Mouse hippocampal phosphorylation footprint induced by generalized seizures: Focus on ERK, mTORC1 and Akt/GSK-3 pathways

Neuroscience

Volumn 311, Issue , 2015, Pages 474-483

  Gangarossa, Giuseppe ^a,b   Sakkaki, Sophie ^a,b,d   Lory, Philippe ^a,b,c   Valjent, Emmanuel ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

^d UNIVERSITY OF VERMONT   (United States)

Author keywords

Akt GSK 3; ERK1 2; Immediate early genes; MTORC; Seizures; Signal transduction

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN S6; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROSHOCK SEIZURE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HIPPOCAMPUS; MALE; MAXIMAL ELECTROSHOCK SEIZURE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOOTPRINTING; SIGNAL TRANSDUCTION; TONIC CLONIC SEIZURE; UPREGULATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; ELECTRIC SHOCK; ELECTROENCEPHALOGRAPHY; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENERALIZED EPILEPSY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; RANDOMIZATION; SEIZURE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; ELECTROSHOCK; EPILEPSY, GENERALIZED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; SEIZURES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84946782249     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.10.051     Document Type: Article

References (68)

1. Backman S.A., Stambolic V., Suzuki A., Haight J., Elia A., Pretorius J., Tsao M.S., Shannon P., Bolon B., Ivy G.O., Mak T.W. Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet 2001, 29:396-403.
2. Bannister A.J., Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011, 21:381-395.
3. Bateup H.S., Johnson C.A., Denefrio C.L., Saulnier J.L., Kornacker K., Sabatini B.L. Excitatory/inhibitory synaptic imbalance leads to hippocampal hyperexcitability in mouse models of tuberous sclerosis. Neuron 2013, 78:510-522.
4. Ben J., de Oliveira P.A., Goncalves F.M., Peres T.V., Matheus F.C., Hoeller A.A., Leal R.B., Walz R., Prediger R.D. Effects of pentylenetetrazole kindling on mitogen-activated protein kinases levels in neocortex and hippocampus of mice. Neurochem Res 2014, 39:2492-2500.
5. Berkeley J.L., Decker M.J., Levey A.I. The role of muscarinic acetylcholine receptor-mediated activation of extracellular signal-regulated kinase 1/2 in pilocarpine-induced seizures. J Neurochem 2002, 82:192-201.
6. Biever A., Puighermanal E., Nishi A., David A., Panciatici C., Longueville S., Xirodimas D., Gangarossa G., Meyuhas O., Herve D., Girault J.A., Valjent E. PKA-dependent phosphorylation of ribosomal protein S6 does not correlate with translation efficiency in striatonigral and striatopallidal medium-sized spiny neurons. J Neurosci 2015, 35:4113-4130.
7. Borbely S., Dobo E., Czege D., Molnar E., Bakos M., Szucs B., Vincze A., Vilagi I., Mihaly A. Modification of ionotropic glutamate receptor-mediated processes in the rat hippocampus following repeated, brief seizures. Neuroscience 2009, 159:358-368.
8. Bozzi Y., Borrelli E. The role of dopamine signaling in epileptogenesis. Front Cell Neurosci 2013, 7:157.
9. Bozzi Y., Dunleavy M., Henshall D.C. Cell signaling underlying epileptic behavior. Front Behav Neurosci 2011, 5:45.
10. Buckmaster P.S., Ingram E.A., Wen X. Inhibition of the mammalian target of rapamycin signaling pathway suppresses dentate granule cell axon sprouting in a rodent model of temporal lobe epilepsy. J Neurosci 2009, 29:8259-8269.
11. Carnevalli L.S., Pereira C.M., Longo B.M., Jaqueta C.B., Avedissian M., Mello L.E., Castilho B.A. Phosphorylation of translation initiation factor eIF2alpha in the brain during pilocarpine-induced status epilepticus in mice. Neurosci Lett 2004, 357:191-194.
12. Carnevalli L.S., Pereira C.M., Jaqueta C.B., Alves V.S., Paiva V.N., Vattem K.M., Wek R.C., Mello L.E., Castilho B.A. Phosphorylation of the alpha subunit of translation initiation factor-2 by PKR mediates protein synthesis inhibition in the mouse brain during status epilepticus. Biochem J 2006, 397:187-194.
13. Carson R.P., Fu C., Winzenburger P., Ess K.C. Deletion of Rictor in neural progenitor cells reveals contributions of mTORC2 signaling to tuberous sclerosis complex. Hum Mol Genet 2013, 22:140-152.
14. Chotiner J.K., Nielson J., Farris S., Lewandowski G., Huang F., Banos K., de Leon R., Steward O. Assessment of the role of MAP kinase in mediating activity-dependent transcriptional activation of the immediate early gene Arc/Arg3.1 in the dentate gyrus in vivo. Learn Mem 2010, 17:117-129.
15. Cotman C.W., Banker G., Zornetzer S.F., McGaugh J.L. Electroshock effects on brain protein synthesis: relation to brain seizures and retrograde amnesia. Science 1971, 173:454-456.
16. Crespo-Biel N., Canudas A.M., Camins A., Pallas M. Kainate induces AKT, ERK and cdk5/GSK3beta pathway deregulation, phosphorylates tau protein in mouse hippocampus. Neurochem Int 2007, 50:435-442.
17. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
18. Curatolo P., D'Argenzio L., Cerminara C., Bombardieri R. Management of epilepsy in tuberous sclerosis complex. Expert Rev Neurother 2008, 8:457-467.
19. Doble B.W., Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003, 116:1175-1186.
20. Dunleavy M., Provenzano G., Henshall D.C., Bozzi Y. Kainic acid-induced seizures modulate Akt (SER473) phosphorylation in the hippocampus of dopamine D2 receptor knockout mice. J Mol Neurosci 2013, 49:202-210.
21. Ferrari S., Bandi H.R., Hofsteenge J., Bussian B.M., Thomas G. Mitogen-activated 70K S6 kinase. Identification of in vitro 40S ribosomal S6 phosphorylation sites. J Biol Chem 1991, 266:22770-22775.
22. Franklin K., Paxinos G. The mouse brain in stereotaxic coordinates 2007, Elsevier, p. 360. third ed.
23. Gangarossa G., Valjent E. Regulation of the ERK pathway in the dentate gyrus by in vivo dopamine D1 receptor stimulation requires glutamatergic transmission. Neuropharmacology 2012, 63:1107-1117.
24. Gangarossa G., Di Benedetto M., O'Sullivan G.J., Dunleavy M., Alcacer C., Bonito-Oliva A., Henshall D.C., Waddington J.L., Valjent E., Fisone G. Convulsant doses of a dopamine D1 receptor agonist result in Erk-dependent increases in Zif268 and Arc/Arg3.1 expression in mouse dentate gyrus. PLoS One 2011, 6:e19415.
25. Gangarossa G., Ceolin L., Paucard A., Lerner-Natoli M., Perroy J., Fagni L., Valjent E. Repeated stimulation of dopamine D1-like receptor and hyperactivation of mTOR signaling lead to generalized seizures, altered dentate gyrus plasticity, and memory deficits. Hippocampus 2014, 24:1466-1481.
26. Garrido Y.C., Sanabria E.R., Funke M.G., Cavalheiro E.A., Naffah-Mazzacoratti M.G. Mitogen-activated protein kinase is increased in the limbic structures of the rat brain during the early stages of status epilepticus. Brain Res Bull 1998, 47:223-229.
27. Gass P., Kiessling M., Bading H. Regionally selective stimulation of mitogen activated protein (MAP) kinase tyrosine phosphorylation after generalized seizures in the rat brain. Neurosci Lett 1993, 162:39-42.
28. Goto E.M., Silva Mde P., Perosa S.R., Arganaraz G.A., Pesquero J.B., Cavalheiro E.A., Naffah-Mazzacoratti M.G., Teixeira V.P., Silva J.A. Akt pathway activation and increased neuropeptide Y mRNA expression in the rat hippocampus: implications for seizure blockade. Neuropeptides 2010, 44:169-176.
29. Hart J.R., Vogt P.K. Phosphorylation of AKT: a mutational analysis. Oncotarget 2011, 2:467-476.
30. Houser C.R., Huang C.S., Peng Z. Dynamic seizure-related changes in extracellular signal-regulated kinase activation in a mouse model of temporal lobe epilepsy. Neuroscience 2008, 156:222-237.
31. Houser C.R., Zhang N., Peng Z., Huang C.S., Cetina Y. Neuroanatomical clues to altered neuronal activity in epilepsy: from ultrastructure to signaling pathways of dentate granule cells. Epilepsia 2012, 53(Suppl. 1):67-77.
32. Huang J., Manning B.D. A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans 2009, 37:217-222.
33. Huang X., Zhang H., Yang J., Wu J., McMahon J., Lin Y., Cao Z., Gruenthal M., Huang Y. Pharmacological inhibition of the mammalian target of rapamycin pathway suppresses acquired epilepsy. Neurobiol Dis 2010, 40:193-199.
34. Isokawa M. Remodeling dendritic spines in the rat pilocarpine model of temporal lobe epilepsy. Neurosci Lett 1998, 258:73-76.
35. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 2007, 27:5967-5975.
36. Jiang M., Lee C.L., Smith K.L., Swann J.W. Spine loss and other persistent alterations of hippocampal pyramidal cell dendrites in a model of early-onset epilepsy. J Neurosci 1998, 18:8356-8368.
37. Kim Y.S., Hong K.S., Seong Y.S., Park J.B., Kuroda S., Kishi K., Kaibuchi K., Takai Y. Phosphorylation and activation of mitogen-activated protein kinase by kainic acid-induced seizure in rat hippocampus. Biochem Biophys Res Commun 1994, 202:1163-1168.
38. Laplante M., Sabatini D.M. MTOR signaling at a glance. J Cell Sci 2009, 122:3589-3594.
39. Lasarge C.L., Danzer S.C. Mechanisms regulating neuronal excitability and seizure development following mTOR pathway hyperactivation. Front Mol Neurosci 2014, 7:18.
40. Loscher W. Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs. Seizure 2011, 20:359-368.
41. Meikle L., Talos D.M., Onda H., Pollizzi K., Rotenberg A., Sahin M., Jensen F.E., Kwiatkowski D.J. A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J Neurosci 2007, 27:5546-5558.
42. Murphy B.L., Danzer S.C. Somatic translocation: a novel mechanism of granule cell dendritic dysmorphogenesis and dispersion. J Neurosci 2011, 31:2959-2964.
43. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997, 17:3727-3738.
44. Park S.A., Kim T.S., Choi K.S., Park H.J., Heo K., Lee B.I. Chronic activation of CREB and p90RSK in human epileptic hippocampus. Exp Mol Med 2003, 35:365-370.
45. Pun R.Y., Rolle I.J., Lasarge C.L., Hosford B.E., Rosen J.M., Uhl J.D., Schmeltzer S.N., Faulkner C., Bronson S.L., Murphy B.L., Richards D.A., Holland K.D., Danzer S.C. Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron 2012, 75:1022-1034.
46. Racine R.J., Gartner J.G., Burnham W.M. Epileptiform activity and neural plasticity in limbic structures. Brain Res 1972, 47:262-268.
47. Rojo A.I., Rada P., Egea J., Rosa A.O., Lopez M.G., Cuadrado A. Functional interference between glycogen synthase kinase-3 beta and the transcription factor Nrf2 in protection against kainate-induced hippocampal cell death. Mol Cell Neurosci 2008, 39:125-132.
48. Roux P.P., Shahbazian D., Vu H., Holz M.K., Cohen M.S., Taunton J., Sonenberg N., Blenis J. RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J Biol Chem 2007, 282:14056-14064.
49. Rowley H.L., Martin K.F., Marsden C.A. Decreased GABA release following tonic-clonic seizures is associated with an increase in extracellular glutamate in rat hippocampus in vivo. Neuroscience 1995, 68:415-422.
50. Sakkaki S., Gangarossa G., Lerat B., Francon D., Forichon L., Chemin J., Valjent E., Lerner-Natoli M., Lory P. Blockade of T-type calcium channels prevents tonic-clonic seizures in a maximal electroshock seizure model. Neuropharmacology 2015, in press.
51. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
52. Scharfman H.E. The neurobiology of epilepsy. Curr Neurol Neurosci Rep 2007, 7:348-354.
53. Scharfman H.E., Smith K.L., Goodman J.H., Sollas A.L. Survival of dentate hilar mossy cells after pilocarpine-induced seizures and their synchronized burst discharges with area CA3 pyramidal cells. Neuroscience 2001, 104:741-759.
54. Sierra A., Grohn O., Pitkanen A. Imaging microstructural damage and plasticity in the hippocampus during epileptogenesis. Neuroscience 2015.
55. Sloviter R.S., Bumanglag A.V. Defining "epileptogenesis" and identifying "antiepileptogenic targets" in animal models of acquired temporal lobe epilepsy is not as simple as it might seem. Neuropharmacology 2013, 69:3-15.
56. Sutula T., He X.X., Cavazos J., Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988, 239:1147-1150.
57. Thomas G.M., Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 2004, 5:173-183.
58. Tripathi P.P., Santorufo G., Brilli E., Borrelli E., Bozzi Y. Kainic acid-induced seizures activate GSK-3beta in the hippocampus of D2R-/- mice. NeuroReport 2010, 21:846-850.
59. Valjent E., Bertran-Gonzalez J., Bowling H., Lopez S., Santini E., Matamales M., Bonito-Oliva A., Herve D., Hoeffer C., Klann E., Girault J.A., Fisone G. Haloperidol regulates the state of phosphorylation of ribosomal protein S6 via activation of PKA and phosphorylation of DARPP-32. Neuropsychopharmacology 2011, 36:2561-2570.
60. Valovka T., Verdier F., Cramer R., Zhyvoloup A., Fenton T., Rebholz H., Wang M.L., Gzhegotsky M., Lutsyk A., Matsuka G., Filonenko V., Wang L., Proud C.G., Parker P.J., Gout I.T. Protein kinase C phosphorylates ribosomal protein S6 kinase betaII and regulates its subcellular localization. Mol Cell Biol 2003, 23:852-863.
61. Wang L., Rhodes C.J., Lawrence J.C. Activation of mammalian target of rapamycin (mTOR) by insulin is associated with stimulation of 4EBP1 binding to dimeric mTOR complex 1. J Biol Chem 2006, 281:24293-24303.
62. Wasterlain C.G. Inhibition of cerebral protein synthesis by epileptic seizures without motor manifestations. Neurology 1974, 24:175-180.
63. Wong M. MTOR as a potential treatment target for epilepsy. Future Neurol 2012, 7:537-545.
64. Xi Z.Q., Wang X.F., He R.Q., Li M.W., Liu X.Z., Wang L.Y., Zhu X., Xiao F., Sun J.J., Li J.M., Gong Y., Guan L.F. Extracellular signal-regulated protein kinase in human intractable epilepsy. Eur J Neurol 2007, 14:865-872.
65. Yamagata Y., Jovanovic J.N., Czernik A.J., Greengard P., Obata K. Bidirectional changes in synapsin I phosphorylation at MAP kinase-dependent sites by acute neuronal excitation in vivo. J Neurochem 2002, 80:835-842.
66. Zeng L.H., Ouyang Y., Gazit V., Cirrito J.R., Jansen L.A., Ess K.C., Yamada K.A., Wozniak D.F., Holtzman D.M., Gutmann D.H., Wong M. Abnormal glutamate homeostasis and impaired synaptic plasticity and learning in a mouse model of tuberous sclerosis complex. Neurobiol Dis 2007, 28:184-196.
67. Zeng L.H., Xu L., Rensing N.R., Sinatra P.M., Rothman S.M., Wong M. Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci 2007, 27:11604-11613.
68. Zeng L.H., Rensing N.R., Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci 2009, 29:6964-6972.