Sex-related differences in the intratubular renin-angiotensin system in two-kidney, one-clip hypertensive rats

American Journal of Physiology - Renal Physiology

Volumn 317, Issue 3, 2019, Pages F670-F682

  Lee, Sang Ho ^a   Lee, Yu Ho ^a   Jung, Su Woong ^a   Kim, Dong Jin ^a   Park, Seon Hwa ^a   Song, Seok Jong ^a   Jeong, Kyung Hwan ^a   Moon, Ju Young ^a   Ihm, Chun Gyoo ^a   Lee, Tae Won ^a   Kim, Jin Sug ^a   Sohn, Il Suk ^a   Lee, So Young ^b   Kim, Dong Ok ^a   Kim, Yang Gyun ^a  

^a Kyung Hee University Hospital   (South Korea)

^b CHA University   (South Korea)

Author keywords

Intrarenal renin angiotensin system; Sex related differences; Two kidney, one clip rat

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; ANGIOTENSIN[1-7]; DIPEPTIDYL CARBOXYPEPTIDASE; ESTROGEN; MAS RECEPTOR; RECEPTOR; UNCLASSIFIED DRUG; AGTR2 PROTEIN, RAT; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN I; ANGIOTENSIN I (1-7); G PROTEIN COUPLED RECEPTOR; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; FEMALE; HEART INJURY; HEART LEFT VENTRICLE HYPERTROPHY; INTERSTITIAL NEPHRITIS; KIDNEY FIBROSIS; KIDNEY TUBULE; MACROPHAGE; MALE; MRNA EXPRESSION LEVEL; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION LEVEL; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RENOVASCULAR HYPERTENSION; SEX DIFFERENCE; SYSTOLIC BLOOD PRESSURE; UPREGULATION; ANIMAL; BLOOD PRESSURE; COMPARATIVE STUDY; DISEASE MODEL; GENETICS; HYPERTENSION; KIDNEY ARTERY; LIGATION; METABOLISM; PATHOPHYSIOLOGY; SEX FACTOR; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SURGERY;

ANGIOTENSIN I; ANGIOTENSIN II; ANIMALS; BLOOD PRESSURE; CONSTRICTION; DISEASE MODELS, ANIMAL; ESTROGENS; FEMALE; HYPERTENSION; HYPERTROPHY, LEFT VENTRICULAR; KIDNEY TUBULES; MACROPHAGES; MALE; OVARIECTOMY; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; PROTO-ONCOGENE PROTEINS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; RECEPTORS, G-PROTEIN-COUPLED; RENAL ARTERY; RENIN-ANGIOTENSIN SYSTEM; SEX FACTORS; SIGNAL TRANSDUCTION;

EID: 85071897557     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00451.2018     Document Type: Article

References (49)

1. Bhatia K, Zimmerman MA, Sullivan JC. Sex differences in angiotensin-converting enzyme modulation of Ang (1-7) levels in normotensive WKY rats. Am J Hypertens 26: 591–598, 2013. doi:10.1093/ajh/hps088.
2. Brosnihan KB, Li P, Ganten D, Ferrario CM. Estrogen protects transgenic hypertensive rats by shifting the vasoconstrictor-vasodilator balance of RAS. Am J Physiol Regul Integr Comp Physiol 273: R1908–R1915, 1997. doi:10.1152/ajpregu.1997.273.6.R1908.
3. Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, Horan MJ, Labarthe D. Prevalence of hypertension in the US adult population. Results from the Third National Health and Nutrition Examination Survey, 1988-1991. Hypertension 25: 305–313, 1995. doi:10.1161/ 01.HYP.25.3.305.
4. Chappell MC. Nonclassical renin-angiotensin system and renal function. Compr Physiol 2: 2733–2752, 2012. doi:10.1002/cphy.c120002.
5. Chen YF, Naftilan AJ, Oparil S. Androgen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension 19: 456–463, 1992. doi:10.1161/01.HYP.19.5.456.
6. Chidambaram M, Duncan JA, Lai VS, Cattran DC, Floras JS, Scholey JW, Miller JA. Variation in the renin angiotensin system throughout the normal menstrual cycle. J Am Soc Nephrol 13: 446–452, 2002.
7. Dean SA, Tan J, O’Brien ER, Leenen FH. 17β-Estradiol downregulates tissue angiotensin-converting enzyme and ANG II type 1 receptor in female rats. Am J Physiol Regul Integr Comp Physiol 288: R759–R766, 2005. doi:10.1152/ajpregu.00595.2004.
8. Dubey RK, Oparil S, Imthurn B, Jackson EK. Sex hormones and hypertension. Cardiovasc Res 53: 688–708, 2002. doi:10.1016/S0008-6363 (01)00527-2.
9. Ferrario CM, Jessup J, Gallagher PE, Averill DB, Brosnihan KB, Ann Tallant E, Smith RD, Chappell MC. Effects of renin-angiotensin system blockade on renal angiotensin-(1-7) forming enzymes and receptors. Kidney Int 68: 2189–2196, 2005. doi:10.1111/j.1523-1755. 2005.00675.x.
10. Gallagher PE, Li P, Lenhart JR, Chappell MC, Brosnihan KB. Estrogen regulation of angiotensin-converting enzyme mRNA. Hypertension 33: 323–328, 1999. doi:10.1161/01.HYP.33.1.323.
11. Garcia M, Mulvagh SL, Bairey Merz CN, Buring JE, Manson JE. Cardiovascular disease in women: clinical perspectives. Circ Res 118: 1273–1293, 2016. doi:10.1161/CIRCRESAHA.116.307547.
12. Gonzalez-Villalobos RA, Satou R, Ohashi N, Semprun-Prieto LC, Katsurada A, Kim C, Upchurch GM, Prieto MC, Kobori H, Navar LG. Intrarenal mouse renin-angiotensin system during ANG II-induced hypertension and ACE inhibition. Am J Physiol Renal Physiol 298: F150 –F157, 2010. doi:10.1152/ajprenal.00477.2009.
13. Guan S, Fox J, Mitchell KD, Navar LG. Angiotensin and angiotensin converting enzyme tissue levels in two-kidney, one clip hypertensive rats. Hypertension 20: 763–767, 1992. doi:10.1161/01.HYP.20.6.763.
14. Harrison-Bernard LM, Zhuo J, Kobori H, Ohishi M, Navar LG. Intrarenal AT1 receptor and ACE binding in ANG II-induced hypertensive rats. Am J Physiol Renal Physiol 282: F19–F25, 2002. doi:10.1152/ajprenal.0335. 2000.
15. Huang XR, Chen WY, Truong LD, Lan HY. Chymase is upregulated in diabetic nephropathy: implications for an alternative pathway of angiotensin II-mediated diabetic renal and vascular disease. J Am Soc Nephrol 14: 1738–1747, 2003. doi:10.1097/01.ASN.0000071512.93927.4E.
16. Ji H, Menini S, Zheng W, Pesce C, Wu X, Sandberg K. Role of angiotensin-converting enzyme 2 and angiotensin(1-7) in 17beta-oestra-diol regulation of renal pathology in renal wrap hypertension in rats. Exp Physiol 93: 648–657, 2008. doi:10.1113/expphysiol.2007.041392.
17. Kim YG, Lee SH, Kim SY, Lee A, Moon JY, Jeong KH, Lee TW, Lim SJ, Sohn IS, Ihm CG. Sequential activation of the intrarenal renin-angiotensin system in the progression of hypertensive nephropathy in Goldblatt rats. Am J Physiol Renal Physiol 311: F195–F206, 2016. doi:10.1152/ajprenal.00001. 2015.
18. Koike G, Horiuchi M, Yamada T, Szpirer C, Jacob HJ, Dzau VJ. Human type 2 angiotensin II receptor gene: cloned, mapped to the X chromosome, and its mRNA is expressed in the human lung. Biochem Biophys Res Commun 203: 1842–1850, 1994. doi:10.1006/bbrc.1994.2402.
19. Koka V, Huang XR, Chung AC, Wang W, Truong LD, Lan HY. Angiotensin II up-regulates angiotensin I-converting enzyme (ACE), but down-regulates ACE2 via the AT1-ERK/p38 MAP kinase pathway. Am J Pathol 172: 1174–1183, 2008. doi:10.2353/ajpath.2008.070762.
20. Komukai K, Mochizuki S, Yoshimura M. Gender and the renin-angiotensin-aldosterone system. Fundam Clin Pharmacol 24: 687–698, 2010. doi:10.1111/j.1472-8206.2010.00854.x.
21. Krishnamurthi K, Verbalis JG, Zheng W, Wu Z, Clerch LB, Sandberg K. Estrogen regulates angiotensin AT1 receptor expression via cytosolic proteins that bind to the 5= leader sequence of the receptor mRNA. Endocrinology 140: 5435–5438, 1999. doi:10.1210/endo.140.11.7242.
22. Lane PH. Estrogen receptors in the kidney: lessons from genetically altered mice. Gend Med 5, Suppl A: S11–S18, 2008. doi:10.1016/j.genm.2008.03. 003.
23. Macova M, Armando I, Zhou J, Baiardi G, Tyurmin D, Larrayoz-Roldan IM, Saavedra JM. Estrogen reduces aldosterone, upregulates adrenal angiotensin II AT2 receptors and normalizes adrenomedullary Fra-2 in ovariectomized rats. Neuroendocrinology 88: 276–286, 2008. doi:10.1159/ 000150977.
24. Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N Engl J Med 340: 1801–1811, 1999. doi:10.1056/ NEJM199906103402306.
25. Milsted A, Underwood AC, Dunmire J, DelPuerto HL, Martins AS, Ely DL, Turner ME. Regulation of multiple renin-angiotensin system genes by Sry. J Hypertens 28: 59–64, 2010. doi:10.1097/HJH.0b013e328332b88d.
26. Navar LG, Harrison-Bernard LM, Wang CT, Cervenka L, Mitchell KD. Concentrations and actions of intraluminal angiotensin II. J Am Soc Nephrol 10, Suppl 11: S189–S195, 1999.
27. Navar LG, Imig JD, Zou L, Wang CT. Intrarenal production of angiotensin II. Semin Nephrol 17: 412–422, 1997.
28. Navar LG, Kobori H, Prieto MC, Gonzalez-Villalobos RA. Intratubular renin-angiotensin system in hypertension. Hypertension 57: 355–362, 2011. doi:10.1161/HYPERTENSIONAHA.110.163519.
29. O’Donnell E, Floras JS, Harvey PJ. Estrogen status and the renin angiotensin aldosterone system. Am J Physiol Regul Integr Comp Physiol 307: R498–R500, 2014. doi:10.1152/ajpregu.00182.2014.
30. Pendergrass KD, Pirro NT, Westwood BM, Ferrario CM, Brosnihan KB, Chappell MC. Sex differences in circulating and renal angiotensins of hypertensive mRen(2). Lewis but not normotensive Lewis rats. Am J Physiol Heart Circ Physiol 295: H10–H20, 2008. doi:10.1152/ajpheart. 01277.2007.
31. Prieto MC, González-Villalobos RA, Botros FT, Martin VL, Pagán J, Satou R, Lara LS, Feng Y, Fernandes FB, Kobori H, Casarini DE, Navar LG. Reciprocal changes in renal ACE/ANG II and ACE2/ANG 1-7 are associated with enhanced collecting duct renin in Goldblatt hypertensive rats. Am J Physiol Renal Physiol 300: F749–F755, 2011. doi:10.1152/ajprenal. 00383.2009.
32. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension 37: 1199–1208, 2001. doi:10.1161/01.HYP.37.5.1199.
33. Rogers JL, Mitchell AR, Maric C, Sandberg K, Myers A, Mulroney SE. Effect of sex hormones on renal estrogen and angiotensin type 1 receptors in female and male rats. Am J Physiol Regul Integr Comp Physiol 292: R794–R799, 2007. doi:10.1152/ajpregu.00424.2006.
34. Safari T, Nematbakhsh M, Hilliard LM, Evans RG, Denton KM. Sex differences in the renal vascular response to angiotensin II involves the Mas receptor. Acta Physiol (Oxf) 206: 150–156, 2012. doi:10.1111/j.1748-1716. 2012.02468.x.
35. Sampson AK, Hilliard LM, Moritz KM, Thomas MC, Tikellis C, Widdop RE, Denton KM. The arterial depressor response to chronic low-dose angiotensin II infusion in female rats is estrogen dependent. Am J Physiol Regul Integr Comp Physiol 302: R159–R165, 2012. doi:10. 1152/ajpregu.00256.2011.
36. Sampson AK, Moritz KM, Denton KM. Postnatal ontogeny of angiotensin receptors and ACE2 in male and female rats. Gend Med 9: 21–32, 2012. doi:10.1016/j.genm.2011.12.003.
37. Sampson AK, Moritz KM, Jones ES, Flower RL, Widdop RE, Denton KM. Enhanced angiotensin II type 2 receptor mechanisms mediate decreases in arterial pressure attributable to chronic low-dose angiotensin II in female rats. Hypertension 52: 666–671, 2008. doi:10.1161/HYPERTENSIONAHA. 108.114058.
38. Silva-Antonialli MM, Tostes RC, Fernandes L, Fior-Chadi DR, Aka-mine EH, Carvalho MH, Fortes ZB, Nigro D. A lower ratio of AT1/AT2 receptors of angiotensin II is found in female than in male spontaneously hypertensive rats. Cardiovasc Res 62: 587–593, 2004. doi:10.1016/j. cardiores.2004.01.020.
39. Sullivan JC. Sex and the renin-angiotensin system: inequality between the sexes in response to RAS stimulation and inhibition. Am J Physiol Regul Integr Comp Physiol 294: R1220 –R1226, 2008. doi:10.1152/ajpregu. 00864.2007.
40. Sullivan JC, Bhatia K, Yamamoto T, Elmarakby AA. Angiotensin (1-7) receptor antagonism equalizes angiotensin II-induced hypertension in male and female spontaneously hypertensive rats. Hypertension 56: 658–666, 2010. doi:10.1161/HYPERTENSIONAHA.110.153668.
41. Tikellis C, Cooper ME, Bialkowski K, Johnston CI, Burns WC, Lew RA, Smith AI, Thomas MC. Developmental expression of ACE2 in the SHR kidney: a role in hypertension? Kidney Int 70: 34–41, 2006. doi:10. 1038/sj.ki.5000428.
42. Tikellis C, Johnston CI, Forbes JM, Burns WC, Burrell LM, Risvanis J, Cooper ME. Characterization of renal angiotensin-converting enzyme 2 in diabetic nephropathy. Hypertension 41: 392–397, 2003. doi:10.1161/ 01.HYP.0000060689.38912.CB.
43. Vío CP, Jeanneret VA. Local induction of angiotensin-converting enzyme in the kidney as a mechanism of progressive renal diseases. Kidney Int Suppl 64: S57–S63, 2003. doi:10.1046/j.1523-1755.64.s86.11.x.
44. Wang Q, Xie D, Xu X, Qin X, Tang G, Wang B, Wang Y, Hou F, Xu X, Wang X. Blood pressure and renal function decline: a 7-year prospective cohort study in middle-aged rural Chinese men and women. J Hypertens 33: 136 –143, 2015. doi:10.1097/HJH.0000000000000360.
45. Wenner MM, Haddadin AS, Taylor HS, Stachenfeld NS. Mechanisms contributing to low orthostatic tolerance in women: the influence of oestradiol. J Physiol 591: 2345–2355, 2013. doi:10.1113/jphysiol. 2012.247882.
46. Wettschureck N, Offermanns S. Mammalian G proteins and their cell type specific functions. Physiol Rev 85: 1159–1204, 2005. doi:10.1152/ physrev.00003.2005.
47. Wu Z, Maric C, Roesch DM, Zheng W, Verbalis JG, Sandberg K. Estrogen regulates adrenal angiotensin AT1 receptors by modulating AT1 receptor translation. Endocrinology 144: 3251–3261, 2003. doi:10.1210/ en.2003-0015.
48. Yanes LL, Romero DG, Iles JW, Iliescu R, Gomez-Sanchez C, Reckelhoff JF. Sexual dimorphism in the renin-angiotensin system in aging spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 291: R383–R390, 2006. doi:10.1152/ajpregu.00510.2005.
49. You D, Loufrani L, Baron C, Levy BI, Widdop RE, Henrion D. High blood pressure reduction reverses angiotensin II type 2 receptor-mediated vasoconstriction into vasodilation in spontaneously hypertensive rats. Circulation 111: 1006–1011, 2005. doi:10.1161/01.CIR.0000156503. 62815.48.