Nitrite-stimulated Gastric Formation of S-nitrosothiols As An Antihypertensive Therapeutic Strategy

Author(s): Gustavo H. Oliveira-Paula, Jose E. Tanus-Santos*.

Journal Name: Current Drug Targets

Volume 20 , Issue 4 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Hypertension is usually associated with deficient nitric oxide (NO) bioavailability, and therefore stimulating NO activity is an important antihypertensive strategy. Recently, many studies have shown that both nitrite and nitrate anions are not simple products of NO metabolism and indeed may be reduced back to NO. While enzymes with nitrite-reductase activity capable of generating NO from nitrite may contribute to antihypertensive effects of nitrite, another mechanism involving the generation of NO-related species in the stomach from nitrite has been validated. Under the acidic conditions of the stomach, nitrite generates NO-related species that form S-nitrosothiols. Conversely, drugs that increase gastric pH may impair the gastric formation of S-nitrosothiols, which may mediate antihypertensive effects of oral nitrite or nitrate. Therefore, it is now becoming clear that promoting gastric formation of S-nitrosothiols may result in effective antihypertensive responses, and this mechanism opens a window of opportunity in the therapy of hypertension. In this review, we discuss the recent studies supporting the gastric generation of S-nitrosothiols as a potential antihypertensive mechanism of oral nitrite. We also highlight some drugs that increase S-nitrosothiols bioavailability, which may also improve the responses to nitrite/nitrate therapy. This new approach may result in increased nitrosation of critical pharmacological receptors and enzymes involved in the pathogenesis of hypertension, which tend to respond less to their activators resulting in lower blood pressure.

Keywords: Hypertension, nitric oxide, nitrite, S-nitrosation, S-nitrosothiols, oral nitrite.

[1]
Pagidipati NJ, Gaziano TA. Estimating deaths from cardiovascular disease: A review of global methodologies of mortality measurement. Circulation 2013; 127: 749-56.
[2]
Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: The JNC 7 report. JAMA 2003; 289: 2560-72.
[3]
Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993; 329: 2002-12.
[4]
Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: Structure, function and inhibition. Biochem J 2001; 357: 593-615.
[5]
Oliveira-Paula GH, Lacchini R, Tanus-Santos JE. Inducible nitric oxide synthase as a possible target in hypertension. Curr Drug Targets 2014; 15: 164-74.
[6]
Cortese-Krott MM, Kelm M. Endothelial nitric oxide synthase in red blood cells: Key to a new erythrocrine function? Redox Biol 2014; 2: 251-8.
[7]
Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 2008; 7: 156-67.
[8]
Kapil V, Weitzberg E, Lundberg JO, Ahluwalia A. Clinical evidence demonstrating the utility of inorganic nitrate in cardiovascular health. Nitric Oxide 2014; 38: 45-57.
[9]
van Velzen AG, Sips AJ, Schothorst RC, Lambers AC, Meulenbelt J. The oral bioavailability of nitrate from nitrate-rich vegetables in humans. Toxicol Lett 2008; 181: 177-81.
[10]
Lundberg JO, Weitzberg E. Biology of nitrogen oxides in the gastrointestinal tract. Gut 2013; 62: 616-29.
[11]
Weitzberg E, Lundberg JO. Novel aspects of dietary nitrate and human health. Annu Rev Nutr 2013; 33: 129-59.
[12]
Kobayashi J. Effect of diet and gut environment on the gastrointestinal formation of N-nitroso compounds: A review. Nitric Oxide 2018; 73: 66-73.
[13]
Pinheiro LC, Amaral JH, Ferreira GC, et al. Gastric S-nitrosothiol formation drives the antihypertensive effects of oral sodium nitrite and nitrate in a rat model of renovascular hypertension. Free Radic Biol Med 2015; 87: 252-62.
[14]
Pinheiro LC, Ferreira GC, Amaral JH, et al. Oral nitrite circumvents antiseptic mouthwash-induced disruption of enterosalivary circuit of nitrate and promotes nitrosation and blood pressure lowering effect. Free Radic Biol Med 2016; 101: 226-35.
[15]
Pinheiro LC, Ferreira GC, Vilalva KH, Toledo JC Jr, Tanus-Santos JE. Contrasting effects of low versus high ascorbate doses on blood pressure responses to oral nitrite in L-NAME-induced hypertension. Nitric Oxide 2018; 74: 65-73.
[16]
Hermann M, Flammer A, Luscher TF. Nitric oxide in hypertension. J Clin Hypertens (Greenwich) 2006; 8: 17-29.
[17]
Thomas GD, Zhang W, Victor RG. Nitric oxide deficiency as a cause of clinical hypertension: Promising new drug targets for refractory hypertension. JAMA 2001; 285: 2055-7.
[18]
Moreno H Jr, Metze K, Bento AC, Antunes E, Zatz R, de Nucci G. Chronic nitric oxide inhibition as a model of hypertensive heart muscle disease. Basic Res Cardiol 1996; 91: 248-55.
[19]
Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H. Protective role of endothelial nitric oxide synthase. J Pathol 2003; 199: 8-17.
[20]
Li H, Wallerath T, Forstermann U. Physiological mechanisms regulating the expression of endothelial-type NO synthase. Nitric Oxide 2002; 7: 132-47.
[21]
Panza JA, Garcia CE, Kilcoyne CM, Quyyumi AA, Cannon RO 3rd. Impaired endothelium-dependent vasodilation in patients with essential hypertension. Evidence that nitric oxide abnormality is not localized to a single signal transduction pathway. Circulation 1995; 91: 1732-8.
[22]
Higashi Y, Oshima T, Ozono R, et al. Effects of L-arginine infusion on renal hemodynamics in patients with mild essential hypertension. Hypertension 1995; 25: 898-902.
[23]
Treasure CB, Klein JL, Vita JA, et al. Hypertension and left ventricular hypertrophy are associated with impaired endothelium-mediated relaxation in human coronary resistance vessels. Circulation 1993; 87: 86-93.
[24]
Stankevicius E, Martinez AC, Mulvany MJ, Simonsen U. Blunted acetylcholine relaxation and nitric oxide release in arteries from renal hypertensive rats. J Hypertens 2002; 20: 1571-9.
[25]
Montezano AC, Dulak-Lis M, Tsiropoulou S. Oxidative stress and human hypertension: Vascular mechanisms, biomarkers, and novel therapies. Can J Cardiol 2015; 31: 631-41.
[26]
Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007; 87: 315-424.
[27]
Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide. Arch Biochem Biophys 1991; 288: 481-7.
[28]
Li Q, Youn JY, Cai H. Mechanisms and consequences of endothelial nitric oxide synthase dysfunction in hypertension. J Hypertens 2015; 33: 1128-36.
[29]
Cardillo C, Panza JA. Impaired endothelial regulation of vascular tone in patients with systemic arterial hypertension. Vasc Med 1998; 3: 138-44.
[30]
Schlaich MP, Parnell MM, Ahlers BA, et al. Impaired L-arginine transport and endothelial function in hypertensive and genetically predisposed normotensive subjects. Circulation 2004; 110: 3680-6.
[31]
Hishikawa K, Nakaki T, Suzuki H, Kato R, Saruta T. Role of L-arginine-nitric oxide pathway in hypertension. J Hypertens 1993; 11: 639-45.
[32]
Chen PY, Sanders PW. L-arginine abrogates salt-sensitive hypertension in Dahl/Rapp rats. J Clin Invest 1991; 88: 1559-67.
[33]
Dong JY, Qin LQ, Zhang Z, et al. Effect of oral L-arginine supplementation on blood pressure: a meta-analysis of randomized, double-blind, placebo-controlled trials. Am Heart J 2011; 162: 959-65.
[34]
Achan V, Broadhead M, Malaki M, et al. Asymmetric dimethylarginine causes hypertension and cardiac dysfunction in humans and is actively metabolized by dimethylarginine dimethylaminohydrolase. Arterioscler Thromb Vasc Biol 2003; 23: 1455-9.
[35]
Cooke JP. Does ADMA cause endothelial dysfunction? Arterioscler Thromb Vasc Biol 2000; 20: 2032-7.
[36]
Maron BA, Michel T. Subcellular localization of oxidants and redox modulation of endothelial nitric oxide synthase. Circ J 2012; 76: 2497-512.
[37]
Luo S, Lei H, Qin H, Xia Y. Molecular mechanisms of endothelial NO synthase uncoupling. Curr Pharm Des 2014; 20: 3548-53.
[38]
Pinheiro LC, Tanus-Santos JE, Castro MM. The potential of stimulating nitric oxide formation in the treatment of hypertension. Expert Opin Ther Targets 2017; 21: 543-56.
[39]
Oliveira-Paula GH, Lacchini R, Tanus-Santos JE. Clinical and pharmacogenetic impact of endothelial nitric oxide synthase polymorphisms on cardiovascular diseases. Nitric Oxide 2017; 63: 39-51.
[40]
Oliveira-Paula GH, Lacchini R, Tanus-Santos JE. Endothelial nitric oxide synthase: From biochemistry and gene structure to clinical implications of NOS3 polymorphisms. Gene 2016; 575: 584-99.
[41]
Murad F, Mittal CK, Arnold WP, Katsuki S, Kimura H. Guanylate cyclase: Activation by azide, nitro compounds, nitric oxide, and hydroxyl radical and inhibition by hemoglobin and myoglobin. Adv Cyclic Nucleotide Res 1978; 9: 145-58.
[42]
Denninger JW, Marletta MA. Guanylate cyclase and the. NO/cGMP signaling pathway. Biochim Biophys Acta 1999; 1411: 334-50.
[43]
Craven PA, DeRubertis FR. Restoration of the responsiveness of purified guanylate cyclase to nitrosoguanidine, nitric oxide, and related activators by heme and hemeproteins. Evidence for involvement of the paramagnetic nitrosyl-heme complex in enzyme activation. J Biol Chem 1978; 253: 8433-43.
[44]
Walford G, Loscalzo J. Nitric oxide in vascular biology. J Thromb Haemost 2003; 1: 2112-8.
[45]
Francis SH, Busch JL, Corbin JD, Sibley D. cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 2010; 62: 525-63.
[46]
Kato M, Blanton R, Wang GR, et al. Direct binding and regulation of RhoA protein by cyclic GMP-dependent protein kinase Ialpha. J Biol Chem 2012; 287: 41342-51.
[47]
Shen Q, Rigor RR, Pivetti CD, Wu MH, Yuan SY. Myosin light chain kinase in microvascular endothelial barrier function. Cardiovasc Res 2010; 87: 272-80.
[48]
Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI. Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res 1997; 80: 557-64.
[49]
Fukai T, Siegfried MR, Ushio-Fukai M, et al. Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training. J Clin Invest 2000; 105: 1631-9.
[50]
Vanhoutte PM, Zhao Y, Xu A, Leung SW. Thirty years of saying no: Sources, fate, actions, and misfortunes of the endothelium-derived vasodilator mediator. Circ Res 2016; 119: 375-96.
[51]
Thomas DD, Liu X, Kantrow SP, Lancaster JR Jr. The biological lifetime of nitric oxide: Implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA 2001; 98: 355-60.
[52]
Kelm M. Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1999; 1411: 273-89.
[53]
Lancaster JR Jr. Nitric oxide: A brief overview of chemical and physical properties relevant to therapeutic applications. Future Sci OA 2015; 1: FSO59.
[54]
Shiva S, Wang X, Ringwood LA, et al. Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis. Nat Chem Biol 2006; 2: 486-93.
[55]
Dejam A, Hunter CJ, Pelletier MM, et al. Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood 2005; 106: 734-9.
[56]
Tang Y, Jiang H, Bryan NS. Nitrite and nitrate: Cardiovascular risk-benefit and metabolic effect. Curr Opin Lipidol 2011; 22: 11-5.
[57]
Hord NG, Tang Y, Bryan NS. Food sources of nitrates and nitrites: The physiologic context for potential health benefits. Am J Clin Nutr 2009; 90: 1-10.
[58]
Kapil V, Webb AJ, Ahluwalia A. Inorganic nitrate and the cardiovascular system. Heart 2010; 96: 1703-9.
[59]
McKnight GM, Smith LM, Drummond RS, et al. Chemical synthesis of nitric oxide in the stomach from dietary nitrate in humans. Gut 1997; 40: 211-4.
[60]
Pannala AS, Mani AR, Spencer JP, et al. The effect of dietary nitrate on salivary, plasma, and urinary nitrate metabolism in humans. Free Radic Biol Med 2003; 34: 576-84.
[61]
Qin L, Liu X, Sun Q, et al. Sialin (SLC17A5) functions as a nitrate transporter in the plasma membrane. Proc Natl Acad Sci USA 2012; 109: 13434-9.
[62]
Lundberg JO, Weitzberg E, Cole JA, Benjamin N. Nitrate, bacteria and human health. Nat Rev Microbiol 2004; 2: 593-602.
[63]
Doel JJ, Benjamin N, Hector MP, Rogers M, Allaker RP. Evaluation of bacterial nitrate reduction in the human oral cavity. Eur J Oral Sci 2005; 113: 14-9.
[64]
Lundberg JO, Weitzberg E, Lundberg JM, Alving K. Intragastric nitric oxide production in humans: Measurements in expelled air. Gut 1994; 35: 1543-6.
[65]
Benjamin N, O’Driscoll F, Dougall H, et al. Stomach NO synthesis. Nature 1994; 368: 502.
[66]
Castiglione N, Rinaldo S, Giardina G, Stelitano V, Cutruzzola F. Nitrite and nitrite reductases: From molecular mechanisms to significance in human health and disease. Antioxid Redox Signal 2012; 17: 684-716.
[67]
Omar SA, Webb AJ. Nitrite reduction and cardiovascular protection. J Mol Cell Cardiol 2014; 73: 57-69.
[68]
Gladwin MT, Kim-Shapiro DB. The functional nitrite reductase activity of the heme-globins. Blood 2008; 112: 2636-47.
[69]
Brooks J. The action of nitrite on haemoglobin in the absence of oxygen. Proceedings of the Royal Society Series B-Biological Sciences 1937; 123: 368-82.
[70]
Doyle MP, Pickering RA, DeWeert TM, Hoekstra JW, Pater D. Kinetics and mechanism of the oxidation of human deoxyhemoglobin by nitrites. J Biol Chem 1981; 256: 12393-8.
[71]
Cosby K, Partovi KS, Crawford JH, et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 2003; 9: 1498-505.
[72]
Angelo M, Singel DJ, Stamler JS. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc Natl Acad Sci USA 2006; 103: 8366-71.
[73]
Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 1996; 380: 221-6.
[74]
Shiva S, Huang Z, Grubina R, et al. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res 2007; 100: 654-61.
[75]
Totzeck M, Hendgen-Cotta UB, Luedike P, et al. Nitrite regulates hypoxic vasodilation via myoglobin-dependent nitric oxide generation. Circulation 2012; 126: 325-34.
[76]
Hendgen-Cotta UB, Merx MW, Shiva S, et al. Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 2008; 105: 10256-61.
[77]
Kim-Shapiro DB, Gladwin MT. Mechanisms of nitrite bioactivation. Nitric Oxide 2014; 38: 58-68.
[78]
Cantu-Medellin N, Kelley EE. Xanthine oxidoreductase-catalyzed reactive species generation: A process in critical need of reevaluation. Redox Biol 2013; 1: 353-8.
[79]
Battelli MG, Bolognesi A, Polito L. Pathophysiology of circulating xanthine oxidoreductase: new emerging roles for a multi-tasking enzyme. Biochim Biophys Acta 2014; 1842: 1502-17.
[80]
Landmesser U, Spiekermann S, Preuss C, et al. Angiotensin II induces endothelial xanthine oxidase activation: Role for endothelial dysfunction in patients with coronary disease. Arterioscler Thromb Vasc Biol 2007; 27: 943-8.
[81]
Swei A, Lacy F, Delano FA, Parks DA, Schmid-Schonbein GW. A mechanism of oxygen free radical production in the Dahl hypertensive rat. Microcirculation 1999; 6: 179-87.
[82]
Suzuki H, DeLano FA, Parks DA, et al. Xanthine oxidase activity associated with arterial blood pressure in spontaneously hypertensive rats. Proc Natl Acad Sci USA 1998; 95: 4754-9.
[83]
Cantu-Medellin N, Kelley EE. Xanthine oxidoreductase-catalyzed reduction of nitrite to nitric oxide: insights regarding where, when and how. Nitric Oxide 2013; 34: 19-26.
[84]
Zhang Z, Naughton DP, Blake DR, et al. Human xanthine oxidase converts nitrite ions into Nitric Oxide (NO). Biochem Soc Trans 1997; 25: 524S.
[85]
Li H, Cui H, Kundu TK, Alzawahra W, Zweier JL. Nitric oxide production from nitrite occurs primarily in tissues not in the blood: Critical role of xanthine oxidase and aldehyde oxidase. J Biol Chem 2008; 283: 17855-63.
[86]
Maia LB, Pereira V, Mira L, Moura JJ. Nitrite reductase activity of rat and human xanthine oxidase, xanthine dehydrogenase, and aldehyde oxidase: evaluation of their contribution to NO formation in vivo. Biochem 2015; 54: 685-710.
[87]
Millar TM, Stevens CR, Benjamin N, et al. Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett 1998; 427: 225-8.
[88]
Kelley EE. A new paradigm for XOR-catalyzed reactive species generation in the endothelium. Pharmacol Rep 2015; 67: 669-74.
[89]
Damacena-Angelis C, Oliveira-Paula GH, Pinheiro LC, et al. Nitrate decreases xanthine oxidoreductase-mediated nitrite reductase activity and attenuates vascular and blood pressure responses to nitrite. Redox Biol 2017; 12: 291-9.
[90]
Maia LB, Moura JJ. Nitrite reduction by xanthine oxidase family enzymes: A new class of nitrite reductases. J Biol Inorg Chem 2011; 16: 443-60.
[91]
Zhang Z, Naughton D, Winyard PG, et al. Generation of nitric oxide by a nitrite reductase activity of xanthine oxidase: A potential pathway for nitric oxide formation in the absence of nitric oxide synthase activity. Biochem Biophys Res Commun 1998; 249: 767-72.
[92]
Godber BL, Doel JJ, Sapkota GP, et al. Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J Biol Chem 2000; 275: 7757-63.
[93]
Webb A, Bond R, McLean P, et al. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 2004; 101: 13683-8.
[94]
Baliga RS, Milsom AB, Ghosh SM, et al. Dietary nitrate ameliorates pulmonary hypertension: Cytoprotective role for endothelial nitric oxide synthase and xanthine oxidoreductase. Circulation 2012; 125: 2922-32.
[95]
Zuckerbraun BS, Shiva S, Ifedigbo E, et al. Nitrite potently inhibits hypoxic and inflammatory pulmonary arterial hypertension and smooth muscle proliferation via xanthine oxidoreductase-dependent nitric oxide generation. Circulation 2010; 121: 98-109.
[96]
Dias-Junior CA, Gladwin MT, Tanus-Santos JE. Low-dose intravenous nitrite improves hemodynamics in a canine model of acute pulmonary thromboembolism. Free Radic Biol Med 2006; 41: 1764-70.
[97]
Khambata RS, Ghosh SM, Ahluwalia A. “Repurposing” of xanthine oxidoreductase as a nitrite reductase: A new paradigm for therapeutic targeting in hypertension. Antioxid Redox Signal 2015; 23: 340-53.
[98]
Ghosh SM, Kapil V, Fuentes-Calvo I, et al. Enhanced vasodilator activity of nitrite in hypertension: Critical role for erythrocytic xanthine oxidoreductase and translational potential. Hypertension 2013; 61: 1091-2.
[99]
Oliveira-Paula GH, Pinheiro LC, Guimaraes DA, et al. Tempol improves xanthine oxidoreductase-mediated vascular responses to nitrite in experimental renovascular hypertension. Redox Biol 2016; 8: 398-406.
[100]
Montenegro MF, Pinheiro LC, Amaral JH, et al. Vascular xanthine oxidoreductase contributes to the antihypertensive effects of sodium nitrite in L-NAME hypertension. Naunyn Schmiedebergs Arch Pharmacol 2014; 387: 591-8.
[101]
Peleli M, Zollbrecht C, Montenegro MF, et al. Enhanced XOR activity in eNOS-deficient mice: Effects on the nitrate-nitrite-NO pathway and ROS homeostasis. Free Radic Biol Med 2016; 99: 472-84.
[102]
Li H, Kundu TK, Zweier JL. Characterization of the magnitude and mechanism of aldehyde oxidase-mediated nitric oxide production from nitrite. J Biol Chem 2009; 284: 33850-8.
[103]
Garattini E, Fratelli M, Terao M. Mammalian aldehyde oxidases: Genetics, evolution and biochemistry. Cell Mol Life Sci 2008; 65: 1019-48.
[104]
Pinder AG, Pittaway E, Morris K, James PE. Nitrite directly vasodilates hypoxic vasculature via nitric oxide-dependent and -independent pathways. Br J Pharmacol 2009; 157: 1523-30.
[105]
Walters CL, Taylor AM. The Reduction of Nitrite by Skeletal-Muscle Mitochondria. Biochim Biophys Acta 1965; 96: 522-4.
[106]
Kozlov AV, Staniek K, Nohl H. Nitrite reductase activity is a novel function of mammalian mitochondria. FEBS Lett 1999; 454: 127-30.
[107]
Belikova NA, Vladimirov YA, Osipov AN, et al. Peroxidase activity and structural transitions of cytochrome c bound to cardiolipin-containing membranes. Biochemistry 2006; 45: 4998-5009.
[108]
Ascenzi P, Marino M, Polticelli F, Santucci R, Coletta M. Cardiolipin modulates allosterically the nitrite reductase activity of horse heart cytochrome c. J Biol Inorg Chem 2014; 19: 1195-201.
[109]
Ascenzi P, Sbardella D, Sinibaldi F, Santucci R, Coletta M. The nitrite reductase activity of horse heart carboxymethylated-cytochrome c is modulated by cardiolipin. J Biol Inorg Chem 2016; 21: 421-32.
[110]
Castello PR, David PS, McClure T, Crook Z, Poyton RO. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: Implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 2006; 3: 277-87.
[111]
Kevil CG, Kolluru GK, Pattillo CB, Giordano T. Inorganic nitrite therapy: Historical perspective and future directions. Free Radic Biol Med 2011; 51: 576-93.
[112]
Shiva S. Mitochondria as metabolizers and targets of nitrite. Nitric Oxide 2010; 22: 64-74.
[113]
Larsen FJ, Schiffer TA, Borniquel S, et al. Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metab 2011; 13: 149-59.
[114]
Montenegro MF, Sundqvist ML, Larsen FJ, et al. Blood pressure-lowering effect of orally ingested nitrite is abolished by a proton pump inhibitor. Hypertension 2017; 69: 23-31.
[115]
Montenegro MF, Pinheiro LC, Amaral JH, et al. Antihypertensive and antioxidant effects of a single daily dose of sodium nitrite in a model of renovascular hypertension. Naunyn Schmiedebergs Arch Pharmacol 2012; 385: 509-17.
[116]
Kapil V, Haydar SM, Pearl V, et al. Physiological role for nitrate-reducing oral bacteria in blood pressure control. Free Radic Biol Med 2013; 55: 93-100.
[117]
Bondonno CP, Liu AH, Croft KD, et al. Antibacterial mouthwash blunts oral nitrate reduction and increases blood pressure in treated hypertensive men and women. Am J Hypertens 2015; 28: 572-5.
[118]
McDonagh ST, Wylie LJ, Winyard PG, Vanhatalo A, Jones AM. The effects of chronic nitrate supplementation and the use of strong and weak antibacterial agents on plasma nitrite concentration and exercise blood pressure. Int J Sports Med 2015; 36: 1177-85.
[119]
Webb AJ, Patel N, Loukogeorgakis S, et al. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 2008; 51: 784-90.
[120]
Woessner M, Smoliga JM, Tarzia B, et al. A stepwise reduction in plasma and salivary nitrite with increasing strengths of mouthwash following a dietary nitrate load. Nitric Oxide 2016; 54: 1-7.
[121]
Petersson J, Carlstrom M, Schreiber O, et al. Gastroprotective and blood pressure lowering effects of dietary nitrate are abolished by an antiseptic mouthwash. Free Radic Biol Med 2009; 46: 1068-75.
[122]
Shapiro KB, Hotchkiss JH, Roe DA. Quantitative relationship between oral nitrate-reducing activity and the endogenous formation of N-nitrosoamino acids in humans. Food Chem Toxicol 1991; 29: 751-5.
[123]
Govoni M, Jansson EA, Weitzberg E, Lundberg JO. The increase in plasma nitrite after a dietary nitrate load is markedly attenuated by an antibacterial mouthwash. Nitric Oxide 2008; 19: 333-7.
[124]
Kramkowski K, Leszczynska A, Przyborowski K, et al. Role of xanthine oxidoreductase in the anti-thrombotic effects of nitrite in rats in vivo. Platelets 2016; 27: 245-53.
[125]
Carvalho CC, Tanus-Santos JE, Oliveira-Paula GH. Impaired xanthine oxidoreductase (XOR)-mediated nitrite reductase activity possibly involved in the lack of antihypertensive effects of XOR inhibitors. Hypertens Res 2017; 40: 301.
[126]
Pascart T, Richette P. Current and future therapies for gout. Expert Opin Pharmacother 2017; 18: 1201-11.
[127]
Pinheiro LC, Oliveira-Paula GH, Portella RL, Guimaraes DA, de Angelis CD, Tanus-Santos JE. Omeprazole impairs vascular redox biology and causes xanthine oxidoreductase-mediated endothelial dysfunction. Redox Biol 2016; 9: 134-43.
[128]
Ghebremariam YT, LePendu P, Lee JC, et al. Unexpected effect of proton pump inhibitors: elevation of the cardiovascular risk factor asymmetric dimethylarginine. Circulation 2013; 128: 845-53.
[129]
Bateman DN, Colin-Jones D, Hartz S, et al. Mortality study of 18 000 patients treated with omeprazole. Gut 2003; 52: 942-6.
[130]
Shah NH, LePendu P, Bauer-Mehren A, et al. Proton Pump Inhibitor Usage and the Risk of Myocardial Infarction in the General Population. PLoS One 2015; 10: e0124653.
[131]
Tsuchiya K, Kanematsu Y, Yoshizumi M, et al. Nitrite is an alternative source of NO in vivo. Am J Physiol Heart Circ Physiol 2005; 288: H2163-70.
[132]
Amaral JH, Montenegro MF, Pinheiro LC, et al. TEMPOL enhances the antihypertensive effects of sodium nitrite by mechanisms facilitating nitrite-derived gastric nitric oxide formation. Free Radical Biology and Medicine 2013; 65: 446-55.
[133]
Rocha BS, Nunes C, Pereira C, Barbosa RM, Laranjinha J. A shortcut to wide-ranging biological actions of dietary polyphenols: modulation of the nitrate-nitrite-nitric oxide pathway in the gut. Food Funct 2014; 5: 1646-52.
[134]
Rocha BS, Gago B, Pereira C, et al. Dietary nitrite in nitric oxide biology: A redox interplay with implications for pathophysiology and therapeutics. Curr Drug Targets 2011; 12: 1351-63.
[135]
Bjorne HH, Petersson J, Phillipson M, et al. Nitrite in saliva increases gastric mucosal blood flow and mucus thickness. J Clin Invest 2004; 113: 106-14.
[136]
Petersson J, Phillipson M, Jansson EA, et al. Dietary nitrate increases gastric mucosal blood flow and mucosal defense. Am J Physiol Gastrointest Liver Physiol 2007; 292: G718-24.
[137]
Caulfield JL, Singh SP, Wishnok JS, Deen WM, Tannenbaum SR. Bicarbonate inhibits N-nitrosation in oxygenated nitric oxide solutions. J Biol Chem 1996; 271: 25859-63.
[138]
Rowland IR, Granli T, Bockman OC, Key PE, Massey RC. Endogenous N-nitrosation in man assessed by measurement of apparent total N-nitroso compounds in faeces. Carcinogenesis 1991; 12: 1395-401.
[139]
Pignatelli B, Malaveille C, Rogatko A, et al. Mutagens, N-nitroso compounds and their precursors in gastric juice from patients with and without precancerous lesions of the stomach. Eur J Cancer 1993; 29A: 2031-9.
[140]
Sobala GM, Schorah CJ, Sanderson M, et al. Ascorbic acid in the human stomach. Gastroenterology 1989; 97: 357-63.
[141]
Helser MA, Hotchkiss JH, Roe DA. Influence of fruit and vegetable juices on the endogenous formation of N-nitrosoproline and N-nitrosothiazolidine-4-carboxylic acid in humans on controlled diets. Carcinogenesis 1992; 13: 2277-80.
[142]
Tannenbaum SR, Wishnok JS, Leaf CD. Inhibition of nitrosamine formation by ascorbic acid. Am J Clin Nutr 1991; 53: 247S-50S.
[143]
Kobayashi J, Ohtake K, Uchida H. NO-rich diet for lifestyle-related diseases. Nutrients 2015; 7: 4911-37.
[144]
Bonetti J, Zhou Y, Parent M, et al. Intestinal absorption of S-nitrosothiols: Permeability and transport mechanisms. Biochem Pharmacol 2018; 155: 21-31.
[145]
Smith BC, Marletta MA. Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling. Curr Opin Chem Biol 2012; 16: 498-506.
[146]
Broniowska KA, Hogg N. The chemical biology of S-nitrosothiols. Antioxid Redox Signal 2012; 17: 969-80.
[147]
Hogg N. Biological chemistry and clinical potential of S-nitrosothiols. Free Radic Biol Med 2000; 28: 1478-86.
[148]
Wolzt M, MacAllister RJ, Davis D, et al. Biochemical characterization of S-nitrosohemoglobin. Mechanisms underlying synthesis, no release, and biological activity. J Biol Chem 1999; 274: 28983-90.
[149]
Ignarro LJ, Lippton H, Edwards JC, et al. Mechanism of vascular smooth muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric oxide: Evidence for the involvement of S-nitrosothiols as active intermediates. J Pharmacol Exp Ther 1981; 218: 739-49.
[150]
Ignarro LJ, Edwards JC, Gruetter DY, Barry BK, Gruetter CA. Possible involvement of S-nitrosothiols in the activation of guanylate cyclase by nitroso compounds. FEBS Lett 1980; 110: 275-8.
[151]
Edwards JC, Ignarro LJ, Hyman AL, Kadowitz PJ. Relaxation of intrapulmonary artery and vein by nitrogen oxide-containing vasodilators and cyclic GMP. J Pharmacol Exp Ther 1984; 228: 33-42.
[152]
Murphy E, Kohr M, Sun J, Nguyen T, Steenbergen C. S-nitrosylation: A radical way to protect the heart. J Mol Cell Cardiol 2012; 52: 568-77.
[153]
Kumar V, Calamaras TD, Haeussler D, et al. Cardiovascular redox and ox stress proteomics. Antioxid Redox Signal 2012; 17: 1528-59.
[154]
Machha A, Schechter AN. Dietary nitrite and nitrate: A review of potential mechanisms of cardiovascular benefits. Eur J Nutr 2011; 50: 293-303.
[155]
Classen HG, Stein-Hammer C, Thoni H. Hypothesis: The effect of oral nitrite on blood pressure in the spontaneously hypertensive rat. Does dietary nitrate mitigate hypertension after conversion to nitrite? J Am Coll Nutr 1990; 9: 500-2.
[156]
Haas M, Classen HG, Thoni H, Classen UG, Drescher B. Persistent antihypertensive effect of oral nitrite supplied up to one year via the drinking water in spontaneously hypertensive rats. Arzneimittelforschung 1999; 49: 318-23.
[157]
Beier S, Classen HG, Loeffler K, Schumacher E, Thoni H. Antihypertensive effect of oral nitrite uptake in the spontaneously hypertensive rat. Arzneimittelforschung 1995; 45: 258-61.
[158]
Pinheiro LC, Amaral JH, Ferreira GC, Montenegro MF, Oliveira-Paula GH, Tanus-Santos JE. The antihypertensive effects of sodium nitrite are not associated with circulating angiotensin converting enzyme inhibition. Nitric Oxide 2014; 40: 52-9.
[159]
Montenegro MF, Amaral JH, Pinheiro LC, et al. Sodium nitrite downregulates vascular NADPH oxidase and exerts antihypertensive effects in hypertension. Free Radic Biol Med 2011; 51: 144-52.
[160]
Amaral JH, Ferreira GC, Pinheiro LC, et al. Consistent antioxidant and antihypertensive effects of oral sodium nitrite in DOCA-salt hypertension. Redox Biol 2015; 5: 340-6.
[161]
Meschiari CA, Pinheiro LC, Guimaraes DA, Gerlach RF, Tanus-Santos JE. Sodium nitrite attenuates MMP-9 production by endothelial cells and may explain similar effects of atorvastatin. Naunyn Schmiedebergs Arch Pharmacol 2016; 389: 223-31.
[162]
Guimaraes DA, Rizzi E, Ceron CS, et al. Atorvastatin and sildenafil lower blood pressure and improve endothelial dysfunction, but only atorvastatin increases vascular stores of nitric oxide in hypertension. Redox Biol 2013; 1: 578-85.
[163]
Oliveira-Paula GH, Lacchini R, Pinheiro LC, et al. Endothelial nitric oxide synthase polymorphisms affect the changes in blood pressure and nitric oxide bioavailability induced by propofol. Nitric Oxide 2018; 75: 77-84.
[164]
Oliveira-Paula GH, Pinheiro LC, Ferreira GC, et al. Angiotensin converting enzyme inhibitors enhance the hypotensive effects of propofol by increasing nitric oxide production. Free Radic Biol Med 2018; 115: 10-7.
[165]
van Faassen EE, Bahrami S, Feelisch M, et al. Nitrite as regulator of hypoxic signaling in mammalian physiology. Med Res Rev 2009; 29: 683-741.
[166]
Kapil V, Milsom AB, Okorie M, et al. Inorganic nitrate supplementation lowers blood pressure in humans: Role for nitrite-derived NO. Hypertension 2010; 56: 274-81.
[167]
Whalen EJ, Foster MW, Matsumoto A, et al. Regulation of beta-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell 2007; 129: 511-22.
[168]
Guimaraes S, Moura D. Vascular adrenoceptors: An update. Pharmacol Rev 2001; 53: 319-56.
[169]
Chruscinski A, Brede ME, Meinel L, et al. Differential distribution of beta-adrenergic receptor subtypes in blood vessels of knockout mice lacking beta(1)- or beta(2)-adrenergic receptors. Mol Pharmacol 2001; 60: 955-62.
[170]
Lefkowitz RJ, Rockman HA, Koch WJ. Catecholamines, cardiac beta-adrenergic receptors, and heart failure. Circulation 2000; 101: 1634-7.
[171]
Motomura S, Reinhard-Zerkowski H, Daul A, Brodde OE. On the physiologic role of beta-2 adrenoceptors in the human heart: in vitro and in vivo studies. Am Heart J 1990; 119: 608-19.
[172]
Zhao Y, Vanhoutte PM, Leung SW. Vascular nitric oxide: Beyond eNOS. J Pharmacol Sci 2015; 129: 83-94.
[173]
Nozik-Grayck E, Whalen EJ, Stamler JS, et al. S-nitrosoglutathione inhibits alpha1-adrenergic receptor-mediated vasoconstriction and ligand binding in pulmonary artery. Am J Physiol Lung Cell Mol Physiol 2006; 290: L136-43.
[174]
Leclerc PC, Lanctot PM, Auger-Messier M, et al. S-nitrosylation of cysteine 289 of the AT1 receptor decreases its binding affinity for angiotensin II. Br J Pharmacol 2006; 148: 306-13.
[175]
Selemidis S, Dusting GJ, Peshavariya H, et al. Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 2007; 75: 349-58.
[176]
Guimaraes DA, Dos Passos MA, Rizzi E, et al. Nitrite exerts antioxidant effects, inhibits the mTOR pathway and reverses hypertension-induced cardiac hypertrophy. Free Radic Biol Med 2018; 120: 25-32.
[177]
Maejima Y, Adachi S, Morikawa K, Ito H, Isobe M. Nitric oxide inhibits myocardial apoptosis by preventing caspase-3 activity via S-nitrosylation. J Mol Cell Cardiol 2005; 38: 163-74.
[178]
Atar S, Ye Y, Lin Y, et al. Atorvastatin-induced cardioprotection is mediated by increasing inducible nitric oxide synthase and consequent S-nitrosylation of cyclooxygenase-2. Am J Physiol Heart Circ Physiol 2006; 290: H1960-8.
[179]
Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ Res 2010; 106: 633-46.
[180]
Tao L, Gao E, Bryan NS, et al. Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: Role of S-nitrosation [corrected]. Proc Natl Acad Sci USA 2004; 101: 11471-6.
[181]
Stsiapura VI, Bederman I, Stepuro II, et al. S-Nitrosoglutathione formation at gastric pH is augmented by ascorbic acid and by the antioxidant vitamin complex, Resiston. Pharm Biol 2018; 56: 86-93.
[182]
Smith JN, Dasgupta TP. Kinetics and mechanism of the decomposition of S-nitrosoglutathione by l-ascorbic acid and copper ions in aqueous solution to produce nitric oxide. Nitric Oxide 2000; 4: 57-66.
[183]
Kashiba-Iwatsuki M, Yamaguchi M, Inoue M. Role of ascorbic acid in the metabolism of S-nitroso-glutathione. FEBS Lett 1996; 389: 149-52.
[184]
Liu L, Hausladen A, Zeng M, et al. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 2001; 410: 490-4.
[185]
Que LG, Liu L, Yan Y, et al. Protection from experimental asthma by an endogenous bronchodilator. Science 2005; 308: 1618-21.
[186]
Liu L, Yan Y, Zeng M, et al. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 2004; 116: 617-28.
[187]
Lima B, Lam GK, Xie L, et al. Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci USA 2009; 106: 6297-302.
[188]
Sanghani PC, Davis WI, Fears SL, et al. Kinetic and cellular characterization of novel inhibitors of S-nitrosoglutathione reductase. J Biol Chem 2009; 284: 24354-62.
[189]
Chen Q, Sievers RE, Varga M, et al. Pharmacological inhibition of S-nitrosoglutathione reductase improves endothelial vasodilatory function in rats in vivo. J Appl Physiol 1985; 2013(114): 752-60.
[190]
Gaucher C, Boudier A, Dahboul F, Parent M, Leroy P. S-nitrosation/denitrosation in cardiovascular pathologies: Facts and concepts for the rational design of S-nitrosothiols. Curr Pharm Des 2013; 19: 458-72.
[191]
Fernandes DC, Manoel AH, Wosniak J Jr, Laurindo FR. Protein disulfide isomerase overexpression in vascular smooth muscle cells induces spontaneous preemptive NADPH oxidase activation and Nox1 mRNA expression: Effects of nitrosothiol exposure. Arch Biochem Biophys 2009; 484: 197-204.
[192]
Galinski CN, Zwicker JI, Kennedy DR. Revisiting the mechanistic basis of the French Paradox: Red wine inhibits the activity of protein disulfide isomerase in vitro. Thromb Res 2016; 137: 169-73.
[193]
Barnett SD, Buxton ILO. The role of S-nitrosoglutathione reductase (GSNOR) in human disease and therapy. Crit Rev Biochem Mol Biol 2017; 52: 340-54.
[194]
Seabra AB, Justo GZ, Haddad PS. State of the art, challenges and perspectives in the design of nitric oxide-releasing polymeric nanomaterials for biomedical applications. Biotechnol Adv 2015; 33: 1370-9.
[195]
De Jong WH, Borm PJ. Drug delivery and nanoparticles: Applications and hazards. Int J Nanomedicine 2008; 3: 133-49.
[196]
Kumari A, Yadav SK, Yadav SC. Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces 2010; 75: 1-18.
[197]
Ferraz LS, Watashi CM, Colturato-Kido C, et al. Antitumor Potential of s-nitrosothiol-containing polymeric nanoparticles against melanoma. Mol Pharm 2018; 15: 1160-8.
[198]
Seabra AB, Pasquoto T, Ferrarini AC, et al. Preparation, characterization, cytotoxicity, and genotoxicity evaluations of thiolated- and s-nitrosated superparamagnetic iron oxide nanoparticles: Implications for cancer treatment. Chem Res Toxicol 2014; 27: 1207-18.
[199]
Cardozo VF, Lancheros CA, Narciso AM, et al. Evaluation of antibacterial activity of nitric oxide-releasing polymeric particles against Staphylococcus aureus and Escherichia coli from bovine mastitis. Int J Pharm 2014; 473: 20-9.
[200]
Wold KA, Damodaran VB, Suazo LA, Bowen RA, Reynolds MM. Fabrication of biodegradable polymeric nanofibers with covalently attached NO donors. ACS Appl Mater Interfaces 2012; 4: 3022-30.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 4
Year: 2019
Page: [431 - 443]
Pages: 13
DOI: 10.2174/1389450119666180816120816

Article Metrics

PDF: 30
HTML: 5