Epochs in the depressor/pressor balance of the renin-angiotensin system

Clinical Science

Volumn 130, Issue 10, 2016, Pages 761-771

  Colafella, Katrina M Mirabito ^a   Hilliard, Lucinda M ^a   Denton, Kate M ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Aging; Angiotensin receptors; Cardiovascular disease; Hypertension; Sex differences

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN 3 RECEPTOR; ANGIOTENSIN 4 RECEPTOR; ANGIOTENSIN 5 RECEPTOR; ANGIOTENSIN 6 RECEPTOR; ANGIOTENSIN 7 RECEPTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN RECEPTOR; UNCLASSIFIED DRUG; DIPEPTIDYL CARBOXYPEPTIDASE; VASOCONSTRICTOR AGENT;

ADULTHOOD; AGING; ARTERIAL PRESSURE; DEPRESSOR RESPONSE; HUMAN; KIDNEY DEVELOPMENT; NONHUMAN; PLASMA RENIN ACTIVITY; PREGNANCY; PRESSOR RESPONSE; PRIORITY JOURNAL; PUBERTY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SEX DIFFERENCE; VASOCONSTRICTION; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; KIDNEY DISEASES; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; BLOOD PRESSURE; HUMANS; KIDNEY DISEASES; PEPTIDYL-DIPEPTIDASE A; RENIN-ANGIOTENSIN SYSTEM; SEX CHARACTERISTICS; VASOCONSTRICTOR AGENTS;

EID: 84974593771     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150939     Document Type: Review

References (132)

1. Bosnyak, S., Jones, E.S., Christopoulos, A., Aguilar, M.I., Thomas, W.G. and Widdop, R.E. (2011) Relative affinity of angiotensin peptides and novel ligands at AT1 and AT2 receptors. Clin. Sci. 121, 297-303
2. Ingelfinger, J.R., Jung, F., Diamant, D., Haveran, L., Lee, E., Brem, A. and Tang, S.S. (1999) Rat proximal tubule cell line transformed with origin-defective SV40 DNA: autocrine Ang II feedback. Am. J. Physiol. 276, F218-F227
3. Donoghue, M., Hsieh, F., Baronas, E., Godbout, K., Gosselin, M., Stagliano, N., Donovan, M., Woolf, B., Robison, K., Jeyaseelan, R. et al. (2000) A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin. Circ. Res. 87, e1-e9
4. Ma, J., Lee, K.V. and Stafford, R.S. (2006) Changes in antihypertensive prescribing during US outpatient visits for uncomplicated hypertension between 1993 and 2004. Hypertension 48, 846-852
5. Castro, C.H., Santos, R.A., Ferreira, A.J., Bader, M., Alenina, N. and Almeida, A.P. (2005) Evidence for a functional interaction of the angiotensin-(1-7) receptor Mas with AT1 and AT2 receptors in the mouse heart. Hypertension 46, 937-942
6. Walters, P.E., Gaspari, T.A. and Widdop, R.E. (2005) Angiotensin-(1-7) acts as a vasodepressor agent via angiotensin II type 2 receptors in conscious rats. Hypertension 45, 960-966
7. Fogo, A. and Ichikawa, I. (1996) Renin angiotensin system in development of mice and men. Am. J. Pathol. 149, 1797-1801
8. Vinturache, A.E. and Smith, F.G. (2014) Angiotensin type 1 and type 2 receptors during ontogeny: cardiovascular and renal effects. Vascul. Pharmacol. 63, 145-154
9. Lumbers, E.R. (1995) Functions of the renin angiotensin system during development. Clin. Exp. Pharmacol. Physiol. 22, 499-505
10. Guron, G. and Friberg, P. (2000) An intact renin angiotensin system is a prerequisite for normal renal development. J. Hypertens. 18, 123-137
11. Davisson, R.L., Kim, H.S., Krege, J.H., Lager, D.J., Smithies, O. and Sigmund, C.D. (1997) Complementation of reduced survival, hypotension, and renal abnormalities in angiotensinogen-deficient mice by the human renin and human angiotensinogen genes. J. Clin. Invest. 99, 1258-1264
12. Esther, Jr, C.R., Howard, T.E., Marino, E.M., Goddard, J.M., Capecchi, M.R. and Bernstein, K.E. (1996) Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab. Invest. 74, 953-965
13. Niimura, F., Labosky, P.A., Kakuchi, J., Okubo, S., Yoshida, H., Oikawa, T., Ichiki, T., Naftilan, A.J., Fogo, A., Inagami, T. et al. (1995) Gene targeting in mice reveals a requirement for angiotensin in the development and maintenance of kidney morphology and growth factor regulation. J. Clin. Invest. 96, 2947-2954
14. Kim, H.S., Krege, J.H., Kluckman, K.D., Hagaman, J.R., Hodgin, J.B., Best, C.F., Jennette, J.C., Coffman, T.M., Maeda, N. and Smithies, O. (1995) Genetic control of blood pressure and the angiotensinogen locus. Proc. Natl. Acad. Sci. U.S.A. 92, 2735-2739
15. Oliverio, M.I., Madsen, K., Best, C.F., Ito, M., Maeda, N., Smithies, O. and Coffman, T.M. (1998) Renal growth and development in mice lacking AT1A receptors for angiotensin II. Am. J. Physiol. 274, F43-F50
16. Oliverio, M.I., Kim, H.S., Ito, M., Le, T., Audoly, L., Best, C.F., Hiller, S., Kluckman, K., Maeda, N., Smithies, O. et al. (1998) Reduced growth, abnormal kidney structure, and type 2 (AT2) angiotensin receptor-mediated blood pressure regulation in mice lacking both AT1A and AT1B receptors for angiotensin II. Proc. Natl. Acad. Sci. U.S.A. 95, 15496-15501
17. Bullo, M., Tschumi, S., Bucher, B.S., Bianchetti, M.G. and Simonetti, G.D. (2012) Pregnancy outcome following exposure to angiotensin-converting enzyme inhibitors or angiotensin receptor antagonists: a systematic review. Hypertension 60, 444-450
18. Hein, L., Barsh, G.S., Pratt, R.E., Dzau, V.J. and Kobilka, B.K. (1995) Behavioural and cardiovascular effects of disrupting the angiotensin II type-2 receptor in mice. Nature 377, 744-747
19. Ichiki, T., Labosky, P.A., Shiota, C., Okuyama, S., Imagawa, Y., Fogo, A., Niimura, F., Ichikawa, I., Hogan, B.L. and Inagami, T. (1995) Effects on blood pressure and exploratory behaviour of mice lacking angiotensin II type-2 receptor. Nature 377, 748-750
20. Gurley, S.B., Allred, A., Le, T.H., Griffiths, R., Mao, L., Philip, N., Haystead, T.A., Donoghue, M., Breitbart, R.E., Acton, S.L. et al. (2006) Altered blood pressure responses and normal cardiac phenotype in ACE2-null mice. J. Clin. Invest. 116, 2218-2225
21. Crackower, M.A., Sarao, R., Oudit, G.Y., Yagil, C., Kozieradzki, I., Scanga, S.E., Oliveira-dos-Santos, A.J., da Costa, J., Zhang, L., Pei, Y. et al. (2002) Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 417, 822-828
22. Alenina, N., Xu, P., Rentzsch, B., Patkin, E.L. and Bader, M. (2008) Genetically altered animal models for Mas and angiotensin-(1-7). Exp. Physiol. 93, 528-537
23. Gomez, R.A., Tufro-McReddie, A., Everett, A.D. and Pentz, E.S. (1993) Ontogeny of renin and AT1 receptor in the rat. Pediatr. Nephrol. 7, 635-638
24. Monument, M.J. and Smith, F.G. (2003) Age-dependent effects of captopril on the arterial baroreflex control of heart rate in conscious lambs. Exp. Physiol. 88, 761-768
25. Chappellaz, M.L. and Smith, F.G. (2007) Systemic and renal hemodynamic effects of the AT1 receptor antagonist, ZD7155, and the AT2 receptor antagonist, PD123319, in conscious lambs. Pflugers Arch. 453, 477-486
26. Brown, R.D., Hilliard, L.M., Mirabito, K.M., Firth, L.C., Moritz, K.M., Evans, R.G. and Denton, K.M. (2014) Reduced sensitivity of the renal vasculature to angiotensin II in young rats, the role of the angiotensin type 2 receptor. Pediatr. Res. 76, 448-452
27. Sampson, A.K., Moritz, K.M. and Denton, K.M. (2012) Postnatal ontogeny of angiotensin receptors and ACE2 in male and female rats. Gend. Med. 9, 21-32
28. Vinturache, A.E. and Smith, F.G. (2014) Do angiotensin type 2 receptors modulate haemodynamic effects of type 1 receptors in conscious newborn lambs? J. Renin. Angiotensin Aldosterone Syst. 15, 450-457
29. Moritz, K.M. and Wintour, E.M. (1999) Functional development of the meso-and metanephros. Pediatr. Nephrol. 13, 171-178
30. Merlet-Benichou, C., Gilbert, T., Muffat-Joly, M., Lelievre-Pegorier, M. and Leroy, B. (1994) Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr. Nephrol. 8, 175-180
31. Stevenson, K.M. and Lumbers, E.R. (1995) Effects of angiotensin II in fetal sheep and modification of its actions by indomethacin. J. Physiol. 487, 147-158
32. Schwepcke, A., Weber, F.D., Mormanova, Z., Cepissak, B. and Genzel-Boroviczeny, O. (2013) Microcirculatory mechanisms in postnatal hypotension affecting premature infants. Pediatr. Res. 74, 186-190
33. Ishiguro, A., Sekine, T., Suzuki, K., Kurishima, C., Ezaki, S., Kunikata, T., Sobajima, H. and Tamura, M. (2011) Changes in skin and subcutaneous perfusion in very low birth weight infants during the transitional period. Neonatology 100, 162-168
34. Stark, M.J., Clifton, V.L. and Wright, I.M. (2008) Microvascular flow, clinical illness severity and cardiovascular function in the preterm infant. Arch. Dis. Child Fetal. Neonatal Ed. 93, F271-F274
35. Stark, M.J., Clifton, V.L. and Wright, I.M. (2008) Sex-specific differences in peripheral microvascular blood flow in preterm infants. Pediatr. Res. 63, 415-419
36. Lee, M.H., Kang, D.R., Kim, H.C., Ahn, S.V., Khaw, K.T. and Suh, I. (2014) A 24-year follow-up study of blood pressure tracking from childhood to adulthood in Korea, the Kangwha Study. Yonsei Med. J. 55, 360-366
37. Bachmann, H., Horacek, U., Leowsky, M. and Hirche, H. (1987) Blood pressure in children and adolescents aged 4 to 18. Correlation of blood pressure values with age, sex, body height, body weight and skinfold thickness (Essen Blood Pressure Study). Monatsschr. Kinderheilkd. 135, 128-134
38. Kotchen, J.M., McKean, H.E. and Kotchen, T.A. (1982) Blood pressure trends with aging. Hypertension 4, III128-III134
39. Hilliard, L.M., Sampson, A.K., Brown, R.D. and Denton, K.M. (2013) The "his and hers" of the renin angiotensin system. Curr. Hypertens. Rep. 15, 71-79
40. Rogers, J.L., Mitchell, A.R., Maric, C., Sandberg, K., Myers, A. and Mulroney, S.E. (2007) 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
41. Armando, I., Jezova, M., Juorio, A.V., Terron, J.A., Falcon-Neri, A., Semino-Mora, C., Imboden, H. and Saavedra, J.M. (2002) Estrogen upregulates renal angiotensin II AT2 receptors. Am. J. Physiol. Renal Physiol. 283, F934-F943
42. Baiardi, G., Macova, M., Armando, I., Ando, H., Tyurmin, D. and Saavedra, J.M. (2005) Estrogen upregulates renal angiotensin II AT1 and AT2 receptors in the rat. Regul. Pept. 124, 7-17
43. Nickenig, G., Baumer, A.T., Grohe, C., Kahlert, S., Strehlow, K., Rosenkranz, S., Stablein, A., Beckers, F., Smits, J.F., Daemen, M.J. et al. (1998) Estrogen modulates AT1 receptor gene expression in vitro and in vivo. Circulation 97, 2197-2201
44. Sampson, A.K., Hilliard, L.M., Moritz, K.M., Thomas, M.C., Tikellis, C., Widdop, R.E. and Denton, K.M. (2012) 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
45. Macova, M., Armando, I., Zhou, J., Baiardi, G., Tyurmin, D., Larrayoz-Roldan, I.M. and Saavedra, J.M. (2008) Estrogen reduces aldosterone, upregulates adrenal angiotensin II AT2 receptors and normalizes adrenomedullary Fra-2 in ovariectomized rats. Neuroendocrinology 88, 276-286
46. Mirabito, K.M., Hilliard, L.M., Kett, M.M., Brown, R.D., Booth, S.C., Widdop, R.E., Moritz, K.M., Evans, R.G. and Denton, K.M. (2014) Sex-and age-related differences in the chronic pressure-natriuresis relationship, role of the angiotensin type 2 receptor. Am. J. Physiol. Renal Physiol. 307, F901-F907
47. Silva-Antonialli, M.M., Tostes, R.C., Fernandes, L., Fior-Chadi, D.R., Akamine, E.H., Carvalho, M.H., Fortes, Z.B. and Nigro, D. (2004) 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
48. Reckelhoff, J.F., Zhang, H. and Granger, J.P. (1998) Testosterone exacerbates hypertension and reduces pressure-natriuresis in male spontaneously hypertensive rats. Hypertension 31, 435-439
49. Pucell, A.G., Hodges, J.C., Sen, I., Bumpus, F.M. and Husain, A. (1991) Biochemical properties of the ovarian granulosa cell type 2-angiotensin II receptor. Endocrinology 128, 1947-1959
50. Yoshimura, Y., Karube, M., Aoki, H., Oda, T., Koyama, N., Nagai, A., Akimoto, Y., Hirano, H. and Nakamura, Y. (1996) Angiotensin II induces ovulation and oocyte maturation in rabbit ovaries via the AT2 receptor subtype. Endocrinology 137, 1204-1211
51. Leblanc, S., Battista, M.C., Noll, C., Hallberg, A., Gallo-Payet, N., Carpentier, A.C., Vine, D.F. and Baillargeon, J.P. (2014) Angiotensin II type 2 receptor stimulation improves fatty acid ovarian uptake and hyperandrogenemia in an obese rat model of polycystic ovary syndrome. Endocrinology 155, 3684-3693
52. Pilote, L., Dasgupta, K., Guru, V., Humphries, K.H., McGrath, J., Norris, C., Rabi, D., Tremblay, J., Alamian, A., Barnett, T. et al. (2007) A comprehensive view of sex-specific issues related to cardiovascular disease. CMAJ 176, S1-S44
53. Silbiger, S. and Neugarten, J. (2008) Gender and human chronic renal disease. Gend. Med. 5 (Suppl. A), S3-S10
54. Danser, A.H., Derkx, F.H., Schalekamp, M.A., Hense, H.W., Riegger, G.A. and Schunkert, H. (1998) Determinants of interindividual variation of renin and prorenin concentrations, evidence for a sexual dimorphism of (pro)renin levels in humans. J. Hypertens. 16, 853-862
55. Sullivan, J.C., Rodriguez-Miguelez, P., Zimmerman, M.A. and Harris, R.A. (2015) Differences in angiotensin (1-7) between men and women. Am. J. Physiol. Heart Circ. Physiol. 308, H1171-H1176
56. Miller, J.A., Anacta, L.A. and Cattran, D.C. (1999) Impact of gender on the renal response to angiotensin II. Kidney Int. 55, 278-285
57. Miller, J.A., Cherney, D.Z., Duncan, J.A., Lai, V., Burns, K.D., Kennedy, C.R., Zimpelmann, J., Gao, W., Cattran, D.C. and Scholey, J.W. (2006) Gender differences in the renal response to renin angiotensin system blockade. J. Am. Soc. Nephrol. 17, 2554-2560
58. Hudson, M., Rahme, E., Behlouli, H., Sheppard, R. and Pilote, L. (2007) Sex differences in the effectiveness of angiotensin receptor blockers and angiotensin converting enzyme inhibitors in patients with congestive heart failure-a population study. Eur. J. Heart Fail. 9, 602-609
59. Brown, R.D., Hilliard, L.M., Head, G.A., Jones, E.S., Widdop, R.E. and Denton, K.M. (2012) Sex differences in the pressor and tubuloglomerular feedback response to angiotensin II. Hypertension 59, 129-135
60. Sampson, A.K., Widdop, R.E. and Denton, K.M. (2008) Sex-differences in circadian blood pressure variations in response to chronic angiotensin II infusion in rats. Clin. Exp. Pharmacol. Physiol. 35, 391-395
61. Sampson, A.K., Moritz, K.M., Jones, E.S., Flower, R.L., Widdop, R.E. and Denton, K.M. (2008) 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
62. Xue, B., Pamidimukkala, J. and Hay, M. (2005) Sex differences in the development of angiotensin II-induced hypertension in conscious mice. Am. J. Physiol. Heart Circ. Physiol. 288, H2177-H2184
63. Tatchum-Talom, R., Eyster, K.M. and Martin, D.S. (2005) Sexual dimorphism in angiotensin II-induced hypertension and vascular alterations. Can. J. Physiol. Pharmacol. 83, 413-422
64. Schneider, M.P., Wach, P.F., Durley, M.K., Pollock, J.S. and Pollock, D.M. (2010) Sex differences in acute ANG II-mediated hemodynamic responses in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R899-R906
65. Mirabito, K.M., Hilliard, L.M., Head, G.A., Widdop, R.E. and Denton, K.M. (2014) Pressor responsiveness to angiotensin II in female mice is enhanced with age, role of the angiotensin type 2 receptor. Biol. Sex Differ. 5, 13
66. Padia, S.H., Kemp, B.A., Howell, N.L., Fournie-Zaluski, M.C., Roques, B.P. and Carey, R.M. (2008) Conversion of renal angiotensin II to angiotensin III is critical for AT2 receptor-mediated natriuresis in rats. Hypertension 51, 460-465
67. Padia, S.H., Kemp, B.A., Howell, N.L., Gildea, J.J., Keller, S.R. and Carey, R.M. (2009) Intrarenal angiotensin III infusion induces natriuresis and angiotensin type 2 receptor translocation in Wistar-Kyoto but not in spontaneously hypertensive rats. Hypertension 53, 338-343
68. Padia, S.H., Kemp, B.A., Howell, N.L., Siragy, H.M., Fournie-Zaluski, M.C., Roques, B.P. and Carey, R.M. (2007) Intrarenal aminopeptidase N inhibition augments natriuretic responses to angiotensin III in angiotensin type 1 receptor-blocked rats. Hypertension 49, 625-630
69. Liu, J., Ji, H., Zheng, W., Wu, X., Zhu, J.J., Arnold, A.P. and Sandberg, K. (2010) Sex differences in renal angiotensin converting enzyme 2 (ACE2) activity are 17beta-oestradiol-dependent and sex chromosome-independent. Biol. Sex Differ. 1, 6
70. Hilliard, L.M., Nematbakhsh, M., Kett, M.M., Teichman, E., Sampson, A.K., Widdop, R.E., Evans, R.G. and Denton, K.M. (2011) Gender differences in pressure-natriuresis and renal autoregulation, role of the angiotensin type 2 receptor. Hypertension 57, 275-282
71. Viegas, V.U., Liu, Z.Z., Nikitina, T., Perlewitz, A., Zavaritskaya, O., Schlichting, J., Persson, P.B., Regitz-Zagrosek, V., Patzak, A. and Sendeski, M.M. (2012) Angiotensin II type 2 receptor mediates sex differences in mice renal interlobar arteries response to angiotensin II. J. Hypertens. 30, 1791-1798
72. Hilliard, L.M., Chow, C.L., Mirabito, K.M., Steckelings, U.M., Unger, T., Widdop, R.E. and Denton, K.M. (2014) Angiotensin type 2 receptor stimulation increases renal function in female, but not male, spontaneously hypertensive rats. Hypertension 64, 378-383
73. Kemp, B.A., Howell, N.L., Gildea, J.J., Keller, S.R., Padia, S.H. and Carey, R.M. (2014) AT2 receptor activation induces natriuresis and lowers blood pressure. Circ. Res. 115, 388-399
74. Xue, B., Zhang, Z., Beltz, T.G., Guo, F., Hay, M. and Johnson, A.K. (2014) Estrogen regulation of the brain renin angiotensin system in protection against angiotensin II-induced sensitization of hypertension. Am. J. Physiol. Heart Circ. Physiol. 307, H191-H198
75. Xue, B., Pamidimukkala, J., Lubahn, D.B. and Hay, M. (2007) Estrogen receptor-alpha mediates estrogen protection from angiotensin II-induced hypertension in conscious female mice. Am. J. Physiol. Heart Circ. Physiol. 292, H1770-H1776
76. Abdulla, M.H. and Johns, E.J. (2014) Nitric oxide impacts on angiotensin AT2 receptor modulation of high-pressure baroreflex control of renal sympathetic nerve activity in anaesthetized rats. Acta Physiol. (Oxf.) 210, 832-844
77. Dai, S.Y., Peng, W., Zhang, Y.P., Li, J.D., Shen, Y. and Sun, X.F. (2015) Brain endogenous angiotensin II receptor type 2 protects against DOCA/salt-induced hypertension in female rats. J. Neuroinflammation 12, 47
78. Sullivan, J.C., Bhatia, K., Yamamoto, T. and Elmarakby, A.A. (2010) Angiotensin (1-7) receptor antagonism equalizes angiotensin II induced hypertension in male and female spontaneously hypertensive rats. Hypertension 56, 658-666
79. Bosnyak, S., Widdop, R.E., Denton, K.M. and Jones, E.S. (2012) Differential mechanisms of ang (1-7)-mediated vasodepressor effect in adult and aged candesartan-treated rats. Int. J. Hypertens. 2012, 192567
80. Safari, T., Nematbakhsh, M., Hilliard, L.M., Evans, R.G. and Denton, K.M. (2012) Sex differences in the renal vascular response to angiotensin II involves the Mas receptor. Acta Physiol. (Oxf.) 206, 150-156
81. Lewis, E.J., Hunsicker, L.G., Bain, R.P. and Rohde, R.D. (1993) The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N. Engl. J. Med. 329, 1456-1462
82. Li, P.K., Leung, C.B., Chow, K.M., Cheng, Y.L., Fung, S.K., Mak, S.K., Tang, A.W., Wong, T.Y., Yung, C.Y., Yung, J.C. et al. (2006) Hong Kong study using valsartan in IgA nephropathy (HKVIN), a double-blind, randomized, placebo-controlled study. Am. J. Kidney Dis. 47, 751-760
83. McCarthy, C.A., Widdop, R.E., Denton, K.M. and Jones, E.S. (2013) Update on the angiotensin AT2 receptor. Curr. Hypertens. Rep. 15, 25-30
84. Steckelings, U.M., Paulis, L., Namsolleck, P. and Unger, T. (2012) AT2 receptor agonists, hypertension and beyond. Curr. Opin. Nephrol. Hypertens. 21, 142-146
85. Foulquier, S., Steckelings, U.M. and Unger, T. (2012) Impact of the AT2 receptor agonist C21 on blood pressure and beyond. Curr. Hypertens. Rep. 14, 403-409
86. Wan, Y., Wallinder, C., Plouffe, B., Beaudry, H., Mahalingam, A.K., Wu, X., Johansson, B., Holm, M., Botoros, M., Karlen, A. et al. (2004) Design, synthesis, and biological evaluation of the first selective nonpeptide AT2 receptor agonist. J. Med. Chem. 47, 5995-6008
87. Bosnyak, S., Welungoda, I.K., Hallberg, A., Alterman, M., Widdop, R.E. and Jones, E.S. (2010) Stimulation of angiotensin AT2 receptors by the non-peptide agonist, compound 21, evokes vasodepressor effects in conscious spontaneously hypertensive rats. Br. J. Pharmacol. 159, 709-716
88. Oparil, S. and Schmieder, R.E. (2015) New approaches in the treatment of hypertension. Circ. Res. 116, 1074-1095
89. Chesley, L.C., Talledo, E., Bohler, C.S. and Zuspan, F.P. (1965) Vascular reactivity to angiotensin II and norepinephrine in pregnant women. Am. J. Obstet. Gynecol. 91, 837-842
90. Anton, L. and Brosnihan, K.B. (2008) Systemic and uteroplacental renin angiotensin system in normal and pre-eclamptic pregnancies. Ther. Adv. Cardiovasc. Dis. 2, 349-362
91. Hladunewich, M.A., Kingdom, J., Odutayo, A., Burns, K., Lai, V., O'Brien, T., Gandhi, S., Zimpelmann, J., Kiss, A., Miller, J. et al. (2011) Postpartum assessment of the renin angiotensin system in women with previous severe, early-onset preeclampsia. J. Clin. Endocrinol. Metab. 96, 3517-3524
92. Merrill, D.C., Karoly, M., Chen, K., Ferrario, C.M. and Brosnihan, K.B. (2002) Angiotensin-(1-7) in normal and preeclamptic pregnancy. Endocrine 18, 239-245
93. Zhou, A., Dekker, G.A., Lumbers, E.R., Lee, S.Y., Thompson, S.D., McCowan, L.M. and Roberts, C.T. (2013) The association of AGTR2 polymorphisms with preeclampsia and uterine artery bilateral notching is modulated by maternal BMI. Placenta 34, 75-81
94. Mirabito, K.M., Hilliard, L.M., Wei, Z., Tikellis, C., Widdop, R.E., Vinh, A. and Denton, K.M. (2014) Role of inflammation and the angiotensin type 2 receptor in the regulation of arterial pressure during pregnancy in mice. Hypertension 64, 626-631
95. Chen, K., Merrill, D.C. and Rose, J.C. (2007) The importance of angiotensin II subtype receptors for blood pressure control during mouse pregnancy. Reprod. Sci. 14, 694-704
96. Carey, L.C. and Rose, J.C. (2011) The midgestational maternal blood pressure decline is absent in mice lacking expression of the angiotensin II AT2 receptor. J. Renin Angiotensin Aldosterone Syst. 12, 29-35
97. Takeda-Matsubara, Y., Iwai, M., Cui, T.X., Shiuchi, T., Liu, H.W., Okumura, M., Ito, M. and Horiuchi, M. (2004) Roles of angiotensin type 1 and 2 receptors in pregnancy-associated blood pressure change. Am. J. Hypertens. 17, 684-689
98. Bharadwaj, M.S., Strawn, W.B., Groban, L., Yamaleyeva, L.M., Chappell, M.C., Horta, C., Atkins, K., Firmes, L., Gurley, S.B. and Brosnihan, K.B. (2011) Angiotensin-converting enzyme 2 deficiency is associated with impaired gestational weight gain and fetal growth restriction. Hypertension 58, 852-858
99. Yamaleyeva, L.M., Pulgar, V.M., Lindsey, S.H., Yamane, L., Varagic, J., McGee, C., daSilva, M., Lopes Bonfa, P., Gurley, S.B. and Brosnihan, K.B. (2015) Uterine artery dysfunction in pregnant ACE2 knockout mice is associated with placental hypoxia and reduced umbilical blood flow velocity. Am. J. Physiol. Endocrinol. Metab. 309, E84-E94
100. Neves, L.A., Stovall, K., Joyner, J., Valdes, G., Gallagher, P.E., Ferrario, C.M., Merrill, D.C. and Brosnihan, K.B. (2008) ACE2 and ANG-(1-7) in the rat uterus during early and late gestation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R151-R161
101. Anton, L., Merrill, D.C., Neves, L.A., Diz, D.I., Corthorn, J., Valdes, G., Stovall, K., Gallagher, P.E., Moorefield, C., Gruver, C. et al. (2009) The uterine placental bed renin angiotensin system in normal and preeclamptic pregnancy. Endocrinology 150, 4316-4325
102. Ferreira, V.M., Gomes, T.S., Reis, L.A., Ferreira, A.T., Razvickas, C.V., Schor, N. and Boim, M.A. (2009) Receptor-induced dilatation in the systemic and intrarenal adaptation to pregnancy in rats. PLoS One 4, e4845
103. Conrad, K.P. (2011) Emerging role of relaxin in the maternal adaptations to normal pregnancy, implications for preeclampsia. Semin. Nephrol. 31, 15-32
104. Hannan, R.E., Davis, E.A. and Widdop, R.E. (2003) Functional role of angiotensin II AT2 receptor in modulation of AT1 receptor-mediated contraction in rat uterine artery, involvement of bradykinin and nitric oxide. Br. J. Pharmacol. 140, 987-995
105. Jones, E.S., Vinh, A., McCarthy, C.A., Gaspari, T.A. and Widdop, R.E. (2008) AT2 receptors, functional relevance in cardiovascular disease. Pharmacol. Ther. 120, 292-316
106. Weiner, C.P., Lizasoain, I., Baylis, S.A., Knowles, R.G., Charles, I.G. and Moncada, S. (1994) Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc. Natl. Acad. Sci. U.S.A. 91, 5212-5216
107. Podymow, T. and August, P. (2008) Update on the use of antihypertensive drugs in pregnancy. Hypertension 51, 960-969
108. Stennett, A.K., Qiao, X., Falone, A.E., Koledova, V.V. and Khalil, R.A. (2009) Increased vascular angiotensin type 2 receptor expression and NOS-mediated mechanisms of vascular relaxation in pregnant rats. Am. J. Physiol. Heart Circ. Physiol. 296, H745-H755
109. Ong, K.L., Cheung, B.M.Y., Man, Y.B., Lau, C.P. and Lam, K.S.L. (2007) Prevalence, awareness, treatment, and control of hypertension among United States adults 1999-2004. Hypertension 49, 69-75
110. Kearney, P.M., Whelton, M., Reynolds, K., Muntner, P., Whelton, P.K. and He, J. (2005) Global burden of hypertension, analysis of worldwide data. Lancet 365, 217-223
111. Wiinberg, N., Hoegholm, A., Christensen, H.R., Bang, L.E., Mikkelsen, K.L., Nielsen, P.E., Svendsen, T.L., Kampmann, J.P., Madsen, N.H. and Bentzon, M.W. (1995) 24-h ambulatory blood pressure in 352 normal Danish subjects, related to age and gender. Am. J. Hypertens. 8, 978-986
112. Wassertheil-Smoller, S., Anderson, G., Psaty, B.M., Black, H.R., Manson, J., Wong, N., Francis, J., Grimm, R., Kotchen, T., Langer, R. et al. (2000) Hypertension and its treatment in postmenopausal women, baseline data from the Women's Health Initiative. Hypertension 36, 780-789
113. Yanes, L.L. and Reckelhoff, J.F. (2011) Postmenopausal hypertension. Am. J. Hypertens. 24, 740-749
114. Fentie, I.H., Greenwood, M.M., Wyss, J.M. and Clark, J.T. (2004) Age-related decreases in gonadal hormones in Long-Evans rats: relationship to rise in arterial pressure. Endocrine 25, 15-22
115. Fortepiani, L.A., Zhang, H., Racusen, L., Roberts, 2nd, L.J. and Reckelhoff, J.F. (2003) Characterization of an animal model of postmenopausal hypertension in spontaneously hypertensive rats. Hypertension 41, 640-645
116. Maric, C. (2009) Sex, diabetes and the kidney. Am. J. Physiol. Renal Physiol. 296, F680-F688
117. Baylis, C. (2008) Sexual dimorphism of the aging kidney: role of nitric oxide deficiency. Physiology 23, 142-150
118. Schunkert, H., Danser, A.H., Hense, H.W., Derkx, F.H., Kurzinger, S. and Riegger, G.A. (1997) Effects of estrogen replacement therapy on the renin angiotensin system in postmenopausal women. Circulation 95, 39-45
119. Okumura, M., Iwai, M., Nakaoka, H., Sone, H., Kanno, H., Senba, I., Ito, M. and Horiuchi, M. (2011) Possible involvement of AT2 receptor dysfunction in age-related gender difference in vascular remodeling. J. Am. Soc. Hypertens. 5, 76-84
120. Wray, D.W., Nishiyama, S.K., Harris, R.A. and Richardson, R.S. (2008) Angiotensin II in the elderly, impact of angiotensin II type 1 receptor sensitivity on peripheral hemodynamics. Hypertension 51, 1611-1616
121. Baylis, C. (2012) Sexual dimorphism, the aging kidney, involvement of nitric oxide deficiency and angiotensin II overactivity. J. Gerontol. A. Biol. Sci. Med. Sci. 67, 1365-1372
122. Cao, X.J. and Li, Y.F. (2009) Alteration of messenger RNA and protein levels of cardiac alpha(1)-adrenergic receptor and angiotensin II receptor subtypes during aging in rats. Can. J. Cardiol. 25, 415-420
123. Kang, A.K. and Miller, J.A. (2002) Effects of gender on the renin angiotensin system, blood pressure, and renal function. Curr. Hypertens. Rep. 4, 143-151
124. Harvey, P.J., Morris, B.L., Miller, J.A. and Floras, J.S. (2005) Estradiol induces discordant angiotensin and blood pressure responses to orthostasis in healthy postmenopausal women. Hypertension 45, 399-405
125. Yanes, L.L., Romero, D.G., Iliescu, R., Zhang, H., Davis, D. and Reckelhoff, J.F. (2010) Postmenopausal hypertension, role of the renin angiotensin system. Hypertension 56, 359-363
126. Hassager, C., Riis, B.J., Strom, V., Guyene, T.T. and Christiansen, C. (1987) The long-term effect of oral and percutaneous estradiol on plasma renin substrate and blood pressure. Circulation 76, 753-758
127. De Lignieres, B., Basdevant, A., Thomas, G., Thalabard, J.C., Mercier-Bodard, C., Conard, J., Guyene, T.T., Mairon, N., Corvol, P., Guy-Grand, B. et al. (1986) Biological effects of estradiol-17 beta in postmenopausal women, oral versus percutaneous administration. J. Clin. Endocrinol. Metab. 62, 536-541
128. Schulman, I.H., Zhou, M.S., Treuer, A.V., Chadipiralla, K., Hare, J.M. and Raij, L. (2010) Altered renal expression of angiotensin II receptors, renin receptor, and ACE-2 precede the development of renal fibrosis in aging rats. Am. J. Nephrol. 32, 249-261
129. Heymes, C., Silvestre, J.S., Llorens-Cortes, C., Chevalier, B., Marotte, F., Levy, B.I., Swynghedauw, B. and Samuel, J.L. (1998) Cardiac senescence is associated with enhanced expression of angiotensin II receptor subtypes. Endocrinology 139, 2579-2587
130. Proudler, A.J., Ahmed, A.I., Crook, D., Fogelman, I., Rymer, J.M. and Stevenson, J.C. (1995) Hormone replacement therapy and serum angiotensin converting enzyme activity in postmenopausal women. Lancet 346, 89-90
131. Groban, L., Pailes, N.A., Bennett, C.D., Carter, C.S., Chappell, M.C., Kitzman, D.W. and Sonntag, W.E. (2006) Growth hormone replacement attenuates diastolic dysfunction and cardiac angiotensin II expression in senescent rats. J. Gerontol. A Biol. Sci. Med. Sci. 61, 28-35
132. Hinojosa-Laborde, C., Craig, T., Zheng, W., Ji, H., Haywood, J.R. and Sandberg, K. (2004) Ovariectomy augments hypertension in aging female Dahl salt-sensitive rats. Hypertension 44, 405-409