Effects of JIP3 on epileptic seizures: Evidence from temporal lobe epilepsy patients, kainic-induced acute seizures and pentylenetetrazole-induced kindled seizures

Neuroscience

Volumn 300, Issue , 2015, Pages 314-324

  Wang, Z ^a,b   Chen, Y ^a   Lu Y ^a   Chen, X ^a   Cheng, L ^a   Mi, X ^a   Xu, X ^a   Deng, W ^a   Zhang, Y ^a   Wang, N ^a   Li, J ^a   Li, Y ^a   Wang, X ^a  

^a THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b Fuling Central Hospital   (China)

Author keywords

Apoptosis; JIP3; JNK; Lentivirus; Temporal lobe epilepsy

Indexed keywords

C JUN AMINO TERMINAL KINASE INTERACTING PROTEIN 3; KAINIC ACID; LENTIVIRUS VECTOR; PENTETRAZOLE; SCAFFOLD PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; MAPK8IP3 PROTEIN, HUMAN; MAPK8IP3 PROTEIN, MOUSE; NERVE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; CELLULAR DISTRIBUTION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; DISEASE DURATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; EPILEPTOGENESIS; EXPERIMENTAL SEIZURE; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; JIP3 GENE; KINDLING; MALE; MOUSE; MOUSE MODEL; NEOCORTEX; NERVE CELL; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RISK REDUCTION; RNA INTERFERENCE; SEIZURE; SEIZURE SUSCEPTIBILITY; SEIZURE THRESHOLD; TEMPORAL CORTEX; TEMPORAL LOBE EPILEPSY; VIRAL GENE DELIVERY SYSTEM; ANIMAL; APOPTOSIS; C57BL MOUSE; DISEASE MODEL; ENZYMOLOGY; EPILEPSY, TEMPORAL LOBE; GENETICS; HIPPOCAMPAL CA3 REGION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRESCHOOL CHILD; YOUNG ADULT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADOLESCENT; ADULT; ANIMALS; APOPTOSIS; CA3 REGION, HIPPOCAMPAL; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; KAINIC ACID; KINDLING, NEUROLOGIC; MALE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; PENTYLENETETRAZOLE; RNA INTERFERENCE; SEIZURES; YOUNG ADULT;

EID: 84930665846     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.008     Document Type: Article

References (40)

1. Akechi M., Ito M., Uemura K., Takamatsu N., Yamashita S., Uchiyama K., Yoshioka K., Shiba T. Expression of JNK cascade scaffold protein JSAP1 in the mouse nervous system. Neurosci Res 2001, 39:391-400.
2. Avignone E., Ulmann L., Levavasseur F., Rassendren F., Audinat E. Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci 2008, 28:9133-9144.
3. Banerjee P.N., Filippi D., Allen Hauser W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res 2009, 85:31-45.
4. Behrens A., Sibilia M., Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat Genet 1999, 21:326-329.
5. Ben-Ari Y., Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 2000, 23:580-587.
6. Bilimoria P.M., de la Torre-Ubieta L., Ikeuchi Y., Becker E.B., Reiner O., Bonni A. A JIP3-regulated GSK3beta/DCX signaling pathway restricts axon branching. J Neurosci 2010, 30:16766-16776.
7. Borsello T., Forloni G. JNK signalling: a possible target to prevent neurodegeneration. Curr Pharm Des 2007, 13:1875-1886.
8. Brecht S., Kirchhof R., Chromik A., Willesen M., Nicolaus T., Raivich G., Wessig J., Waetzig V., Goetz M., Claussen M., Pearse D., Kuan C.-Y., Vaudano E., Behrens A., Wagner E., Flavell R.A., Davis R.J., Herdegen T. Specific pathophysiological functions of JNK isoforms in the brain. Eur J Neurosci 2005, 21:363-377.
9. Chen X., Wu J., Hua D., Shu K., Wang J.Z., Li L., Lei T. The c-Jun N-terminal kinase inhibitor SP600125 is neuroprotective in amygdala kindled rats. Brain Res 2010, 1357:104-114.
10. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
11. French J.A. Refractory epilepsy: clinical overview. Epilepsia 2007, 48(Suppl. 1):3-7.
12. Friedman L.K., Pellegrini-Giampietro D.E., Sperber E.F., Bennett M.V., Moshe S.L., Zukin R.S. Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 1994, 14:2697-2707.
13. Ha H.Y., Cho I.H., Lee K.W., Song J.Y., Kim K.S., Yu Y.M., Lee J.K., Song J.S., Yang S.D., Shin H.S., Han P.L. The axon guidance defect of the telencephalic commissures of the JSAP1-deficient brain was partially rescued by the transgenic expression of JIP1. Dev Biol 2005, 277:184-199.
14. Henshall D.C., Simon R.P. Epilepsy and apoptosis pathways. J Cereb Blood Flow Metab 2005, 25:1557-1572.
15. Kelkar N., Gupta S., Dickens M., Davis R.J. Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3. Mol Cell Biol 2000, 20:1030-1043.
16. Koushika S.P. "JIP"ing along the axon: the complex roles of JIPs in axonal transport. Bioessays 2008, 30:10-14.
17. Matsuguchi T., Masuda A., Sugimoto K., Nagai Y., Yoshikai Y. JNK-interacting protein 3 associates with Toll-like receptor 4 and is involved in LPS-mediated JNK activation. EMBO J 2003, 22:4455-4464.
18. Matsuura H., Nishitoh H., Takeda K., Matsuzawa A., Amagasa T., Ito M., Yoshioka K., Ichijo H. Phosphorylation-dependent scaffolding role of JSAP1/JIP3 in the ASK1-JNK signaling pathway. A new mode of regulation of the MAP kinase cascade. J Biol Chem 2002, 277:40703-40709.
19. McNamara J.O. Emerging insights into the genesis of epilepsy. Nature 1999, 399:A15-A22.
20. Mishra A., Goel R.K. Age dependent learning and memory deficit in Pentylenetetrazol kindled mice. Eur J Pharmacol 2012, 674:315-320.
21. Monory K., Massa F., Egertova M., Eder M., Blaudzun H., Westenbroek R., Kelsch W., Jacob W., Marsch R., Ekker M., Long J., Rubenstein J.L., Goebbels S., Nave K.A., During M., Klugmann M., Wolfel B., Dodt H.U., Zieglgansberger W., Wotjak C.T., Mackie K., Elphick M.R., Marsicano G., Lutz B. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 2006, 51:455-466.
22. Muresan Z., Muresan V. C-Jun NH2-terminal kinase-interacting protein-3 facilitates phosphorylation and controls localization of amyloid-beta precursor protein. J Neurosci 2005, 25:3741-3751.
23. Ongusaha P.P., Qi H.H., Raj L., Kim Y.B., Aaronson S.A., Davis R.J., Shi Y., Liao J.K., Lee S.W. Identification of ROCK1 as an upstream activator of the JIP-3 to JNK signaling axis in response to UVB damage. Sci Signal 2008, 1:ra14.
24. Park H.J., Kim H.J., Ra J., Zheng L.T., Yim S.V., Chung J.H. Protective effect of topiramate on kainic acid-induced cell death in mice hippocampus. Epilepsia 2008, 49:163-167.
25. Perez Y., Morin F., Beaulieu C., Lacaille J.C. Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 1996, 8:736-748.
26. Schmidt D., Loscher W. Drug resistance in epilepsy: putative neurobiologic and clinical mechanisms. Epilepsia 2005, 46:858-877.
27. Song J.J., Lee Y.J. Differential activation of the JNK signal pathway by UV irradiation and glucose deprivation. Cell Signal 2007, 19:563-572.
28. Spigolon G., Veronesi C., Bonny C., Vercelli A. C-Jun N-terminal kinase signaling pathway in excitotoxic cell death following kainic acid-induced status epilepticus. Eur J Neurosci 2010, 31:1261-1272.
29. Sun T., Yu N., Zhai L.K., Li N., Zhang C., Zhou L., Huang Z., Jiang X.Y., Shen Y., Chen Z.Y. C-Jun NH2-terminal kinase (JNK)-interacting protein-3 (JIP3) regulates neuronal axon elongation in a kinesin- and JNK-dependent manner. J Biol Chem 2013, 288:14531-14543.
30. Szaroma W., Dziubek K., Gren A., Kreczmer B., Kapusta E. Influence of the kainic acid on antioxidant status in the brain, liver and kidneys of the mouse. Acta Physiol Hung 2012, 99:447-459.
31. Takino T., Nakada M., Miyamori H., Watanabe Y., Sato T., Gantulga D., Yoshioka K., Yamada K.M., Sato H. JSAP1/JIP3 cooperates with focal adhesion kinase to regulate c-Jun N-terminal kinase and cell migration. J Biol Chem 2005, 280:37772-37781.
32. Takino T., Yoshioka K., Miyamori H., Yamada K.M., Sato H. A scaffold protein in the c-Jun N-terminal kinase signaling pathway is associated with focal adhesion kinase and tyrosine-phosphorylated. Oncogene 2002, 21:6488-6497.
33. Tang F.R., Loke W.K. Cyto-, axo- and dendro-architectonic changes of neurons in the limbic system in the mouse pilocarpine model of temporal lobe epilepsy. Epilepsy Res 2010, 89:43-51.
34. Verhey K.J., Meyer D., Deehan R., Blenis J., Schnapp B.J., Rapoport T.A., Margolis B. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 2001, 152:959-970.
35. Waetzig V., Herdegen T. Context-specific inhibition of JNKs: overcoming the dilemma of protection and damage. Trends Pharmacol Sci 2005, 26:455-461.
36. Xu B., Zhou O K Y., Choy P.C., Pierce G.N., Siow Y.L. Regulation of stress-associated scaffold proteins JIP1 and JIP3 on the c-Jun NH2-terminal kinase in ischemia-reperfusion. Can J Physiol Pharmacol 2010, 88:1084-1092.
37. Yang D.D., Kuan C.Y., Whitmarsh A.J., Rincon M., Zheng T.S., Davis R.J., Rakic P., Flavell R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997, 389:865-870.
38. Zelano J., Halawa I., Clausen F., Kumlien E. Hyponatremia augments kainic-acid induced status epilepticus in the mouse: a model for dysmetabolic status epilepticus. Epilepsy Res 2013, 106:29-34.
39. Zhang X., Chen G., Lu Y., Liu J., Fang M., Luo J., Cao Q., Wang X. Association of mitochondrial Letm1 with epileptic seizures. Cereb Cortex 2014, 24:2533-2540.
40. Zhao Y., Spigolon G., Bonny C., Culman J., Vercelli A., Herdegen T. The JNK inhibitor D-JNKI-1 blocks apoptotic JNK signaling in brain mitochondria. Mol Cell Neurosci 2012, 49:300-310.