Activation of cerebral peroxisome proliferator-activated receptors gamma exerts neuroprotection by inhibiting oxidative stress following pilocarpine-induced status epilepticus

Brain Research

Volumn 1200, Issue , 2008, Pages 146-158

  Yu, Xin ^a,b   Shao, Xiao Guang ^b   Sun, Hong ^a   Li, Yong Nan ^a   Yang, Jun ^a   Deng, Yan Chun ^a   Huang, Yuan Gui ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b 401 Hospital of PLA   (China)

Author keywords

Heme oxygenase 1; Neuroprotection; Oxidative stress; PPAR ; Rosiglitazone; Status epilepticus

Indexed keywords

2 CHLORO 5 NITRO N (4 PYRIDYL)BENZAMIDE; GLUTATHIONE; HEME OXYGENASE 1; LIPID; LITHIUM; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PILOCARPINE; REACTIVE OXYGEN METABOLITE; ROSIGLITAZONE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN INJURY; CELL LOSS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DRUG EFFECT; EPILEPTIC STATE; LIPID PEROXIDATION; MALE; NERVE CELL; NERVE INJURY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION;

ANIMALS; BENZAMIDES; CELL DEATH; CONVULSANTS; DISEASE MODELS, ANIMAL; GLUTATHIONE; HEME OXYGENASE (DECYCLIZING); HIPPOCAMPUS; LIPID PEROXIDATION; LITHIUM; MALE; MUSCARINIC AGONISTS; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PILOCARPINE; PPAR GAMMA; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; STATUS EPILEPTICUS; SUPEROXIDE DISMUTASE; THIAZOLIDINEDIONES;

RATTUS;

EID: 40849135452     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.01.047     Document Type: Article

References (63)

1. Ahmad A.S., Zhuang H., and Dore S. Heme oxygenase-1 protects brain from acute excitotoxicity. Neuroscience 141 (2006) 1703-1708
2. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., and Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274 (1999) 26071-26078
3. Alvarez-Maqueda M., El Bekay R., Alba G., Monteseirín J., Chacón P., Vega A., Martín-Nieto J., Bedoya F.J., Pintado E., and Sobrino F. 15-deoxy-delta 12, 14-prostaglandin J2 induces heme oxygenase-1 gene expression in a reactive oxygen species-dependent manner in human lymphocytes. J. Biol. Chem. 279 (2004) 21929-21937
4. Aoun P., Watson D.G., and Simpkins J.W. Neuroprotective effects of PPARgamma agonists against oxidative insults in HT-22 cells. Eur. J. Pharmacol. 472 (2003) 65-71
5. Brunmair B., Staniek K., Gras F., Scharf N., Althaym A., Clara R., Roden M., Gnaiger E., Nohl H., Waldhäusl W., and Fürnsinn C. Thiazolidinediones, like metformin, inhibit respiratory complex I: a common mechanism contributing to theirantidiabetic actions?. Diabetes 53 (2004) 1052-1059
6. Camhi S.L., Alam J., Wiegand G.W., Chin B.Y., and Choi A.M. Transcriptional activation of the HO-1 gene by lipopolysaccharide is mediated by 5′ distal enhancers: role of reactive oxygen intermediates and AP-1. Am. J. Respir. Cell Mol. Biol. 18 (1998) 226-234
7. Chen K., Gunter K., and Maines M.D. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 75 (2000) 304-313
8. Collino M., Aragno M., Mastrocola R., Gallicchio M., Rosa A.C., Dianzani C., Danni O., Thiemermann C., and Fantozzi R. Modulation of the oxidative stress and inflammatory response by PPAR-gamma agonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion. Eur. J. Pharmacol. 530 (2006) 70-80
9. Costa M.S., Rocha J.B., Perosa S.R., Cavalheiro E.A., and Naffah-Mazzacoratti M.G. Pilocarpine-induced status epilepticus increases glutamate release in rat hippocampal synaptosomes. Neurosci. Lett. 356 (2004) 41-44
10. Chung S.Y., and Han S.H. Melatonin attenuates kainic acid-induced hippocampal neurodegeneration and oxidative stress through microglial inhibition. J. Pineal Res. 34 (2003) 95-102
11. Dehmer T., Heneka M.T., Sastre M., Dichgans J., and Schulz J.B. Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with I kappa B alpha induction and block of NF kappa B and iNOS activation. J. Neurochem. 88 (2004) 494-501
12. Dello R.C., Gavrilyuk V., Weinberg G., Almeida A., Bolanos J.P., Palmer J., Pelligrino D., Galea E., and Feinstein D.L. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J. Biol. Chem. 278 (2003) 5828-5836
13. Ding G., Fu M., Qin Q., Lewis W., Kim H.W., Fukai T., Bacanamwo M., Chen Y.E., Schneider M.D., Mangelsdorf D.J., Evans R.M., and Yang Q. Cardiac peroxisome proliferator-activated receptor γ is essential in protecting cardiomyocytes from oxidative damage. Cardiovasc. Res. 76 (2007) 269-279
14. Eder C. Regulation of microglial behavior by ion channel activity. J. Neurosci. Res. 81 (2005) 314-321
15. Frankel D., Mehindate K., and Schipper H.M. Role of heme oxygenase-1 in the regulation of manganese superoxide dismutase gene expression in oxidatively-challenged astrocyte. J. Cell. Physiol. 185 (2000) 80-86
16. Frantseva M.V., Perez Velazquez J.L., Tsoraklidis G., Mendonca A.J., Adamchik Y., Mills L.R., Carlen P.L., and Burnham M.W. Oxidative stress is involved in seizure-induced neurodegeneration in the kindling model of epilepsy. Neuroscience 97 (2000) 431-435
17. Freitas R.M., Vasconcelos S.M., Souza F.C., Viana G.S., and Fonteles M.M. Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J. 272 (2005) 1307-1312
18. Fujikawa D.G. The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res. 725 (1996) 11-22
19. Gao H.M., Hong J.S., Zhang W., and Liu B. Synergistic dopaminergicneurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide:relevance to the etiology of Parkinson's disease. J. Neurosci. 23 (2003) 1228-1236
20. Girnun G.D., Domann F.E., Moore S.A., and Robbins M.E. Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter. Mol. Endocrinol. 16 (2002) 2793-2801
21. Gong P., Stewart D., Hu B., Li N., Cook J., Nel A., and Alam J. Activation of the mouse heme oxygenase-1 gene by 15-deoxy-Delta (12, 14)-prostaglandin J (2) is mediated by the stress response elements and transcription factor Nrf2. Antioxid. Redox Signal. 4 (2002) 249-257
22. Halliwell B., and Gutteridge J.M. Biologically relevant metal ion-dependent hydroxyl radical generation. An update. FEBS Lett. 307 (1992) 108-112
23. Henshall D.C., and Murphy B.M. Modulators of neuronal cell death in epilepsy. Curr. Opin. Pharmacol. 8 (2007) 1-7
24. Huang E., Ong W.Y., Go M.L., and Garey L.J. Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment. J. Neurosci. Res. 80 (2005) 268-278
25. Hwang J., Kleinhenz D.J., Lassegue B., Griendling K.K., Dikalov S., and Hart C.M. Peroxisome proliferator-activated receptor-gamma ligands regulate endothelial membrane superoxide production. Am. J. Physiol., Cell Physiol. 288 (2005) C899-C905
26. Ilhan A., Aladag M.A., Kocer A., Boluk A., Gurel A., and Armutcu F. Erdosteine ameliorates PTZ-induced oxidative stress in mice seizure model. Brain Res. Bull. 65 (2005) 495-499
27. Ilhan A., Gurel A., Armutcu F., Kamisli S., and Iraz M. Antiepileptogenic and antioxidant effects of Nigella sativa oil against pentylenetetrazol-induced kindling in mice. Neuropharmacology 49 (2005) 456-464
28. Ishida H., Takizawa M., Ozawa S., Nakamichi Y., Yamaguchi S., Katsuta H., Tanaka T., Maruyama M., Katahira H., Yoshimoto K., Itagaki E., and Nagamatsu S. Pioglitazone improves insulin secretory capacity and prevents the loss of beta-cell mass in obese diabetic db/db mice: possible protection of beta cells from oxidative stress. Metabolism 53 (2004) 488-494
29. Ito K., Shimada J., Kato D., Toda S., Takagi T., Naito Y., Yoshikawa T., and Kitamura N. Protective effects of preischemic treatment with pioglitazone, a peroxisome proliferator-activated receptor-gamma ligand, on lung ischemia-reperfusion injury in rats. Eur. J. Cardiothorac. Surg. 25 (2004) 530-536
30. Jiang C., Ting A.T., and Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391 (1998) 82-86
31. Jung K.H., Chu K., Lee S.T., Kim J., Sinn D.I., Kim J.M., Park D.K., Lee J.J., Kim S.U., Kim M., Lee S.K., and Roh J.K. Cyclooxygenase-2 inhibitor, celecoxib, inhibits the altered hippocampal neurogenesis with attenuation of spontaneous recurrent seizures following pilocarpine-induced status epilepticus. Neurobiol. Dis. 23 (2006) 237-246
32. Koeppen A., Dickson A., and Smith J. Heme oxygenase in brain hemorrhage: the benefit of tin-mesoporphyrin. J. Neuropathol. Exp. Neurol. 63 (2004) 587-597
33. Kronke G., Kadl A., Ikonomu E., Bluml S., Furnkranz A., Sarembock I.J., Bochkov V.N., Exner M., Binder B.R., and Leitinger N. Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 1276-1282
34. Kudin A.P., Debska-Vielhaber G., and Kunz W.S. Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomed. Pharmacother. 59 (2005) 163-168
35. Kweon M.H., Jung M.J., and Sung H.C. Cytoprotective effects of heme oxygenase-1 induction by 3-O-caffeoyl-1-methylquinic acid. Free Radic. Biol. Med. 36 (2004) 40-52
36. Landreth G.E., and Heneka M.T. Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol. Aging 22 (2001) 937-944
37. Mizuno T., Kuno R., Nitta A., Nabeshima T., Zhang G., Kawanokuchi J., Wang J., Jin S., Takeuchi H., and Suzumura A. Protective effects of nicergoline against neuronal cell death induced by activated microglia and astrocytes. Brain Res. 1066 (2005) 78-85
38. Moreira T.J., Cebere A., Cebers G., Ostenson C.G., Efendic S., and Liljequist S. Reduced HO-1 protein expression is associated with more severe neurodegeneration after transient ischemia induced by cortical compression in diabetic Goto-Kakizaki rats. J. Cereb. Blood Flow Metab. 27 (2007) 1710-1723
39. Oliveira A.A., Almeida J.P., Freitas R.M., Nascimento V.S., Aguiar L.M., Junior H.V., Fonseca F.N., Viana G.S., Sousa F.C., and Fonteles M.M. Effects of levetiracetam in lipid peroxidation level, nitrite-nitrate formation and antioxidant enzymatic activity in mice brain after pilocarpine-induced seizures. Cell. Mol. Neurobiol. 27 (2007) 395-406
40. Park S.W., Yi J.H., Miranpuri G., Satriotomo I., Bowen K., Resnick D.K., and Vemuganti R. Thiazolidinedione class of peroxisome proliferator-activated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J. Pharmacol. Exp. Ther. 320 (2007) 1002-1012
41. Parfenova H., Carratu P., Tcheranova D., Fedinec A., Pourcyrous M., and Leffler C.W. Epileptic seizures cause extended postictal cerebral vascular dysfunction that is prevented by HO-1 overexpression. Am. J. Physiol, Heart Circ. Physiol. 288 (2005) H2843-H2850
42. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1997), Academic Press, Inc., San Diego
43. Pereira M.P., Hurtado O., Cárdenas A., Alonso-Escolano D., Boscá L., Vivancos J., Nombela F., Leza J.C., Lorenzo P., Lizasoain I., and Moro M.A. The nonthiazolidinedione PPARgamma agonist L-796,449 is neuroprotective in experimental stroke. J. Neuropathol. Exp. Neurol. 64 (2005) 797-805
44. Racine R.J. Modification of seizure activity by electrical stimulation: IIR Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
45. Ravindranath V. Animal models and molecular markers for cerebral ischemia-reperfusion injury in brain. Methods Enzymol. 233 (1994) 610-619
46. Ribeiro M.C., de Avila D.S., Schneider C.Y., Hermes F.S., Furian A.F., Oliveira M.S., Rubin M.A., Lehmann M., Krieglstein J., and Mello C.F. alpha-Tocopherol protects against pentylenetetrazol- and methylmalonate-induced convulsions. Epilepsy Res. 66 (2005) 185-194
47. Ricote M., Li A.C., Willson T.M., Kelly C.J., and Glass C.K. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391 (1998) 79-82
48. Rothfuss A., Radermacher P., and Speit G. Involvement of heme oxygenase-1 (HO-1) in the adaptive protection of human lymphocytes after hyperbaric oxygen (HBO) treatment. Carcinogenesis 22 (2001) 1979-1985
49. Scapagnini G., Colombrita C., Amadio M., D'Agata V., Arcelli E., Sapienza M., Quattrone A., and Calabrese V. Curcumin activates defensive genes and protects neurons against oxidative stress. Antioxid. Redox Signal. 8 (2006) 395-403
50. Sener G., Sehirli A.O., Gedik N., and Dulger G.A. Rosiglitazone, a PPAR-gamma ligand, protects against burn-induced oxidative injury of remote organs. Burns 33 (2007) 587-593
51. Shibahara S., Han F., Li B., and Takeda K. Hypoxia and heme oxygenases: oxygen sensing and regulation of expression. Antioxid. Redox Signal. 9 (2007) 2209-2226
52. Shimazu T., Inoue I., Araki N., Asano Y., Sawada M., Furuya D., Nagoya H., and Greenberg J.H. A peroxisome proliferator-activated receptor-gamma agonist reduces infarct size in transient but not in permanent ischemia. Stroke 36 (2005) 353-359
53. Shin E.J., Suh S.K., Lim Y.K., Jhoo W.K., Hjelle O.P., Ottersen O.P., Shin C.Y., Ko K.H., Kim W.K., Kim D.S., Chun W., Ali S., and Kim H.C. Ascorbate attenuates trimethyltin-induced oxidative burden and neuronal degeneration in the rat hippocampus by maintaining glutathione homeostasis. Neuroscience 133 (2005) 715-727
54. Shin H.J., Lee J.Y., Son E., Lee D.H., Kim H.J., Kang S.S., Cho G.J., Choi W.S., and Roh G.S. Curcumin attenuates the kainic acid-induced hippocampal cell death in the mice. Neurosci. Lett. 416 (2007) 49-54
55. Suzuki H., Muramatsu M., Kojima T., and Taki W. Intracranial heme metabolism and cerebral vasospasm after aneurismal subarachnoid hemorrhage. Stroke 34 (2003) 2796-2800
56. Tejada S., Sureda A., Roca C., Gamundi A., and Esteban S. Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine. Brain Res. Bull. 71 (2007) 372-375
57. Vajda F.J. Neuroprotection and neurodegenerative disease. J. Clin. Neurosci. 9 (2002) 4-8
58. Villegas I., Martin A.R., Toma W., and de la Lastra C.A. Rosiglitazone, an agonist of peroxisome proliferator-activated receptor gamma, protects against gastric ischemia-reperfusion damage in rats: role of oxygen free radicals generation. Eur. J. Pharmacol. 505 (2004) 195-203
59. Wang J., and Dore S. Heme oxygenase-1 exacerbates early brain injury after intracerebral haemorrhage. Brain 130 (2007) 1643-1652
60. Wayman N.S., Hattori Y., McDonald M.C., Mota-Filipe H., Cuzzocrea S., Pisano B., Chatterjee P.K., and Thiemermann C. Ligands of the peroxisome proliferator-activated receptors (PPAR-gamma and PPAR-alpha) reduce myocardial infarct size. FASEB J. 16 (2002) 1027-1040
61. Wijayanti N., Huber S., Samoylenko A., Kietzmann T., and Immenschuh S. Role of NF-kappaB and p38 MAP kinase signaling pathways in the lipopolysaccharide-dependent activation of heme oxygenase-1 gene expression. Antioxid. Redox Signal. 6 (2004) 802-810
62. Yi J.H., and Hazell A.S. N-acetylcysteine attenuates early induction of heme oxygenase-1 following traumatic brain injury. Brain Res. 1033 (2005) 13-19
63. Zhao Y., Patzer A., Herdegen T., Gohlke P., and Culman J. Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J. 20 (2006) 1162-1175