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

Journal of Neuroscience

Volumn 31, Issue 13, 2011, Pages 4978-4990

  Zhang, Sheng Jia ^a,b   Buchthal, Bettina ^a   Lau, David ^a   Hayer, Stefanie ^a   Dick, Oliver ^a   Schwaninger, Markus ^a   Veltkamp, Roland ^a   Zou, Ming ^a,c   Weiss, Ursula ^a   Bading, Hilmar ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVOVIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; BRAIN ISCHEMIA; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; GENE REPRESSION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; SYNAPSE;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; BRAIN ISCHEMIA; CALCIUM SIGNALING; CELL DEATH; CELL NUCLEUS; CELLS, CULTURED; CHICKENS; CREB-BINDING PROTEIN; GENE SILENCING; MALE; MICE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 79955721239     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2672-10.2011     Document Type: Article

References (61)

1. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C (1998) A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 18:967-977.
2. Anderson DJ (1999) Lineages and transcription factors in the specification of vertebrate primary sensory neurons. Curr Opin Neurobiol 9:517-524.
3. 2+/calmodulin-dependent protein kinase IV. Mol Endocrinol 11:725-737.
4. Arnold FJ, Hofmann F, Bengtson CP, Wittmann M, Vanhoutte P, Bading H (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesisdependent plasticity. J Physiol 564:3-19.
5. Bading H (2000) Transcription-dependent neuronal plasticity: The nuclear calcium hypothesis. Eur J Biochem 267:5280-5283.
6. Bading H, Greenberg ME (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253:912-914.
7. Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181-186.
8. Bading H, Segal MM, Sucher NJ, Dudek H, Lipton SA, Greenberg ME (1995) N-methyl-D-aspartate receptors are critical for mediating the effects of glutamate on intracellular calcium concentration and immediate early gene expression in cultured hippocampal neurons. Neuroscience 64:653-664.
9. Bengtson CP, Weislogel J-M, Freitag HE, Bading H (2010) Nuclear calcium sensors reveal that repetition of trains of synaptic stimuli boosts nuclear calcium signaling in CA1 pyramidal neurons. Biophys J 99:4066-4077.
10. Bossy-Wetzel E, Schwarzenbacher R, Lipton SA (2004) Molecular pathways to neurodegeneration. Nat Med 10:S2-S9.
11. Carlezon WA Jr, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science 282:2272-2275.
12. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436-445.
13. Chawla S, Hardingham GE, Quinn DR, Bading H (1998) CBP: a signalregulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science 281:1505-1509.
14. Chen BP, Liang G, Whelan J, Hai T (1994) ATF3 and ATF3ΔZip: transcriptional repression versus activation by alternatively spliced isoforms. J Biol Chem 269:15819-15826.
15. Curran T, Morgan JI (1995) Fos: an immediate-early transcription factor in neurons. J Neurobiol 26:403-412.
16. DeKosky ST, Scheff SW (1990) Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27:457-464.
17. Dequéant ML, Pourquié O (2008) Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9:370-382.
18. Fan MM, Fernandes HB, Zhang LY, Hayden MR, Raymond LA (2007) Altered NMDA receptor trafficking in a yeast artificial chromosome transgenic mouse model of Huntington's disease. J Neurosci 27:3768-3779.
19. Fernandes HB, Baimbridge KG, Church J, Hayden MR, Raymond LA (2007) Mitochondrial sensitivity and altered calcium handling underlie enhanced NMDA-induced apoptosis in YAC128 model of Huntington's disease. J Neurosci 27:13614-13623.
20. Fujita N, Jaye DL, Geigerman C, Akyildiz A, Mooney MR, Boss JM, Wade PA (2004) MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119:75-86.
21. Giachino C, De Marchis S, Giampietro C, Parlato R, Perroteau I, Schütz G, Fasolo A, Peretto P (2005) cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J Neurosci 25:10105-10118.
22. Han J, Jiang Y, Li Z, Kravchenko VV, Ulevitch RJ (1997) Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386:296-299.
23. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696.
24. Hardingham GE, Chawla S, Johnson CM, Bading H (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260-265.
25. Hardingham GE, Arnold FJ, Bading H (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4:261-267.
26. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414.
27. Herrmann O, Baumann B, de Lorenzi R, Muhammad S, Zhang W, Kleesiek J, Malfertheiner M, Köhrmann M, Potrovita I, Maegele I, Beyer C, Burke JR, Hasan MT, Bujard H, Wirth T, Pasparakis M, Schwaninger M (2005) IKK mediates ischemia-induced neuronal death. Nat Med 11:1322-1329.
28. Klugmann M, Symes CW, Leichtlein CB, Klaussner BK, Dunning J, Fong D, Young D, During MJ (2005) AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adults rats. Mol Cell Neurosci 28:347-360.
29. Lassmann H, Fischer P, Jellinger K (1993) Synaptic pathology of Alzheimer's disease. Ann NY Acad Sci 695:59-64.
30. Lau D, 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.
31. Lee B, Butcher GQ, Hoyt KR, Impey S, Obrietan K (2005) Activitydependent 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.
32. Lemrow SM, Anderson KA, Joseph JD, Ribar TJ, Noeldner PK, Means AR (2004) Catalytic activity is required for calcium/calmodulin-dependent protein kinase IV to enter the nucleus. J Biol Chem 279:11664-11671.
33. Liang G, Wolfgang CD, Chen BP, Chen TH, Hai T (1996) ATF3 gene: genomic organization, promoter, and regulation. J Biol Chem 271:1695-1701.
34. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
35. Mantamadiotis T, Lemberger T, Bleckmann SC, Kern H, Kretz O, Martin Villalba A, Tronche F, Kellendonk C, Gau D, Kapfhammer J, Otto C, Schmid W, Schütz G (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat Genet 31:47-54.
36. Mao Z, Bonni A, Xia F, Nadal-Vicens M, Greenberg ME (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 286:785-790.
37. Martinou JC, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, Talabot D, Catsicas S, Pietra C, Huarte J (1994) Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030.
38. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599-609.
39. McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27:40-47.
40. Milnerwood AJ, Gladding CM, Pouladi MA, Kaufman AM, Hines RM, Boyd JD, Ko RW, Vasuta OC, Graham RK, Hayden MR, Murphy TH, Raymond LA (2010) Early increase in extrasynapticNMDAreceptor signaling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 65:178-190.
41. Molkentin JD, Black BL, Martin JF, Olson EN (1996) Mutational analysis of the DNA binding, dimerization, and transcriptional activation domains of MEF2C. Mol Cell Biol 16:2627-2636.
42. Murikinati S, Jüttler E, Keinert T, Ridder DA, Muhammad S, Waibler Z, Ledent C, Zimmer A, Kalinke U, Schwaninger M (2010) Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment. FASEB J 24:788-798.
43. Okamoto S, Pouladi MA, Talantova M, Yao D, Xia P, Ehrnhoefer DE, Zaidi R, Clemente A, Kaul M, Graham RK, Zhang D, Vincent Chen HS, Tong G, Hayden MR, Lipton SA (2009) Balance between synaptic versus extrasynaptic NMD Areceptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15:1407-1413.
44. Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443:768-773.
45. Papadia S, Stevenson P, Hardingham NR, Bading H, Hardingham GE (2005) Nuclear calcium and CREB family mediate a late phase of activitydependent neuroprotection. J Neurosci 25:4279-4287.
46. Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6:893-904.
47. Peel AD, Chipman AD, Akam M (2005) Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6:905-916.
48. Riccio A, Ahn S, Davenport CM, Blendy JA, Ginty DD (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286:2358-2361.
49. Schmued LC, Stowers CC, Scallet AC, Xu L (2005) Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res 1035:24-31.
50. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27:2866-2875.
51. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-148.
52. Smith R, Brundin P, Li JY (2005) Synaptic dysfunction in Huntington's disease: a new perspective. Cell Mol Life Sci 62:1901-1912.
53. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev 8:2527-2539.
54. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
55. Wang J, Campos B, Jamieson GA Jr, Kaetzel MA, Dedman JR (1995) Functional elimination of calmodulin within the nucleus by targeted expression of an inhibitor peptide. J Biol Chem 270:30245-30248.
56. Yamamoto-Sasaki M, Ozawa H, Saito T, Rösler M, Riederer P (1999) Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res 824:300-303.
57. Youn HD, Chatila TA, Liu JO (2000) Integration of calcineurin and MEF2 signals by the coactivator p300 during T-cell apoptosis. EMBO J 19:4323-4331.
58. Zhang SJ, Steijaert MN, Lau D, Schütz G, Delucinge-Vivier C, Descombes P, Bading H (2007) Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53:549-562.
59. Zhang SJ, Zou M, Lu L, Lau D, Ditzel DA, Delucinge-Vivier C, Aso Y, Descombes P, 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.
60. Zhang W, Potrovita I, Tarabin V, Herrmann O, Beer V, Weih F, Schneider A, Schwaninger M (2005) Neuronal activation of NF-kappaB contributes to cell death in cerebral ischemia. J Cereb Blood Flow Metab 25:30-40.
61. Zhu DY, Lau L, Liu SH, Wei JS, Lu YM (2004) Activation of cAMPresponse-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A 101:9453-9457.