Sex-Specific Effect of Endothelin in the Blood Pressure Response to Acute Angiotensin II in Growth-Restricted Rats

Hypertension

Volumn 66, Issue 6, 2015, Pages 1260-1266

  Intapad, Suttira ^a,b   Ojeda, Norma B ^a,b   Varney, Elliott ^a   Royals, Thomas P ^a   Alexander, Barbara T ^a,b  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

angiotensin II; blood pressure; endothelins; renin angiotensin system; sex characteristics

Indexed keywords

ANGIOTENSIN II; ATRASENTAN; ENALAPRIL; ENDOTHELIN; MESSENGER RNA; PREPROENDOTHELIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIN 1; ENDOTHELIN A RECEPTOR; ENDOTHELIN B RECEPTOR; ENDOTHELIN RECEPTOR ANTAGONIST; PYRROLIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH WEIGHT; BLOOD PRESSURE; BODY WEIGHT; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GLOMERULUS FILTRATION RATE; INTRAUTERINE GROWTH RETARDATION; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; KIDNEY MASS; KIDNEY PLASMA FLOW; KIDNEY VASCULAR RESISTANCE; MALE; MEAN ARTERIAL PRESSURE; NEWBORN; NONHUMAN; OVARIECTOMY; PRESSOR RESPONSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BLOCKING; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SEX DIFFERENCE; SEXUAL DEVELOPMENT; ANIMAL; DRUG EFFECTS; GENETICS; HEMODYNAMICS; KIDNEY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; URINE; VASCULARIZATION; WESTERN BLOTTING;

ANGIOTENSIN II; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BLOOD PRESSURE; BLOTTING, WESTERN; ENALAPRIL; ENDOTHELIN RECEPTOR ANTAGONISTS; ENDOTHELIN-1; FEMALE; FETAL GROWTH RETARDATION; GLOMERULAR FILTRATION RATE; HEMODYNAMICS; KIDNEY; MALE; OVARIECTOMY; PREGNANCY; PYRROLIDINES; RATS; RECEPTOR, ENDOTHELIN A; RECEPTOR, ENDOTHELIN B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX FACTORS;

EID: 84947495766     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.06257     Document Type: Article

References (44)

1. Davis EF, Lewandowski AJ, Aye C, Williamson W, Boardman H, Huang RC, Mori TA, Newnham J, Beilin LJ, Leeson P. Clinical cardiovascular risk during young adulthood in offspring of hypertensive pregnancies: insights from a 20-year prospective follow-up birth cohort. BMJ Open. 2015;5:e008136. doi: 10.1136/bmjopen-2015-008136.
2. Fraser A, Nelson SM, Macdonald-Wallis C, Sattar N, Lawlor DA. Hypertensive disorders of pregnancy and cardiometabolic health in adolescent offspring. Hypertension. 2013;62:614-620. doi: 10.1161/HYPERTENSIONAHA.113.01513.
3. Herrera-Garcia G, Contag S. Maternal preeclampsia and risk for cardiovascular disease in offspring. Curr Hypertens Rep. 2014;16:475. doi: 10.1007/s11906-014-0475-3.
4. Alexander BT, Kassab SE, Miller MT, Abram SR, Reckelhoff JF, Bennett WA, Granger JP. Reduced uterine perfusion pressure during pregnancy in the rat is associated with increases in arterial pressure and changes in renal nitric oxide. Hypertension. 2001;37:1191-1195. doi: 10.1161/01. HYP.37.4.1191.
5. Alexander BT. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension. 2003;41:457-462. doi: 10.1161/01.HYP.0000053448.95913.3D.
6. Ojeda NB, Royals TP, Black JT, Dasinger JH, Johnson JM, Alexander BT. Enhanced sensitivity to acute angiotensin II is testosterone dependent in adult male growth-restricted offspring. Am J Physiol Regul Integr Comp Physiol. 2010;298:R1421-R1427. doi: 10.1152/ajpregu.00096.2010.
7. Ojeda NB, Grigore D, Yanes LL, Iliescu R, Robertson EB, Zhang H, Alexander BT. Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Regul Integr Comp Physiol. 2007;292:R758-R763. doi: 10.1152/ajpregu.00311.2006.
8. Song J, Kost CK Jr, Martin DS. Androgens potentiate renal vascular responses to angiotensin II via amplification of the Rho kinase signaling pathway. Cardiovasc Res. 2006;72:456-463. doi: 10.1016/j.cardiores.2006.09.007.
9. Ojeda NB, Royals TP, Alexander BT. Sex differences in the enhanced responsiveness to acute angiotensin II in growth-restricted rats: role of fasudil, a Rho kinase inhibitor. Am J Physiol Renal Physiol. 2013;304:F900-F907. doi: 10.1152/ajprenal.00687.2012.
10. Kohan DE. Endothelin, hypertension and chronic kidney disease: new insights. Curr Opin Nephrol Hypertens. 2010;19:134-139. doi: 10.1097/MNH.0b013e328335f91f.
11. Speed JS, Pollock DM. Endothelin, kidney disease, and hypertension. Hypertension. 2013;61:1142-1145. doi: 10.1161/HYPERTENSIONAHA.113.00595.
12. Alexander BT, Cockrell KL, Rinewalt AN, Herrington JN, Granger JP. Enhanced renal expression of preproendothelin mRNA during chronic angiotensin II hypertension. Am J Physiol Regul Integr Comp Physiol. 2001;280:R1388-R1392.
13. Yoshida K, Yasujima M, Kohzuki M, Kanazawa M, Yoshinaga K, Abe K. Endothelin-1 augments pressor response to angiotensin II infusion in rats. Hypertension. 1992;20:292-297. doi: 10.1161/01.HYP.20.3.292.
14. Kittikulsuth W, Sullivan JC, Pollock DM. ET-1 actions in the kidney: evidence for sex differences. Br J Pharmacol. 2013;168:318-326. doi: 10.1111/j.1476-5381.2012.01922.x.
15. Ojeda NB, Grigore D, Robertson EB, Alexander BT. Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension. 2007;50:679-685. doi: 10.1161/HYPERTENSIONAHA.107.091785.
16. Ojeda NB, Intapad S, Royals TP, Black JT, Dasinger JH, Tull FL, Alexander BT. Hypersensitivity to acute ANG II in female growth-restricted offspring is exacerbated by ovariectomy. Am J Physiol Regul Integr Comp Physiol. 2011;301:R1199-R1205. doi: 10.1152/ajpregu.00219.2011.
17. Loria AS, Yamamoto T, Pollock DM, Pollock JS. Early life stress induces renal dysfunction in adult male rats but not female rats. Am J Physiol Regul Integr Comp Physiol. 2013;304:R121-R129. doi: 10.1152/ajpregu.00364.2012.
18. Loria AS, Pollock DM, Pollock JS. Early life stress sensitizes rats to angiotensin II-induced hypertension and vascular inflammation in adult life. Hypertension. 2010;55:494-499. doi: 10.1161/HYPERTENSIONAHA.109.145391.
19. Bourque SL, Gragasin FS, Quon AL, Mansour Y, Morton JS, Davidge ST. Prenatal hypoxia causes long-term alterations in vascular endothelin-1 function in aged male, but not female, offspring. Hypertension. 2013;62:753-758. doi: 10.1161/HYPERTENSIONAHA.113.01516.
20. Woods LL, Ingelfinger JR, Rasch R. Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol. 2005;289:R1131-R1136. doi: 10.1152/ajpregu.00037.2003.
21. Xue B, Pamidimukkala J, Hay M. Sex differences in the development of angiotensin II-induced hypertension in conscious mice. Am J Physiol Heart Circ Physiol. 2005;288:H2177-H2184. doi: 10.1152/ajpheart.00969.2004.
22. Crofton JT, Share L. Gonadal hormones modulate deoxycorticosterone-salt hypertension in male and female rats. Hypertension. 1997;29(1 pt 2):494-499. doi: 10.1161/01.HYP.29.1.494.
23. Kittikulsuth W, Looney SW, Pollock DM. Endothelin ET(B) receptors contribute to sex differences in blood pressure elevation in angiotensin II hypertensive rats on a high-salt diet. Clin Exp Pharmacol Physiol. 2013;40:362-370. doi: 10.1111/1440-1681.12084.
24. Touyz RM, Turgeon A, Schiffrin EL. Endothelin-A-receptor blockade improves renal function and doubles the lifespan of stroke-prone spontaneously hypertensive rats. J Cardiovasc Pharmacol. 2000;36(5 suppl 1):S300-S304.
25. Yanes LL, Romero DG, Cucchiarelli VE, Fortepiani LA, Gomez-Sanchez CE, Santacruz F, Reckelhoff JF. Role of endothelin in mediating postmenopausal hypertension in a rat model. Am J Physiol Regul Integr Comp Physiol. 2005;288:R229-R233. doi: 10.1152/ajpregu.00697.2003.
26. Donato AJ, Gano LB, Eskurza I, Silver AE, Gates PE, Jablonski K, Seals DR. Vascular endothelial dysfunction with aging: endothelin-1 and endothelial nitric oxide synthase. Am J Physiol Heart Circ Physiol. 2009;297:H425-H432. doi: 10.1152/ajpheart.00689.2008.
27. Maturana MA, Breda V, Lhullier F, Spritzer PM. Relationship between endogenous testosterone and cardiovascular risk in early postmenopausal women. Metabolism. 2008;57:961-965. doi: 10.1016/j. metabol.2008.02.012.
28. Christakou C, Economou F, Livadas S, Piperi C, Adamopoulos C, Marinakis E, Jdiamanti-Kandarakis E. Strong and positive association of endothelin-1 with AGEs in PCOS: a causal relationship or a bystander? Hormones (Athens). 2011;10:292-297.
29. Pearson LJ, Yandle TG, Nicholls MG, Evans JJ. Regulation of endothelin-1 release from human endothelial cells by sex steroids and angiotensin-II. Peptides. 2008;29:1057-1061. doi: 10.1016/j.peptides.2008.02.003.
30. Riggleman A, Harvey J, Baylis C. Endothelin mediates some of the renal actions of acutely administered angiotensin II. Hypertension. 2001;38:105-109. doi: 10.1161/01.HYP.38.1.105.
31. Balakrishnan SM, Wang HD, Gopalakrishnan V, Wilson TW, McNeill JR. Effect of an endothelin antagonist on hemodynamic responses to angiotensin II. Hypertension. 1996;28:806-809. doi: 10.1161/01.HYP.28.5.806.
32. Bunkenburg B, van Amelsvoort T, Rogg H, Wood JM. Receptor-mediated effects of angiotensin II on growth of vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension. 1992;20:746-754. doi: 10.1161/01.HYP.20.6.746.
33. Sahajpal V, Ashton N. Increased glomerular angiotensin II binding in rats exposed to a maternal low protein diet in utero. J Physiol. 2005;563(pt 1):193-201. doi: 10.1113/jphysiol.2004.078642.
34. Sahajpal V, Ashton N. Renal function and angiotensin AT1 receptor expression in young rats following intrauterine exposure to a maternal low-protein diet. Clin Sci (Lond). 2003;104:607-614. doi: 10.1042/CS20020355.
35. Grigore D, Ojeda NB, Robertson EB, Dawson AS, Huffman CA, Bourassa EA, Speth RC, Brosnihan KB, Alexander BT. Placental insufficiency results in temporal alterations in the renin angiotensin system in male hypertensive growth restricted offspring. Am J Physiol Regul Integr Comp Physiol. 2007;293:R804-R811. doi: 10.1152/ajpregu.00725.2006.
36. Oriji GK, Keiser HR. Protein kinase C mediates angiotensin II-induced contractions and the release of endothelin and prostacyclin in rat aortic rings. Prostaglandins Leukot Essent Fatty Acids. 1997;57:135-141.
37. Taylor TA, Gariepy CE, Pollock DM, Pollock JS. Gender differences in ET and NOS systems in ETB receptor-deficient rats: effect of a high salt diet. Hypertension. 2003;41(3 pt 2):657-662. doi: 10.1161/01. HYP.0000048193.85814.78.
38. Jin C, Speed JS, Hyndman KA, O'Connor PM, Pollock DM. Sex differences in ET-1 receptor expression and Ca2+ signaling in the IMCD. Am J Physiol Renal Physiol. 2013;305:F1099-F1104. doi: 10.1152/ajprenal.00400.2013.
39. Sullivan JC, Goodchild TT, Cai Z, Pollock DM, Pollock JS. Endothelin(A) (ET(A)) and ET(B) receptor-mediated regulation of nitric oxide synthase 1 (NOS1) and NOS3 isoforms in the renal inner medulla. Acta Physiol (Oxf). 2007;191:329-336. doi: 10.1111/j.1748-1716.2007.01754.x.
40. Hodgin JB, Knowles JW, Kim HS, Smithies O, Maeda N. Interactions between endothelial nitric oxide synthase and sex hormones in vascular protection in mice. J Clin Invest. 2002;109:541-548. doi: 10.1172/JCI14066.
41. Reckelhoff JF, Hennington BS, Moore AG, Blanchard EJ, Cameron J. Gender differences in the renal nitric oxide (NO) system: dissociation between expression of endothelial NO synthase and renal hemodynamic response to NO synthase inhibition. Am J Hypertens. 1998;11(1 pt 1):97-104.
42. Hage FG, Mansur SJ, Xing D, Oparil S. Hypertension in women. Kidney Int Suppl (2011). 2013;3:352-356. doi: 10.1038/kisup.2013.76.
43. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298:564-567.
44. Vos LE, Oren A, Bots ML, Gorissen WH, Grobbee DE, Uiterwaal CS. Birth size and coronary heart disease risk score in young adulthood. The Atherosclerosis Risk in Young Adults (ARYA) study. Eur J Epidemiol. 2006;21:33-38. doi: 10.1007/s10654-005-4658-8.