Transgenic Overexpression of 14-3-3 Zeta Protects Hippocampus against Endoplasmic Reticulum Stress and Status Epilepticus In Vivo

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Brennan, Gary P ^a   Jimenez Mateos, Eva M ^a   McKiernan, Ross C ^a   Engel, Tobias ^a   Tzivion, Guri ^b   Henshall, David C ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; ISOPROTEIN; PROTEIN 14 3 3; PROTEIN 14 3 3 ZETA; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; DISEASE DURATION; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; EPILEPTIC STATE; FEMALE; HIPPOCAMPUS; IN VIVO STUDY; MOUSE; NERVE CELL NECROSIS; NEUROANATOMY; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN UNFOLDING; SEIZURE; TRANSGENE; TRANSGENICS; UNFOLDED PROTEIN RESPONSE;

14-3-3 PROTEINS; ANIMALS; APOPTOSIS; BASE SEQUENCE; CELLS, CULTURED; DNA PRIMERS; ENDOPLASMIC RETICULUM; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; REAL-TIME POLYMERASE CHAIN REACTION; STATUS EPILEPTICUS;

MUS; MUS MUSCULUS;

EID: 84872873302     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054491     Document Type: Article

References (55)

1. van Hemert MJ, Steensma HY, van Heusden GP, (2001) 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. Bioessays 23: 936-946.
2. Berg D, Holzmann C, Riess O, (2003) 14-3-3 proteins in the nervous system. Nature Rev Neurosci 4: 752-762.
3. Kaneko K, Hachiya NS, (2006) The alternative role of 14-3-3 zeta as a sweeper of misfolded proteins in disease conditions. Med Hypotheses 67: 169-171.
4. O'Kelly I, Butler MH, Zilberberg N, Goldstein SA, (2002) Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111: 577-588.
5. Toyo-oka K, Shionoya A, Gambello MJ, Cardoso C, Leventer R, et al. (2003) 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat Genet 34: 274-285.
6. Cheah PS, Ramshaw HS, Thomas PQ, Toyo-Oka K, Xu X, et al. (2012) Neurodevelopmental and neuropsychiatric behaviour defects arise from 14-3-3zeta deficiency. Mol Psychiatry 17: 451-466.
7. Henshall DC, Meldrum BS (2012) Cell death and survival mechanisms after single and repeated brief seizures. Jasper's Basic Mechanisms of the Epilepsies (4th Edition). Bethesda, MD, USA: Oxford University Press. 262-276.
8. Olney JW, Collins RC, Sloviter RS, (1986) Excitotoxic mechanisms of epileptic brain damage. Adv Neurol 44: 857-877.
9. Fujikawa DG (2006) Neuroprotective strategies in status epilepticus. In: Wasterlain CG, Treiman DM, editors. Status epilepticus: Mechanisms and management. Cambridge: MIT Press. 463-480.
10. Liou AK, Clark RS, Henshall DC, Yin XM, Chen J, (2003) To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 69: 103-142.
11. Engel T, Plesnila N, Prehn JH, Henshall DC, (2011) In vivo contributions of BH3-only proteins to neuronal death following seizures, ischemia, and traumatic brain injury. J Cereb Blood Flow Metab 31: 1196-1210.
12. Henshall DC, Araki T, Schindler CK, Lan JQ, Tiekoter KL, et al. (2002) Activation of Bcl-2-associated death protein and counter-response of Akt within cell populations during seizure-induced neuronal death. J Neurosci 22: 8458-8465.
13. Shinoda S, Skradski SL, Araki T, Schindler CK, Meller R, et al. (2003) Formation of a tumour necrosis factor receptor 1 molecular scaffolding complex and activation of apoptosis signal-regulating kinase 1 during seizure-induced neuronal death. Eur J Neurosci 17: 2065-2076.
14. Noh HS, Kim YS, Kim YH, Han JY, Park CH, et al. (2006) Ketogenic diet protects the hippocampus from kainic acid toxicity by inhibiting the dissociation of bad from 14-3-3. J Neurosci Res 84: 1829-1836.
15. Schindler CK, Heverin M, Henshall DC, (2006) Isoform- and subcellular fraction-specific differences in hippocampal 14-3-3 levels following experimentally evoked seizures and in human temporal lobe epilepsy. J Neurochem 99: 561-569.
16. van der Brug MP, Goodenough S, Wilce P, (2002) Kainic acid induces 14-3-3 zeta expression in distinct regions of rat brain. Brain Res 956: 110-115.
17. Murphy N, Bonner HP, Ward MW, Murphy BM, Prehn JH, et al. (2008) Depletion of 14-3-3 zeta elicits endoplasmic reticulum stress and cell death, and increases vulnerability to kainate-induced injury in mouse hippocampal cultures. J Neurochem 106: 978-988.
18. Lukasiuk K, Kontula L, Pitkanen A, (2003) cDNA profiling of epileptogenesis in the rat brain. Eur J Neurosci 17: 271-279.
19. Nellist M, Goedbloed MA, de Winter C, Verhaaf B, Jankie A, et al. (2002) Identification and characterization of the interaction between tuberin and 14-3-3zeta. J Biol Chem 277: 39417-39424.
20. Martin H, Rostas J, Patel Y, Aitken A, (1994) Subcellular localisation of 14-3-3 isoforms in rat brain using specific antibodies. J Neurochem 63: 2259-2265.
21. Xu C, Bailly-Maitre B, Reed JC, (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115: 2656-2664.
22. Hetz C, (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13: 89-102.
23. Lin JH, Walter P, Yen TS (2007) Endoplasmic Reticulum Stress in Disease Pathogenesis. Annu Rev Pathol.
24. Wang S, Longo FM, Chen J, Butman M, Graham SH, et al. (1993) Induction of glucose regulated protein (grp78) and inducible heat shock protein (hsp70) mRNAs in rat brain after kainic acid seizures and focal ischemia. Neurochem Int 23: 575-582.
25. Kitao Y, Ozawa K, Miyazaki M, Tamatani M, Kobayashi T, et al. (2001) Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity. J Clin Invest 108: 1439-1450.
26. Yamamoto A, Murphy N, Schindler CK, So NK, Stohr S, et al. (2006) Endoplasmic reticulum stress and apoptosis signaling in human temporal lobe epilepsy. J Neuropathol Exp Neurol 65: 217-225.
27. Liu G, Guo H, Guo C, Zhao S, Gong D, et al. (2011) Involvement of IRE1alpha signaling in the hippocampus in patients with mesial temporal lobe epilepsy. Brain Res Bull 84: 94-102.
28. Liu GL, Wang KY, Guo H, Zhao SJ, Shen Y, et al. (2012) Inositol-requiring protein 1alpha signaling pathway is activated in the temporal cortex of patients with mesial temporal lobe epilepsy. Neurol Sci.
29. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, et al. (2007) Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 27: 901-908.
30. Bronisz A, Sharma SM, Hu R, Godlewski J, Tzivion G, et al. (2006) Microphthalmia-associated transcription factor interactions with 14-3-3 modulate differentiation of committed myeloid precursors. Mol Biol Cell 17: 3897-3906.
31. Tanaka K, Jimenez-Mateos EM, Matsushima S, Taki W, Henshall DC, (2010) Hippocampal damage after intra-amygdala kainic acid-induced status epilepticus and seizure preconditioning-mediated neuroprotection in SJL mice. Epilepsy Res 88: 151-161.
32. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, second edition. San Diego, CA: Elsevier.
33. Engel T, Gomez-Villafuertes R, Tanaka K, Mesuret G, Sanz-Rodriguez A, et al. (2012) Seizure suppression and neuroprotection by targeting the purinergic P2X7 receptor during status epilepticus in mice. FASEB J 26: 1616-1628.
34. Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, et al. (2012) Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18: 1087-1094.
35. Miller-Delaney SF, Das S, Sano T, Jimenez-Mateos EM, Bryan K, et al. (2012) Differential DNA methylation patterns define status epilepticus and epileptic tolerance. J Neurosci 32: 1577-1588.
36. Dunleavy M, Shinoda S, Schindler C, Ewart C, Dolan R, et al. (2010) Experimental neonatal status epilepticus and the development of temporal lobe epilepsy with unilateral hippocampal sclerosis. Am J Pathol 176: 330-342.
37. Wang B, Ling S, Lin WC, (2010) 14-3-3Tau regulates Beclin 1 and is required for autophagy. PLoS One 5: e10409.
38. Pozuelo-Rubio M, (2011) 14-3-3zeta binds class III phosphatidylinositol-3-kinase and inhibits autophagy. Autophagy 7: 240-242.
39. Steinacker P, Schwarz P, Reim K, Brechlin P, Jahn O, et al. (2005) Unchanged survival rates of 14-3-3gamma knockout mice after inoculation with pathological prion protein. Mol Cell Biol 25: 1339-1346.
40. Yacoubian TA, Slone SR, Harrington AJ, Hamamichi S, Schieltz JM, et al. (2010) Differential neuroprotective effects of 14-3-3 proteins in models of Parkinson's disease. Cell Death Dis 1: e2.
41. Umahara T, Uchihara T, Nakamura A, Iwamoto T, (2011) Differential expression of 14-3-3 protein isoforms in developing rat hippocampus, cortex, rostral migratory stream, olfactory bulb, and white matter. Brain Res 1410: 1-11.
42. Ramser EM, Wolters G, Dityateva G, Dityatev A, Schachner M, et al. (2010) The 14-3-3zeta protein binds to the cell adhesion molecule L1, promotes L1 phosphorylation by CKII and influences L1-dependent neurite outgrowth. PLoS One 5: e13462.
43. Stetler RA, Cao G, Gao Y, Zhang F, Wang S, et al. (2008) Hsp27 protects against ischemic brain injury via attenuation of a novel stress-response cascade upstream of mitochondrial cell death signaling. J Neurosci 28: 13038-13055.
44. Lindholm D, Wootz H, Korhonen L, (2006) ER stress and neurodegenerative diseases. Cell Death Differ 13: 385-392.
45. Concannon CG, Ward MW, Bonner HP, Kuroki K, Tuffy LP, et al. (2008) NMDA receptor-mediated excitotoxic neuronal apoptosis in vitro and in vivo occurs in an ER stress and PUMA independent manner. J Neurochem 105: 891-903.
46. Maruo K, Nagata T, Yamamoto S, Nagai K, Yajima Y, et al. (2003) Tunicamycin inhibits NMDA and AMPA receptor responses independently of N-glycosylation. Brain Res 977: 294-297.
47. Rao RV, Bredesen DE, (2004) Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr Opin Cell Biol 16: 653-662.
48. Murphy N, Yamamoto A, Henshall DC, (2008) Detection of 14-3-3zeta in cerebrospinal fluid following experimentally evoked seizures. Biomarkers 13: 377-384.
49. Murphy BM, Engel T, Paucard A, Hatazaki S, Mouri G, et al. (2010) Contrasting patterns of Bim induction and neuroprotection in Bim-deficient mice between hippocampus and neocortex after status epilepticus. Cell Death Differ 17: 459-468.
50. Engel T, Caballero-Caballero A, Schindler CK, Plesnila N, Strasser A, et al. (2010) BH3-only protein Bid is dispensable for seizure-induced neuronal death and the associated nuclear accumulation of apoptosis-inducing factor. J Neurochem 115: 92-101.
51. Engel T, Murphy BM, Hatazaki S, Jimenez-Mateos EM, Concannon CG, et al. (2010) Reduced hippocampal damage and epileptic seizures after status epilepticus in mice lacking proapoptotic Puma. FASEB J 24: 853-861.
52. Shinoda S, Schindler CK, Meller R, So NK, Araki T, et al. (2004) Bim regulation may determine hippocampal vulnerability after injurious seizures and in temporal lobe epilepsy. J Clin Invest 113: 1059-1068.
53. Jimenez-Mateos EM, Hatazaki S, Johnson MB, Bellver-Estelles C, Mouri G, et al. (2008) Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol Dis 32: 442-453.
54. Hashiguchi M, Sobue K, Paudel HK, (2000) 14-3-3zeta is an effector of tau protein phosphorylation. J Biol Chem 275: 25247-25254.
55. Umahara T, Uchihara T, Tsuchiya K, Nakamura A, Iwamoto T, et al. (2004) 14-3-3 proteins and zeta isoform containing neurofibrillary tangles in patients with Alzheimer's disease. Acta Neuropathol (Berl) 108: 279-286.