Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats

FASEB Journal

Volumn 20, Issue 8, 2006, Pages 1162-1175

  Zhao, Yi ^a   Patzer, Andreas ^a   Herdegen, Thomas ^a   Gohlke, Peter ^a   Culman, Juraj ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Cerebral ischemia; Cyclooxygenase 1; Cyclooxygenase 2; Pioglitazone; PPAR ; Rat

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; TUMOR NECROSIS FACTOR ALPHA; 2,4 THIAZOLIDINEDIONE DERIVATIVE; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ATTENUATION; BRAIN CELL; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DISEASE EXACERBATION; DRUG EFFECT; DRUG MECHANISM; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME REGULATION; HORMONAL REGULATION; IMMUNOCHEMISTRY; IMMUNOFLUORESCENCE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; UPREGULATION; WESTERN BLOTTING; ANIMAL; BRAIN CIRCULATION; BRAIN CORTEX; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG POTENTIATION; ENZYMOLOGY; METABOLISM; NERVE CELL; WISTAR RAT;

ANIMALS; BRAIN ISCHEMIA; CELL SURVIVAL; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; MALE; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PPAR GAMMA; RATS; RATS, WISTAR; THIAZOLIDINEDIONES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33745983234     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-5007com     Document Type: Article

References (60)

1. Dirnagl, U., Iadecola, C., and Moskowitz, M. A. (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397
2. Lee, J. M., Grabb, M. C., Zipfel, G. J., and Choi, D. W. (2000) Brain tissue responses to ischemia. J. Clin. Invest. 106, 723-731
3. Iadecola, C., and Alexander, M. (2001) Cerebral ischemia and inflammation. Curr. Opin. Neurol. 14, 89-94
4. Chandrasekharan, N. V., Dai, H., Roos, K. L., Evanson, N. K., Tomsik, J., Elton, T. S., and Simmons, D. L. (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc. Natl. Acad. Sci. U. S. A. 99, 13926-13931
5. Phillis, J. W., and O'Regan, M. H. (2003) The role of phospholipases, cyclooxygenases, and lipoxygenases in cerebral ischemic/traumatic injuries. Crypt. Rev. Neurobiol. 15, 61-90
6. Graham, S. H., and Hickey, R. W. (2003) Cyclooxygenases in central nervous system diseases: a special role for cyclooxygenase 2 in neuronal cell death. Arch. Neurol. 60, 628-630
7. Miettinen, S., Fusco, F. R., Yrjanheikki, J., Keinanen, R., Hirvonen, T., Roivainen, R., Narhi, M., Hokfelt, T., and Koistinaho, J. (1997) Spreading depression and focal brain ischemia induce cyclooxygenase-2 in cortical neurons through N-methyl-D-aspartic acid-receptors and phospholipase A2. Proc. Natl. Acad. Sci. U. S. A. 94, 6500-6505
8. Pepicelli, O., Fedele, E., Bonanno, G., Raiteri, M., Ajmone-Cat, M. A., Greco, A., Levi, G., and Minghetti, L. (2002) 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, 1028-1034
9. Nogawa, S., Zhang, F., Ross, M. E., and Iadecola, C. (1997) Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci. 17, 2746-2755
10. Candelario-Jalil, E., Mhadu, N. H., Gonzalez-Falcon, A., Garcia-Cabrera, M., Munoz, E., Leon, O. S., and Fiebich, B. L. (2005) Effects of the cyclooxygenase-2 inhibitor nimesulide on cerebral infarction and neurological deficits induced by permanent middle cerebral artery occlusion in the rat. J. Neuroinflammation 2, 3
11. Iadecola, C., Niwa, K., Nogawa, S., Zhao, X., Nagayama, M., Araki, E., Morham, S., and Ross, M. E. (2001) Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2- deficient mice. Proc. Natl. Acad. Sci. U. S. A. 98, 1294-1299
12. Sasaki, T., Kitagawa, K., Yamagata, K., Takemiya, T., Tanaka, S., Omura-Matsuoka, E., Sugiura, S., Matsumoto, M., and Hori, M. (2004) Amelioration of hippocampal neuronal damage after transient forebrain ischemia in cyclooxygenase-2-deficient mice. J. Cereb. Blood Flow Metab. 24, 107-113
13. Schwab, J. M., and Schluesener, H. J. (2003) Cyclooxygenases and central nervous system inflammation: conceptual neglect of cyclooxygenase 1. Arch Neurol. 60, 630-632
14. Ricote, M., Li, A. C., Willson, T. M., Kelly, C. J., and Glass, C. K. (1998) The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391, 79-82
15. Jiang, C., Ting, A. T., and Seed, B. (1998) PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391, 82-86
16. Kim, E. J., Kwon, K. J., Park, J. Y., Lee, S. H., Moon, C. H., and Baik, E. J. (2002) Effects of peroxisome proliferator-activated receptor agonists on LPS-induced neuronal death in mixed cortical neurons: associated with iNOS and COX-2. Brain Res. 941, 1-10
17. Heneka, M. T., Feinstein, D. L., Galea, E., Gleichmann, M., Wullner, U., and Klockgether, T. (1999) Peroxisome proliferator-activated receptor gamma agonists protect cerebellar granule cells from cytokine-induced apoptotic cell death by inhibition of inducible nitric oxide synthase. J. Neuroimmunol. 100, 156-168
18. Heneka, M. T., Klockgether, T., and Feinstein, D. L. (2000) Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J. Neurosci. 20, 6862-6867
19. Shiraz, T., Inoue, I., Araki, N., Asano, Y., Sawada, M., Fuquay, D., Nagoya, H., and Greenberg, J. H. (2005) A peroxisome proliferator-activated receptor-gamma agonist reduces infarct size in transient but not in permanent ischemia. Stroke 36, 353-359
20. Sundararajan, S., Gamboa, J. L., Victor, N. A., Wanderi, E. W., Lust, W. D., and Landreth, G. E. (2005) Peroxisome proliferator-activated receptor-gamma ligands reduce inflammation and infarction size in transient focal ischemia. Neuroscience 130, 685-696
21. Zhao, Y., Patzer, A., Gohlke, P., Herdegen, T., and Culman, J. (2005) The intracerebral application of the PPARgamma-ligand pioglitazone confers neuroprotection against focal ischaemia in the rat brain. Eur. J. Neurosci. 22, 278-282
22. Dai, W. J., Funk, A., Herdegen, T., Unger, T., and Culman, J. (1999) Blockade of central angiotensin AT(1) receptors improves neurological outcome and reduces expression of AP-1 transcription factors after focal brain ischemia in rats. Stroke 30, 2391-2398; discussion 2398-2399
23. Schmid-Elsaesser, R., Zausinger, S., Hungerhuber, E., Baethmann, A., and Reulen, H. J. (1998) A critical reevaluation of the intraluminal thread model of focal cerebral ischemia: evidence of inadvertent premature reperfusion and subarachnoid hemorrhage in rats by laser-Doppler flowmetry. Stroke 29, 2162-2170
24. Lou, M., Blume, A., Zhao, Y., Gohlke, P., Deuschl, G., Herdegen, T., and Culman, J. (2004) Sustained blockade of brain AT1 receptors before and after focal cerebral ischemia alleviates neurologic deficits and reduces neuronal injury, apoptosis, and inflammatory responses in the rat. J. Cereb. Blood Flow Metab. 24, 536-547
25. Xu, J., Culman, J., Blume, A., Brecht, S., and Gohlke, P. (2003) Chronic treatment with a low dose of lithium protects the brain against ischemic injury by reducing apoptotic death. Stroke 34, 1287-1292
26. Brewer, G. J. (1995) Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42, 674-683
27. Cullingford, T. E., Bhakoo, K., Peuchen, S., Dolphin, C. T., Patel, R., and Clark, J. B. (1998) Distribution of mRNAs encoding the peroxisome proliferator-activated receptor alpha, beta, and gamma and the retinoid X receptor alpha, beta, and gamma in rat central nervous system. J. Neurochem. 70, 1366-1375
28. Bernardo, A., Levi, G., and Minghetti, L. (2000) Role of the peroxisome proliferator-activated receptor-gamma (PPARgamma) and its natural ligand 15-deoxy-Delta12, 14-prostaglandin J2 in the regulation of microglial functions. Eur. J. Neurosci. 12, 2215-2223
29. Cristiano, L., Bernardo, A., and Ceru, M. P. (2001) Peroxisome proliferator-activated receptors (PPARs) and peroxisomes in rat cortical and cerebellar astrocytes. J. Neurocytol. 30, 671-683
30. Moreno, S., Farioli-Vecchioli, S., and Ceru, M. P. (2004) Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 123, 131-145
31. Cimini, A., Benedetti, E., Cristiano, L., Sebastiani, P., D'Amico, M. A., D'Angelo, B., and Di Loreto, S. (2005) Expression of peroxisome proliferator-activated receptors (PPARs) and retinoic acid receptors (RXRs) in rat cortical neurons. Neuroscience 130, 325-337
32. Sundararajan, S., and Landreth, G. E. (2004) Antiinflammatory properties of PPARgamma agonists following ischemia. Drug News Perspect. 17, 229-236
33. Desvergne, B., and Wahli, W. (1999) Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20, 649-688
34. Yamagata, K., Andreasson, K. I., Kaufmann, W. E., Barnes, C. A., and Worley, P. F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11, 371-386
35. Collaco-Moraes, Y., Aspey, B., Harrison, M., and de Belleroche, J. (1996) Cyclo-oxygenase-2 messenger RNA induction in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 16, 1366-1372
36. Yokota, C., Kaji, T., Kuge, Y., Inoue, H., Tamaki, N., and Minematsu, K. (2004) Temporal and topographic profiles of cyclooxygenase-2 expression during 24 h of focal brain ischemia in rats. Neurosci. Lett. 357, 219-222
37. Iadecola, C., Forster, C., Nogawa, S., Clark, H. B., and Ross, M. E. (1999) Cyclooxygenase-2 immunoreactivity in the human brain following cerebral ischemia. Acta Neuropathol. (Berlin) 98, 9-14
38. Tomimoto, H., Shibata, M., Ihara, M., Akiguchi, I., Ohtani, R., and Budka, H. (2002) A comparative study on the expression of cyclooxygenase and 5-lipoxygenase during cerebral ischemia in humans. Acta Neuropathol. (Berlin) 104, 601-607
39. Dobrian, A. D., Schriver, S. D., Khraibi, A. A., and Prewitt, R. L. (2004) Pioglitazone prevents hypertension and reduces oxidative stress in diet-induced obesity. Hypertension 43, 48-56
40. Hewett, S. J., Uliasz, T. F., Vidwans, A. S., and Hewett, J. A. (2000) Cyclooxygenase-2 contributes to N-methyl-D-aspartate-mediated neuronal cell death in primary cortical cell culture. J. Pharmacol. Exp. Ther. 293, 417-425
41. Araki, E., Forster, C., Dubinsky, J. M., Ross, M. E., and Iadecola, C. (2001) Cyclooxygenase-2 inhibitor ns-398 protects neuronal cultures from lipopolysaccharide-induced neurotoxicity. Stroke 32, 2370-2375
42. Nakayama, M., Uchimura, K., Zhu, R. L., Nagayama, T., Rose, M. E., Stetler, R. A., Isakson, P. C., Chen, J., and Graham, S. H. (1998) Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc. Natl. Acad. Sci. U. S. A. 95, 10954-10959
43. Koistinaho, J., Koponen, S., and Chan, P. H. (1999) Expression of cyclooxygenase-2 mRNA after global ischemia is regulated by AMPA receptors and glucocorticoids. Stroke 30, 1900-1905; discussion 1905-1906
44. Chawla, A., Barak, Y., Nagy, L., Liao, D., Tontonoz, P., and Evans, R. M. (2001) PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7, 48-52
45. Smith, S. A., Monteith, G. R., Holman, N. A., Robinson, J. A., May, F. J., and Roberts-Thomson, S. J. (2003) Effects of peroxisome proliferator- activated receptor gamma ligands ciglitazone and 15-deoxy-delta 12,14-prostaglandin J2 on rat cultured cerebellar granule neuronal viability. J. Neurosci. Res. 72, 747-755
46. Drew, P. D., Storer, P. D., Xu, J., and Chavis, J. A. (2005) Hormone regulation of microglial cell activation: relevance to multiple sclerosis. Brain Res. Rev. 48, 322-327
47. Kielian, T., and Drew, P. D. (2003) Effects of peroxisome proliferator-activated receptor-gamma agonists on central nervous system inflammation. J. Neurosci. Res. 71, 315-325
48. Luna-Medina, R., Cortes-Canteli, M., Alonso, M., Santos, A., Martinez, A., and Perez-Castillo, A. (2005) Regulation of inflammatory response in neural cells in vitro by thiadiazolidinones derivatives through peroxisome proliferator-activated receptor gamma activation. J. Biol. Chem. 280, 21453-21462
49. Zhao, Y., Foryst-Ludwig, A., Bruemmer, D., Culman, J., Bader, M., Unger, T., and Kintscher, U. (2005) Angiotensin II induces peroxisome proliferator-activated receptor gamma in PC12W cells via angiotensin type 2 receptor activation. J. Neurochem. 94, 1395-1401
50. Niwa, K., Haensel, C., Ross, M. E., and Iadecola, C. (2001) Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ. Res. 88, 600-608
51. Iadecola, C., Sugimoto, K., Niwa, K., Kazama, K., and Ross, M. E. (2001) Increased susceptibility to ischemic brain injury in cyclooxigenase-1-deficient mice. J. Cereb. Blood Flow Metab. 21, 1436-1441
52. Lin, H., Lin, T. N., Cheung, W. M., Nian, G. M., Tseng, P. H., Chen, S. F., Chen, J. J., Shyue, S. K., Liou, J. Y., Wu, C. W., and Wu, K. K. (2002) Cyclooxygenase-1 and bicistronic cyclooxygenase-1/prostacyclin synthase gene transfer protect against ischemic cerebral infarction. Circulation 105, 1962-1969
53. Candelario-Jalil, E., Gonzalez-Falcon, A., Garcia-Cabrera, M., Alvarez, D., Al-Dalain, S., Martinez, G., Leon, O. S., and Springer, J. E. (2003) 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, 545-555
54. Koizumi, J., Yoshida, Y., Nakazawa, T., and Ooneda, G. (1986) Experimental studies of ischemic brain edema, I: a new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jon. J. Stroke 8, 1-8
55. Hosomi, N., Ban, C.R., Nay, T., Takahashi, T., GAO, P., Song, X-y. R, and Kohno, M. (2005) Tumor necrosis factor-α neutralization reduced cerebral edema through inhibition of matrix metalloproteinase production after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 25, 959-967
56. Subbaramaiah K., Lin, D. T., Hart, J. C., and Dannenberg, A. J. (2001) Peroxisome proliferator-activated receptor γ ligands suppress the transcriptional activation of cyclooxygenase-2. J. Biol. Chem. 276, 1440-12448
57. Han, S., Inoue, H., Flowers, L. C., and Sidell, N. (2003) Control of COX-2 gene expression through peroxisome proliferator-activated receptor γ in human cervical cancer cells. Clin. Cancer Res. 9, 4627-4635
58. 2 synthase, and inducible nitric oxide synthase in cardiac myocytes. Hypertension 42, 844-850
59. Vasudevan, A. R., and Balasubramanyam, A. (2004) Thiazolidinediones: a review of their mechanisms of insulin sensitisation, therapeutic potential, clinical efficacy, and tolerability. Diabetes Technol. Therap. 6, 850-863
60. Dormandy, J. A, Charbonnel, B., Eckland, D. J. A., Erdmann, E, Massi-Benedetti, M., Moules, I. K., Skene, A. M., Tan, M. H., Lefebvre, P. J., Murray, G. D., et al. (2005) Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial in macroVascular Events): a randomised controlled trial. Lancet 366, 1279-1289