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Research Article

Red wine but not alcohol consumption improves cardiovascular function and oxidative stress of the hypertensive-SHR and diabetic-STZ rats

ORCID Icon, ORCID Icon, , &
Pages 573-584 | Received 09 Apr 2022, Accepted 16 May 2022, Published online: 14 Jun 2022

References

  • Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4(7):517–29. doi:10.1038/nrm1155.
  • Berridge MJ. Calcium microdomains: organization and function. Cell Calcium. 2006;40(5–6):405–12. doi:10.1016/j.ceca.2006.09.002.
  • Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415(6868):198–205. doi:10.1038/415198a.
  • Chahoud J, Mrad J, Semaan A, Asmar R. Prevalence of diabetes mellitus among patients with essential arterial hypertensiON. J Med Liban. 2015;63(2):74–80. doi:10.12816/0012554.
  • Gohardehi F, Seyedin H, Moslehi S. Prevalence rate of diabetes and hypertension in disaster-exposed populations: a systematic review and meta-analysis. Ethiop J Health Sci. 2020;30(3):439–48. doi:10.4314/ejhs.v30i3.15.
  • Gomes CS, Bernal RTI, Moreira AD, Teixeira RA, Cardoso LSM, Ribeiro ALP, et al. Estimates of hypertension and diabetes mellitus prevalence according to Health vulnerability index in belo horizonte, MG, Brazil. Rev Bras Epidemiol. 2021;24(1):e210015. doi:10.1590/1980-549720210015.supl.1.
  • Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J. Global burden of hypertension: analysis of worldwide data. Lancet. 2005;365(9455):217–23. doi:10.1016/S0140-6736(05)17741-1.
  • Landsberg L, Molitch M. Diabetes and hypertension: pathogenesis, prevention and treatment. Clin Exp Hypertens. 2004;26(7–8):621–28. doi:10.1081/CEH-200031945.
  • Anderson EA, Sinkey CA, Lawton WJ, Mark AL. Elevated sympathetic nerve activity in borderline hypertensive humans. Evidence from direct intraneural recordings. Hypertension. 1989;14(2):177–83. doi:10.1161/01.HYP.14.2.177.
  • de Champlain J, Farley L, Cousineau D, van Ameringen MR. Circulating catecholamine levels in human and experimental hypertension. Circ Res. 1976;38(2):109–14. doi:10.1161/01.RES.38.2.109.
  • Donohue SJ, Stitzel RE, Head RJ. Time course of changes in the norepinephrine content of tissues from spontaneously hypertensive and Wistar Kyoto rats. J Pharmacol Exp Ther. 1988;245(1):24–31.
  • Musial DC, Bomfim GH, Arranz-Tagarro JA, Mendez-Lopez I, Miranda-Ferreira R, Jurkiewicz A, Jurkiewicz NH, García AG, Padín JF, et al. Altered mitochondrial function, calcium signaling, and catecholamine release in chromaffin cells of diabetic and SHR rats. Eur J Pharmacol. 2017;815:416–26.
  • Konukoglu D, Uzun H. Endothelial dysfunction and hypertension. Adv Exp Med Biol. 2017;956:511–40.
  • Lv Q, Wang Y, Li Y, Zhao L, Gong Y, Wang M, Wang M, Fu G, Zhang W, et al. Rosuvastatin reverses hypertension-induced changes in the aorta structure and endothelium-dependent relaxation in rats through suppression of apoptosis and inflammation. J Cardiovasc Pharmacol. 2020;75(6):584–95. doi:10.1097/FJC.0000000000000828.
  • Pinheiro LC, Oliveira-Paula GH. Sources and effects of oxidative stress in hypertension. Curr Hypertens Rev. 2020;16(3):166–80. doi:10.2174/1573402115666190531071924.
  • Sinha N, Dabla PK. Oxidative stress and antioxidants in hypertension-a current review. Curr Hypertens Rev. 2015;11(2):132–42. doi:10.2174/1573402111666150529130922.
  • Dzau VJ, Balatbat CA. Future of hypertension. Hypertension. 2019;74(3):450–57. doi:10.1161/HYPERTENSIONAHA.119.13437.
  • Esler M. The sympathetic nervous system in hypertension: back to the future?. Curr Hypertens Rep. 2015;17(2):11. doi:10.1007/s11906-014-0519-8.
  • Morrison SF, Whitehorn D. Enhanced preganglionic sympathetic nerve responses in spontaneously hypertensive rats. Brain Res. 1984;296(1):152–55. doi:10.1016/0006-8993(84)90522-5.
  • Bomfim GHS, Musial DC, Miranda-Ferreira R, Nascimento SR, Jurkiewicz A, Jurkiewicz NH, de Moura RS, et al. Antihypertensive effects of the vitis vinifera grape skin (ACH09) extract consumption elicited by functional improvement of P1 (A1) and P2 (P2X1) purinergic receptors in diabetic and hypertensive rats. PharmaNutrition. 2019;8:100146.
  • Bertelli AA. Wine, research and cardiovascular disease: instructions for use. Atherosclerosis. 2007;195(2):242–47. doi:10.1016/j.atherosclerosis.2007.04.006.
  • Orallo F, Alvarez E, Camiña M, Leiro JM, Gómez E, Fernández P. The possible implication of trans-Resveratrol in the cardioprotective effects of long-term moderate wine consumption. Mol Pharmacol. 2002;61(2):294–302. doi:10.1124/mol.61.2.294.
  • Renaud S, de Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet. 1992;339(8808):1523–26. doi:10.1016/0140-6736(92)91277-F.
  • Fogacci F, Tocci G, Presta V, Fratter A, Borghi C, Cicero AFG. Effect of resveratrol on blood pressure: a systematic review and meta-analysis of randomized, controlled, clinical trials. Crit Rev Food Sci Nutr. 2019;59(10):1605–18. doi:10.1080/10408398.2017.1422480.
  • Orallo F. Comparative studies of the antioxidant effects of cis- and trans-resveratrol. Curr Med Chem. 2006;13(1):87–98. doi:10.2174/092986706775197962.
  • Singh S, Shankar R, Singh GP. Prevalence and associated risk factors of hypertension: a cross-sectional study in urban Varanasi. Int J Hypertens. 2017;2017:5491838. doi:10.1155/2017/5491838.
  • O’Keefe JH, Bhatti SK, Bajwa A, DiNicolantonio JJ, Lavie CJ. Alcohol and cardiovascular health: the dose makes the poison … or the remedy. Mayo Clin Proc. 2014;89(3):382–93. doi:10.1016/j.mayocp.2013.11.005.
  • Zhang X, Liu Y, Li S, Lichtenstein AH, Chen S, Na M, Veldheer S, Xing A, Wang Y, Wu S, et al. Alcohol consumption and risk of cardiovascular disease, cancer and mortality: a prospective cohort study. Nutr J. 2021;20(1):13. doi:10.1186/s12937-021-00671-y.
  • Bomfim GHS, Mendez-Lopez I, Fernandez-Morales JC, Padin JF, Jurkiewicz A, Jurkiewicz NH, García AG, et al. Electrophysiological properties and augmented catecholamine release from chromaffin cells of WKY and SHR rats contributing to the hypertension development elicited by chronic EtOH consumption. Eur J Pharmacol. 2017;803:65–77.
  • Musial DC, Bomfim GH, Miranda-Ferreira R, Caricati-Neto A, Jurkiewicz A, Jurkiewicz NH. Chronic treatment with red wine modulates the purinergic neurotransmission and decreases blood pressure in hypertensive SHR and diabetic-STZ rats. Int J Food Sci Nutr. 2015;66(5):579–86. doi:10.3109/09637486.2015.1056110.
  • Lassègue B, Griendling KK. Reactive oxygen species in hypertension; an update. Am J Hypertens. 2004;17(9):852–60. doi:10.1016/j.amjhyper.2004.02.004.
  • Musial DC, de Magalhães Galvão K, Miranda-Ferreira R, Dantas da Silva Júnior E, Caricati-Neto A, Jurkiewicz NH, Jurkiewicz A, Broetto Biazon AC, et al. Alteration of purinergic neurotransmission in isolated atria of streptozotocin-induced diabetic rats. J Cardiovasc Pharmacol. 2012;59(2):158–64. doi:10.1097/FJC.0b013e31823a0f31.
  • Musial DC, Bomfim GH, Arranz-Tagarro JA, Méndez-López I, Miranda-Ferreira R, Jurkiewicz A, Jurkiewicz NH, García AG, Padín JF, et al. Altered mitochondrial function, calcium signaling, and catecholamine release in chromaffin cells of diabetic and SHR rats. Eur J Pharmacol. 2017;815:416–26.
  • Elsner M, Guldbakke B, Tiedge M, Munday R, Lenzen S. Relative importance of transport and alkylation for pancreatic beta-cell toxicity of streptozotocin. Diabetologia. 2000;43(12):1528–33. doi:10.1007/s001250051564.
  • Caillaud K, Boisseau N, Ennequin G, Chavanelle V, Etienne M, Li X, Denis P, Dardevet D, Lacampagne A, Sirvent P, et al. Neuregulin 1 improves glucose tolerance in adult and old rats. Diabetes Metab. 2016;42(2):96–104. doi:10.1016/j.diabet.2015.08.003.
  • Le Floch JP, Escuyer P, Baudin E, Baudon D, Perlemuter L. Blood glucose area under the curve. Methodol Aspects Diabetes Care. 1990;13(2):172–75. doi:10.2337/diacare.13.2.172.
  • Fanzone M, Peña-Neira A, Jofré V, Assof M, Zamora F. Phenolic characterization of malbec wines from mendoza province (Argentina). J Agric Food Chem. 2010;58(4):2388–97. doi:10.1021/jf903690v.
  • Bomfim GHS, Musial DC, Méndez-López I, Jurkiewicz A, Jurkiewicz NH, Padín JF, García AG, et al. Chronic resveratrol consumption prevents hypertension development altering electrophysiological currents and Ca(2+) signaling in chromaffin cells from SHR rats. Cell Signal. 2020;76:109811.
  • Souza Bomfim GH, Mendez-Lopez I, Arranz-Tagarro JA, Ferraz Carbonel AA, Roman-Campos D, Padín JF, et al. Functional upregulation of STIM-1/Orai-1-Mediated store-operated Ca2+ contributing to the hypertension development elicited by chronic EtOH consumption. Curr Vasc Pharmacol. 2017;15(3):265–81. doi:10.2174/1570161115666170201122750.
  • Wilson C, Lee MD, McCarron JG. Acetylcholine released by endothelial cells facilitates flow-mediated dilatation. J Physiol. 2016;594(24):7267–307. doi:10.1113/JP272927.
  • Do KH, Kim MS, Kim JH, Rhim BY, Lee WS, Kim CD, Bae SS, et al. Angiotensin II-induced aortic ring constriction is mediated by phosphatidylinositol 3-kinase/L-type calcium channel signaling pathway. Exp Mol Med. 2009;41(8):569–76. doi:10.3858/emm.2009.41.8.062.
  • Doggrell SA. Functional beta1- and beta2-adrenoceptors in the left and right atrium of pre-hypertensive rats. J Pharm Pharmacol. 2002;54(10):1407–12. doi:10.1211/002235702760345509.
  • Jiang ZY, Woollard AC, Wolff SP. Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids. 1991;26(10):853–56. doi:10.1007/BF02536169.
  • Ferro Cde O, Chagas VL, de Oliveira Mf, de Oliveira Pl, Schanaider A, de Oliveira MF, de Oliveira PL. Catalase activity in lung, kidney and small bowel non-ischemic in rats after intestinal reperfusion. Rev Col Bras Cir. 2010;37(1):31–38. doi:10.1590/s0100-69912010000100008.
  • Friedman J, Peleg E, Kagan T, Shnizer S, Rosenthal T. Oxidative stress in hypertensive,diabetic, and diabetic hypertensive rats. Am J Hypertens. 2003;16(12):1049–52. doi:10.1016/j.amjhyper.2003.07.013.
  • Szmitko PE, Verma S. Cardiology patient pages. Red wine and your heart. Circulation. 2005;111(2):e10–1. doi:10.1161/01.CIR.0000151608.29217.62.
  • Bradamante S, Barenghi L, Villa A. Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev. 2009;22(3):169–88. doi:10.1111/j.1527-3466.2004.tb00139.x.
  • Breuss JM, Atanasov AG, Uhrin P. Resveratrol and its effects on the vascular system. Int J Mol Sci. 2019;20(7):1523. doi:10.3390/ijms20071523.
  • Wu JM, Wang ZR, Hsieh TC, Bruder JL, Zou JG, Huang YZ. Mechanism of cardioprotection by resveratrol, a phenolic antioxidant present in red wine (Review). Int J Mol Med. 2001;8(1):3–17. doi:10.3892/ijmm.8.1.3.
  • Su HC, Hung LM, Chen JK. Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am J Physiol Endocrinol Metab. 2006;290(6):E1339–46. doi:10.1152/ajpendo.00487.2005.
  • López-Fernández-Sobrino R, Soliz-Rueda JR, Ávila-Román J, Arola-Arnal A, Suárez M, Muguerza B, et al. Blood Pressure-lowering effect of wine lees phenolic compounds is mediated by endothelial-derived factors: role of sirtuin 1. Antioxid. 2021;10(7).
  • Idris Khodja N, Chataigneau T, Auger C, Schini-Kerth VB. Grape-derived polyphenols improve aging-related endothelial dysfunction in rat mesenteric artery: role of oxidative stress and the angiotensin system. PLoS One. 2012;7(2):e32039. doi:10.1371/journal.pone.0032039.
  • Cishek MB, Galloway MT, Karim M, German JB, Kappagoda CT. Effect of red wine on endothelium-dependent relaxation in rabbits. Clin Sci (Lond). 1997;93(6):507–11. doi:10.1042/cs0930507.
  • Zenebe W, Pechánová O, Andriantsitohaina R. Red wine polyphenols induce vasorelaxation by increased nitric oxide bioactivity. Physiol Res. 2003;52(4):425–32.
  • Alhosin M, Anselm E, Rashid S, Kim JH, Madeira SV, Bronner C, Schini-Kerth VB, et al. Redox-sensitive up-regulation of eNOS by purple grape juice in endothelial cells: role of PI3-kinase/Akt, p38 MAPK, JNK, FoxO1 and FoxO3a. PLoS One. 2013;8(3):e57883. doi:10.1371/journal.pone.0057883.
  • Anselm E, Chataigneau M, Ndiaye M, Chataigneau T, Schini-Kerth VB. Grape juice causes endothelium-dependent relaxation via a redox-sensitive Src- and Akt-dependent activation of eNOS. Cardiovasc Res. 2007;73(2):404–13. doi:10.1016/j.cardiores.2006.08.004.
  • Petrie JR, Guzik TJ, Touyz RM. Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms. Can J Cardiol. 2018;34(5):575–84. doi:10.1016/j.cjca.2017.12.005.
  • Kotchen TA, Guthrie GP. Renin-angiotensin-aldosterone and hypertension. Endocr Rev. 1980;1(1):78–99. doi:10.1210/edrv-1-1-78.
  • Touyz RM. Molecular and cellular mechanisms in vascular injury in hypertension: role of angiotensin II. Curr Opin Nephrol Hypertens. 2005;14(2):125–31. doi:10.1097/00041552-200503000-00007.
  • Shimizu S, Tsounapi P, Honda M, Dimitriadis F, Taniuchi K, Shimizu T, et al. Effect of an angiotensin II receptor blocker and a calcium channel blocker on hypertension associated penile dysfunction in a rat model. Biomed Res. 2014;35(3):215–21. doi:10.2220/biomedres.35.215.
  • Sarr M, Chataigneau M, Martins S, Schott C, El Bedoui J, Oak MH, et al. Red wine polyphenols prevent angiotensin II-induced hypertension and endothelial dysfunction in rats: role of NADPH oxidase. Cardiovasc Res. 2006;71(4):794–802. doi:10.1016/j.cardiores.2006.05.022.
  • Inanaga K, Ichiki T, Matsuura H, Miyazaki R, Hashimoto T, Takeda K, Sunagawa K, et al. Resveratrol attenuates angiotensin II-induced interleukin-6 expression and perivascular fibrosis. Hypertens Res. 2009;32(6):466–71. doi:10.1038/hr.2009.47.
  • Rodrigo R, Gil D, Miranda-Merchak A, Kalantzidis G. Antihypertensive role of polyphenols. Adv Clin Chem. 2012;58:225–54.
  • Guyton AC. The relationship of cardiac output and arterial pressure control. Circulation. 1981;64(6):1079–88. doi:10.1161/01.CIR.64.6.1079.
  • Dornas WC, Cardoso LM, Silva M, Machado NL, Chianca DA, Alzamora AC, Lima WG, Lagente V, Silva ME, et al. Oxidative stress causes hypertension and activation of nuclear factor-κB after high-fructose and salt treatments. Sci Rep. 2017;7(1):46051. doi:10.1038/srep46051.
  • Chia TY, Murugaiyah V, Khan NA, Sattar MA, Abdulla MH, Johns EJ, Ahmad A, Hassan Z, Kaur G, Mei H, et al. Inhibition of L-NAME-induced hypertension by combined treatment with apocynin and catalase: the role of Nox 4 expression. Physiol Res. 2021;70(1):13–26. doi:10.33549/physiolres.934497.
  • Unudurthi SD, Wolf RM, Hund TJ. Role of sinoatrial node architecture in maintaining a balanced source-sink relationship and synchronous cardiac pacemaking. Front Physiol. 2014;5:446. doi:10.3389/fphys.2014.00446.
  • Pignatelli P, Menichelli D, Pastori D, Violi F. Oxidative stress and cardiovascular disease: new insights. Kardiol Pol. 2018;76(4):713–22. doi:10.5603/KP.a2018.0071.
  • Schmidt L, Heck NV, Ferreira I, Göethel G, Somacal S, Emanuelli T, Rodrigues E, Garcia SC, Welke JE, Augusti PR, et al. Ochratoxin A presence in cabernet sauvignon wine changes antioxidant activity in vitro and oxidative stress markers in vivo. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2020;37(10):1755–64. doi:10.1080/19440049.2020.1802067.
  • Liu FC, Tsai HI, Yu HP. Organ-Protective effects of red wine extract, resveratrol, in oxidative stress-mediated reperfusion injury. Oxid Med Cell Longev. 2015;2015:568634. doi:10.1155/2015/568634.
  • Schrieks IC, van den Berg R, Sierksma A, Beulens JW, Vaes WH, Hendriks HF. Effect of red wine consumption on biomarkers of oxidative stress. Alcohol Alcohol. 2013;48(2):153–59. doi:10.1093/alcalc/ags086.
  • Pignatelli P, Ghiselli A, Buchetti B, Carnevale R, Natella F, Germanò G, Fimognari F, Di Santo S, Lenti L, Violi F, et al. Polyphenols synergistically inhibit oxidative stress in subjects given red and white wine. Atherosclerosis. 2006;188(1):77–83. doi:10.1016/j.atherosclerosis.2005.10.025.

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