary forebrain neurons. J. Neurosci. 23, 7881-7888
37. Greenwood, S. M., Mizielinska, S. M., Frenguelli, B. G., Harvey, J., and Connolly, C. N. (2007) Mitochondrial dysfunction and dendritic beading during neuronal toxicity. J. Biol. Chem. 282, 26235-26244
38. Macaskill, A. F., Rinholm, J. E., Twelvetrees, A. E., Arancibia-Carcamo, I. L., Muir, J., Fransson, A., Aspenstrom, P., Attwell, D., and Kittler, J. T. (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541-555
39. Andrew, R. D., Labron, M.W., Boehnke, S.E., Carnduff, L., and Kirov, S. A. (2007) Physiological evidence that pyramidal neurons lack functional water channels. Cereb. Cortex 17, 787-802
40. Li, P., and Murphy, T. H. (2008) Two-photon imaging during prolonged middle cerebral artery occlusion in mice reveals recovery of dendritic structure after reperfusion. J. Neurosci. 28, 11970-11979
41. Petito, C. K., and Pulsinelli, W. A. (1984) Delayed neuronal recovery and neuronal death in rat hippocampus following severe cerebral ischemia: possible relationship to abnormalities in neuronal processes. J. Cereb. Blood Flow Metab. 4, 194-205
42. Hasbani, M. J., Viquez, N. M., and Goldberg, M. P. (2001) NMDA receptors mediate hypoxic spine loss in cultured neurons. Neuroreport 12, 2731-2735
43. Risher, W. C., Andrew, R. D., and Kirov, S. A. (2009) Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57, 207-221
44. Bengtson, C. P., Dick, O., and Bading, H. (2008) A quantitative method to assess extrasynaptic NMDA receptor function in the protective effect of synaptic activity against neurotoxicity. BMC Neurosci. 9, 11
45. Papadia, S., Soriano, F. X., Léveillé, F., Martel, M. A., Dakin, K. A., Hansen, H. H., Kaindl, A., Sifringer, M., Fowler, J., Stefovska, V., McKenzie, G., Craigon, M., Corriveau, R., Ghazal, P., Horsburgh, K., Yankner, B. A., Wyllie, D. J., Ikonomidou, C, and Hardingham, G. E. (2008) Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476-487
46. Buchs, P. A., andMuller, D. (1996) Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc. Natl. Acad. Sci. U.S.A. 93, 8040-8045
47. Wang, J., Campos, B., Jamieson, G. A., Jr., Kaetzel, M. A., andDedman, J. R. (1995) Functional elimination of calmodulin within the nucleus by targeted expression of an inhibitor peptide. J. Biol. Chem. 270, 30245-30248
48. Seijffers, R., Allchorne, A. J., and Woolf, C. J. (2006) The transcription factor ATF-3 promotes neurite outgrowth. Mol. Cell. Neurosci. 32, 143-154
49. Seijffers, R., Mills, C. D., and Woolf, C. J. (2007) ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J. Neurosci. 27, 7911-7920
50. Matesic, D. F., and Lin, R. C. (1994) Microtubule-associated protein 2 as an early indicator of ischemia-induced neurodegeneration in the gerbil fore-brain. J. Neurochem. 63, 1012-1020
51. Dreier, J. P. (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med. 17, 439-447
52. Schliwa, M., Euteneuer, U., Bulinski, J. C., and Izant, J. G. (1981) Calcium lability of cytoplasmic microtubules and its modulation by microtubule-associated proteins. Proc. Natl. Acad. Sci. U.S.A. 78, 1037-1041
53. Hoskison, M. M., andShuttleworth, C. W. (2006) Microtubule disruption, not calpain-dependent loss of MAP2, contributes to enduring NMDA-induced dendritic dysfunction in acute hippocampal slices. Exp. Neurol. 202, 302-312
54. Emery, D. G., and Lucas, J. H. (1995) Ultrastructural damage and neuritic beading in cold-stressed spinal neurons with comparisons to NMDA and A23187 toxicity. Brain Res. 692, 161-173
55. 2+]i and protects hippocampal neurons against excitotoxicity. Brain Res. 689, 141-146
56. Tseng, C. Y., and Firestein, B. L. (2011) The role of PSD-95 and cypin in morphological changes in dendrites following sublethal NMDA exposure. J. Neurosci. 31, 15468-15480
57. Pekny, M., and Nilsson, M. (2005) Astrocyte activation and reactive gliosis. Glia 50, 427-434
58. Amiry-Moghaddam, M., and Ottersen, O. P. (2003) The molecular basis of water transport in the brain. Nat. Rev. Neurosci. 4, 991-1001
59. Nielsen, S., Nagelhus, E. A., Amiry-Moghaddam, M., Bourque, C, Agre, P., and Ottersen, O. P. (1997) Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17, 171-180
60. Somjen, G. G., Faas, G. C, Vreugdenhil, M., and Wadman, W. J. (1993) Channel shutdown: A response of hippocampal neurons to adverse environments. Brain Res. 632, 180-194
61. MacAulay, N, and Zeuthen, T. (2010) Water transport between CNS compartments: Contributions of aquaporins and cotransporters. Neuro-science 168, 941-956
62. Anderson, T. R., Jarvis, C. R., Biedermann, A. J., Molnar, C, and Andrew, R. D. (2005) Blocking the anoxic depolarization protects without functional compromise following simulated stroke in cortical brain slices. J. Neurophysiol. 93, 963-979
63. 2+ homeostasis in neuronal dendrites is a downstream consequence of metabolic compromise during extended NMDA exposures. J. Neurosci. 28, 5029-5039
64. 2+ homeostasis and mitochondrial dysfunction following in vitro ischemia. J. Biol. Chem. 285, 35155-35168
65. Dick, O., and Bading, H. (2010) Synaptic activity and nuclear calcium signaling protect hippocampal neurons from death signal-associated nuclear translocation of FoxO3a induced by extrasynaptic N-methyl-D-as-partate receptors. J. Biol. Chem. 285, 19354-19361
66. Léveillé, F., El Gaamouch, F., Gouix, E., Lecocq, M., Lobner, D., Nicole, O., and Buisson, A. (2008) Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J. 22, 4258-4271
67. Nakagomi, S., Suzuki, Y., Namikawa, K., Kiryu-Seo, S., and Kiyama, H. (2003) Expression of the activating transcription factor 3 prevents c-Jun N-terminal kinase-induced neuronal death by promoting heat shock protein 27 expression and Akt activation. J. Neurosci. 23, 5187-5196