Pituitary adenylate cyclase-activating peptide induces long-lasting neuroprotection through the induction of activity-dependent signaling via the cyclic AMP response element-binding protein-regulated transcription co-activator 1

Journal of Neurochemistry

Volumn 118, Issue 3, 2011, Pages 365-378

  Baxter, Paul S ^a   Martel, Marc Andre ^a   McMahon, Aoife ^a   Kind, Peter C ^a   Hardingham, Giles E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Ca2+ signaling; CREB; gene regulation; neuroprotective signalling; neurotoxicity; transcription factors

Indexed keywords

ADENYLATE CYCLASE; CALCINEURIN; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN REGULATED TRANSCRIPTION COACTIVATOR 1; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; SERINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INDUCTION; GENE EXPRESSION; NERVE CELL STIMULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CALCINEURIN; CALCIUM; CELL DEATH; CELL NUCLEUS; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHYSIOLOGICAL PHENOMENA; NEUROPROTECTIVE AGENTS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STAUROSPORINE; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 79960313884     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07330.x     Document Type: Article

References (91)

1. Al-Mubarak B., Soriano F. X., and, Hardingham G. E., (2009) Synaptic NMDAR activity suppresses FOXO1 expression via a cis-acting FOXO binding site: FOXO1 is a FOXO target gene. Channels (Austin, Tex) 3, 233-238.
2. Atlasz T., Szabadfi K., Kiss P., et al. (2010) Pituitary adenylate cyclase activating polypeptide in the retina: focus on the retinoprotective effects. Ann. N Y Acad. Sci. 1200, 128-139.
3. Aubert N., Falluel-Morel A., Vaudry D., et al. (2006) PACAP and C2-ceramide generate different AP-1 complexes through a MAP-kinase-dependent pathway: involvement of c-Fos in PACAP-induced Bcl-2 expression. J. Neurochem. 99, 1237-1250. (Pubitemid 44655288)
4. Bading H., and, Greenberg M. E., (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science 253, 912-914. (Pubitemid 21917237)
5. Banke T. G., Bowie D., Lee H., Huganir R. L., Schousboe A., and, Traynelis S. F., (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 20, 89-102. (Pubitemid 30220495)
6. Bell K. F., and, Hardingham G. E., (2011) The influence of synaptic activity on neuronal health. Curr. Opin. Neurobiol. 21, 299-305.
7. Biegon A., Fry P. A., Paden C. M., Alexandrovich A., Tsenter J., and, Shohami E., (2004) Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: implications for treatment of neurological and cognitive deficits. Proc. Natl Acad. Sci. USA 101, 5117-5122. (Pubitemid 38469212)
8. Bittinger M. A., McWhinnie E., Meltzer J., et al. (2004) Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins. Curr. Biol. 14, 2156-2161. (Pubitemid 39623199)
9. Bonni A., Brunet A., West A. E., Datta S. R., Takasu M. A., and, Greenberg M. E., (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358-1362.
10. Botia B., Basille M., Allais A., et al. (2007) Neurotrophic effects of PACAP in the cerebellar cortex. Peptides 28, 1746-1752. (Pubitemid 47361422)
11. Brandon E. P., Logue S. F., Adams M. R., et al. (1998) Defective motor behavior and neural gene expression in RIIbeta-protein kinase A mutant mice. J. Neurosci. 18, 3639-3649. (Pubitemid 28225672)
12. Brenneman D. E., (2007) Neuroprotection: a comparative view of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Peptides 28, 1720-1726. (Pubitemid 47371032)
13. Chawla S., Hardingham G. E., Quinn D. R., and, Bading H., (1998) CBP: a signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science 281, 1505-1509. (Pubitemid 28425574)
14. Chen Y., Samal B., Hamelink C. R., Xiang C. C., Chen M., Vaudry D., Brownstein M. J., Hallenbeck J. M., and, Eiden L. E., (2006) Neuroprotection by endogenous and exogenous PACAP following stroke. Regul. Pept. 137, 4-19. (Pubitemid 44751193)
15. Chrivia J. C., Kwok R. P. S., Lamb N., Hagiwara M., Montminy M. R., and, Goodman R. H., (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859. (Pubitemid 23341031)
16. Conkright M. D., Canettieri G., Screaton R., Guzman E., Miraglia L., Hogenesch J. B., and, Montminy M., (2003) TORCs: transducers of regulated CREB activity. Mol. Cell 12, 413-423. (Pubitemid 37238928)
17. Costa L., Santangelo F., Li Volsi G., and, Ciranna L., (2009) Modulation of AMPA receptor-mediated ion current by pituitary adenylate cyclase-activating polypeptide (PACAP) in CA1 pyramidal neurons from rat hippocampus. Hippocampus 19, 99-109.
18. De Cesare D., and, Sassone-Corsi P., (2000) Transcriptional regulation by cyclic AMP-responsive factors. Prog. Nucleic Acid Res. Mol. Biol. 64, 343-369.
19. Dejda A., Jolivel V., Bourgault S., Seaborn T., Fournier A., Vaudry H., and, Vaudry D., (2008) Inhibitory effect of PACAP on caspase activity in neuronal apoptosis: a better understanding towards therapeutic applications in neurodegenerative diseases. J. Mol. Neurosci. 36, 26-37.
20. Dickson L., and, Finlayson K., (2009) VPAC and PAC receptors: from ligands to function. Pharmacol. Ther. 121, 294-316.
21. Esteban J. A., Shi S. H., Wilson C., Nuriya M., Huganir R. L., and, Malinow R., (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 6, 136-143. (Pubitemid 36182782)
22. Falktoft B., Georg B., and, Fahrenkrug J., (2009) Signaling pathways in PACAP regulation of VIP gene expression in human neuroblastoma cells. Neuropeptides 43, 387-396.
23. Falluel-Morel A., Aubert N., Vaudry D., Basille M., Fontaine M., Fournier A., Vaudry H., and, Gonzalez B. J., (2004) Opposite regulation of the mitochondrial apoptotic pathway by C2-ceramide and PACAP through a MAP-kinase-dependent mechanism in cerebellar granule cells. J. Neurochem. 91, 1231-1243. (Pubitemid 39587461)
24. Farkas O., Tamas A., Zsombok A., Reglodi D., Pal J., Buki A., Lengvari I., Povlishock J. T., and, Doczi T., (2004) Effects of pituitary adenylate cyclase activating polypeptide in a rat model of traumatic brain injury. Regul. Pept. 123, 69-75. (Pubitemid 39424151)
25. Ferguson G. D., and, Storm D. R., (2004) Why calcium-stimulated adenylyl cyclases? Physiology (Bethesda) 19, 271-276. (Pubitemid 39472638)
26. Frechilla D., Garcia-Osta A., Palacios S., Cenarruzabeitia E., and, Del Rio J., (2001) BDNF mediates the neuroprotective effect of PACAP-38 on rat cortical neurons. Neuroreport 12, 919-923. (Pubitemid 32281447)
27. Gonzalez G., and, Montminy M., (1989) cAMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine-133. Cell 59, 675-680. (Pubitemid 19282874)
28. Gonzalez-Rey E., Varela N., Chorny A., and, Delgado M., (2007) Therapeutical approaches of vasoactive intestinal peptide as a pleiotropic immunomodulator. Curr. Pharm. Des. 13, 1113-1139. (Pubitemid 46744821)
29. Hardingham G. E., (2006) Pro-survival signalling from the NMDA receptor. Biochem. Soc. Trans. 34, 936-938. (Pubitemid 44796454)
30. Hardingham G. E., (2009) Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem. Soc. Trans. 37, 1147-1160.
31. Hardingham G. E., and, Bading H., (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682-696.
32. Hardingham G. E., Chawla S., Johnson C. M., and, Bading H., (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260-265. (Pubitemid 27043726)
33. Hardingham G. E., Chawla S., Cruzalegui F. H., and, Bading H., (1999) Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22, 789-798. (Pubitemid 29203501)
34. Hardingham G. E., Arnold F. J., and, Bading H., (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 4, 261-267. (Pubitemid 32194873)
35. 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. (Pubitemid 34454245)
36. Hetman M., and, Kharebava G., (2006) Survival signaling pathways activated by NMDA receptors. Curr. Top. Med. Chem. 6, 787-799.
37. Hu E., Demmou L., Cauli B., et al. (2011) VIP, CRF, and PACAP act at distinct receptors to elicit different cAMP/PKA dynamics in the neocortex. Cereb. Cortex 21, 708-718.
38. Impey S., Fong A. L., Wang Y., et al. (2002) Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34, 235-244. (Pubitemid 34442566)
39. Kovacs K. A., Steullet P., Steinmann M., Do K. Q., Magistretti P. J., Halfon O., and, Cardinaux J. R., (2007) TORC1 is a calcium- and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc. Natl Acad. Sci. USA 104, 4700-4705. (Pubitemid 47186288)
40. Lancaster B., Hu H., Gibb B., and, Storm J. F., (2006) Kinetics of ion channel modulation by cAMP in rat hippocampal neurones. J. Physiol. 576, 403-417. (Pubitemid 44490134)
41. Lee H. K., Takamiya K., Han J. S., et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631-643. (Pubitemid 36331776)
42. 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. (Pubitemid 40268955)
43. Leveille F., Papadia S., Fricker M., et al. (2010) Suppression of the intrinsic apoptosis pathway by synaptic activity. J. Neurosci. 30, 2623-2635.
44. Li S., Zhang C., Takemori H., Zhou Y., and, Xiong Z. Q., (2009) TORC1 regulates activity-dependent CREB-target gene transcription and dendritic growth of developing cortical neurons. J. Neurosci. 29, 2334-2343.
45. Lonze B. E., and, Ginty D. D., (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623. (Pubitemid 35229980)
46. Lonze B. E., Riccio A., Cohen S., and, Ginty D. D., (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34, 371-385. (Pubitemid 34465496)
47. MacDonald J. F., Jackson M. F., and, Beazely M. A., (2007) G protein-coupled receptors control NMDARs and metaplasticity in the hippocampus. Biochim. Biophys. Acta 1768, 941-951. (Pubitemid 46452551)
48. Mantamadiotis T., Lemberger T., Bleckmann S. C., et al. (2002) Disruption of CREB function in brain leads to neurodegeneration. Nat. Genet. 31, 47-54.
49. McKenzie G. J., Stevenson P., Ward G., Papadia S., Bading H., Chawla S., Privalsky M., and, Hardingham G. E., (2005) Nuclear Ca2+ and CaM kinase IV specify hormonal- and Notch-responsiveness. J. Neurochem. 93, 171-185. (Pubitemid 40463527)
50. McKenzie G., Ward G., Stallwood Y., Briend E., Papadia S., Lennard A., Turner M., Champion B., and, Hardingham G. E., (2006) Cellular Notch responsiveness is defined by phosphoinositide 3-kinase-dependent signals. BMC Cell Biol. 7, 10.
51. Mennerick S., and, Zorumski C. F., (2000) Neural activity and survival in the developing nervous system. Mol. Neurobiol. 22, 41-54.
52. Minta A., Kao J., and, Tsien R., (1989) Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 264, 8171-8178. (Pubitemid 19137304)
53. Miyata A., Arimura A., Dahl R. R., Minamino N., Uehara A., Jiang L., Culler M. D., and, Coy D. H., (1989) Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Biophys. Res. Commun. 164, 567-574. (Pubitemid 19269770)
54. Nguyen P. V., and, Woo N. H., (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog. Neurobiol. 71, 401-437. (Pubitemid 38173011)
55. Ohtaki H., Nakamachi T., Dohi K., and, Shioda S., (2008) Role of PACAP in ischemic neural death. J. Mol. Neurosci. 36, 16-25.
56. Otto C., Kovalchuk Y., Wolfer D. P., et al. (2001) Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J. Neurosci. 21, 5520-5527. (Pubitemid 32692150)
57. Papadia S., Stevenson P., Hardingham N. R., Bading H., and, Hardingham G. E., (2005) Nuclear Ca2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J. Neurosci. 25, 4279-4287. (Pubitemid 40628772)
58. Papadia S., Soriano F. X., Leveille F., et al. (2008) Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476-487. (Pubitemid 351441886)
59. Pedarzani P., and, Storm J. F., (1995) Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J. Neurophysiol. 74, 2749-2753. (Pubitemid 26012330)
60. Pohl D., Ishmaru M. J., Bittigau P., Stadhaus D., Hubner C., Olney J. W., Turski L., and, Ikonomidou C., (1999) NMDA antagonists and apoptotic cell death triggered by head trauma in developing rat brain. Proc. Natl Acad. Sci. USA 96, 2508-2513. (Pubitemid 29117946)
61. Pokorska A., Vanhoutte P., Arnold F. J., Silvagno F., Hardingham G. E., and, Bading H., (2003) Synaptic activity induces signalling to CREB without increasing global levels of cAMP in hippocampal neurons. J. Neurochem. 84, 447-452. (Pubitemid 36182243)
62. Racz B., Tamas A., Kiss P., et al. (2006) Involvement of ERK and CREB signaling pathways in the protective effect of PACAP in monosodium glutamate-induced retinal lesion. Ann. N Y Acad. Sci. 1070, 507-511. (Pubitemid 44126694)
63. Ravnskjaer K., Kester H., Liu Y., Zhang X., Lee D., Yates J. R. III, and, Montminy M., (2007) Cooperative interactions between CBP and TORC2 confer selectivity to CREB target gene expression. EMBO J. 26, 2880-2889. (Pubitemid 46975772)
64. Reglodi D., Somogyvari-Vigh A., Vigh S., Kozicz T., and, Arimura A., (2000) Delayed systemic administration of PACAP38 is neuroprotective in transient middle cerebral artery occlusion in the rat. Stroke; a journal of cerebral circulation 31, 1411-1417. (Pubitemid 30351265)
65. Reglodi D., Tamas A., Somogyvari-Vigh A., Szanto Z., Kertes E., Lenard L., Arimura A., and, Lengvari I., (2002) Effects of pretreatment with PACAP on the infarct size and functional outcome in rat permanent focal cerebral ischemia. Peptides 23, 2227-2234. (Pubitemid 36092058)
66. Reglodi D., Tamas A., Lubics A., Szalontay L., and, Lengvari I., (2004) Morphological and functional effects of PACAP in 6-hydroxydopamine-induced lesion of the substantia nigra in rats. Regul. Pept. 123, 85-94. (Pubitemid 39424153)
67. Reglodi D., Tamas A., Lengvari I., Toth G., Szalontay L., and, Lubics A., (2006) Comparative study of the effects of PACAP in young, aging, and castrated males in a rat model of Parkinson's disease. Ann. N Y Acad. Sci. 1070, 518-524. (Pubitemid 44126696)
68. Riccio A., Ahn S., Davenport C. M., Blendy J. A., and, Ginty D. D., (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286, 2358-2361. (Pubitemid 30016901)
69. Screaton R. A., Conkright M. D., Katoh Y., et al. (2004) The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119, 61-74. (Pubitemid 39349320)
70. Shintani N., Suetake S., Hashimoto H., et al. (2005) Neuroprotective action of endogenous PACAP in cultured rat cortical neurons. Regul. Pept. 126, 123-128. (Pubitemid 40037754)
71. Shioda S., Ozawa H., Dohi K., et al. (1998) PACAP protects hippocampal neurons against apoptosis: involvement of JNK/SAPK signaling pathway. Ann. N Y Acad. Sci. 865, 111-117. (Pubitemid 29047818)
72. Shioda S., Ohtaki H., Nakamachi T., et al. (2006) Pleiotropic functions of PACAP in the CNS: neuroprotection and neurodevelopment. Ann. N Y Acad. Sci. 1070, 550-560. (Pubitemid 44126702)
73. Siu Y. T., Chin K. T., Siu K. L., Yee Wai Choy E., Jeang K. T., and, Jin D. Y., (2006) TORC1 and TORC2 coactivators are required for tax activation of the human T-cell leukemia virus type 1 long terminal repeats. J. Virol. 80, 7052-7059.
74. Somogyvari-Vigh A., and, Reglodi D., (2004) Pituitary adenylate cyclase activating polypeptide: a potential neuroprotective peptide. Curr. Pharm. Des. 10, 2861-2889. (Pubitemid 39172068)
75. Soriano F. X., and, Hardingham G. E., (2007) Compartmentalized NMDA receptor signalling to survival and death. J. Physiol. 584, 381-387. (Pubitemid 47578325)
76. Soriano F. X., Leveille F., Papadia S., Higgins L. G., Varley J., Baxter P., Hayes J. D., and, Hardingham G. E., (2008a) Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3H-1,2-dithiole-3-thione. J. Neurochem. 107, 533-543.
77. Soriano F. X., Martel M. A., Papadia S., et al. (2008b) Specific targeting of pro-death NMDA receptor signals with differing reliance on the NR2B PDZ ligand. J. Neurosci. 28, 10696-10710.
78. Soriano F. X., Leveille F., Papadia S., Bell K. F., Puddifoot C., and, Hardingham G. E., (2011) Neuronal activity controls the antagonistic balance between PGC-1α and SMRT in regulating antioxidant defences. Antioxid. Redox Signal. 14, 1425-1436.
79. Stehle J. H., Foulkes N. S., Molina C. A., Simonneaux V., Pevet P., and, Sassone-Corsi P., (1993) Adrenergic signals direct rhythmic expression of transcriptional repressor CREM in the pineal gland. Nature 365, 314-320. (Pubitemid 23288971)
80. Tamas A., Lubics A., Lengvari I., and, Reglodi D., (2006a) Protective effects of PACAP in excitotoxic striatal lesion. Ann. N Y Acad. Sci. 1070, 570-574. (Pubitemid 44126705)
81. Tamas A., Zsombok A., Farkas O., Reglodi D., Pal J., Buki A., Lengvari I., Povlishock J. T., and, Doczi T., (2006b) Postinjury administration of pituitary adenylate cyclase activating polypeptide (PACAP) attenuates traumatically induced axonal injury in rats. J. Neurotrauma 23, 686-695. (Pubitemid 43728055)
82. Tauskela J. S., Fang H., Hewitt M., Brunette E., Ahuja T., Thivierge J. P., Comas T., and, Mealing G. A., (2008) Elevated synaptic activity preconditions neurons against an in vitro model of ischemia. J. Biol. Chem. 283, 34667-34676.
83. Uchida D., Arimura A., Somogyvari-Vigh A., Shioda S., and, Banks W. A., (1996) Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide. Brain Res. 736, 280-286. (Pubitemid 26356486)
84. Vaudry D., Falluel-Morel A., Bourgault S., et al. (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol. Rev. 61, 283-357.
85. Walton M., Woodgate A. M., Muravlev A., Xu R., During M. J., and, Dragunow M., (1999) CREB phosphorylation promotes nerve cell survival. J. Neurochem. 73, 1836-1842. (Pubitemid 29491796)
86. Wang G., Pan J., Tan Y. Y., Sun X. K., Zhang Y. F., Zhou H. Y., Ren R. J., Wang X. J., and, Chen S. D., (2008) Neuroprotective effects of PACAP27 in mice model of Parkinson's disease involved in the modulation of K(ATP) subunits and D2 receptors in the striatum. Neuropeptides 42, 267-276.
87. Watson R. F., Abdel-Majid R. M., Barnett M. W., Willis B. S., Katsnelson A., Gillingwater T. H., McKnight G. S., Kind P. C., and, Neumann P. E., (2006) Involvement of protein kinase A in patterning of the mouse somatosensory cortex. J. Neurosci. 26, 5393-5401. (Pubitemid 44318391)
88. Yaka R., Biegon A., Grigoriadis N., et al. (2007) D-cycloserine improves functional recovery and reinstates long-term potentiation (LTP) in a mouse model of closed head injury. FASEB J. 21, 2033-2041. (Pubitemid 47026439)
89. 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 Genetics 5, e1000604.
90. Zhang S. J., Buchthal B., Lau D., et al. (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.
91. Zhou Y., Wu H., Li S., Chen Q., Cheng X. W., Zheng J., Takemori H., and, Xiong Z. Q., (2006) Requirement of TORC1 for late-phase long-term potentiation in the hippocampus. PLoS ONE 1, e16.