Prostaglandin E2 and BDNF levels in rat hippocampus are negatively correlated with status epilepticus severity: No impact on survival of seizure-generated neurons

Neurobiology of Disease

Volumn 23, Issue 1, 2006, Pages 23-35

  Ajmone Cat, Maria Antonietta ^a,b,d   Iosif, Robert E ^b,d   Ekdahl, Christine T ^b,d   Kokaia, Zaal ^c,d   Minghetti, Luisa ^a   Lindvall, Olle ^b,d  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b LUND UNIVERSITY   (Sweden)

^c Stem Cell Institute   (Sweden)

^d Lund Strategic Research Center for Stem Cell Biology and Cell Therapy   (Sweden)

Author keywords

Brain derived neurotrophic factor (BDNF); Cyclooxygenase 2 (COX 2); EP2; EP3; Flurbiprofen; Isoprostanes; Neurogenesis; Prostaglandin E2 (PGE2); Status epilepticus

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN PROTEIN; CYCLOOXYGENASE 2 INHIBITOR; FLURBIPROFEN; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SEVERITY; EPILEPTIC STATE; EPILEPTOGENESIS; FOCAL EPILEPSY; GRAND MAL SEIZURE; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE; SURVIVAL; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STEM CELL;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL PROLIFERATION; CELL SURVIVAL; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; FLURBIPROFEN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NEURONAL PLASTICITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; STATUS EPILEPTICUS; STEM CELLS;

EID: 33745122517     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.01.010     Document Type: Article

References (86)

1. Adams J., Collaco-Moraes Y., and de Belleroche J. Cyclooxygenase-2 induction in cerebral cortex: an intracellular response to synaptic excitation. J. Neurochem. 66 (1996) 6-13
2. Andreasson K.I., Savonenko A., Vidensky S., Goellner J.J., Zhang Y., Shaffer A., Kaufmann W.E., Worley P.F., Isakson P., and Markowska A.L. Age-dependent cognitive deficits and neuronal apoptosis in cyclooxygenase-2 transgenic mice. J. Neurosci. 21 (2001) 8198-8209
3. Ariumi H., Takano Y., Masumi A., Takahashi S., Hirabara Y., Honda K., Saito R., and Kamiya H.O. Roles of the central prostaglandin EP3 receptors in cardiovascular regulation in rats. Neurosci. Lett. 324 (2002) 61-64
4. Arvidsson A., Kokaia Z., and Lindvall O. N-methyl-d-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur. J. Neurosci. 14 (2001) 10-18
5. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970 Epub 2002 Aug 5
6. Baik E.J., Kim E.J., Lee S.H., and Moon C. Cyclooxygenase-2 selective inhibitors aggravate kainic acid induced seizure and neuronal cell death in the hippocampus. Brain Res. 843 (1999) 118-129
7. Baran H., Vass K., Lassmann H., and Hornykiewicz O. The cyclooxygenase and lipoxygenase inhibitor BW755C protects rats against kainic acid-induced seizures and neurotoxicity. Brain Res. 646 (1994) 201-206
8. Barnabé-Heider F., and Miller F.D. Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J. Neurosci. 23 (2003) 5149-5160
9. Barton M.E., and Shannon H.E. The seizure-related phenotype of brain-derived neurotrophic factor knockdown mice. Neuroscience 136 (2005) 563-569 Electronic publication 2005 Sep 28
10. Batshake B., Nilsson C., and Sundelin J. Molecular characterization of the mouse prostanoid EP1 receptor gene. Eur. J. Biochem. 231 (1995) 809-814
11. Bengzon J., Kokaia Z., Elmer E., Nanobashvili A., Kokaia M., and Lindvall O. Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 10432-10437
12. Bilak M., Wu L., Wang Q., Haughey N., Conant K., St Hillaire C., and Andreasson K. PGE2 receptors rescue motor neurons in a model of amyotrophic lateral sclerosis. Ann. Neurol. 56 (2004) 240-248
13. Binder D.K. The role of BDNF in epilepsy and other diseases of the mature nervous system. Adv. Exp. Med. Biol. 548 (2004) 34-56
14. Binder D.K., Croll S.D., Gall C.M., and Scharfman H.E. BDNF and epilepsy: too much of a good thing?. Trends Neurosci. 24 (2001) 47-53
15. Breder C.D., Dewitt D., and Kraig R.P. Characterization of inducible cyclooxygenase in rat brain. J. Comp. Neurol. 355 (1995) 296-315
16. Candelario-Jalil E., Gonzalez-Falcon A., Garcia-Cabrera M., Alvarez D., Al-Dalain S., Martinez G., Leon O.S., and Springer J.E. Assessment of the relative contribution of COX-1 and COX-2 isoforms to ischemia-induced oxidative damage and neurodegeneration following transient global cerebral ischemia. J. Neurochem. 86 (2003) 545-555
17. Castren E., Berninger B., Leingartner A., and Lindholm D. Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity. Prog. Brain Res. 117 (1998) 57-64
18. Chen C., and Bazan N.G. Endogenous PGE2 regulates membrane excitability and synaptic transmission in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 93 (2005) 929-941
19. Chen C., Magee J.C., and Bazan N.G. Cyclooxygenase-2 regulates prostaglandin E2 signaling in hippocampal long-term synaptic plasticity. J. Neurophysiol. 87 (2002) 2851-2857
20. Coggeshall R.E., and Lekan H.A. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J. Comp. Neurol. 364 (1996) 6-15 Erratum in: J. Comp. Neurol. 1996. 369, 162
21. De Simone R., Ajmone-Cat M.A., and Minghetti L. Atypical antiinflammatory activation of microglia induced by apoptotic neurons: possible role of phosphatidylserine-phosphatidylserine receptor interaction. Mol. Neurobiol. 29 (2004) 197-212
22. Desjardins P., Sauvageau A., Bouthillier A., Navarro D., Hazell A.S., Rose C., and Butterworth R.F. Induction of astrocytic cyclooxygenase-2 in epileptic patients with hippocampal sclerosis. Neurochem. Int. 42 (2003) 299-303
23. Ekdahl C.T., Mohapel P., Elmer E., and Lindvall O. Caspase inhibitors increase short-term survival of progenitor-cell progeny in the adult rat dentate gyrus following status epilepticus. Eur. J. Neurosci. 14 (2001) 937-945
24. Ekdahl C.T., Mohapel P., Weber E., Bahr B., Blomgren K., and Lindvall O. Caspase-mediated death of newly formed neurons in the adult rat dentate gyrus following status epilepticus. Eur. J. Neurosci. 16 (2002) 1463-1471
25. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., and Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13632-13637
26. Ekdahl C.T., Zhu C., Bonde S., Bahr B.A., Blomgren K., and Lindvall O. Death mechanisms in status epilepticus-generated neurons and effects of additional seizures on their survival. Neurobiol. Dis. 14 (2003) 513-523
27. Elmer E., Kokaia Z., Kokaia M., Carnahan J., Nawa H., and Lindvall O. Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience 83 (1998) 351-362
28. Forstermann U., Seregi A., and Hertting G. Anticonvulsive effects of endogenous prostaglandins formed in brain of spontaneously convulsing gerbils. Prostaglandins 27 (1984) 913-923
29. Friedman W.J., Larkfors L., Ayer-LeLievre C., Ebendal T., Olson L., and Persson H. Regulation of beta-nerve growth factor expression by inflammatory mediators in hippocampal cultures. J. Neurosci. Res. 27 (1990) 374-382
30. Fukuchi M., Tabuchi A., and Tsuda M. Transcriptional regulation of neuronal genes and its effect on neural functions: cumulative mRNA expression of PACAP and BDNF genes controlled by calcium and cAMP signals in neurons. J. Pharmacol. Sci. 98 (2005) 212-218
31. Fukumitsu H., Furukawa Y., Tsusaka M., Kinukawa H., Nitta A., Nomoto H., Mima T., and Furukawa S. Simultaneous expression of brain-derived neurotrophic factor and neurotrophin-3 in Cajal-Retzius, subplate and ventricular progenitor cells during early development stages of the rat cerebral cortex. Neuroscience 84 (1998) 115-127
32. Gage F.H. Neurogenesis in the adult brain. J. Neurosci. 22 (2002) 612-613
33. Gascon E., Vutskits L., Zhang H., Barral-Moran M.J., Kiss P.J., Mas C., and Kiss J.Z. Sequential activation of p75 and TrkB is involved in dendritic development of subventricular zone-derived neuronal progenitors in vitro. Eur. J. Neurosci. 21 (2005) 69-80
34. Gobbo O.L., and O'Mara S.M. Post-treatment, but not pre-treatment, with the selective cyclooxygenase-2 inhibitor celecoxib markedly enhances functional recovery from kainic acid-induced neurodegeneration. Neuroscience 125 (2004) 317-327
35. Gustafsson E., Lindvall O., and Kokaia Z. Intraventricular infusion of TrkB-Fc fusion protein promotes ischemia-induced neurogenesis in adult rat dentate gyrus. Stroke 34 (2003) 2710-2715
36. Hirst W.D., Young K.A., Newton R., Allport V.C., Marriott D.R., and Wilkin G.P. Expression of COX-2 by normal and reactive astrocytes in the adult rat central nervous system. Mol. Cell. Neurosci. 13 (1999) 57-68
37. Ji Y., Pang P.T., Feng L., and Lu B. Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat. Neurosci. 8 (2005) 164-172
38. Jiang J., Borisenko G.G., Osipov A., Martin I., Chen R., Shvedova A.A., Sorokin A., Tyurina Y.Y., Potapovich A., Tyurin V.A., Graham S.H., and Kagan V.E. Arachidonic acid-induced carbon-centered radicals and phospholipid peroxidation in cyclo-oxygenase-2-transfected PC12 cells. J. Neurochem. 90 (2004) 1036-1049
39. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., and Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4710-4715
40. Kaufmann W.E., Worley P.F., Pegg J., Bremer M., and Isakson P. COX-2, a synaptically induced enzyme, is expressed by excitatory neurons as postsynaptic sites in rat cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2317-2321
41. Kaufmann W.E., Worley P.F., Taylor C.V., Bremer M., and Isakson P.C. Cyclooxygenase-2 expression during rat neocortical development and in Rett syndrome. Brain Dev. 19 (1997) 25-34
42. Kunz T., and Oliw E.H. The selective cyclooxygenase-2 inhibitor rofecoxib reduces kainate-induced cell death in the rat hippocampus. Eur. J. Neurosci. 13 (2001) 569-575
43. Larsson E., Mandel R.J., Klein R.L., Muzyczka N., Lindvall O., and Kokaia Z. Suppression of insult-induced neurogenesis in adult rat brain by brain-derived neurotrophic factor. Exp. Neurol. 177 (2002) 1-8
44. Lee J., Duan W., and Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J. Neurochem. 82 (2002) 1367-1375
45. Levi G., Minghetti L., and Aloisi F. Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin E2 on microglial functions. Biochimie 80 (1998) 899-904
46. Lie D.C., Song H., Colamarino S.A., Ming G.L., and Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 399-421
47. Linnarsson S., Willson C.A., and Ernfors P. Cell death in regenerating populations of neurons in BDNF mutant mice. Brain Res. Mol. Brain Res. 75 (2000) 61-69
48. Liu J., Solway K., Messing R.O., and Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci. 18 (1998) 7768-7778
49. Liu H., Kaur J., Dashtipour K., Kinyamu R., Ribak C.E., and Friedman L.K. Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticosteroid level. Exp. Neurol. 184 (2003) 196-213
50. Liu D., Wu L., Breyer R., Mattson M.P., and Andreasson K. Neuroprotection by the PGE2 EP2 receptor in permanent focal cerebral ischemia. Ann. Neurol. 57 (2005) 758-761
51. Lothman E.W., Bertram E.H., Bekenstein J.W., and Perlin J.B. Self-sustaining limbic status epilepticus induced by 'continuous' hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res. 3 (1989) 107-119
52. Manabe Y., Anrather J., Kawano T., Niwa K., Zhou P., Ross M.E., and Iadecola C. Prostanoids, not reactive oxygen species, mediate COX-2-dependent neurotoxicity. Ann. Neurol. 55 (2004) 668-675
53. Marcheselli V.L., and Bazan N.G. Sustained induction of prostaglandin endoperoxide synthase-2 by seizures in hippocampus. Inhibition by a platelet-activating factor antagonist. J. Biol. Chem. 271 (1996) 24794-24799
54. McCullough L., Wu L., Haughey N., Liang X., Hand T., Wang Q., Breyer R.M., and Andreasson K. Neuroprotective function of the PGE2 EP2 receptor in cerebral ischemia. J. Neurosci. 24 (2004) 257-268
55. Minghetti L. Cyclooxygenase-2 (COX-2) in inflammatory and degenerative brain diseases. J. Neuropathol. Exp. Neurol. 63 (2004) 901-910
56. Minghetti L., Greco A., Cardone F., Puopolo M., Ladogana A., Almonti S., Cunningham C., Perry V.H., Pocchiari M., and Levi G. Increased brain synthesis of prostaglandin E2 and F2-isoprostane in human and experimental transmissible spongiform encephalopathies. J. Neuropathol. Exp. Neurol. 59 (2000) 866-871
57. Mohapel P., Ekdahl C.T., and Lindvall O. Status epilepticus severity influences the long-term outcome of neurogenesis in the adult dentate gyrus. Neurobiol. Dis. 15 (2004) 196-205
58. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
59. Nakamura K., Kaneko T., Yamashita Y., Hasegawa H., Katoh H., and Negishi M. Immunohistochemical localization of prostaglandin EP3 receptor in the rat nervous system. J. Comp. Neurol. 421 (2000) 543-569
60. Nakayama M., Uchimura K., Zhu R.L., Nagayama T., Rose M.E., Stetler R.A., Isakson P.C., Chen J., and Graham S.H. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 10954-10959
61. Paoletti A.M., Piccirilli S., Costa N., Rotiroti D., Bagetta G., and Nistico G. Systemic administration of N omega-nitro-l-arginine methyl ester and indomethacin reduces the elevation of brain PGE2 content and prevents seizures and hippocampal damage evoked by LiCl and tacrine in rat. Exp. Neurol. 149 (1998) 349-355
62. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17 (1997) 3727-3738
63. Patel M., Liang L.P., and Roberts II L.J. Enhanced hippocampal F2-isoprostane formation following kainate-induced seizures. J. Neurochem. 79 (2001) 1065-1069
64. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1997), Academic Press, Paper Back, New York
65. Pepicelli O., Fedele E., Bonanno G., Raiteri M., Ajmone-Cat M.A., Greco A., Levi G., and Minghetti L. In vivo activation of N-methyl-d-aspartate receptors in the rat hippocampus increases prostaglandin E(2) extracellular levels and triggers lipid peroxidation through cyclooxygenase-mediated mechanisms. J. Neurochem. 81 (2002) 1028-1034
66. Pepicelli O., Fedele E., Berardi M., Raiteri M., Levi G., Greco A., Ajmone-Cat M.A., and Minghetti L. Cyclo-oxygenase-1 and -2 differently contribute to prostaglandin E2 synthesis and lipid peroxidation after in vivo activation of N-methyl-d-aspartate receptors in rat hippocampus. J. Neurochem. 93 (2005) 1561-1567
67. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
68. Sairanen M., Lucas G., Ernfors P., Castren M., and Castren E. Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25 (2005) 1089-1094
69. Sandhya T.L., Ong W.Y., Horrocks L.A., and Farooqui A.A. A light and electron microscopic study of cytoplasmic phospholipase A2 and cyclooxygenase-2 in the hippocampus after kainate lesions. Brain Res. 788 (1998) 223-231
70. Sasaki T., Kitagawa K., Sugiura S., Omura-Matsuoka E., Tanaka S., Yagita Y., Okano H., Matsumoto M., and Hori M. Implication of cyclooxygenase-2 on enhanced proliferation of neural progenitor cells in the adult mouse hippocampus after ischemia. J. Neurosci. Res. 72 (2003) 461-471
71. Scharfman H.E. Functional implications of seizure-induced neurogenesis. Adv. Exp. Med. Biol. 548 (2004) 192-212
72. Seregi A., Forstermann U., and Hertting G. Decreased levels of brain cyclo-oxygenase products as a possible cause of increased seizure susceptibility in convulsion-prone gerbils. Brain Res. 305 (1984) 393-395
73. Shaw K.N., Commins S., and O'Mara S.M. Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur. J. Neurosci. 17 (2003) 2438-2446
74. Shaw K.N., Commins S., and O'Mara S.M. Cyclooxygenase inhibition attenuates endotoxin-induced spatial learning deficits, but not an endotoxin-induced blockade of long-term potentiation. Brain Res. 1038 (2005) 231-237
75. Steinhauer H.B., and Hertting G. Lowering of the convulsive threshold by non-steroidal anti-inflammatory drugs. Eur. J. Pharmacol. 69 (1981) 199-203
76. Tilley S.L., Hartney J.M., Erikson C.J., Jania C., Nguyen M., Stock J., McNeisch J., Valancius C., Panettieri Jr. R.A., Penn R.B., and Koller B.H. Receptors and pathways mediating the effects of prostaglandin E2 on airway tone. Am. J. Physiol.: Lung Cell. Mol. Physiol. 284 (2003) 599-606
77. Toyomoto M., Ohta M., Okumura K., Yano H., Matsumoto K., Inoue S., Hayashi K., and Ikeda K. Prostaglandins are powerful inducers of NGF and BDNF production in mouse astrocyte cultures. FEBS Lett. 562 (2004) 211-215
78. Tu B., and Bazan N.G. Hippocampal kindling epileptogenesis upregulates neuronal cyclooxygenase-2 expression in neocortex. Exp. Neurol. 179 (2003) 167-175
79. Turrin N.P., and Rivest S. Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol. Dis. 16 (2004) 321-334
80. Uchida K., Kumihashi K., Kurosawa S., Kobayashi T., Itoi K., and Machida T. Stimulatory effects of prostaglandin E2 on neurogenesis in the dentate gyrus of the adult rat. Zool. Sci. 19 (2002) 1211-1216
81. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
82. Voutsinos-Porche B., Koning E., Kaplan H., Ferrandon A., Guenounou M., Nehlig A., and Motte J. Temporal patterns of the cerebral inflammatory response in the rat lithium-pilocarpine model of temporal lobe epilepsy. Neurobiol. Dis. 17 (2004) 385-402
83. Yamagata K.I., Andreasson W.E., Kaufmann C.A., and Worley P.F. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11 (1993) 371-386
84. Zhang J., and Rivest S. Distribution, regulation and colocalization of the genes encoding the EP2- and EP4-PGE2 receptors in the rat brain and neuronal responses to systemic inflammation. Eur. J. Neurosci. 11 (1999) 2651-2668
85. Zhang J., and Rivest S. Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J. Neurochem. 76 (2001) 855-864
86. Zhu P., Genc A., Zhang X., Zhang J., Bazan N.G., and Chen C. Heterogeneous expression and regulation of hippocampal prostaglandin E2 receptors. J. Neurosci. Res. 81 (2005) 817-826