Involvement of cytochrome P-450 1B1 in renal dysfunction, injury, and inflammation associated with angiotensin II-induced hypertension in rats

American Journal of Physiology - Renal Physiology

Volumn 302, Issue 4, 2012, Pages

  Jennings, Brett L ^a   Anderson, Larry J ^a   Estes, Anne M ^a   Fang, Xiao R ^a   Song, Chi Young ^a   Campbell, William B ^b   Malik, Kafait U ^a  

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

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

2,4,3',5' tetramethoxystilbene

Indexed keywords

2,4,3',5' TETRAMETHOXYSTILBENE; ALPHA SMOOTH MUSCLE ACTIN; ANGIOTENSIN II; COLLAGEN; CYTOCHROME P450 1B1; CYTOCHROME P450 INHIBITOR; FIBRONECTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; POTASSIUM ION; PROTEIN KINASE P60; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM ION; UNCLASSIFIED DRUG; VASOCONSTRICTOR AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL REACTIVITY; CD3+ T LYMPHOCYTE; CELL SELECTION; CONTROLLED STUDY; DRUG INFUSION; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVITY; FLUID INTAKE; GLOMERULUS FILTRATION RATE; HYPERTENSION; INJECTION; KIDNEY; KIDNEY ARTERY; KIDNEY DYSFUNCTION; KIDNEY FIBROSIS; KIDNEY HYPERTROPHY; KIDNEY INJURY; KIDNEY VASCULAR RESISTANCE; MALE; NEPHRITIS; NONHUMAN; OXIDATIVE STRESS; POTASSIUM EXCRETION; POTASSIUM URINE LEVEL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; RAT; SODIUM EXCRETION; SODIUM URINE LEVEL; URINE VOLUME;

EID: 84856690531     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00542.2011     Document Type: Article

References (58)

1. Agarwal R. Proinflammatory effects of oxidative stress in chronic kidney disease: role of additional angiotensin II blockade. Am J Physiol Renal Physiol 284: F863-F869, 2003.
2. Alonso-Galicia M, Maier KG, Greene AS, Cowley AW Jr, Roman RJ. Role of 20-hydroxyeicosatetraenoic acid in the renal and vasoconstrictor actions of angiotensin II. Am J Physiol Regul Integr Comp Physiol 283: R60-R68, 2002.
3. Bao W, Behm DJ, Nerurkar SS, Ao Z, Bentley R, Mirabile RC, Johns DG, Woods TN, Doe CPA, Coatney RW, Ohlstein JF, Douglas SA, Willette RN, Yue TL. Effects of p38 MAPK inhibitor on angiotensin II-dependent hypertension, organ damage, and superoxide anion production. J Cardiovasc Pharmacol 49: 362-368, 2007.
4. Chen CCA, Pedraza PL, Hao S, Stier CT, Ferreri NR. TNFR1-deficient mice display altered blood pressure and renal responses to ANG II infusion. Am J Physiol Renal Physiol 299: F1141-F1150, 2010.
5. Choudhary D, Jansson I, Stoilov I, Sarfarazi M, Schenkman JB. Metabolism of retinoids and arachidonic acid by human and mouse cytochrome P450 1B1. Drug Metab Dispos 32: 840-847, 2004.
6. Chun YJ, Kim S, Kim D, Lee SK, Guengerich FP. A new selective and potent inhibitor of human cytochrome P450 1B1 and its application to antimutagenesis. Cancer Res 61: 8164-8170, 2001.
7. Crowley SD, Gurley SB, Oliverio MI, Pazmino AK, Griffiths R, Flannery PJ, Spurney RF, Kim HS, Smithies O, Le TH, Coffman TM. Distinct roles for the kidney and systemic tissues in blood pressure regulation by the renin-angiotensin system. J Clin Invest 115: 1092-1099, 2005.
8. Csiky B, Simon G. Effect of neonatal sympathectomy on development of angiotensin II-induced hypertension. Am J Physiol Heart Circ Physiol 272: H648-H656, 1997.
9. Dobrowolski L, Walkowska A, Kompanowska-Jezierske E, Kuczeriszka M, Sadowski. Effects of ATP on rat renal haemodynamics and excretion: role of sodium intake, nitric oxide and cytochrome P450. Acta Phsyiol 189: 77-85, 2007.
10. Fan YY, Kohno M, Nakano D, Ohsaki H, Kobori H, Diah S, Ohashi N, Hitomi H, Asanuma K, Noma T, Tomino Y, Fujita T, Nishiyama A. Cilnidipine suppresses podocyte injury and proteinuria in metabolic syndrome rats: possible involvement of N-type calcium channel in podocyte. J Hypertens 28: 1034-1043, 2010.
11. Hall JE. Control of sodium excretion by angiotensin II: intrarenal mechanisms and blood pressure regulation. Am J Physiol Regul Integr Comp Physiol 250: R960-R972, 1986.
12. Haque MZ, Majid DSA. High salt intake delayed angiotensin II-induced hypertension in mice with a genetic variant of NADPH oxidase. Am J Hypertens 24: 114-118, 2011.
13. 1 receptor: novel insights into mechanisms and pathophysiology. Clin Sci 112: 417-428, 2007.
14. Imig JD. Epoxide hydrolase and epoxygenase metabolites as therapeutic targets for renal diseases. Am J Physiol Renal Physiol 289: F496-F503, 2005.
15. Israel A, Arzola J, De Jesús S, Varela M. Role of oxidative stress in the natriuresis induced by central administration of angiotensin II. J Renin Angiotensin Aldosterone Syst 10: 9-14, 2009.
16. Jennings BL, Sahan-Firat S, Estes AM, Das K, Farjana N, Fang XR, Gonzalez FJ, Malik KU. Cytochrome P450 1B1 contributes to angiotensin II-induced hypertension and associated pathophysiology. Hypertension 56: 667-674, 2010.
17. Jin C, Hu C, Polichnowski A, Mori T, Skelton M, Ito S, Cowley AW Jr. Effects of renal perfusion pressure on renal medullary hydrogen peroxide and nitric oxide production. Hypertension 53: 1048-1053, 2009.
18. Kim S, Ohta K, Hamaguchi A, Yukimura T, Miura K, Iwao H. Angiotensin II induces cardiac phenotypic modulation and remodeling in vivo in rats. Hypertension 25: 1252-1259, 1995.
19. Kobori H, Nangaku M, Navar LG, Nishiyama A. The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 59: 251-287, 2007.
20. Liao TD, Yang XP, Liu YH, Shesely EG, Cavasin MA, Kuziel WA, Pagano PJ, Carretero OA. Role of inflammation in the development of renal damage and dysfunction in angiotensin II-induced hypertension. Hypertension 52: 256-263, 2008.
21. Lin HS, Choo QY, Ho PC. Quantification of oxyresveratrol analog trans-2,4,3',5'-tetramethoxystilbene in rat plasma by a rapid HPLC method: application in a pre-clinical pharmacokinetic study. Biomed Chromatogr 24: 1373-1378, 2010.
22. Marvar PJ, Thabet SR, Guzik TJ, Lob HE, McCann LA, Weyand C, Gordon FJ, Harrison DG. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res 107: 263-270, 2010.
23. McGiff JC, Quilley J. 20-Hydroxyeicosatetraenoic acid and epoxyeicosatrienoic acids and blood pressure. Curr Opin Nephrol Hypertens 10: 231-237, 2001.
24. 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 NADPH oxidase in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 294: L902-L911, 2008.
25. Mervaala E, Müller DN, Schmidt F, Park JK, Gross V, Bader M, Breu V, Ganten D, Haller H, Luft FC. Blood pressure-independent effects in rats with human renin and angiotensinogen genes. Hypertension 35: 587-594, 2000.
26. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD, Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res 82: 1298-1305, 1998.
27. Mori T, Cowley AW Jr. Role of pressure in angiotensin II-induced renal injury. Chronic servo-control of renal perfusion pressure in rats. Hypertension 43: 752-759, 2004.
28. Muskhelishvili L, Thompson PA, Kusewitt DF, Wang C, Kadlubar FF. In situ hybridization and immunohistochemical analysis of cytochrome P450 1B1 expression in human normal tissues. J Histochem Cytochem 49: 229-236, 2001.
29. Muthalif MM, Benter IF, Uddin MR, Harper JL, Malik KU. Signal transduction mechanisms involved in angiotensin-(1-7)-stimulated arachidonic acid release and prostanoid synthesis in rabbit aortic smooth muscle cells. J Pharmacol Exp Ther 284: 388-398, 1998.
30. Muthalif MM, Karzoun NA, Gaber L, Khandekar Z, Benter IF, Saeed AE, Parmentier JH, Estes A, Malik KU. Angiotensin II-induced hypertension: contribution of Ras GTPase/mitogen-activated protein kinase and cytochrome P450 metabolites. Hypertension 36: 604-609, 2000.
31. Nithipatikom K, Grall AJ, Holmes BB, Harder DR, Falck JR, Campbell WB. Liquid chromatographic-electrospray ionization-mass spectrometric analysis of cytochrome P450 metabolites of arachidonic acid. Anal Biochem 298: 327-336, 2001.
32. Oliveira-Sales EB, Colombari DSA, Davisson RL, Kasparov S, Hirata AE, Campos RR, Paton JFR. Kidney-induced hypertension depends on superoxide signaling in the rostral ventrolateral medulla. Hypertension 56: 290-296, 2010.
33. Olsen F. Type and course of the inflammatory cellular reaction in acute angiotensin-hypertensive vascular disease in rats. Correlation between its modification by cortisone and prolonged elimination of fluorescent proteins deposited in the arteriolar walls. Acta Pathol Microbiol Scand 78: 143-150, 1970.
34. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension. Clinical implications and therapeutic possibilities. Diabetes Care 31, Suppl 2: S170-S180, 2008.
35. Patel S, Rademacher DJ, Hillard CJ. Differential regulation of the endocannabinoids anandamide and 2-arachidonylglycerol within the limbic forebrain by dopamine receptor activity. J Pharmacol Exp Ther 306: 880-888, 2003.
36. Polichnowski AJ, Jin C, Yang C, Cowley AW Jr. Role of renal perfusion pressure versus angiotensin II on renal oxidative stress in angiotensin II-induced hypertensive rats. Hypertension 55: 1425-1430, 2010.
37. Polichnowski AJ, Lu L, Cowley AW Jr. Renal injury in angiotensin II+L-NAME-induced hypertensive rats is independent of elevated blood pressure. Am J Physiol Renal Physiol 300: F1008-F1016, 2011.
38. Rajagopalan S, Kurz S, Münzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG. 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, 1996.
39. 2 in vascular smooth-muscle cells. Biochem J 299: 197-201, 1994.
40. Reckelhoff JF, Romero JC. Role of oxidative stress in angiotensininduced hypertension. Am J Physiol Regul Integr Comp Physiol 284: R893-R912, 2003.
41. Reddy MA, Thimmalapura PR, Lanting L, Nadler JL, Fatima S, Natarajan R. The oxidized lipid and lipoxygenase product 12(S)-hydroxyeicosatetraenoic acid induces hypertrophy and fibronectin transcription in vascular smooth muscle cells via p38 MAPK and cAMP response element-binding protein activation. Mediation of angiotensin II effects. J Biol Chem 277: 9920-9928, 2002.
42. Roman RJ. P-450 Metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 82: 131-185, 2002.
43. Roman RJ, Hoagland KM, Lopez B, Kwitek AE, Garrett MR, Rapp JP, Lazar J, Jacob HJ, Sarkis A. Characterization of blood pressure and renal function in chromosome 5 congenic strains of Dahl S rats. Am J Physiol Renal Physiol 290: F1463-F1471, 2006.
44. Sacerdoti D, Escalante B, Abraham NG, McGiff JC, Levere RD, Schwatzman ML. Treatment with tin prevents the development of hypertension in spontaneously hypertensive rats. Science 243: 388-390, 1989.
45. Sahan-Firat S, Jennings BL, Yaghini FA, Song CY, Estes AM, Fang XR, Farjana N, Khan AI, Malik KU. 2,3',4,5'-Tetramethoxystilbene prevents deoxycorticosterone-salt-induced hypertension: contribution of cytochrome P-450 1B1. Am J Physiol Heart Circ Physiol 299: H1891-H1901, 2010.
46. Sánchez M, Galisteo M, Vera R, Villar IC, Zarzuelo A, Tamargo J, Pérez-Vizcaíno F, Duarte J. Quercetin downregulates NADPH oxidase, increases eNOS activity and prevents endothelial dysfunction in spontaneously hypertensive rats. J Hypertens 24: 75-84, 2006.
47. Sarr M, Chataigneau M, Martins S, Schott C, El Bedoui J, Oak MH, Muller B, Chataigneau T, Schini-Kerth VB. Red wine polyphenols prevent angiotensin II-induced hypertension and endothelial dysfunction in rats: role of NADPH oxidase. Cardiovasc Res 71: 794-802, 2006.
48. Somers MJ, Mavromatis K, Galis ZS, Harrison DG. Vascular superoxide production and vasomotor function in hypertension induced by deoxycorticosterone acetate-salt. Circulation 101: 1722-1728, 2000.
49. Stec DE, Gannon KP, Beaird JS, Drummond HA. 20-Hydroxyeicosatetraenoic acid (20-HETE) stimulates migration of vascular smooth muscle cells. Cell Physiol Biochem 19: 121-128, 2007.
50. Su P, Kaushal KM, Kroetz DL. Inhibition of renal arachidonic acid ω-hydroxylase activity with ABT reduces blood pressure in the SHR. Am J Physiol Regul Integr Comp Physiol 275: R426-R438, 1998.
51. Uddin MR, Muthalif MM, Karzoun NA, Benter IF, Malik KU. Cytochrome P-450 metabolites mediate norepinephrine-induced mitogenic signaling. Hypertension 31: 242-247, 1998.
52. Von Thun AM, Vari RC, El-Dahr SS, Navar LG. Augmentation of intrarenal angiotensin II levels by chronic angiotensin II infusion. Am J Physiol Renal Fluid Electrolyte Physiol 266: F120-F128, 1994.
53. Welch WJ, Blau J, Xie H, Chabrashvili T, Wilcox CS. Angiotensininduced defects in renal oxygenation: role of oxidative stress. Am J Physiol Heart Circ Physiol 288: H22-H28, 2005.
54. Yaghini FA, Li F, Malik KU. Expression and mechanism of spleen tyrosine kinase activation by angiotensin II and its implication in protein synthesis in rat vascular smooth muscle cells. J Biol Chem 282: 16878-16890, 2007.
55. Yaghini FA, Song CY, Lavrentyev EN, Ghafoor HUB, Fang XR, Estes AM, Campbell WB, Malik KU. Angiotensin II-induced vascular smooth muscle cell migration and growth are mediated by cytochrome P450 1B1-dependent superoxide generation. Hypertension 55: 1461-1467, 2010.
56. Yoshida K, Kobayashi N, Ohno T, Fukushima H, Matsuoka H. Cardioprotective effect of angiotensin II type 1 receptor antagonist associated with bradykinin-endothelial nitric oxide synthase and oxidative stress in Dahl salt-sensitive hypertensive rats. J Hypertens 25: 1633-1642, 2007.
57. Zafari AM, Ushio-Fukai M, Minieri CA, Akers M, Lassègue B, Griendling KK. Arachidonic acid metabolites mediate angiotensin IIinduced NADH/NADPH oxidase activity and hypertrophy in vascular smooth muscle cells. Antioxid Redox Signal 1: 167-179, 1999.
58. Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 95: 210-216, 2004.