JNK1 inhibits GluR1 expression and GluR1-mediated calcium influx through phosphorylation and stabilization of Hes-1

Journal of Neuroscience

Volumn 32, Issue 5, 2012, Pages 1826-1846

  Lin, Cheng H ^a   Lee, Eminy H Y ^b  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; NOTCH RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR MASH1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM TRANSPORT; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; IMMUNOFLUORESCENCE; MALE; MUTAGENESIS; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SYNAPSE; WESTERN BLOTTING;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 8; PHOSPHORYLATION; PROTEIN STABILITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA;

EID: 84863054653     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3380-11.2012     Document Type: Article

References (47)

1. Bhat KM, Maddodi N, Shashikant C, Setaluri V (2006) Transcriptional regulation of human MAP2 gene in melanoma: role of neuronal bHLH factors and Notch1 signaling. Nucleic Acids Res 34:3819-3832.
2. Björkblom B, Ostman N, Hongisto V, Komarovski V, Filén JJ, Nyman TA, Kallunki T, Courtney MJ, Coffey ET (2005) Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 25:6350-6361.
3. Bogoyevitch MA, Kobe B (2006) Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases. Microbiol Mol Biol Rev 70:1061-1095.
4. Borges K, Dingledine R (2001) Functional organization of the GluR1 glutamate receptor promoter. J Biol Chem 276:25929-25938.
5. Boudreau AC, Reimers JM, Milovanovic M, Wolf ME (2007) Cell surface AMPAreceptors in the rat nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases. J Neurosci 27:10621-10635.
6. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37-40.
7. Chuang JY, Wang YT, Yeh SH, Liu YW, Chang WC, Hung JJ (2008) Phosphorylation by c-Jun NH2-terminal kinase 1 regulates the stability of transcription factor Sp1 during mitosis. Mol Biol Cell 19:1139-1151.
8. Costello DA, Herron CE (2004) The role of c-Jun N-terminal kinase in the A_-mediated impairment of LTP and regulation of synaptic transmission in the hippocampus. Neuropharmacology 46:655-662.
9. Curran BP, Murray HJ, O'Connor JJ (2003) A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1beta and long-term depression in the rat dentate gyrus in vitro. Neuroscience 118:347-357.
10. Curry CL, Reed LL, Nickoloff BJ, Miele L, Foreman KE (2006) Notchindependent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab Invest 86:842-852.
11. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
12. Dehmelt L, Smart FM, Ozer RS, Halpain S (2003) The role of microtubuleassociated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J Neurosci 23:9479-9490.
13. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
14. Fosbrink M, Aye-Han NN, Cheong R, Levchenko A, Zhang J (2010) Visualization of JNK activity dynamics with a genetically encoded fluorescent biosensor. Proc Natl Acad Sci U S A 107:5459-5464.
15. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
16. Fuchs SY, Adler V, Pincus MR, Ronai Z (1998) MEKK1/JNK signaling stabilizes and activates p53. Proc Natl Acad Sci U S A 95:10541-10546.
17. Grandbarbe L, Michelucci A, Heurtaux T, Hemmer K, Morga E, Heuschling P (2007) Notch signaling modulates the activation of microglial cells. Glia 55:1519-1530.
18. Gupta S, Campbell D, Dérijard B, Davis RJ (1995) Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267:389-393.
19. Gurd JW, Jones LR, Mahler HR, Moore WJ (1974) Isolation and partial characterization of rat brain synaptic plasma membranes. J Neurochem 22:281-290.
20. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
21. Humeau Y, Reisel D, Johnson AW, Borchardt T, Jensen V, Gebhardt C, Bosch V, Gass P, Bannerman DM, Good MA, Hvalby Ø, Sprengel R, Lüthi A (2007) A pathway-specific function for different AMPA receptor subunits in amygdala long-term potentiation and fear conditioning. J Neurosci 27:10947-10956.
22. Iordanov MS, Pribnow D, Magun JL, Dinh TH, Pearson JA, Chen SL, Magun BE (1997) Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the _-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17:3373-3381.
23. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13:1799-1805.
24. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9:3136-3148.
25. Ju BG, Solum D, Song EJ, Lee KJ, Rose DW, Glass CK, Rosenfeld MG (2004) Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell 119:815-829.
26. Kageyama R, Ohtsuka T (1999) The Notch-Hes pathway in mammalian neural development. Cell Res 9:179-188.
27. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306:343-348.
28. Kageyama R, Ohtsuka T, Kobayashi T (2008) Roles of Hes genes in neural development. Dev Growth Differ 50 [Suppl 1]:S97-S103.
29. Lee CT, Ma YL, Lee EH (2007) Serum-and glucocorticoid-inducible kinase1 enhances contextual fear memory formation through downregulation of the expression of Hes5. J Neurochem 100:1531-1542.
30. Mack V, Burnashev N, Kaiser KM, Rozov A, Jensen V, Hvalby O, Seeburg PH, Sakmann B, Sprengel R (2001) Conditional restoration of hippocampal synaptic potentiation in Glur-A-deficient mice. Science 292:2501-2504.
31. Makino H, Malinow R (2009) AMPAreceptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64:381-390.
32. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
33. Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006) Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res 1099:101-108.
34. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13-25.
35. Sanalkumar R, Indulekha CL, Divya TS, Divya MS, Anto RJ, Vinod B, Vidyanand S, Jagatha B, Venugopal S, James J (2010) ATF2 maintains a subset of neural progenitors through CBF1/Notch independent Hes-1 expression and synergistically activates the expression of Hes-1 in Notchdependent neural progenitors. J Neurochem 113:807-818.
36. Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev 6:2620-2634.
37. Schmitt WB, Sprengel R, Mack V, Draft RW, Seeburg PH, Deacon RM, Rawlins JN, Bannerman DM (2005) Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat Neurosci 8:270-272.
38. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331-343.
39. Stockhausen MT, Sjölund J, Axelson H (2005) Regulation of the Notch target gene Hes-1 by TGFalpha-induced Ras/MAPK signaling in human neuroblastoma cells. Exp Cell Res 310:218-228.
40. Ström A, Castella P, Rockwood J, Wagner J, Caudy M (1997) Mediation ofNGF signaling by post-translational inhibition of HES-1, a basic helix-loop-helix repressor of neuronal differentiation. Genes Dev 11:3168-3181.
41. Tai DJ, Hsu WL, Liu YC, Ma YL, Lee EH (2011) Novel role and mechanism of protein inhibitor of activated STAT1 in spatial learning. EMBO J 30:205-220.
42. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, Kageyama R (1994) Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem 269:5150-5156.
43. Thomas GM, Lin DT, Nuriya M, Huganir RL (2008) Rapid and bidirectional regulation of AMPA receptor phosphorylation and trafficking by JNK. EMBO J 27:361-372.
44. Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, Levit O, Zangen A (2008) Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem 107:522-532.
45. Yang YC, Lin CH, Lee EH (2006) Serum-and glucocorticoid-inducible kinase 1 (SGK1) increases neurite formation through microtubule depolymerization by SGK1 and by SGK1 phosphorylation of tau. Mol Cell Biol 26:8357-8370.
46. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Köster HJ, Borchardt T, Worley P, Lübke J, Frotscher M, Kelly PH, Sommer B, Andersen P, Seeburg PH, Sakmann B (1999) Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284:1805-1811.
47. Zhu Y, Pak D, Qin Y, McCormack SG, Kim MJ, Baumgart JP, Velamoor V, Auberson YP, Osten P, van Aelst L, Sheng M, Zhu JJ (2005) Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46: 905-916.