N-methyl-D-aspartate-stimulated ERK1/2 signaling and the transcriptional up-regulation of plasticity-related genes are developmentally regulated following in vitro neuronal maturation

Journal of Neuroscience Research

Volumn 87, Issue 12, 2009, Pages 2632-2644

  Zhou, Xianju ^a   Moon, Changjong ^a,b   Zheng, Fei ^c   Luo, Yongneng ^a   Soellner, Deborah ^a   Nuñez, Joseph L ^a   Wang, Hongbing ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Chonnam National University   (South Korea)

^c Michigan State University   (United States)

Author keywords

BDNF; Ca2+ stimulated signaling; CREB; ERK; Neuronal maturation; NMDA receptors

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMEDIATE EARLY PROTEIN; IMMEDIATE EARLY PROTEIN ZIF268; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIFEDIPINE; POTASSIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN CELL; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXON; GENETIC TRANSCRIPTION; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNEL BLOCKERS; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 70449487175     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22103     Document Type: Article

References (58)

1. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. 2007. Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85:525-535. (Pubitemid 46318317)
2. Akopian G, Walsh JP. 2006. Pre- and postsynaptic contributions to age-related alterations in corticostriatal synaptic plasticity. Synapse 60:223-238. (Pubitemid 44036717)
3. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, Mansuy I, Hawkins RD, Kandel ER. 1999. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci U S A 96:5280-5285. (Pubitemid 29214574)
4. 2+ - and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
5. Bozon B, Davis S, Laroche S. 2002. Regulated transcription of the immediate- early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation. Hippocampus 12:570-577. (Pubitemid 35363951)
6. Brewer LD, Thibault O, Staton J, Thibault V, Rogers JT, Garcia-Ramos G, Kraner S, Landfield PW, Porter NM. 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. (Pubitemid 46709872)
7. Carmignoto G, Vicini S. 1992. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258:1007-1011.
8. Davis S, Vanhoutte P, Pages C, Caboche J, Laroche S. 2000. 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. (Pubitemid 30396622)
9. Dotti CG, Sullivan CA, Banker GA. 1988. The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
10. English JD, Sweatt JD. 1997. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
11. Fogal B, Trettel J, Uliasz TF, Levine ES, Hewett SJ. 2005. Changes in secondary glutamate release underlie the developmental regulation of excitotoxic neuronal cell death. Neuroscience 132:929-942. (Pubitemid 40602529)
12. Foster TC, Kumar A. 2002. Calcium dysregulation in the aging brain. Neuroscientist 8:297-301.
13. 2+-dependent processes: relation to hippocampal synaptic plasticity. Hippocampus 7:602-612.
14. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM. 2002. Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418:970-975. (Pubitemid 34976031)
15. Ghosh A, Greenberg ME. 1995. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268:239-247.
16. Ginty DD. 1997. Calcium regulation of gene expression: isn't that spatial? Neuron 18:183-186.
17. Hagiwara M, Alberts A, Brindle P, Meinkoth J, Feramisco J, Deng T, Karin M, Shenolikar S, Montminy M. 1992. Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell 70:105-113.
18. 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. (Pubitemid 34454245)
19. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
20. 2+/calmodulin- dependent protein kinases in cultured rat hippocampal neurons. J Biol Chem 274:9061-9067.
21. Kemp N, Bashir ZI. 2001. Long-term depression: a cascade of induction and expression mechanisms. Prog Neurobiol 65:339-365. (Pubitemid 32781668)
22. Kitagawa K. 2007. CREB and cAMP response element-mediated gene expression in the ischemic brain. FEBS J 274:3210-3217. (Pubitemid 47024985)
23. Konur S, Ghosh A. 2005. Calcium signaling and the control of dendritic development. Neuron 46:401-405. (Pubitemid 40616883)
24. Lanahan A, Worley P. 1998. Immediate-early genes and synaptic function. Neurobiol Learn Mem 70:37-43.
25. Lopez de Armentia M, Jancic D, Olivares R, Alarcon JM, Kandel ER, Barco A. 2007. cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J Neurosci 27:13909-13918. (Pubitemid 350278263)
26. Lynch MA. 2004. Long-term potentiation and memory. Physiol Rev 84:87-136.
27. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
28. Mao L, Yang L, Arora A, Choe ES, Zhang G, Liu Z, Fibuch EE, Wang JQ. 2005. Role of protein phosphatase 2A in mGluR5-regulated MEK/ERK phosphorylation in neurons. J Biol Chem 280:12602-12610. (Pubitemid 40491078)
29. Mazzucchelli C, Brambilla R. 2000. Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell Mol Life Sci 57:604-611. (Pubitemid 30311431)
30. McNaughton BL, Barnes CA, Rao G, Baldwin J, Rasmussen M. 1986. Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci 6:563-571. (Pubitemid 16125051)
31. Moser EI, Krobert KA, Moser MB, Morris RG. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-2042. (Pubitemid 28475493)
32. Norris CM, Korol DL, Foster TC. 1996. Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 16:5382-5392. (Pubitemid 26277867)
33. Nunez JL, McCarthy MM. 2007. Evidence for an extended duration of GABA-mediated excitation in the developing male vs. female hippocampus. Dev Neurobiol 67:1879-1890.
34. Peltier J, O'Neill A, Schaffer DV. 2007. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol 67:1348-1361. (Pubitemid 47242761)
35. Porte Y, Buhot MC, Mons N. 2008. Alteration of CREB phosphorylation and spatial memory deficits in aged 129T2/Sv mice. Neurobiol Aging 29:1533-1546.
36. Porter NM, Thibault O, Thibault V, Chen KC, Landfield PW. 1997. Calcium channel density and hippocampal cell death with age in long-term culture. J Neurosci 17:5629-5639. (Pubitemid 27300327)
37. Rolli M, Kotlyarov A, Sakamoto KM, Gaestel M, Neininger A. 1999. Stress-induced stimulation of early growth response gene-1 by p38/ stress-activated protein kinase 2 is mediated by a cAMP-responsive promoter element in a MAPKAP kinase 2-independent manner. J Biol Chem 274:19559-19564. (Pubitemid 129519395)
38. Rosenzweig ES, Barnes CA. 2003. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179.
39. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA. 1997. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7:549-558. (Pubitemid 27453811)
40. Sala C, Rudolph-Correia S, Sheng M. 2000. Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element- binding protein (CREB) in hippocampal neurons. J Neurosci 20:3529-3536. (Pubitemid 30266214)
41. Shankar S, Teyler TJ, Robbins N. 1998. Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 79:334-341. (Pubitemid 28133824)
42. Soriano FX, Papadia S, Hofmann F, Hardingham NR, Bading H, Hardingham GE. 2006. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 26:4509-4518. (Pubitemid 44315350)
43. Suuronen T, Kolehmainen P, Salminen A. 2000. Protective effect of L-deprenyl against apoptosis induced by okadaic acid in cultured neuronal cells. Biochem Pharmacol 59:1589-1595. (Pubitemid 30229893)
44. Sweatt JD. 2004. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317. (Pubitemid 38759861)
45. 2+ channels. J Biol Chem 275:17269-17275.
46. Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME. 1998. Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726. (Pubitemid 28199050)
47. Tian J, Karin M. 1999. Stimulation of Elk1 transcriptional activity by mitogen-activated protein kinases is negatively regulated by protein phosphatase 2B (calcineurin). J Biol Chem 274:15173-15180. (Pubitemid 129518856)
48. Tomobe K, Okuma Y, Nomura Y. 2007. Impairment of CREB phosphorylation in the hippocampal CA1 region of the senescence-accelerated mouse (SAM) P8. Brain Res 1141:214-217. (Pubitemid 46365635)
49. Waltereit R, Weller M. 2003. Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27:99-106. (Pubitemid 36515162)
50. 2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J Neurosci 21: 5484-5493.
51. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME. 2001. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031. (Pubitemid 32928677)
52. West AE, Griffith EC, Greenberg ME. 2002. Regulation of transcription factors by neuronal activity. Nat Rev Neurosci 3:921-931. (Pubitemid 135715879)
53. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER. 1999. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
54. Xia Z, Dudek H, Miranti CK, Greenberg ME. 1996. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J Neurosci 16:5425-5436. (Pubitemid 26277871)
55. Yi KD, Covey DF, Simpkins JW. 2009. Mechanism of okadaic acid induced neuronal death and the effect of estrogens. J Neurochem 108:732-740.
56. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, Bliss TV, Bramham CR. 2002. Brain-derived neurotrophic factor induces longterm potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22:1532-1540. (Pubitemid 35386272)
57. Yoon S, Choi J, Yoon J, Huh JW, Kim D. 2006. Okadaic acid induces JNK activation, bim overexpression and mitochondrial dysfunction in cultured rat cortical neurons. Neurosci Lett 394:190-195. (Pubitemid 43144848)
58. Zheng F, Soellner D, Nunez J, Wang H. 2008. The basal level of intracellular calcium gates the activation of phosphoinositide 3-kinase-Akt signaling by brain-derived neurotrophic factor in cortical neurons. J Neurochem 106:1259-1274.