Influence of Extra Virgin Olive Oil on Blood Pressure and Kidney Angiotensinase Activities in Spontaneously Hypertensive Rats

Abstract

High-fat diets are associated with the development of cardiovascular diseases. The efficacy of the current strategies of treatment is still not entirely satisfactory, and new approaches are being considered. To analyze the beneficial effects of extra virgin olive oil as a major component of the Mediterranean diet, we studied systolic blood pressure and angiotensinase activities, since this enzyme is involved in the metabolism of angiotensins, in the kidney of hypertensive rats fed during 12 weeks with a diet enriched with extra virgin olive oil compared with a standard diet. As a reflex of oxidative stress, 8-isoprostanes and nitric oxide were quantified in urine. Results demonstrated a progressive increase in systolic blood pressure until the end of the feeding period in both groups. However, this increase was delayed in the extra virgin olive oil group until week six, with the systolic blood pressure being always lower in this group. Nitric oxide and 8-isoprostanes were lower in the extra virgin olive oil group. While we can deduce a higher formation of angiotensin 2–10 in the renal cortex, a higher availability of angiotensin II may be presumed in the renal medulla of animals fed an extra virgin olive oil diet than in animals fed a standard diet. Our results support the beneficial influence of extra virgin olive oil on cardiovascular function and suggest that the Mediterranean diet may be beneficial in itself but it may also be an effective tool in the treatment of hypertension.

Key words

Olea europaea - Oleaceae - extra virgin olive oil - cardiovascular diseases - kidney - angiotensinases

• References

• 1 Reams G, Bauer J. Pharmacologic treatment of hypertension. In: Wilcox CS, editor Atlas of diseases of the kidney, Vol. 3. London: Blackwell Science; 1999
• 2 Ferdinand KC. Update in pharmacologic treatment of hypertension. Cardiol Clin 2001; 19: 279-294
• 3 Cogolludo A, Pérez-Vizcaino F, Tamargo J. New insights in the pharmacological therapy of arterial hypertension. Curr Opin Nephrol Hypertens 2005; 14: 423-427
• 4 Chen Q, Turban S, Miller ER, Appel LJ. The effects of dietary patterns on plasma renin activity: results from the Dietary Approaches to Stop Hypertension trial. J Hum Hypertens 2012; 26: 664-669
• 5 Engler MM, Schambelan M, Engler MB, Ball DL, Goodfriend TL. Effects of dietary gamma-linolenic acid on blood pressure and adrenal angiotensin receptors in hypertensive rats. Proc Soc Exp Biol Med 1998; 218: 234-237
• 6 Pérez-Jiménez F, Ruano J, Perez-Martinez P, Lopez-Segura F, Lopez-Miranda J. The influence of olive oil on human health: not a question of fat alone. Mol Nutr Food Res 2007; 51: 1199-1208
• 7 Covas MI, Konstantinidou V, Fitó M. Olive oil and cardiovascular health. J Cardiovasc Pharmacol 2009; 54: 477-482
• 8 Kanakis P, Termentzi A, Michel T, Gikas E, Halabalaki M, Skaltsounis AL. From olive drupes to olive oil. An HPLC-orbitrap-based qualitative and quantitative exploration of olive key metabolites. Planta Med 2013; 79: 1576-1587
• 9 Segarra AB, Ramirez M, Banegas I, Alba F, Vives F, Gasparo MD, Ortega E, Ruiz E, Prieto I. Dietary fat influences testosterone, cholesterol, aminopeptidase A, and blood pressure in male rats. Horm Metab Res 2008; 40: 289-291
• 10 Elased KM, Cunha TS, Marcondes FK, Morris M. Brain angiotensin-converting enzymes: role of angiotensin-converting enzyme 2 in processing angiotensin II in mice. Exp Physiol 2008; 93: 665-675
• 11 Speth RC, Karamyan VT. The significance of brain aminopeptidases in the regulation of the actions of angiotensin peptides in the brain. Heart Fail Rev 2008; 13: 299-309
• 12 Vauquelin G, Michotte Y, Smolders I, Sarre S, Ebinger G, Dupont A, Vanderheyden P. Cellular targets for angiotensin II fragments: pharmacological and molecular evidence. J Renin Angiotensin Aldosterone Syst 2003; 3: 195-204
• 13 Wallis MG, Lankford MF, Keller SR. Vasopressin is a physiological substrate for the insulin-regulated aminopeptidase IRAP. Am J Physiol Endocrinol Metab 2007; 293: E1092-E1102
• 14 Ramírez M, Prieto I, Alba F, Vives F, Banegas I, de Gasparo M. Role of central and peripheral aminopeptidase activities in the control of blood pressure: a working hypothesis. Heart Fail Rev 2008; 13: 339-353
• 15 Ramírez-Sánchez M, Prieto I, Wangensteen R, Banegas I, Segarra AB, Villarejo AB, Vives F, Cobo J, de Gasparo M. The renin-angiotensin system: new insight into old therapies. Curr Med Chem 2013; 20: 1313-1322
• 16 Leung PS. Local RAS. Adv Exp Med Biol 2010; 690: 69-87
• 17 Prieto I, Hermoso F, Gasparo MD, Vargas F, Alba F, Segarra AB, Banegas I, Ramírez M. Angiotensinase activities in the kidney of renovascular hypertensive rats. Peptides 2003; 24: 755-760
• 18 Kobori H, Nangaku M, Navar LG, Nishiyama A. The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev 2007; 59: 251-287
• 19 Navar LG, Prieto MC, Satou R, Kobori H. Intrarenal angiotensin II and its contribution to the genesis of chronic hypertension. Curr Opin Pharmacol 2011; 11: 180-186
• 20 Villarejo AB, Segarra AB, Ramírez M, Banegas I, Wangensteen R, de Gasparo M, Cobo J, Alba F, Vives F, Prieto I. Angiotensinase and vasopressinase activities in hypothalamus, plasma, and kidney after inhibition of angiotensin-converting enzyme: basis for a new working hypothesis. Horm Metab Res 2012; 44: 152-154
• 21 Seet RC, Lee CY, Loke WM, Huang SH, Huang H, Looi WF, Chew ES, Quek AM, Lim EC, Halliwell B. Biomarkers of oxidative damage in cigarette smokers: which biomarkers might reflect acute versus chronic oxidative stress?. Free Radic Biol Med 2011; 50: 1787-1793
• 22 Youn M, Csallany AS, Gallaher DD. Whole grain consumption has a modest effect on the development of diabetes in the Goto-Kakisaki rat. Br J Nutr 2012; 107: 192-201
• 23 Grisk O, Klöting I, Exner J, Spiess S, Schmidt R, Junghans D, Lorenz G, Rettig R. Long-term arterial pressure in spontaneously hypertensive rats is set by the kidney. J Hypertens 2002; 20: 131-138
• 24 Dornas WC, Silva ME. Animal models for the study of arterial hypertension. J Biosci 2011; 36: 731-737
• 25 Fernández O, Wangensteen R, Osuna A, Vargas F. Renal vascular reactivity to P(2) purinoceptor activation in spontaneously hypertensive rats. Pharmacology 2000; 60: 47-50
• 26 De Gasparo M. Angiotensin II and nitric oxide interaction. Heart Fail Rev 2002; 7: 347-358
• 27 Isabelle M, Simonet S, Ragonnet C, Sansilvestri-Morel P, Clavreul N, Vayssettes-Courchay C, Verbeuren TJ. Chronic reduction of nitric oxide level in adult spontaneously hypertensive rats induces aortic stiffness similar to old spontaneously hypertensive rats. J Vasc Res 2012; 49: 309-318
• 28 Visioli F, Poli A, Galli A. Antioxidant and other biological activities of phenols from olives and olive oil. Med Res Rev 2002; 22: 65-75
• 29 Acín S, Navarro MA, Perona JS, Arbonés-Mainar JM, Surra JC, Guzmán MA, Carnicer R, Arnal C, Orman I, Segovia JC, Osada J, Ruiz-Gutiérrez V. Olive oil preparation determines the atherosclerotic protection in apolipoprotein E knockout mice. J Nutr Biochem 2007; 18: 418-424
• 30 Raederstorff D. Antioxidant activity of olive polyphenols in humans: a review. Int J Vitam Nutr Res 2009; 79: 152-165
• 31 Velez JC, Ryan KJ, Harbeson CE, Bland AM, Budisavljevic MN, Arthur JM, Fitzgibbon WR, Raymond JR, Janech MG. Angiotensin I is largely converted to angiotensin (1–7) and angiotensin (2–10) by isolated rat glomeruli. Hypertension 2009; 53: 790-797
• 32 Burns KD, Li N. The role of angiotensin II-stimulated renal tubular transport in hypertension. Curr Hypertens Rep 2003; 5: 165-171
• 33 Banegas I, Prieto I, Vives F, Alba F, de Gasparo M, Duran R, Luna Jde D, Segarra AB, Hermoso F, Ramírez M. Asymmetrical response of aminopeptidase A and nitric oxide in plasma of normotensive and hypertensive rats with experimental hemiparkinsonism. Neuropharmacology 2009; 56: 573-579
• 34 Prieto I, Segarra AB, Vargas F, Alba F, de Gasparo M, Ramirez M. Angiotensinase activity in hypothalamus and pituitary of hypothyroid, euthyroid and hyperthyroid adult male rats. Horm Metab Res 2003; 35: 279-281
• 35 Segarra AB, Ramírez M, Banegas I, Hermoso F, Vargas F, Vives F, Alba F, de Gasparo M, Prieto I. Influence of thyroid disorders on kidney angiotensinase activity. Horm Metab Res 2006; 38: 48-52
• 36 Grima M, Ingert C, Michel B, Barthelmebs M, Imbs JL. Renal tissue angiotensins during converting enzyme inhibition in the spontaneously hypertensive rat. Clin Exp Hypertens 1997; 19: 671-685
• 37 Ramírez M, Prieto I, Banegas I, Segarra AB, Alba F. Neuropeptidases methods. Mol Biol 2011; 789: 287-294
• 38 Prieto I, Arechaga G, Segarra AB, Alba F, de Gasparo M, Ramirez M. Effects of dehydration on renal aminopeptidase activities in adult male and female rats. Regul Pept 2002; 106: 27-32