Protective effect of 20-HETE inhibition in a model of oxygen-glucose deprivation in hippocampal slice cultures

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 6, 2012, Pages

  Renic, Marija ^a   Kumar, Suresh N ^a   Gebremedhin, Debebe ^a   Florence, Matthew A ^a   Gerges, Nashaat Z ^a   Falck, John R ^b   Harder, David R ^a,d   Roman, Richard J ^c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^d CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

20 hydroxyeicosatetraenoic acid; Brain; Caspase 3; Ischemic injury; Superoxide

Indexed keywords

20 HYDROXYEICOSA 6,15 DIENOIC ACID; 20 HYDROXYICOSATETRAENOIC ACID; CASPASE 3; HYDROXY FATTY ACID; N HYDROXY N' (4 BUTYL 2 METHYLPHENOL)FORMAMIDINE; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG;

ARTICLE; BRAIN BLOOD FLOW; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN SLICE; ENZYME ACTIVATION; HIPPOCAMPUS; MEDICAL PROCEDURES; NERVE CELL NECROSIS; NEUROPROTECTION; OXYGEN GLUCOSE DEPRIVATION; PRIORITY JOURNAL; REOXYGENATION; REPERFUSION INJURY;

AMIDINES; ANIMALS; ANIMALS, NEWBORN; CASPASE 3; CELL DEATH; CELL HYPOXIA; CYTOPROTECTION; GLUCOSE; HIPPOCAMPUS; HYDROXYEICOSATETRAENOIC ACIDS; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDES; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 84863229646     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00340.2011     Document Type: Article

References (45)

1. Arai K, Ikegaya Y, Nakatani Y, Kudo I, Nishiyama N, Matsuki N. Phospholipase A2 mediates ischemic injury in the hippocampus: a regional difference of neuronal vulnerability. Eur J Neurosci 13: 2319-2323, 2001.
2. Baker K, Marcus CB, Huffman K, Kruk H, Malfroy B, Doctrow SR. Synthetic combined superoxide dismutase/catalase mimetics are protective as a delayed treatment in a rat stroke model: a key role for reactive oxygen species in ischemic brain injury. J Pharmacol Exp Ther 284: 215-221, 1998.
3. Bao Y, Wang X, Li W, Huo D, Shen X, Han Y, Tan J, Zeng Q, Sun C. 20-Hydroxyeicosatetraenoic acid induces apoptosis in neonatal rat cardiomyocytes through mitochondrial-dependent pathways. J Cardiovasc Pharmacol 57: 294-301, 2011.
4. Bonde C, Noraberg J, Noer H, Zimmer J. Ionotropic glutamate receptors and glutamate transporters are involved in necrotic neuronal cell death induced by oxygen-glucose deprivation of hippocampal slice cultures. Neuroscience 136: 779-794, 2005.
5. Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21: 2-14, 2001.
6. Cheng J, Ou JS, Singh H, Falck JR, Narsimhaswamy D, Pritchard KA Jr, Schwartzman ML. 20-Hydroxyeicosatetraenoic acid causes endothelial dysfunction via eNOS uncoupling. Am J Physiol Heart Circ Physiol 294: H1018-H1026, 2008.
7. Cho S, Liu D, Fairman D, Li P, Jenkins L, McGonigle P, Wood A. Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures. Neurochem Int 45: 117-127, 2004.
8. 2+ current. J Physiol 507: 771-781, 1998.
9. Gross ER, Nithipatikom K, Hsu AK, Peart JN, Falck JR, Campbell WB, Gross GJ. Cytochrome P450 omega-hydroxylase inhibition reduces infarct size during reperfusion via the sarcolemmal KATP channel. J Mol Cell Cardiol 37: 1245-1249, 2004.
10. Gross GJ, Falck JR, Gross ER, Isbell M, Moore J, Nithipatikom K. Cytochrome P450 and arachidonic acid metabolites: role in myocardial ischemia/reperfusion injury revisited. Cardiovasc Res 68: 18-25, 2005.
11. Guo AM, Arbab AS, Falck JR, Chen P, Edwards PA, Roman RJ, Scicli AG. Activation of vascular endothelial growth factor through reactive oxygen species mediates 20-hydroxyeicosatetraenoic acid-induced endothelial cell proliferation. J Pharmacol Exp Ther 321: 18-27, 2007.
12. Harder DR, Gebremedhin D, Narayanan J, Jefcoat C, Falck JR, Campbell WB, Roman R. Formation and action of a P-450 4A metabolite of arachidonic acid in cat cerebral microvessels. Am J Physiol Heart Circ Physiol 266: H2098-H2107, 1994.
13. Kruman I, Bruce-Keller AJ, Bredesen D, Waeg G, Mattson MP. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 17: 5089-5100, 1997.
14. Laake JH, Haug FM, Wieloch T, Ottersen OP. A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence. Brain Res Brain Res Protoc 4: 173-184, 1999.
15. Lawrence MS, Ho DY, Sun GH, Steinberg GK, Sapolsky RM. Overexpression of Bcl-2 with herpes simplex virus vectors protects CNS neurons against neurological insults in vitro and in vivo. J Neurosci 16: 486-496, 1996.
16. Le DA, Wu Y, Huang Z, Matsushita K, Plesnila N, Augustinack JC, Hyman BT, Yuan J, Kuida K, Flavell RA, Moskowitz MA. Caspase activation and neuroprotection in caspase-3-deficient mice after in vivo cerebral ischemia and in vitro oxygen glucose deprivation. Proc Natl Acad Sci USA 99: 15188-15193, 2002.
17. Liang HL, Hilton G, Mortensen J, Regner K, Johnson CP, Nilakantan V. MnTMPyP, a cell-permeant SOD mimetic, reduces oxidative stress and apoptosis following renal ischemia-reperfusion. Am J Physiol Renal Physiol 296: F266-F276, 2009.
18. Loh KP, Huang SH, De Silva R, Tan BK, Zhu YZ. Oxidative stress: apoptosis in neuronal injury. Curr Alzheimer Res 3: 327-337, 2006.
19. Lv X, Wan J, Yang J, Cheng H, Li Y, Ao Y, Peng R. Cytochrome P450 omega-hydroxylase inhibition reduces cardiomyocyte apoptosis via activation of ERK1/2 signaling in rat myocardial ischemia-reperfusion. Eur J Pharmacol 596: 118-126, 2008.
20. Medhora M, Chen Y, Gruenloh S, Harland D, Bodiga S, Zielonka J, Gebremedhin D, Gao Y, Falck JR, Anjaiah S, Jacobs ER. 20-HETE increases superoxide production and activates NAPDH oxidase in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 294: L902-L911, 2008.
21. Miyata N, Taniguchi K, Seki T, Ishimoto T, Sato-Watanabe M, Yasuda Y, Doi M, Kametani S, Tomishima Y, Ueki T, Sato M, Kameo K. HET0016, a potent and selective inhibitor of 20-HETE synthesizing enzyme. Br J Pharmacol 133: 325-329, 2001.
22. Morita-Fujimura Y, Fujimura M, Yoshimoto T, Chan PH. Superoxide during reperfusion contributes to caspase-8 expression and apoptosis after transient focal stroke. Stroke 32: 2356-2361, 2001.
23. Nilakantan V, Maenpaa C, Jia G, Roman RJ, Park F. 20-HETEmediated cytotoxicity and apoptosis in ischemic kidney epithelial cells. Am J Physiol Renal Physiol 294: F562-F570, 2008.
24. Nithipatikom K, Gross ER, Endsley MP, Moore JM, Isbell MA, Falck JR, Campbell WB, Gross GJ. Inhibition of cytochrome P450 omega-hydroxylase: a novel endogenous cardioprotective pathway. Circ Res 95: e65-e71, 2004.
25. Noraberg J, Poulsen FR, Blaabjerg M, Kristensen BW, Bonde C, Montero M, Meyer M, Gramsbergen JB, Zimmer J. Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 4: 435-452, 2005.
26. Omura T, Tanaka Y, Miyata N, Koizumi C, Sakurai T, Fukasawa M, Hachiuma K, Minagawa T, Susumu T, Yoshida S, Nakaike S, Okuyama S, Harder DR, Roman RJ. Effect of a new inhibitor of the synthesis of 20-HETE on cerebral ischemia reperfusion injury. Stroke 37: 1307-1313, 2006.
27. Pilitsis JG, Coplin WM, O'Regan MH, Wellwood JM, Diaz FG, Fairfax MR, Michael DB, Phillis JW. Free fatty acids in cerebrospinal fluids from patients with traumatic brain injury. Neurosci Lett 349: 136-138, 2003.
28. Poloyac SM, Zhang Y, Bies RR, Kochanek PM, Graham SH. Protective effect of the 20-HETE inhibitor HET0016 on brain damage after temporary focal ischemia. J Cereb Blood Flow Metab 26: 1551-1561, 2006.
29. Ratan RR, Murphy TH, Baraban JM. Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62: 376-379, 1994.
30. Ray AM, Owen DE, Evans ML, Davis JB, Benham CD. Caspase inhibitors are functionally neuroprotective against oxygen glucose deprivation induced CA1 death in rat organotypic hippocampal slices. Brain Res 867: 62-69, 2000.
31. Renic M, Klaus JA, Omura T, Kawashima N, Onishi M, Miyata N, Koehler RC, Harder DR, Roman RJ. Effect of 20-HETE inhibition on infarct volume and cerebral blood flow after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 29: 629-639, 2009.
32. Saluja I, Song D, O'Regan MH, Phillis JW. Role of phospholipase A2 in the release of free fatty acids during ischemia-reperfusion in the rat cerebral cortex. Neurosci Lett 233: 97-100, 1997.
33. Seki T, Wang MH, Miyata N, Laniado-Schwartzman M. Cytochrome P450 4A isoform inhibitory profile of N-hydroxy-N=-(4-butyl-2-methylphenyl)- formamidine (HET0016), a selective inhibitor of 20-HETE synthesis. Biol Pharm Bull 28: 1651-1654, 2005.
34. Sharma SS, Gupta S. Neuroprotective effect of MnTMPyP, a superoxide dismutase/catalase mimetic in global cerebral ischemia is mediated through reduction of oxidative stress and DNA fragmentation. Eur J Pharmacol 561: 72-79, 2007.
35. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. J Neurosci Meth 37: 173-182, 1991.
36. Strasser U, Fischer G. Quantitative measurement of neuronal degeneration in organotypic hippocampal cultures after combined oxygen/glucose deprivation. J Neurosci Meth 57: 177-186, 1995.
37. Sugawara T, Chan PH. Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxid Redox Signal 5: 597-607, 2003.
38. Sugawara T, Noshita N, Lewen A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, Chan PH. Overexpression of copper/ zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22: 209-217, 2002.
39. Tanaka Y, Omura T, Fukasawa M, Horiuchi N, Miyata N, Minagawa T, Yoshida S, Nakaike S. Continuous inhibition of 20-HETE synthesis by TS-011 improves neurological and functional outcomes after transient focal cerebral ischemia in rats. Neurosci Res 59: 475-480, 2007.
40. Won SJ, Kim DY, Gwag BJ. Cellular and molecular pathways of ischemic neuronal death. J Biochem Mol Biol 35: 67-86, 2002.
41. Yang W, Guastella J, Huang JC, Wang Y, Zhang L, Xue D, Tran M, Woodward R, Kasibhatla S, Tseng B, Drewe J, Cai SX. MX1013, a dipeptide caspase inhibitor with potent in vivo antiapoptotic activity. Br J Pharmacol 140: 402-412, 2003.
42. Yu M, Alonso-Galicia M, Sun CW, Roman RJ, Ono N, Hirano H, Ishimoto T, Reddy YK, Katipally KR, Reddy KM, Gopal VR, Yu J, Takhi M, Falck JR. 20-hydroxyeicosatetraenoic acid (20-HETE): structural determinants for renal vasoconstriction. Bioorg Med Chem 11: 2803-2821, 2003.
43. Zhao H, Yenari MA, Cheng D, Sapolsky RM, Steinberg GK. Bcl-2 overexpression protects against neuron loss within the ischemic margin following experimental stroke and inhibits cytochrome c translocation and caspase-3 activity. J Neurochem 85: 1026-1036, 2003.
44. Zhou M, Baudry M. EUK-207, a superoxide dismutase/catalase mimetic, is neuroprotective against oxygen/glucose deprivation-induced neuronal death in cultured hippocampal slices. Brain Res 1247: 28-37, 2009.
45. Zhou M, Dominguez R, Baudry M. Superoxide dismutase/catalase mimetics but not MAP kinase inhibitors are neuroprotective against oxygen/glucose deprivation-induced neuronal death in hippocampus. J Neurochem 103: 2212-2223, 2007.