Sexual dimorphism in rodent models of hypertension and atherosclerosis

British Journal of Pharmacology

Volumn 167, Issue 2, 2012, Pages 298-312

  Bubb, Kristen J ^a   Khambata, Rayomand S ^a   Ahluwalia, Amrita ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

angiotensin; apolipoprotein; blood pressure; Dahl; deoxycorticosterone; gender; low density lipoprotein; mouse; oestrogen; rat; SHR; testosterone

Indexed keywords

ALDOSTERONE; ANGIOTENSIN; ANGIOTENSIN II; APOLIPOPROTEIN E; AROMATASE; CHOLESTEROL; DEOXYCORTICOSTERONE ACETATE; ESTROGEN; ESTROGEN RECEPTOR BETA; FRACTALKINE; LOW DENSITY LIPOPROTEIN RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PADGEM PROTEIN; RENIN; TESTOSTERONE; VASCULAR CELL ADHESION MOLECULE 1; VASOPRESSIN;

ATHEROSCLEROSIS; BLOOD PRESSURE MEASUREMENT; CASTRATION; DAHL SALT SENSITIVE RAT; DIASTOLIC BLOOD PRESSURE; DISEASE MODEL; ENDOTHELIAL DYSFUNCTION; ESSENTIAL HYPERTENSION; FEMALE; GENETICALLY HYPERTENSIVE RAT; HYPERTENSION; KNOCKOUT MOUSE; MALE; MEDICAL RESEARCH; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT STRAIN; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SEX CHROMOSOME; SEX DIFFERENCE; SPONTANEOUSLY HYPERTENSIVE RAT; SRY GENE; SYSTOLIC BLOOD PRESSURE; TELEMETRY;

ANIMALS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; FEMALE; HYPERTENSION; MALE; RODENTIA; SEX FACTORS;

EID: 84865442743     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02036.x     Document Type: Review

References (140)

1. Adams MR, Kaplan JR, Clarkson TB, Koritnik DR, (1985). Ovariectomy, social status, and atherosclerosis in cynomolgus monkeys. Arteriosclerosis 5: 192-200. (Pubitemid 15145376)
2. Alexander BT, (2003). Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41: 457-462. (Pubitemid 36314616)
3. Arai T, Wang N, Bezouevski M, Welch C, Tall AR, (1999). Decreased atherosclerosis in heterozygous low density lipoprotein receptor-deficient mice expressing the scavenger receptor BI transgene. J Biol Chem 274: 2366-2371.
4. Arias-Loza PA, Hu K, Dienesch C, Mehlich AM, Konig S, Jazbutyte V, et al,. (2007). Both estrogen receptor subtypes, alpha and beta, attenuate cardiovascular remodeling in aldosterone salt-treated rats. Hypertension 50: 432-438. (Pubitemid 47205796)
5. Ashraf MS, Vongpatanasin W, (2006). Estrogen and hypertension. Curr Hypertens Rep 8: 368-376. (Pubitemid 44463720)
6. Ashton N, Balment RJ, (1991). Sexual dimorphism in renal function and hormonal status of New Zealand genetically hypertensive rats. Acta Endocrinol (Copenh) 124: 91-97.
7. Barrett-Connor E, (1997). Sex differences in coronary heart disease. Why are women so superior? The 1995 Ancel Keys Lecture. Circulation 95: 252-264. (Pubitemid 27029969)
8. Bayorh MA, Eatman D, Walton M, Socci RR, Thierry-Palmer M, Emmett N, (2002). 1A-779 attenuates angiotensin-(1-7) depressor response in salt-induced hypertensive rats. Peptides 23: 57-64. (Pubitemid 34113763)
9. Beierwaltes WH, Arendshorst WJ, Klemmer PJ, (1982). Electrolyte and water balance in young spontaneously hypertensive rats. Hypertension 4: 908-915. (Pubitemid 13176960)
10. Bhatnagar D, Soran H, Durrington PN, (2008). Hypercholesterolaemia and its management. BMJ 337: a993.
11. Bird JE, Moreland S, Waldron TL, Powell JR, (1995). Antihypertensive effects of a novel endothelin-A receptor antagonist in rats. Hypertension 25: 1191-1195.
12. Bourassa PA, Milos PM, Gaynor BJ, Breslow JL, Aiello RJ, (1996). Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A 93: 10022-10027.
13. Buja LM, Kita T, Goldstein JL, Watanabe Y, Brown MS, (1983). Cellular pathology of progressive atherosclerosis in the WHHL rabbit. An animal model of familial hypercholesterolemia. Arteriosclerosis 3: 87-101. (Pubitemid 13083095)
14. Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, et al,. (1995). Prevalence of hypertension in the US adult population. Results from the Third National Health and Nutrition Examination Survey, 1988-1991. Hypertension 25: 305-313.
15. Calhoun DA, Zhu ST, Chen YF, Oparil S, (1995). Gender and dietary NaCl in spontaneously hypertensive and Wistar-Kyoto rats. Hypertension 26: 285-289.
16. Caligiuri G, Nicoletti A, Zhou X, Tornberg I, Hansson GK, (1999). Effects of sex and age on atherosclerosis and autoimmunity in apoE-deficient mice. Atherosclerosis 145: 301-308. (Pubitemid 29359138)
17. Champagne C, Yoshinari N, Oetjen JA, Riche EL, Beck JD, Offenbacher S, (2009). Gender differences in systemic inflammation and atheroma formation following Porphyromonas gingivalis infection in heterozygous apolipoprotein E-deficient mice. J Periodontal Res 44: 569-577.
18. Chan V, Fenning A, Levick SP, Loch D, Chunduri P, Iyer A, et al,. (2011). Cardiovascular changes during maturation and ageing in male and female spontaneously hypertensive rats. J Cardiovasc Pharmacol 57: 469-478.
19. Charchar FJ, Tomaszewski M, Strahorn P, Champagne B, Dominiczak AF, (2003). Y is there a risk to being male? Trends Endocrinol Metab 14: 163-168. (Pubitemid 36733901)
20. Chen YF, Meng QC, (1991). Sexual dimorphism of blood pressure in spontaneously hypertensive rats is androgen dependent. Life Sci 48: 85-96.
21. Cook DN, Chen SC, Sullivan LM, Manfra DJ, Wiekowski MT, Prosser DM, et al,. (2001). Generation and analysis of mice lacking the chemokine fractalkine. Mol Cell Biol 21: 3159-3165. (Pubitemid 32298382)
22. Crofton JT, Share L, (1997). Gonadal hormones modulate deoxycorticosterone-salt hypertension in male and female rats. Hypertension 29 (Pt 2): 494-499. (Pubitemid 27074089)
23. Crofton JT, Share L, Brooks DP, (1989). Gonadectomy abolishes the sexual dimorphism in DOC-salt hypertension in the rat. Clin Exp Hypertens A 11: 1249-1261. (Pubitemid 19228214)
24. Dahl LK, Knudsen KD, Ohanian EV, Muirhead M, Tuthill R, (1975). Role of the gonads in hypertension-prone rats. J Exp Med 142: 748-759.
25. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, et al,. (2011). National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378: 31-40.
26. David FL, Carvalho MH, Cobra AL, Nigro D, Fortes ZB, Reboucas NA, et al,. (2001). Ovarian hormones modulate endothelin-1 vascular reactivity and mRNA expression in DOCA-salt hypertensive rats. Hypertension 38 (Pt 2): 692-696.
27. David FL, Montezano AC, Reboucas NA, Nigro D, Fortes ZB, Carvalho MH, et al,. (2002). Gender differences in vascular expression of endothelin and ET(A)/ET(B) receptors, but not in calcium handling mechanisms, in deoxycorticosterone acetate-salt hypertension. Braz J Med Biol Res 35: 1061-1068. (Pubitemid 35476804)
28. Dawson TC, Kuziel WA, Osahar TA, Maeda N, (1999). Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 143: 205-211. (Pubitemid 29138720)
29. Denton KM, Flower RL, Stevenson KM, Anderson WP, (2003). Adult rabbit offspring of mothers with secondary hypertension have increased blood pressure. Hypertension 41 (Pt 2): 634-639. (Pubitemid 36314566)
30. Doggrell SA, Brown L, (1998). Rat models of hypertension, cardiac hypertrophy and failure. Cardiovasc Res 39: 89-105. (Pubitemid 28322382)
31. Dong ZM, Chapman SM, Brown AA, Frenette PS, Hynes RO, Wagner DD, (1998). The combined role of P- and E-selectins in atherosclerosis. J Clin Invest 102: 145-152. (Pubitemid 28323841)
32. Dubey RK, Imthurn B, Zacharia LC, Jackson EK, (2004). Hormone replacement therapy and cardiovascular disease: what went wrong and where do we go from here? Hypertension 44: 789-795. (Pubitemid 39577398)
33. Eatman D, Wang M, Socci RR, Thierry-Palmer M, Emmett N, Bayorh MA, (2001). Gender differences in the attenuation of salt-induced hypertension by angiotensin (1-7). Peptides 22: 927-933. (Pubitemid 32522970)
34. Elhage R, Arnal JF, Pieraggi MT, Duverger N, Fievet C, Faye JC, et al,. (1997). 17 beta-estradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 17: 2679-2684. (Pubitemid 28016008)
35. Ely DL, Turner ME, (1990). Hypertension in the spontaneously hypertensive rat is linked to the Y chromosome. Hypertension 16: 277-281. (Pubitemid 20313289)
36. Fischer M, Baessler A, Schunkert H, (2002). Renin angiotensin system and gender differences in the cardiovascular system. Cardiovasc Res 53: 672-677. (Pubitemid 34175260)
37. Fisher CR, Graves KH, Parlow AF, Simpson ER, (1998). Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci U S A 95: 6965-6970. (Pubitemid 28278090)
38. Gilbert JS, Nijland MJ, (2008). Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Heart Circ Physiol 295: R1941-R1952.
39. Gluckman PD, Hanson MA, Cooper C, Thornburg KL, (2008). Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359: 61-73.
40. Gourdy P, Mallat Z, Castano C, Garmy-Susini B, Mac Gregor JL, Tedgui A, et al,. (2003). The atheroprotective effect of 17 beta-estradiol is not altered in P-selectin- or ICAM-1-deficient hypercholesterolemic mice. Atherosclerosis 166: 41-48. (Pubitemid 35449599)
41. Grady D, Herrington D, Bittner V, Blumenthal R, Davidson M, Hlatky M, et al,. (2002). Cardiovascular disease outcomes during 6.8 years of hormone therapy: heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA 288: 49-57. (Pubitemid 34705518)
42. Grimsditch DC, Penfold S, Latcham J, Vidgeon-Hart M, Groot PH, Benson GM, (2000). C3H apoE(-/-) mice have less atherosclerosis than C57BL apoE(-/-) mice despite having a more atherogenic serum lipid profile. Atherosclerosis 151: 389-397. (Pubitemid 30618755)
43. Harrap SB, Van der Merwe WM, Griffin SA, Macpherson F, Lever AF, (1990). Brief angiotensin converting enzyme inhibitor treatment in young spontaneously hypertensive rats reduces blood pressure long-term. Hypertension 16: 603-614.
44. Harrison-Bernard LM, Schulman IH, Raij L, (2003). Postovariectomy hypertension is linked to increased renal AT1 receptor and salt sensitivity. Hypertension 42: 1157-1163. (Pubitemid 37549071)
45. Hayashi T, Fukuto JM, Ignarro LJ, Chaudhuri G, (1995). Gender differences in atherosclerosis: possible role of nitric oxide. J Cardiovasc Pharmacol 26: 792-802.
46. Hayashi T, Esaki T, Sumi D, Mukherjee T, Iguchi A, Chaudhuri G, (2006). Modulating role of estradiol on arginase II expression in hyperlipidemic rabbits as an atheroprotective mechanism. Proc Natl Acad Sci U S A 103: 10485-10490. (Pubitemid 44051193)
47. Haywood JR, Hinojosa-Laborde C, (1997). Sexual dimorphism of sodium-sensitive renal-wrap hypertension. Hypertension 30 (Pt 2): 667-671. (Pubitemid 27444252)
48. Hinojosa-Laborde C, Craig T, Zheng W, Ji H, Haywood JR, Sandberg K, (2004). Ovariectomy augments hypertension in aging female Dahl salt-sensitive rats. Hypertension 44: 405-409. (Pubitemid 39281487)
49. Hoeg JM, Willis LR, Weinberger MH, (1977). Estrogen attenuation of the development of hypertension in spontaneously hypertensive rats. Am J Physiol 233: H369-H373.
50. Huxley R, Woodward M, (2011). Cigarette smoking as a risk factor for coronary heart disease in women compared with men: a systematic review and meta-analysis of prospective cohort studies. Lancet 378: 1297-1305.
51. Iams SG, Wexler BC, (1977). Retardation in the development of spontaneous hypertension in SH rats by gonadectomy. J Lab Clin Med 90: 997-1003. (Pubitemid 8235973)
52. Ji H, Zheng W, Wu X, Liu J, Ecelbarger CM, Watkins R, et al,. (2010). Sex chromosome effects unmasked in angiotensin II-induced hypertension. Hypertension 55: 1275-1282.
53. Johnson RC, Chapman SM, Dong ZM, Ordovas JM, Mayadas TN, Herz J, et al,. (1997). Absence of P-selectin delays fatty streak formation in mice. J Clin Invest 99: 1037-1043. (Pubitemid 27123641)
54. Kannel WB, Hjortland MC, McNamara PM, Gordon T, (1976). Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med 85: 447-452.
55. Kapil V, Milsom AB, Okorie M, Maleki-Toyserkani S, Akram F, Rehman F, et al,. (2010). Inorganic nitrate supplementation lowers blood pressure in humans: role for nitrite-derived NO. Hypertension 56: 274-281.
56. Karatas A, Hegner B, de Windt LJ, Luft FC, Schubert C, Gross V, et al,. (2008). Deoxycorticosterone acetate-salt mice exhibit blood pressure-independent sexual dimorphism. Hypertension 51: 1177-1183. (Pubitemid 351398989)
57. Kaushik M, Sontineni SP, Hunter C, (2010). Cardiovascular disease and androgens: a review. Int J Cardiol 142: 8-14.
58. Khan IY, Taylor PD, Dekou V, Seed PT, Lakasing L, Graham D, et al,. (2003). Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41: 168-175. (Pubitemid 36056810)
59. Kienitz T, Quinkler M, (2008). Testosterone and blood pressure regulation. Kidney Blood Press Res 31: 71-79. (Pubitemid 351630063)
60. Kobori H, Nishiyama A, Abe Y, Navar LG, (2003). Enhancement of intrarenal angiotensinogen in Dahl salt-sensitive rats on high salt diet. Hypertension 41: 592-597. (Pubitemid 36314637)
61. Koike G, Horiuchi M, Yamada T, Szpirer C, Jacob HJ, Dzau VJ, (1994). 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. (Pubitemid 24321580)
62. Lariviere R, Day R, Schiffrin EL, (1993a). Increased expression of endothelin-1 gene in blood vessels of deoxycorticosterone acetate-salt hypertensive rats. Hypertension 21 (Pt 2): 916-920. (Pubitemid 23166939)
63. Lariviere R, Thibault G, Schiffrin EL, (1993b). Increased endothelin-1 content in blood vessels of deoxycorticosterone acetate-salt hypertensive but not in spontaneously hypertensive rats. Hypertension 21: 294-300. (Pubitemid 23065167)
64. Lee MA, Bohm M, Paul M, Bader M, Ganten U, Ganten D, (1996). Physiological characterization of the hypertensive transgenic rat TGR(mREN2)27. Am J Physiol 270 (Pt 1): E919-E929. (Pubitemid 26298572)
65. Lerman LO, Chade AR, Sica V, Napoli C, (2005). Animal models of hypertension: an overview. J Lab Clin Med 146: 160-173. (Pubitemid 41208265)
66. Lerner DJ, Kannel WB, (1986). Patterns of coronary heart disease morbidity and mortality in the sexes: a 26-year follow-up of the Framingham population. Am Heart J 111: 383-390. (Pubitemid 16107280)
67. Libby P, Okamoto Y, Rocha VZ, Folco E, (2010). Inflammation in atherosclerosis: transition from theory to practice. Circ J 74: 213-220.
68. Lucas AD, Bursill C, Guzik TJ, Sadowski J, Channon KM, Greaves DR, (2003). Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1). Circulation 108: 2498-2504. (Pubitemid 37444412)
69. Maeda N, Johnson L, Kim S, Hagaman J, Friedman M, Reddick R, (2007). Anatomical differences and atherosclerosis in apolipoprotein E-deficient mice with 129/SvEv and C57BL/6 genetic backgrounds. Atherosclerosis 195: 75-82. (Pubitemid 47561948)
70. Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germano G, et al,. (2007). 2007 Guidelines for the Management of Arterial Hypertension: the Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). J Hypertens 25: 1105-1187. (Pubitemid 46924065)
71. Manson JE, Allison MA, Rossouw JE, Carr JJ, Langer RD, Hsia J, et al,. (2007). Estrogen therapy and coronary-artery calcification. N Engl J Med 356: 2591-2602. (Pubitemid 46961004)
72. Marques FZ, Campain AE, Yang YH, Morris BJ, (2010). Meta-analysis of genome-wide gene expression differences in onset and maintenance phases of genetic hypertension. Hypertension 56: 319-324.
73. Marsh MM, Walker VR, Curtiss LK, Banka CL, (1999). Protection against atherosclerosis by estrogen is independent of plasma cholesterol levels in LDL receptor-deficient mice. J Lipid Res 40: 893-900. (Pubitemid 29220530)
74. Mayadas TN, Johnson RC, Rayburn H, Hynes RO, Wagner DD, (1993). Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell 74: 541-554. (Pubitemid 23244619)
75. Mikkola TS, Clarkson TB, (2002). Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc Res 53: 605-619. (Pubitemid 34175253)
76. Mukherjee TK, Dinh H, Chaudhuri G, Nathan L, (2002). Testosterone attenuates expression of vascular cell adhesion molecule-1 by conversion to estradiol by aromatase in endothelial cells: implications in atherosclerosis. Proc Natl Acad Sci U S A 99: 4055-4060. (Pubitemid 34252228)
77. Murphy E, Steenbergen C, (2007). Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res 75: 478-486. (Pubitemid 47080962)
78. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R, (1994). ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 14: 133-140.
79. Nelken NA, Coughlin SR, Gordon D, Wilcox JN, (1991). Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest 88: 1121-1127.
80. O'Brien KD, McDonald TO, Chait A, Allen MD, Alpers CE, (1996). Neovascular expression of E-selectin, intercellular adhesion molecule-1, and vascular cell adhesion molecule-1 in human atherosclerosis and their relation to intimal leukocyte content. Circulation 93: 672-682. (Pubitemid 26052452)
81. Ojeda NB, Grigore D, Yanes LL, Iliescu R, Robertson EB, Zhang H, et al,. (2007). Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am J Physiol Heart Circ Physiol 292: R758-R763. (Pubitemid 46207727)
82. Orshal JM, Khalil RA, (2004). Gender, sex hormones, and vascular tone. Am J Physiol Heart Circ Physiol 286: R233-R249. (Pubitemid 38140366)
83. Ouchi Y, Share L, Crofton JT, Iitake K, Brooks DP, (1987). Sex difference in the development of deoxycorticosterone-salt hypertension in the rat. Hypertension 9: 172-177. (Pubitemid 17027831)
84. Ozaki T, Nishina H, Hanson MA, Poston L, (2001). Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 530 (Pt 1): 141-152. (Pubitemid 32998894)
85. Pendergrass KD, Pirro NT, Westwood BM, Ferrario CM, Brosnihan KB, Chappell MC, (2008). 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.
86. Pereira TM, Nogueira BV, Lima LC, Porto ML, Arruda JA, Vasquez EC, et al,. (2010). Cardiac and vascular changes in elderly atherosclerotic mice: the influence of gender. Lipids Health Dis 9: 87-96.
87. Perez-Lopez FR, Larrad-Mur L, Kallen A, Chedraui P, Taylor HS, (2010). Gender differences in cardiovascular disease: hormonal and biochemical influences. Reprod Sci 17: 511-531.
88. Pinto YM, Paul M, Ganten D, (1998). Lessons from rat models of hypertension: from Goldblatt to genetic engineering. Cardiovasc Res 39: 77-88. (Pubitemid 28322381)
89. Reckelhoff JF, Zhang H, Granger JP, (1998). Testosterone exacerbates hypertension and reduces pressure-natriuresis in male spontaneously hypertensive rats. Hypertension 31 (Pt 2): 435-439.
90. Reckelhoff JF, Zhang H, Srivastava K, (2000). Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension 35: 480-483. (Pubitemid 30054220)
91. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, et al,. (2011). Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation 123: e18-e209.
92. Rosenfeld ME, Campbell LA, (2011). Pathogens and atherosclerosis: update on the potential contribution of multiple infectious organisms to the pathogenesis of atherosclerosis. Thromb Haemost 106: 858-867.
93. Ross R, (1999). Atherosclerosis-an inflammatory disease. N Engl J Med 340: 115-126. (Pubitemid 29054847)
94. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, et al,. (2002). Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333. (Pubitemid 34761611)
95. Sainz J, Osuna A, Wangensteen R, de Dios Luna J, Rodriguez-Gomez I, Duarte J, et al,. (2004). Role of sex, gonadectomy and sex hormones in the development of nitric oxide inhibition-induced hypertension. Exp Physiol 89: 155-162. (Pubitemid 38386592)
96. Sampson AK, Moritz KM, Jones ES, Flower RL, Widdop RE, Denton KM, (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.
97. Sampson AK, Jennings GL, Chin-Dusting JP, (2012). Y are males so difficult to understand?: a case where 'X' does not mark the spot. Hypertension 59: 525-531.
98. Sartori-Valinotti JC, Iliescu R, Yanes LL, Dorsett-Martin W, Reckelhoff JF, (2008). Sex differences in the pressor response to angiotensin II when the endogenous renin-angiotensin system is blocked. Hypertension 51: 1170-1176. (Pubitemid 351398978)
99. Schiffrin EL, Sventek P, Li JS, Turgeon A, Reudelhuber T, (1995). Antihypertensive effect of an endothelin receptor antagonist in DOCA-salt spontaneously hypertensive rats. Br J Pharmacol 115: 1377-1381.
100. Schulz E, Gori T, Munzel T, (2011). Oxidative stress and endothelial dysfunction in hypertension. Hypertens Res 34: 665-673.
101. Scotland RS, Madhani M, Chauhan S, Moncada S, Andresen J, Nilsson H, et al,. (2005). Investigation of vascular responses in endothelial nitric oxide synthase/cyclooxygenase-1 double-knockout mice: key role for endothelium-derived hyperpolarizing factor in the regulation of blood pressure in vivo. Circulation 111: 796-803. (Pubitemid 40259720)
102. Seidman DS, Laor A, Gale R, Stevenson DK, Mashiach S, Danon YL, (1991). Pre-eclampsia and offspring's blood pressure, cognitive ability and physical development at 17-years-of-age. Br J Obstet Gynaecol 98: 1009-1014.
103. Sharp BR, Jones SP, Rimmer DM, Lefer DJ, (2002). Differential response to myocardial reperfusion injury in eNOS-deficient mice. Am J Physiol Heart Circ Physiol 282: H2422-H2426. (Pubitemid 34663055)
104. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, et al,. (1996). Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 93: 13176-13181. (Pubitemid 26382789)
105. Silva-Antonialli MM, Tostes RC, Fernandes L, Fior-Chadi DR, Akamine EH, Carvalho MH, et al,. (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. (Pubitemid 38648973)
106. Simpson ER, Clyne C, Rubin G, Boon WC, Robertson K, Britt K, et al,. (2002). Aromatase-a brief overview. Annu Rev Physiol 64: 93-127. (Pubitemid 34259227)
107. Smith DD, Tan X, Tawfik O, Milne G, Stechschulte DJ, Dileepan KN, (2010). Increased aortic atherosclerotic plaque development in female apolipoprotein E-null mice is associated with elevated thromboxane A2 and decreased prostacyclin production. J Physiol Pharmacol 61: 309-316.
108. Smith JD, Breslow JL, (1997). The emergence of mouse models of atherosclerosis and their relevance to clinical research. J Intern Med 242: 99-109. (Pubitemid 27351607)
109. Song J, Kost CK Jr, Martin DS, (2006). Androgens augment renal vascular responses to ANG II in New Zealand genetically hypertensive rats. Am J Physiol Heart Circ Physiol 290: R1608-R1615. (Pubitemid 43830827)
110. Stampfer MJ, Colditz GA, Willett WC, Manson JE, Rosner B, Speizer FE, et al,. (1991). Postmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the nurses' health study. N Engl J Med 325: 756-762.
111. Stork S, von Schacky C, Angerer P, (2002). The effect of 17beta-estradiol on endothelial and inflammatory markers in postmenopausal women: a randomized, controlled trial. Atherosclerosis 165: 301-307. (Pubitemid 35333356)
112. Sullivan JC, Bhatia K, Yamamoto T, Elmarakby AA, (2010). Angiotensin (1-7) receptor antagonism equalizes angiotensin II-induced hypertension in male and female spontaneously hypertensive rats. Hypertension 56: 658-666.
113. Surra JC, Guillen N, Arbones-Mainar JM, Barranquero C, Navarro MA, Arnal C, et al,. (2010). Sex as a profound modifier of atherosclerotic lesion development in apolipoprotein E-deficient mice with different genetic backgrounds. J Atheroscler Thromb 17: 712-721.
114. Tabibiazar R, Wagner RA, Ashley EA, King JY, Ferrara R, Spin JM, et al,. (2005). Signature patterns of gene expression in mouse atherosclerosis and their correlation to human coronary disease. Physiol Genomics 22: 213-226. (Pubitemid 41356355)
115. Tangirala RK, Rubin EM, Palinski W, (1995). Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res 36: 2320-2328.
116. Tanzawa K, Shimada Y, Kuroda M, Tsujita Y, Arai M, Watanabe H, (1980). WHHL-rabbit: a low density lipoprotein receptor-deficient animal model for familial hypercholesterolemia. FEBS Lett 118: 81-84. (Pubitemid 11245469)
117. Tatchum-Talom R, Eyster KM, Martin DS, (2005). Sexual dimorphism in angiotensin II-induced hypertension and vascular alterations. Can J Physiol Pharmacol 83: 413-422. (Pubitemid 41003316)
118. Teupser D, Persky AD, Breslow JL, (2003). Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler Thromb Vasc Biol 23: 1907-1913. (Pubitemid 37254883)
119. Teupser D, Pavlides S, Tan M, Gutierrez-Ramos JC, Kolbeck R, Breslow JL, (2004). Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci U S A 101: 17795-17800. (Pubitemid 40051966)
120. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ, (2000). A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem 275: 33238-33243.
121. Touyz RM, Endemann D, He G, Li JS, Schiffrin EL, (1999). Role of AT2 receptors in angiotensin II-stimulated contraction of small mesenteric arteries in young SHR. Hypertension 33 (Pt 2): 366-372. (Pubitemid 29065686)
122. Turner ME, Farkas J, Dunmire J, Ely D, Milsted A, (2009). Which Sry locus is the hypertensive Y chromosome locus? Hypertension 53: 430-435.
123. Vaccarino V, Badimon L, Corti R, de Wit C, Dorobantu M, Hall A, et al,. (2011). Ischaemic heart disease in women: are there sex differences in pathophysiology and risk factors? Position paper from the working group on coronary pathophysiology and microcirculation of the European Society of Cardiology. Cardiovasc Res 90: 9-17.
124. VanderLaan PA, Reardon CA, Thisted RA, Getz GS, (2009). VLDL best predicts aortic root atherosclerosis in LDL receptor deficient mice. J Lipid Res 50: 376-385.
125. Villar IC, Hobbs AJ, Ahluwalia A, (2008). Sex differences in vascular function: implication of endothelium-derived hyperpolarizing factor. J Endocrinol 197: 447-462. (Pubitemid 351803950)
126. Villar IC, Scotland RS, Khambata RS, Chan M, Duchene J, Sampaio AL, et al,. (2011). Suppression of endothelial P-selectin expression contributes to reduced cell trafficking in females: an effect independent of NO and prostacyclin. Arterioscler Thromb Vasc Biol 31: 1075-1083.
127. Wassmann S, Baumer AT, Strehlow K, van Eickels M, Grohe C, Ahlbory K, et al,. (2001). Endothelial dysfunction and oxidative stress during estrogen deficiency in spontaneously hypertensive rats. Circulation 103: 435-441. (Pubitemid 32105985)
128. Wiinberg N, Hoegholm A, Christensen HR, Bang LE, Mikkelsen KL, Nielsen PE, et al,. (1995). 24-h ambulatory blood pressure in 352 normal Danish subjects, related to age and gender. Am J Hypertens 8 (Pt 1): 978-986.
129. Williams SP, Shackelford DP, Iams SG, Mustafa SJ, (1988). Endothelium-dependent relaxation in estrogen-treated spontaneously hypertensive rats. Eur J Pharmacol 145: 205-207. (Pubitemid 18028504)
130. Wilson PW, Garrison RJ, Castelli WP, (1985). Postmenopausal estrogen use, cigarette smoking, and cardiovascular morbidity in women over 50. The Framingham Study. N Engl J Med 313: 1038-1043. (Pubitemid 16243330)
131. Woods LL, Ingelfinger JR, Nyengaard JR, Rasch R, (2001). Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 49: 460-467. (Pubitemid 32274957)
132. Woods LL, Ingelfinger JR, Rasch R, (2005). Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Heart Circ Physiol 289: R1131-R1136. (Pubitemid 41397063)
133. Xue B, Pamidimukkala J, 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. (Pubitemid 40604103)
134. Xue B, Pamidimukkala J, Lubahn DB, 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. (Pubitemid 46572400)
135. Yanes LL, Romero DG, Iles JW, Iliescu R, Gomez-Sanchez C, Reckelhoff JF, (2006). Sexual dimorphism in the renin-angiotensin system in aging spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 291: R383-R390. (Pubitemid 44035645)
136. Yanes LL, Sartori-Valinotti JC, Iliescu R, Romero DG, Racusen LC, Zhang H, et al,. (2009). Testosterone-dependent hypertension and upregulation of intrarenal angiotensinogen in Dahl salt-sensitive rats. Am J Physiol Renal Physiol 296: F771-F779.
137. Yanes LL, Romero DG, Iliescu R, Zhang H, Davis D, Reckelhoff JF, (2010). Postmenopausal hypertension: role of the renin-angiotensin system. Hypertension 56: 359-363.
138. Youn BS, Mantel C, Broxmeyer HE, (2000). Chemokines, chemokine receptors and hematopoiesis. Immunol Rev 177: 150-174.
139. Zhan E, Keimig T, Xu J, Peterson E, Ding J, Wang F, et al,. (2008). Dose-dependent cardiac effect of oestrogen replacement in mice post-myocardial infarction. Exp Physiol 93: 982-993. (Pubitemid 352000276)
140. Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, et al,. (2002). Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science 295: 505-508. (Pubitemid 34101642)