Treatment with the cytochrome P450 ω-hydroxylase inhibitor HET0016 attenuates cerebrovascular inflammation, oxidative stress and improves vasomotor function in spontaneously hypertensive rats

British Journal of Pharmacology

Volumn 168, Issue 8, 2013, Pages 1878-1888

  Toth, Peter ^a,b   Csiszar, Anna ^a,b   Sosnowska, Danuta ^a   Tucsek, Zsuzsanna ^a   Cseplo, Peter ^b   Springo, Zsolt ^b   Tarantini, Stefano ^a   Sonntag, William E ^a   Ungvari, Zoltan ^a,b   Koller, Akos ^b,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

^c NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

20 HETE; cerebral blood flow; cytokines; ischaemic stroke; NF B; ROS; vascular cognitive impairment

Indexed keywords

20 HYDROXYICOSATETRAENOIC ACID; 4 HYDROXYNONENAL; CYTOCHROME P450 INHIBITOR; HET 0016; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; N HYDROXY N' (4 BUTYL 2 METHYLPHENYL) FORMAMIDINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 20-HYDROXY-5,8,11,14-EICOSATETRAENOIC ACID; AMIDINE; CYTOCHROME P-450 OMEGA-HYDROXYLASE; CYTOCHROME P450; CYTOKINE; HYDROXYICOSATETRAENOIC ACID; N-HYDROXY-N'-(4-BUTYL-2-METHYLPHENYL)FORMAMIDINE; REACTIVE OXYGEN METABOLITE;

AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; BRAIN ARTERY; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; HYPERTENSION; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; SYSTOLIC BLOOD PRESSURE; TREATMENT RESPONSE; VASOMOTOR REFLEX; ADRENERGIC SYSTEM; ANIMAL; BLOOD PRESSURE; CELL CULTURE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE CEREBRAL ARTERY; PHYSIOLOGY; WISTAR KYOTO RAT;

AMIDINES; ANIMALS; BLOOD PRESSURE; CELLS, CULTURED; CEREBROVASCULAR DISORDERS; CYTOCHROME P-450 ENZYME SYSTEM; CYTOKINES; HYDROXYEICOSATETRAENOIC ACIDS; MALE; MIDDLE CEREBRAL ARTERY; NF-KAPPA B; OXIDATIVE STRESS; RATS; RATS, INBRED SHR; RATS, INBRED WKY; REACTIVE OXYGEN SPECIES; VASOMOTOR SYSTEM;

EID: 84875473946     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12079     Document Type: Article

References (55)

1. Aiyagari V, Gorelick PB, (2009). Management of blood pressure for acute and recurrent stroke. Stroke 40: 2251-2256.
2. Alonso-Galicia M, Maier KG, Greene AS, Cowley AW, Jr, Roman RJ, (2002). Role of 20-hydroxyeicosatetraenoic acid in the renal and vasoconstrictor actions of angiotensin II. Am J Physiol Regul Integr Comp Physiol 283: R60-R68.
3. Amenta F, Di Tullio MA, Tomassoni D, (2003). Arterial hypertension and brain damage-evidence from animal models (review). Clin Exp Hypertens 25: 359-380.
4. Ando H, Zhou J, Macova M, Imboden H, Saavedra JM, (2004). Angiotensin II AT1 receptor blockade reverses pathological hypertrophy and inflammation in brain microvessels of spontaneously hypertensive rats. Stroke 35: 1726-1731.
5. Bagi Z, Feher A, Cassuto J, Akula K, Labinskyy N, Kaley G, et al. (2011). Increased availability of angiotensin AT 1 receptors leads to sustained arterial constriction to angiotensin II in diabetes-role for Rho-kinase activation. Br J Pharmacol 163: 1059-1068.
6. Bailey-Downs LC, Mitschelen M, Sosnowska D, Toth P, Pinto JT, Ballabh P, et al. (2012). Liver-specific knockdown of IGF-1 decreases vascular oxidative stress resistance by impairing the Nrf2-dependent antioxidant response: a novel model of vascular aging. J Gerontol A Biol Sci Med Sci 67: 313-329.
7. Barry DI, (1985). Cerebral blood flow in hypertension. J Cardiovasc Pharmacol 7 (Suppl. 2): S94-S98.
8. Beason-Held LL, Moghekar A, Zonderman AB, Kraut MA, Resnick SM, (2007). Longitudinal changes in cerebral blood flow in the older hypertensive brain. Stroke 38: 1766-1773.
9. Cheng J, Ou JS, Singh H, Falck JR, Narsimhaswamy D, Pritchard KA, Jr, et al. (2008). 20-hydroxyeicosatetraenoic acid causes endothelial dysfunction via eNOS uncoupling. Am J Physiol Heart Circ Physiol 294: H1018-H1026.
10. Cheng J, Wu CC, Gotlinger KH, Zhang F, Falck JR, Narsimhaswamy D, et al. (2010). 20-hydroxy-5,8,11,14-eicosatetraenoic acid mediates endothelial dysfunction via IkappaB kinase-dependent endothelial nitric-oxide synthase uncoupling. J Pharmacol Exp Ther 332: 57-65.
11. Cheng J, Garcia V, Ding Y, Wu CC, Thakar K, Falck JR, et al. (2012). Induction of angiotensin-converting enzyme and activation of the renin-angiotensin system contribute to 20-hydroxyeicosatetraenoic acid-mediated endothelial dysfunction. Arterioscler Thromb Vasc Biol 32: 1917-1924.
12. Craig J, Martin W, (2012). Dominance of flow-mediated constriction over flow-mediated dilatation in the rat carotid artery. Br J Pharmacol 167: 527-536.
13. Csiszar A, Ungvari Z, Koller A, Edwards JG, Kaley G, (2004). Proinflammatory phenotype of coronary arteries promotes endothelial apoptosis in aging. Physiol Genomics 17: 21-30.
14. Csiszar A, Smith KE, Koller A, Kaley G, Edwards JG, Ungvari Z, (2005). Regulation of bone morphogenetic protein-2 expression in endothelial cells: role of nuclear factor-kappaB activation by tumor necrosis factor-alpha, H2O2, and high intravascular pressure. Circulation 111: 2364-2372.
15. Csiszar A, Ahmad M, Smith KE, Labinskyy N, Gao Q, Kaley G, et al. (2006a). Bone morphogenetic protein-2 induces proinflammatory endothelial phenotype. Am J Pathol 168: 629-638.
16. Csiszar A, Smith K, Labinskyy N, Orosz Z, Rivera A, Ungvari Z, (2006b). Resveratrol attenuates TNF-{alpha}-induced activation of coronary arterial endothelial cells: role of NF-{kappa}B inhibition. Am J Physiol 291: H1694-H1699.
17. Csiszar A, Labinskyy N, Zhao X, Hu F, Serpillon S, Huang Z, et al. (2007). Vascular superoxide and hydrogen peroxide production and oxidative stress resistance in two closely related rodent species with disparate longevity. Aging Cell 6: 783-797.
18. Di Napoli M, Papa F, (2003). Association between blood pressure and C-reactive protein levels in acute ischemic stroke. Hypertension 42: 1117-1123.
19. Dunn KM, Renic M, Flasch AK, Harder DR, Falck J, Roman RJ, (2008). Elevated production of 20-HETE in the cerebral vasculature contributes to severity of ischemic stroke and oxidative stress in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 295: H2455-H2465.
20. Gebremedhin D, Lange AR, Lowry TF, Taheri MR, Birks EK, Hudetz AG, et al. (2000). Production of 20-HETE and its role in autoregulation of cerebral blood flow. Circ Res 87: 60-65.
21. Gelosa P, Ballerio R, Banfi C, Nobili E, Gianella A, Pignieri A, et al. (2010). Terutroban, a thromboxane/prostaglandin endoperoxide receptor antagonist, increases survival in stroke-prone rats by preventing systemic inflammation and endothelial dysfunction: comparison with aspirin and rosuvastatin. J Pharmacol Exp Ther 334: 199-205.
22. Gelosa P, Sevin G, Pignieri A, Budelli S, Castiglioni L, Blanc-Guillemaud V, et al. (2011). Terutroban, a thromboxane/prostaglandin endoperoxide receptor antagonist, prevents hypertensive vascular hypertrophy and fibrosis. Am J Physiol Heart Circ Physiol 300: H762-H768.
23. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. (2011). Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42: 2672-2713.
24. Heistad DD, Mayhan WG, Coyle P, Baumbach GL, (1990). Impaired dilatation of cerebral arterioles in chronic hypertension. Blood Vessels 27: 258-262.
25. Huang A, Koller A, (1996). Both nitric oxide and prostaglandin-mediated responses are impaired in skeletal muscle arterioles of hypertensive rats. J Hypertens 14: 887-895.
26. Huang A, Sun D, Kaley G, Koller A, (1998). Superoxide released to high intra-arteriolar pressure reduces nitric oxide-mediated shear stress- and agonist-induced dilations. Circ Res 83: 960-965.
27. Iadecola C, Davisson RL, (2008). Hypertension and cerebrovascular dysfunction. Cell Metab 7: 476-484.
28. Inoue K, Sodhi K, Puri N, Gotlinger KH, Cao J, Rezzani R, et al. (2009). Endothelial-specific CYP4A2 overexpression leads to renal injury and hypertension via increased production of 20-HETE. Am J Physiol Renal Physiol 297: F875-F884.
29. Ishizuka T, Cheng J, Singh H, Vitto MD, Manthati VL, Falck JR, et al. (2008). 20-Hydroxyeicosatetraenoic acid stimulates nuclear factor-kappaB activation and the production of inflammatory cytokines in human endothelial cells. J Pharmacol Exp Ther 324: 103-110.
30. Jacobs ER, Bodiga S, Ali I, Falck AM, Falck JR, Medhora M, et al. (2012). Tissue protection and endothelial cell signaling by 20-HETE analogs in intact ex vivo lung slices. Exp Cell Res 318: 2143-2152.
31. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
32. Koller A, Toth P, (2012). Contribution of flow-dependent vasomotor mechanisms to the autoregulation of cerebral blood flow. J Vasc Res 49: 375-389.
33. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. Medhora M, Chen Y, Gruenloh S, Harland D, Bodiga S, Zielonka J, et al. (2008). 20-HETE increases superoxide production and activates NAPDH oxidase in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 294: L902-L911.
35. Mies G, Hermann D, Ganten U, Hossmann KA, (1999). Hemodynamics and metabolism in stroke-prone spontaneously hypertensive rats before manifestation of brain infarcts. J Cereb Blood Flow Metab 19: 1238-1246.
36. Miyata N, Taniguchi K, Seki T, Ishimoto T, Sato-Watanabe M, Yasuda Y, et al. (2001). HET0016, a potent and selective inhibitor of 20-HETE synthesizing enzyme. Br J Pharmacol 133: 325-329.
37. O'Sullivan M, Lythgoe DJ, Pereira AC, Summers PE, Jarosz JM, Williams SC, et al. (2002). Patterns of cerebral blood flow reduction in patients with ischemic leukoaraiosis. Neurology 59: 321-326.
38. Poloyac SM, Zhang Y, Bies RR, Kochanek PM, Graham SH, (2006). Protective effect of the 20-HETE inhibitor HET0016 on brain damage after temporary focal ischemia. J Cereb Blood Flow Metab 26: 1551-1561.
39. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, et al. (1996). Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 97: 1916-1923.
40. Renic M, Klaus JA, Omura T, Kawashima N, Onishi M, Miyata N, et al. (2009). 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.
41. Riou S, Mees B, Esposito B, Merval R, Vilar J, Stengel D, et al. (2007). High pressure promotes monocyte adhesion to the vascular wall. Circ Res 100: 1226-1233.
42. Sacerdoti D, Escalante B, Abraham NG, McGiff JC, Levere RD, Schwartzman ML, (1989). Treatment with tin prevents the development of hypertension in spontaneously hypertensive rats. Science 243: 388-390.
43. Singh H, Cheng J, Deng H, Kemp R, Ishizuka T, Nasjletti A, et al. (2007). Vascular cytochrome P450 4A expression and 20-hydroxyeicosatetraenoic acid synthesis contribute to endothelial dysfunction in androgen-induced hypertension. Hypertension 50: 123-129.
44. Sodhi K, Wu CC, Cheng J, Gotlinger K, Inoue K, Goli M, et al. (2010). CYP4A2-induced hypertension is 20-hydroxyeicosatetraenoic acid- and angiotensin II-dependent. Hypertension 56: 871-878.
45. Toth P, Rozsa B, Springo Z, Doczi T, Koller A, (2011). Isolated human and rat cerebral arteries constrict to increases in flow: role of 20-HETE and TP receptors. J Cereb Blood Flow Metab 31: 2096-2105.
46. Ungvari Z, Pacher P, Kecskemeti V, Koller A, (1999). Fluoxetine dilates isolated small cerebral arteries of rats and attenuates constrictions to serotonin, norepinephrine, and a voltage- dependent Ca(2+) channel opener. Stroke 30: 1949-1954.
47. Ungvari Z, Csiszar A, Huang A, Kaminski PM, Wolin MS, Koller A, (2003). High pressure induces superoxide production in isolated arteries via protein kinase C-dependent activation of NAD(P)H oxidase. Circulation 108: 1253-1258.
48. Ungvari Z, Csiszar A, Kaminski PM, Wolin MS, Koller A, (2004). Chronic high pressure-induced arterial oxidative stress: involvement of protein kinase C-dependent NAD(P)H oxidase and local renin-angiotensin system. Am J Pathol 165: 219-226.
49. Wang JS, Singh H, Zhang F, Ishizuka T, Deng H, Kemp R, et al. (2006). Endothelial dysfunction and hypertension in rats transduced with CYP4A2 adenovirus. Circ Res 98: 962-969.
50. Wang MH, Zhang F, Marji J, Zand BA, Nasjletti A, Laniado-Schwartzman M, (2001). CYP4A1 antisense oligonucleotide reduces mesenteric vascular reactivity and blood pressure in SHR. Am J Physiol Regul Integr Comp Physiol 280: R255-R261.
51. Williams JM, Sarkis A, Lopez B, Ryan RP, Flasch AK, Roman RJ, (2007). Elevations in renal interstitial hydrostatic pressure and 20- hydroxyeicosatetraenoic acid contribute to pressure natriuresis. Hypertension 49: 687-694.
52. Wu CC, Cheng J, Zhang FF, Gotlinger KH, Kelkar M, Zhang Y, et al. (2011). Androgen-dependent hypertension is mediated by 20-hydroxy-5,8,11,14- eicosatetraenoic acid-induced vascular dysfunction: role of inhibitor of kappaB kinase. Hypertension 57: 788-794.
53. Zeng Q, Han Y, Bao Y, Li W, Li X, Shen X, et al. (2010). 20-HETE increases NADPH oxidase-derived ROS production and stimulates the L-type Ca2+ channel via a PKC-dependent mechanism in cardiomyocytes. Am J Physiol Heart Circ Physiol 299: H1109-H1117.
54. Zhou J, Ando H, Macova M, Dou J, Saavedra JM, (2005). Angiotensin II AT1 receptor blockade abolishes brain microvascular inflammation and heat shock protein responses in hypertensive rats. J Cereb Blood Flow Metab 25: 878-886.
55. Zou AP, Imig JD, Ortiz de Montellano PR, Sui Z, Falck JR, Roman RJ, (1994). Effect of P-450 omega-hydroxylase metabolites of arachidonic acid on tubuloglomerular feedback. Am J Physiol 266 (6 Pt 2): F934-F941.