The prostaglandin EP1 receptor potentiates kainate receptor activation via a protein kinase C pathway and exacerbates status epilepticus

Neurobiology of Disease

Volumn 70, Issue , 2014, Pages 74-89

  Rojas, Asheebo ^a   Gueorguieva, Paoula ^a   Lelutiu, Nadia ^a   Quan, Yi ^a   Shaw, Renee ^a   Dingledine, Raymond ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA; EP1; EP2; GluK2; GluK4; GluK5; Kainate receptor; Protein Kinase C; Status epilepticus

Indexed keywords

CALCIUM; KAINIC ACID RECEPTOR; PHOSPHOLIPASE C; PROSTAGLANDIN E RECEPTOR 1; PROSTANOID RECEPTOR; PROTEIN GLUK2; PROTEIN GLUK5; PROTEIN KINASE C; RECEPTOR PROTEIN; SERINE; UNCLASSIFIED DRUG; KAINIC ACID; PROSTANOID; GLUK1 KAINATE RECEPTOR; PTGER1 PROTEIN, MOUSE; PTGER1 PROTEIN, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL CULTURE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; DISEASE EXACERBATION; EMBRYO; EP1 GENE; EPILEPTIC STATE; GENE; GENE ACTIVATION; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SECOND MESSENGER; SEIZURE THRESHOLD; SIGNAL TRANSDUCTION; XENOPUS; CONTROLLED STUDY; INFLAMMATION; SEIZURE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOMODULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROIMMUNOMODULATION; OOCYTES; PROTEIN KINASE C; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE; SEIZURES; SIGNAL TRANSDUCTION; STATUS EPILEPTICUS; XENOPUS;

EID: 84904540901     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.06.004     Document Type: Article

References (54)

1. Ahmad A.S., Saleem S., Ahmad M., Dore S. Prostaglandin EP1 receptor contributes to excitotoxicity and focal ischemic brain damage. Toxicol. Sci. 2006, 89:265-270.
2. Ahmad A.S., Maruyama T., Narumiya S., Dore S. PGE2 EP1 receptor deletion attenuates 6-OHDA-induced Parkinsonism in mice: old switch, new target. Neurotox. Res. 2013, 23:260-266.
3. Ben-Ari Y., Lagowska J., Tremblay E., Le Gal La Salle G. A new model of focal status epilepticus: intra-amygdaloid application of kainic acid elicits repetitive secondarily generalized convulsive seizures. Brain Res. 1979, 163:176-179.
4. Benveniste M., Wilhelm J., Dingledine R.J., Mott D.D. Subunit-dependent modulation of kainate receptors by muscarinic acetylcholine receptors. Brain Res. 2010, 1352:61-69.
5. Bettler B., Mulle C. Review: neurotransmitter receptors. II. AMPA and kainate receptors. Neuropharmacology 1995, 34:123-139.
6. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 2003, 182:21-34.
7. Breyer M.D., Jacobson H.R., Breyer R.M. Functional and molecular aspects of renal prostaglandin receptors. J. Am. Soc. Nephrol. 1996, 7:8-17.
8. Chamberlain S.E., Gonzalez-Gonzalez I.M., Wilkinson K.A., Konopacki F.A., Kantamneni S., Henley J.M., Mellor J.R. SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat. Neurosci. 2012, 15:845-852.
9. Chen C., Bazan N.G. Endogenous PGE2 regulates membrane excitability and synaptic transmission in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2005, 93:929-941.
10. Chen C., Leonard J.P. Protein tyrosine kinase-mediated potentiation of currents from cloned NMDA receptors. J. Neurochem. 1996, 67:194-200.
11. Curras M.C., Dingledine R. Selectivity of amino acid transmitters acting at N-methyl-d-aspartate and amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptors. Mol. Pharmacol. 1992, 41:520-526.
12. Darstein M., Petralia R.S., Swanson G.T., Wenthold R.J., Heinemann S.F. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J. Neurosci. 2003, 23:8013-8019.
13. Fukumoto K., Takagi N., Yamamoto R., Moriyama Y., Takeo S., Tanonaka K. Prostanoid EP1 receptor antagonist reduces blood-brain barrier leakage after cerebral ischemia. Eur. J. Pharmacol. 2010, 640:82-86.
14. Guan Y., Zhang Y., Wu J., Qi Z., Yang G., Dou D., Gao Y., Chen L., Zhang X., Davis L.S., Wei M., Fan X., Carmosino M., Hao C., Imig J.D., Breyer R.M., Breyer M.D. Antihypertensive effects of selective prostaglandin E2 receptor subtype 1 targeting. J. Clin. Invest. 2007, 117:2496-2505.
15. Hellier J.L., Patrylo P.R., Buckmaster P.S., Dudek F.E. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 1998, 31:73-84.
16. Huettner J.E. Kainate receptors and synaptic transmission. Prog. Neurobiol. 2003, 70:387-407.
17. Jiang J., Ganesh T., Du Y., Thepchatri P., Rojas A., Lewis I., Kurtkaya S., Li L., Qui M., Serrano G., Shaw R., Sun A., Dingledine R. Neuroprotection by selective allosteric potentiators of the EP2 prostaglandin receptor. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2307-2312.
18. Jiang J., Quan Y., Ganesh T., Pouliot W.A., Dudek F.E., Dingledine R. Inhibition of the prostaglandin receptor EP2 following status epilepticus reduces delayed mortality and brain inflammation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:3591-3596.
19. Kamiya H. Kainate receptor-dependent presynaptic modulation and plasticity. Neurosci. Res. 2002, 42:1-6.
20. Kawano T., Anrather J., Zhou P., Park L., Wang G., Frys K.A., Kunz A., Cho S., Orio M., Iadecola C. Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat. Med. 2006, 12:225-229.
21. Kohr G., Seeburg P.H. Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J. Physiol. 1996, 492(Pt 2):445-452.
22. Konopacki F.A., Jaafari N., Rocca D.L., Wilkinson K.A., Chamberlain S., Rubin P., Kantamneni S., Mellor J.R., Henley J.M. Agonist-induced PKC phosphorylation regulates GluK2 SUMOylation and kainate receptor endocytosis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:19772-19777.
23. Kornreich B.G., Niu L., Roberson M.S., Oswald R.E. Identification of C-terminal domain residues involved in protein kinase A-mediated potentiation of kainate receptor subtype 6. Neuroscience 2007, 146:1158-1168.
24. Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 2003, 4:481-495.
25. Lerma J., Paternain A.V., Rodriguez-Moreno A., Lopez-Garcia J.C. Molecular physiology of kainate receptors. Physiol. Rev. 2001, 81:971-998.
26. MacDonald J.F., Jackson M.F., Beazely M.A. G protein-coupled receptors control NMDARs and metaplasticity in the hippocampus. Biochim. Biophys. Acta 2007, 1768:941-951.
27. Martin S., Nishimune A., Mellor J.R., Henley J.M. SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 2007, 447:321-325.
28. Matsuoka Y., Furuyashiki T., Yamada K., Nagai T., Bito H., Tanaka Y., Kitaoka S., Ushikubi F., Nabeshima T., Narumiya S. Prostaglandin E receptor EP1 controls impulsive behavior under stress. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16066-16071.
29. Mott D.D., Rojas A., Fisher J.L., Dingledine R.J., Benveniste M. Subunit-specific desensitization of heteromeric kainate receptors. J. Physiol. 2010, 588:683-700.
30. Nadler J.V., Perry B.W., Cotman C.W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature 1978, 271:676-677.
31. Nasu-Nishimura Y., Jaffe H., Isaac J.T., Roche K.W. Differential regulation of kainate receptor trafficking by phosphorylation of distinct sites on GluR6. J. Biol. Chem. 2010, 285:2847-2856.
32. Pickering D.S., Taverna F.A., Salter M.W., Hampson D.R. Palmitoylation of the GluR6 kainate receptor. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:12090-12094.
33. Pinheiro P., Mulle C. Kainate receptors. Cell Tissue Res. 2006, 326:457-482.
34. Quan Y., Jiang J., Dingledine R. EP2 receptor signaling pathways regulate classical activation of microglia. J. Biol. Chem. 2013, 288:9293-9302.
35. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
36. Raymond L.A., Blackstone C.D., Huganir R.L. Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 1993, 361:637-641.
37. Raymond L.A., Tingley W.G., Blackstone C.D., Roche K.W., Huganir R.L. Glutamate receptor modulation by protein phosphorylation. J. Physiol. Paris 1994, 88:181-192.
38. Rojas A., Dingledine R. Ionotropic glutamate receptors: regulation by G-protein-coupled receptors. Mol. Pharmacol. 2013, 83:746-752.
39. Rojas A., Wetherington J., Shaw R., Serrano G., Swanger S., Dingledine R. Activation of group I metabotropic glutamate receptors potentiates heteromeric kainate receptors. Mol. Pharmacol. 2013, 83:106-121.
40. Schmued L.C., Albertson C., Slikker W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 1997, 751:37-46.
41. Serrano G.E., Lelutiu N., Rojas A., Cochi S., Shaw R., Makinson C.D., Wang D., FitzGerald G.A., Dingledine R. Ablation of cyclooxygenase-2 in forebrain neurons is neuroprotective and dampens brain inflammation after status epilepticus. J. Neurosci. 2011, 31:14850-14860.
42. Sharma A.K., Searfoss G.H., Reams R.Y., Jordan W.H., Snyder P.W., Chiang A.Y., Jolly R.A., Ryan T.P. Kainic acid-induced F-344 rat model of mesial temporal lobe epilepsy: gene expression and canonical pathways. Toxicol. Pathol. 2009, 37:776-789.
43. Shimamura M., Zhou P., Casolla B., Qian L., Capone C., Kurinami H., Iadecola C., Anrather J. Prostaglandin E2 type 1 receptors contribute to neuronal apoptosis after transient forebrain ischemia. J. Cereb. Blood Flow Metab. 2013, 33:1207-1214.
44. Sperk G., Lassmann H., Baran H., Kish S.J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 1983, 10:1301-1315.
45. Stock J.L., Shinjo K., Burkhardt J., Roach M., Taniguchi K., Ishikawa T., Kim H.S., Flannery P.J., Coffman T.M., McNeish J.D., Audoly L.P. The prostaglandin E2 EP1 receptor mediates pain perception and regulates blood pressure. J. Clin. Invest. 2001, 107:325-331.
46. Traynelis S.F., Wahl P. Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J. Physiol. 1997, 503(Pt 3):513-531.
47. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
48. Wang Y.T., Salter M.W. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 1994, 369:233-235.
49. Wang L.Y., Taverna F.A., Huang X.P., MacDonald J.F., Hampson D.R. Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 1993, 259:1173-1175.
50. Wang Q., Yu S., Simonyi A., Sun G.Y., Sun A.Y. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 2005, 31:3-16.
51. Wilkinson K.A., Nishimune A., Henley J.M. Analysis of SUMO-1 modification of neuronal proteins containing consensus SUMOylation motifs. Neurosci. Lett. 2008, 436:239-244.
52. Wilkinson K.A., Konopacki F., Henley J.M. Modification and movement: phosphorylation and SUMOylation regulate endocytosis of GluK2-containing kainate receptors. Commun. Integr. Biol. 2012, 5:223-226.
53. Zhen G., Kim Y.T., Li R.C., Yocum J., Kapoor N., Langer J., Dobrowolski P., Maruyama T., Narumiya S., Dore S. PGE2 EP1 receptor exacerbated neurotoxicity in a mouse model of cerebral ischemia and Alzheimer's disease. Neurobiol. Aging 2012, 33:2215-2219.
54. Zhu P., Genc A., Zhang X., Zhang J., Bazan N.G., Chen C. Heterogeneous expression and regulation of hippocampal prostaglandin E2 receptors. J. Neurosci. Res. 2005, 81:817-826.