Sex differences in the enhanced responsiveness to acute angiotensin II in growth-restricted rats: Role of fasudil, a Rho kinase inhibitor

American Journal of Physiology - Renal Physiology

Volumn 304, Issue 7, 2013, Pages

  Ojeda, Norma B ^a,b,c   Royals, Thomas P ^b   Alexander, Barbara T ^b,c  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Angiotensin II; Developmental programmed hypertension; Intrauterine growth restriction; Rho kinase; Sex differences

Indexed keywords

ANGIOTENSIN II; FASUDIL; RHO KINASE; 1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; DRUG DERIVATIVE; ENALAPRIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GLOMERULUS FILTRATION RATE; GONADECTOMY; HYPERTENSION; INTRAUTERINE GROWTH RETARDATION; KIDNEY BLOOD FLOW; KIDNEY FUNCTION; KIDNEY VASCULAR RESISTANCE; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PRESSOR RESPONSE; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; ANIMAL; CASTRATION; DRUG ANTAGONISM; DRUG EFFECT; HEMODYNAMICS; KIDNEY; KIDNEY CIRCULATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA INSUFFICIENCY; PREGNANCY; PRENATAL EXPOSURE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SEXUAL DEVELOPMENT; VASCULAR RESISTANCE;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANGIOTENSIN II; ANIMALS; BLOOD PRESSURE; CASTRATION; ENALAPRIL; FEMALE; FETAL GROWTH RETARDATION; GLOMERULAR FILTRATION RATE; HEMODYNAMICS; KIDNEY; MALE; PLACENTAL INSUFFICIENCY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RENAL CIRCULATION; RENIN-ANGIOTENSIN SYSTEM; RHO-ASSOCIATED KINASES; SEX CHARACTERISTICS; VASCULAR RESISTANCE;

MLCS; MLOWN;

EID: 84878233101     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00687.2012     Document Type: Article

References (45)

1. Alexander BT. Intrauterine growth restriction and reduced glomerular number: role of apoptosis. Am J Physiol Regul Integr Comp Physiol 285: R933-R934, 2003.
2. Alexander BT. Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41: 457-462, 2003.
3. Alexander BT, Hendon AE, Ferril G, Dwyer TM. Renal denervation abolishes hypertension in low-birth-weight offspring from pregnant rats with reduced uterine perfusion. Hypertension 45: 754-758, 2005.
4. Ferrario CM. ACE2: more of Ang-(1-7) or less Ang II? Curr Opin Nephrol Hypertens 20: 1-6, 2011.
5. Fibbi B, Filippi S, Morelli A, Vignozzi L, Silvestrini E, Chavalmane A, De Vita G, Marini M, Gacci M, Manieri C, Vannelli GB, Maggi M. Estrogens regulate humans and rabbit epididymal contractility through the RhoA/Rho-kinase pathway. J Sex Med 6: 2173-2186, 2009.
6. Franco Mdo C, Dantas AP, Akamine EH, Kawamoto EM, Fortes ZB, Scavone C, Tostes RC, Carvalho MH, Nigro D. Enhanced oxidative stress as a potential mechanism underlying the programming of hypertension in utero. J Cardiovasc Pharmacol 40: 501-509, 2002.
7. Gayard M, Guilluy C, Rousselle A, Viollet B, Henrion D, Pacaud P, Loirand G, Rolli-Derkinderen M. AMPK alpha 1-induced RhoA phos-phorylation mediates vasoprotective effect of estradiol. Arterioscler Thromb Vasc Biol 31: 2634-2642, 2011.
8. Goel A, Zhang Y, Anderson L, Rahimian R. Gender difference in rat aorta vasodilation after acute exposure to high glucose: involvement of protein kinase C beta and superoxide but not of Rho kinase. Cardiovasc Res 76: 351-360, 2007.
9. 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 293: R804-R811, 2007.
10. Guilluy C, Bregeon J, Toumaniantz G, Rolli-Derkinderen M, Retail-leau K, Loufrani L, Henrion D, Scalbert E, Bril A, Torres RM, Offermanns S, Pacaud P, Loirand G. The Rho exchange factor Arhgef1 mediates the effects of angiotensin II on vascular tone and blood pressure. Nat Med 16: 183-190, 2010.
11. Guyton AC, Coleman TG, Cowley AV Jr, Scheel KW, Manning RD Jr, Norman RA Jr. Arterial pressure regulation. Overriding dominance of the kidneys in long-term regulation and in hypertension. Am J Med 52: 584-594, 1972.
12. Hilliard LM, Jones ES, Steckelings UM, Unger T, Widdop RE, Denton KM. Sex-specific influence of angiotensin type 2 receptor stimulation on renal function: a novel therapeutic target for hypertension. Hypertension 59: 409-414, 2012.
13. Hilliard LM, Nematbakhsh M, Kett MM, Teichman E, Sampson AK, Widdop RE, Evans RG, Denton KM. Gender differences in pressure-natriuresis and renal autoregulation: role of the Angiotensin type 2 receptor. Hypertension 57: 275-282, 2011.
14. Ito K, Hirooka Y, Kimura Y, Sagara Y, Sunagawa K. Ovariectomy augments hypertension through rho-kinase activation in the brain stem in female spontaneously hypertensive rats. Hypertension 48: 651-657, 2006.
15. Lamireau D, Nuyt AM, Hou X, Bernier S, Beauchamp M, Gobeil F Jr, Lahaie I, Varma DR, Chemtob S. Altered vascular function in fetal programming of hypertension. Stroke 33: 2992-2998, 2002.
16. Lopez-Ruiz A, Sartori-Valinotti J, Yanes LL, Iliescu R, Reckelhoff JF. Sex differences in control of blood pressure: role of oxidative stress in hypertension in females. Am J Physiol Heart Circ Physiol 295: H466- H474, 2008.
17. Loria AS, Kang KT, Pollock DM, Pollock JS. Early life stress enhances angiotensin II-mediated vasoconstriction by reduced endothelial nitric oxide buffering capacity. Hypertension 58: 619-626, 2011.
18. Mazzuca MQ, Wlodek ME, Dragomir NM, Parkington HC, Tare M. Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol 588: 1997-2010, 2010.
19. Morton JS, Rueda-Clausen CF, Davidge ST. Mechanisms of endothe-lium-dependent vasodilation in male and female, young and aged offspring born growth restricted. Am J Physiol Regul Integr Comp Physiol 298: R930-R938, 2010.
20. Nguyen Dinh Cat A, Touyz RM. Cell signaling of angiotensin II on vascular tone: novel mechanisms. Curr Hypertens Rep 13: 122-128, 2011.
21. Nuno DW, Lamping KG. The role of rho kinase in sex-dependent vascular dysfunction in type 1 diabetes. Exp Diabetes Res 2010.
22. Ojeda NB. Low birth weight increases susceptibility to renal injury in a rat model of mild ischemia-reperfusion. Am J Physiol Renal Physiol 301: F420-F426, 2011.
23. Ojeda NB, Grigore D, Robertson EB, Alexander BT. Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension 50: 679-685, 2007.
24. 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 292: R758-R763, 2007.
25. Ojeda NB, Hennington BS, Williamson DT, Hill ML, Betson NE, Sartori-Valinotti JC, Reckelhoff JF, Royals TP, Alexander BT. Oxi-dative stress contributes to sex differences in blood pressure in adult growth-restricted offspring. Hypertension 60: 114-122, 2012.
26. 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 301: R1199-R1205, 2011.
27. 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 298: R1421-R1427, 2010.
28. Payne JA, Alexander BT, Khalil RA. Decreased endothelium-dependent NO-cGMP vascular relaxation and hypertension in growth-restricted rats on a high-salt diet. Hypertension 43: 420-427, 2004.
29. Rasch R, Skriver E, Woods LL. The role of the RAS in programming of adult hypertension. Acta Physiol Scand 181: 537-542, 2004.
30. 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.
31. Sandberg K, Ji H. Sex differences in primary hypertension. Biol Sex Differ 3: 7, 2012.
32. Schneider MP, Wach PF, Durley MK, Pollock JS, Pollock DM. Sex differences in acute ANG II-mediated hemodynamic responses in mice. Am J Physiol Regul Integr Comp Physiol 299: R899-R906, 2010.
33. Song J, Kost CK Jr, Martin DS. Androgens augment renal vascular responses to ANG II in New Zealand genetically hypertensive rats. Am J Physiol Regul Integr Comp Physiol 290: R1608-R1615, 2006.
34. 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 72: 456-463, 2006.
35. 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.
36. Touyz RM. Reactive oxygen species as mediators of calcium signaling by angiotensin II: implications in vascular physiology and pathophysiology. Antioxid Redox Signal 7: 1302-1314, 2005.
37. Viegas VU, Liu ZZ, Nikitina T, Perlewitz A, Zavaritskaya O, Schlichting J, Persson PB, Regitz-Zagrosek V, Patzak A, Sendeski MM. Angiotensin II type 2 receptor mediates sex differences in mice renal interlobar arteries response to angiotensin II. J Hypertens 30: 1791-1798, 2012.
38. Williams J, Bogwu J, Oyekan A. The role of the RhoA/Rho-kinase signaling pathway in renal vascular reactivity in endothelial nitric oxide synthase null mice. J Hypertens 24: 1429-1436, 2006.
39. Williams SJ, Campbell ME, McMillen IC, Davidge ST. Differential effects of maternal hypoxia or nutrient restriction on carotid and femoral vascular function in neonatal rats. Am J Physiol Regul Integr Comp Physiol 288: R360-R367, 2005.
40. Williams SJ, Hemmings DG, Mitchell JM, McMillen IC, Davidge ST. Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol 565: 125-135, 2005.
41. Woods LL. Fetal origins of adult hypertension: a renal mechanism? Curr Opin Nephrol Hypertens 9: 419-425, 2000.
42. Woods LL, Ingelfinger JR, Nyengaard JR, Rasch R. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 49: 460-467, 2001.
43. 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 289: R1131-R1136, 2005.
44. Xiao D, Huang X, Yang S, Zhang L. Antenatal nicotine induces heightened oxidative stress and vascular dysfunction in rat offspring. Br J Pharmacol 164: 1400-1409, 2011.
45. Xiao D, Xu Z, Huang X, Longo LD, Yang S, Zhang L. Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension 51: 1239-1247, 2008.