Antihypertensive action of soluble epoxide hydrolase inhibition in Ren-2 transgenic rats is mediated by suppression of the intrarenal renin-angiotensin system

Clinical and Experimental Pharmacology and Physiology

Volumn 40, Issue 4, 2013, Pages 273-281

  Varcabova, Sarka ^a   Huskova, Zuzana ^a   Kramer, Herbert J ^b   Hwang, Sung Hee ^c   Hammock, Bruce D ^c   Imig, John D ^d   Kitada, Kento ^e   Cervenka, Ludek ^f  

^a INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e KAGAWA UNIVERSITY   (Japan)

^f CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Cytochrome P450 metabolites; Epoxyeicosatrienoic acids; Glomerular filtration rate; Hypertension; Pressure natriuresis; Renal blood flow; Renin angiotensin system; Soluble epoxide hydrolase

Indexed keywords

BENZOIC ACID; CIS 4 (4 (3 ADAMANTAN 1 YLUREIDO)CYCLOHEXYLOXY)BENZOIC ACID; EPOXYICOSATRIENOIC ACID; HYDROLASE INHIBITOR; UNCLASSIFIED DRUG; 4-(4-(3-ADAMANTAN-1-YLUREIDO)CYCLOHEXYLOXY)BENZOIC ACID; ANTIHYPERTENSIVE AGENT; BENZOIC ACID DERIVATIVE; EPOXIDE HYDROLASE; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIHYPERTENSIVE ACTIVITY; ARTERIAL PRESSURE; ARTICLE; AUTOREGULATION; BLOOD PRESSURE; CONTROLLED STUDY; ENZYME INHIBITION; GLOMERULUS FILTRATION RATE; KIDNEY BLOOD FLOW; NATRIURESIS; NONHUMAN; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SODIUM URINE LEVEL; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DOWN REGULATION; DRUG EFFECTS; FEMALE; HYPERTENSION; KIDNEY; KIDNEY CIRCULATION; MALE; METABOLISM; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

ANIMALS; ANTIHYPERTENSIVE AGENTS; BENZOATES; BLOOD PRESSURE; DOWN-REGULATION; EPOXIDE HYDROLASES; FEMALE; GLOMERULAR FILTRATION RATE; HYPERTENSION; KIDNEY; MALE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RENAL CIRCULATION; RENIN-ANGIOTENSIN SYSTEM; UREA;

EID: 84875652885     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12018     Document Type: Article

References (46)

1. Mullins JJ, Peters J, Ganten D. Fulminant hypertension in transgenic rats harboring the mouse Ren-2 gene. Nature 1990; 344: 541-4.
2. Husková Z, Kramer HJ, Vanourkova Z, Cervenka L. Effects of changes in sodium balance on plasma and kidney angiotensin II levels in anesthetized and conscious Ren-2 transgenic rats. J. Hypertens. 2006; 24: 517-27.
3. Kujal P, Certikova Chábová V, Vernerová Z et al. Similar renoprotection after renin-angiotensin-dependent and -independent antihypertensive therapy in 5/6-nephrectomized Ren-2 transgenic rats: Are there blood pressure-independent effects? Clin. Exp. Pharmacol. Physiol. 2010; 37: 1159-69.
4. Hartner A, Porst M, Klanke B, Cordasic N, Veelken R, Hilgers KF. Angiotensin II formation in the kidney and nephrosclerosis in Ren-2 hypertensive rats. Nephrol. Dial. Transplant. 2006; 21: 1778-85.
5. Jacinto SM, Mullins JJ, Mitchell KD. Enhanced renal vascular responsiveness to angiotensin II in hypertensive ren-2 transgenic rats. Am. J. Physiol. 1999; 276: F315-22.
6. Kopkan L, Kramer HJ, Huskova Z et al. The role of intrarenal angiotensin II in the development of hypertension in Ren-2 transgenic rats. J. Hypertens. 2005; 23: 1531-9.
7. Lee MA, Böhm M, Paul M, Bader M, Ganten U, Ganten D. Physiological characterization of the hypertensive transgenic rat TGR(mRen2)27. Am. J. Physiol. 1990; 270: E919-29.
8. Kopkan L, Husková Z, Vanourkova Z et al. Reduction of oxidative stress does not attenuate the development of angiotensin II-dependent hypertension in Ren-2 transgenic rats. Curr. Vasc. Pharmacol. 2009; 51: 175-81.
9. Kopkan L, Husková Z, Vanourková Z et al. Superoxide and its interaction with nitric oxide modulates renal function in prehypertensive Ren-2 transgenic rats. J. Hypertens. 2007; 25: 2257-65.
10. Vernerová Z, Kujal P, Kramer HJ, Bäcker A, Cervenka L, Vaneckova I. End-organ damage in hypertensive transgenic Ren-2 rats: Influence of early and late endothelin receptor blockade. Physiol. Res. 2009; 58(Suppl. 2): S69-78.
11. Campbell WB, Fleming I. Epoxyeicosatrienoic acids and endothelium-dependent response. Pflugers Arch. 2010; 459: 881-95.
12. Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol. Rev. 2002; 82: 131-85.
13. Imig JD. Epoxides and soluble epoxide hydrolase in cardiovascular physiology. Physiol. Rev. 2012; 92: 101-30.
14. Imig JD, Zhao X, Falck JR, Wei S, Capdevila JH. Enhanced renal mircovascular reactivity to angiotensin II in hypertension is ameliorated by the sulfonimide analog of 11, 12-epoxyeicosatrienoic acid. J. Hypertens. 2001; 19: 983-92.
15. Lee CR, Imig JD, Edin ML et al. Endothelial expression of human cytochrome P450 epoxygenases lowers blood pressure and attenuates hypertension-induced renal injury in mice. FASEB J. 2010; 24: 3770-81.
16. Honetschlägerová Z, Husková Z, Vanourkova Z et al. Renal mechanisms contributing to the antihypertensive action of soluble epoxide hydrolase inhibition in Ren-2 transgenic rats with inducible hypertension. J. Physiol. 2011; 589: 207-19.
17. Sporková A, Kopkan L, Varcabová Š et al. Role of cytochrome P450 metabolites in the regulation of renal function and blood pressure in 2-kidney, 1-clip hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011; 300: R1468-75.
18. Honetschlägerová Z, Sporková A, Kopkan L et al. Inhibition of soluble epoxide hydrolyse improves the impaired pressure-natriuresis relationship and attenuates the development of hypertension and hypertension-associated end-organ damage in Cyp1a1-Ren-2 transgenic rats. J. Hypertens. 2011; 29: 1590-601.
19. Springate J, Van Liew J, Ganten D. Enalapril and pressure-diuresis in hypertensive rats transgenic for mouse renin gene. Kidney Blood Press. Res. 1997; 20: 1-5.
20. Lippoldt A, Gross V, Bohlender J, Ganten U, Luft FC. Lifelong angiotensin-converting enzyme inhibition, pressure natriuresis, and renin-angiotensin system gene expression in transgenic(mRen-2)27 rats. J. Am. Soc. Nephrol. 1996; 7: 2119-29.
21. Neckar J, Kopkan L, Husková Z et al. Inhibition of soluble epoxide hydrolase by cis-4-[4-(3-adamantan-1-yl-ureido)cyclohexyloxy]benzoic acid exhibits antihypertensive and cardioprotective actions in transgenic rats with angiotensin II-dependent hypertension. Clin. Sci. 2012; 122: 513-25.
22. Cervenka L, Wang CT, Navar LG. Effects of acute AT1 receptor blockade by candesartanu on arterial pressure and renal function in rats. Am. J. Physiol. 1998; 274: F940-5.
23. Wang CT, Chin SY, Navar LG. Impairment of pressure-natriuresis and renal autoregulation in ANG II-infused hypertensive rats. Am. J. Physiol. Renal Physiol. 2000; 279: F319-25.
24. Erbanová M, Thumová M, Husková Z et al. Impairment of the autoregulation of renal hemodynamics and of the pressure-natriuresis relationship precedes the development of hypertension in Cyp1a1-Ren-2 transgenic rats. J. Hypertens. 2009; 27: 575-86.
25. Semple SJ, de Wardener HE. Effect of increased renal venous pressure on circulatory autoregulation of isolated dog kidneys. Circ. Res. 1959; 7: 643-8.
26. Husková Z, Kramer HJ, Thumová M et al. Effects of anaesthesia on plasma and kidney ANG II levels in normotensive and ANG II-dependent hypertensive rats. Kidney Blood Press. Res. 2006; 29: 74-83.
27. Walkowska A, Škaroupková P, Husková Z et al. Intrarenal cytochrome P-450 metabolites of arachidonic acid in the regulation of the nonclipped kidney function in two-kidney, one-clip Goldblatt hypertensive rats. J. Hypertens. 2010; 28: 582-93.
28. Li PL, Campbell WB. Regulation of potassium channels in coronary smooth muscle through a guanine nucleotide binding protein. Circ. Res. 1997; 80: 877-84.
29. Wang D, Borrego-Conde LJ, Falck JR, Sharma KK, Wilcox CS, Umans JG. Contribution of nitric oxide, EDHF, and EETs to endothelium-dependent relaxation in renal afferent arterioles. Kidney Int. 2003; 63: 2187-93.
30. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ. Res. 1996; 78: 415-23.
31. Kohagure K, Endo Y, Ito O, Arima S, Omata K, Ito S. Endogenous nitric oxide and epoxyeicosatrienoic acids modulate angiotensin II-induced constriction in the rabbit afferent arteriole. Acta Physiol. Scand. 2000; 168: 107-12.
32. Madhun ZT, Goldthwait DA, McKay D, Hopfer U, Douglas JG. An epoxygenase metabolite of arachidonic acid mediates angiotensin II-induced rises in cytosolic calcium in rabbit proximal tubule epithelial cells. J. Clin. Invest. 1991; 88: 456-61.
33. Sakairi Y, Jacobson HR, Noland DT, Capdevila JH, Falck JR, Breyer MD. 5, 6-EET inhibits ion transport in collecting duct by stimulating endogenous prostaglandin synthesis. Am. J. Physiol. 1995; 268: F931-9.
34. Imig JD, Falck JR, Inscho EW. Contribution of cytochrome P450 epoxygenase and hydroxylase pathways to afferent arteriolar autoregulatory responsiveness. Br. J. Pharmacol. 1999; 127: 1399-405.
35. Guyton AC, Hall JE, Coleman TG, Manning RD Jr. The dominant role of the kidneys in the long term regulation of arterial pressure in normal and hypertensive states. In: Laragh JH, Brenner BM (eds). Hypertension: Pathophysiology, Diagnosis and Management. Raven Press, New York. 1990; 1029-52.
36. Roman RJ, Cowley AW Jr. Abnormal pressure-diuresis-natriuresis response in spontaneously hypertensive rats. Am. J. Physiol. 1985; 248: F199-205.
37. Miao CY, Liu KL, Benzoni D, Sassard J. Acute pressure-natriuresis function shows early impairment in Lyon hypertensive rats. J. Hypertens. 2005; 23: 1225-31.
38. Van der Mark J, Kline RL. Altered pressure natriuresis in chronic angiotensin II hypertension in rats. Am. J. Physiol. 1994; 266: F739-48.
39. Hall JE, Mizelle HL, Brands MV, Hildebrandt DA. Pressure natriuresis and angiotensin II in reduced kidney mass, salt-induced hypertension. Am. J. Physiol. 1992; 262: R61-71.
40. 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. 2007; 59: 251-87.
41. Kline RL, Liu F. Modification of pressure natriuresis by long-term losartan in spontaneously hypertensive rats. Hypertension 1994; 24: 467-73.
42. Vaneckova I, Dobešová Z, Kuneš J, Zicha J. The effects of repeated delivery of angiotensin II AT1 receptor antisense on distinct vasoactive systems in Ren-2 transgenic rats: Young vs. adult animals. Hypertens. Res. 2012; 35: 761-8.
43. Henrich WL, Falck JR, Campbell WB. Inhibition of renin release by 14, 15-epoxyeicosatrienoic acid in renal cortical slices. Am. J. Physiol. 1990; 258: E269-74.
44. Bohlender J, Ménard J, Edling O, Ganten D, Luft FC. Mouse and rat plasma renin concentration and gene expression in (mRen2)27 transgenic rats. Am. J. Physiol. 1998; 274: H1450-6.
45. Cervenka L, Vaneckova I, Huskova Z et al. Pivotal role of angiotensin II receptor subtype 1A in the development of two-kidney, one-clip hypertension: Study in angiotensin II receptor subtype 1A knockout mice. J. Hypertens. 2008; 26: 1379-89.
46. Welch WJ. Angiotensin II-dependent superoxide. Effects on hypertension and vascular dysfunction. Hypertension 2008; 52: 51-6.