Inorganic nitrate attenuates cardiac dysfunction: roles for xanthine oxidoreductase and nitric oxide.
NO
heart failure
hypertension
nitrate
oxidative stress
xanthine dehydrogenase
Journal
British journal of pharmacology
ISSN: 1476-5381
Titre abrégé: Br J Pharmacol
Pays: England
ID NLM: 7502536
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
01
07
2021
received:
29
01
2021
accepted:
03
07
2021
pubmed:
27
7
2021
medline:
21
9
2022
entrez:
26
7
2021
Statut:
ppublish
Résumé
NO is a vasodilator and independent modulator of cardiac remodelling. Commonly, in cardiac disease (e.g., heart failure), endothelial dysfunction (synonymous with NO deficiency) has been implicated in increased BP, cardiac hypertrophy and fibrosis. Currently, no effective therapies replacing NO have succeeded in the clinic. Inorganic nitrate (NO We analysed demographics in a nested age- and sex-matched case-control study of hypertensive patients with or without left ventricular hypertrophy (NCT03088514) and assessed the effects of dietary nitrate in mouse models of cardiac dysfunction. Lower plasma nitrite concentrations and vascular dysfunction accompanied cardiac hypertrophy and fibrosis in patients. In mouse models of cardiac remodelling, restoration of circulating nitrite levels using dietary nitrate improved endothelial dysfunction through targeting the xanthine oxidoreductase-driven increase in levels of H Dietary nitrate offers easily translatable therapeutic options for delivery of NO and thereby treatment of cardiac dysfunction.
Sections du résumé
BACKGROUND AND PURPOSE
NO is a vasodilator and independent modulator of cardiac remodelling. Commonly, in cardiac disease (e.g., heart failure), endothelial dysfunction (synonymous with NO deficiency) has been implicated in increased BP, cardiac hypertrophy and fibrosis. Currently, no effective therapies replacing NO have succeeded in the clinic. Inorganic nitrate (NO
EXPERIMENTAL APPROACH
We analysed demographics in a nested age- and sex-matched case-control study of hypertensive patients with or without left ventricular hypertrophy (NCT03088514) and assessed the effects of dietary nitrate in mouse models of cardiac dysfunction.
KEY RESULTS
Lower plasma nitrite concentrations and vascular dysfunction accompanied cardiac hypertrophy and fibrosis in patients. In mouse models of cardiac remodelling, restoration of circulating nitrite levels using dietary nitrate improved endothelial dysfunction through targeting the xanthine oxidoreductase-driven increase in levels of H
CONCLUSIONS AND IMPLICATIONS
Dietary nitrate offers easily translatable therapeutic options for delivery of NO and thereby treatment of cardiac dysfunction.
Substances chimiques
Nitrates
0
Nitrites
0
Vasodilator Agents
0
Superoxides
11062-77-4
Nitric Oxide
31C4KY9ESH
Xanthine Dehydrogenase
EC 1.17.1.4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4757-4777Subventions
Organisme : British Heart Foundation
ID : PG/19/4/33995
Pays : United Kingdom
Organisme : Medical Research Council
Pays : United Kingdom
Informations de copyright
© 2021 The Authors. British Journal of Pharmacology published by John Wiley & Sons Ltd on behalf of British Pharmacological Society.
Références
Adlam, D., De Bono, J. P., Danson, E. J., Zhang, M. H., Casadei, B., Paterson, D. J., & Channon, K. M. (2011). Telemetric analysis of haemodynamic regulation during voluntary exercise training in mouse models. Experimental Physiology, 96(11), 1118-1128. https://doi.org/10.1113/expphysiol.2011.059261
Ahluwalia, A., Gladwin, M., Coleman, G. D., Hord, N., Howard, G., Kim-Shapiro, D. B., Lajous, M., Larsen, F. J., Lefer, D. J., McClure, L. A., Nolan, B. T., Pluta, R., Schechter, A., Wang, C. Y., Ward, M. H., & Harman, J. L. (2016). Dietary nitrate and the epidemiology of cardiovascular disease: Report from a National Heart, Lung, and Blood Institute Workshop. Journal of the American Heart Association, 5(7), e003402. https://doi.org/10.1161/JAHA.1116.003402
Akiyama, E., Sugiyama, S., Matsuzawa, Y., Konishi, M., Suzuki, H., Nozaki, T., Ohba, K., Matsubara, J., Maeda, H., Horibata, Y., Sakamoto, K., Sugamura, K., Yamamuro, M., Sumida, H., Kaikita, K., Iwashita, S., Matsui, K., Kimura, K., Umemura, S., & Ogawa, H. (2012). Incremental prognostic significance of peripheral endothelial dysfunction in patients with heart failure with normal left ventricular ejection fraction. Journal of the American College of Cardiology, 60(18), 1778-1786. https://doi.org/10.1016/j.jacc.2012.07.036
Alexander, S. P., Christopoulos, A., Davenport, A. P., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Abbracchio, M. P., Alexander, W., Al-hosaini, K., Bäck, M., Barnes, N. M., Bathgate, R., … Ye, R. D. (2021). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: G protein-coupled receptors. British Journal of Pharmacology, 178, S27-S156. https://doi.org/10.1111/bph.15538
Alexander, S. P., Fabbro, D., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Boison, D., Burns, K. E., Dessauer, C., Gertsch, J., Helsby, N. A., Izzo, A. A., Koesling, D., … Wong, S. S. (2021a). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: Enzymes. British Journal of Pharmacology, 178, S313-S411. https://doi.org/10.1111/bph.15542
Alexander, S. P., Fabbro, D., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Beuve, A., Brouckaert, P., Bryant, C., Burnett, J. C., Farndale, R. W., Friebe, A., Garthwaite, J., … Waldman, S. A. (2021b). THE CONCISE GUIDE TO PHARMACOLOGY 2021/22: Catalytic receptors. British Journal of Pharmacology, 178, S264-S312. https://doi.org/10.1111/bph.15541
Amado, L. C., Saliaris, A. P., Raju, S. V. Y., Lehrke, S., St John, M., Xie, J., Stewart, G., Fitton, T., Minhas, K. M., Brawn, J., & Hare, J. M. (2005). Xanthine oxidase inhibition ameliorates cardiovascular dysfunction in dogs with pacing-induced heart failure. Journal of Molecular and Cellular Cardiology, 39(3), 531-536. https://doi.org/10.1016/j.yjmcc.2005.04.008
Barouch, L. A., Cappola, T. P., Harrison, R. W., Crone, J. K., Rodriguez, E. R., Burnett, A. L., & Hare, J. M. (2003). Combined loss of neuronal and endothelial nitric oxide synthase causes premature mortality and age-related hypertrophic cardiac remodeling in mice. Journal of Molecular and Cellular Cardiology, 35(6), 637-644. https://doi.org/10.1016/S0022-2828(03)00079-8
Barouch, L. A., Harrison, R. W., Skaf, M. W., Rosas, G. O., Cappola, T. P., Kobeissi, Z. A., Hobai, I. A., Lemmon, C. A., Burnett, A. L., O'Rourke, B., Rodriguez, E. R., Huang, P. L., Lima, J. A. C., Berkowitz, D. E., & Hare, J. M. (2002). Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature, 416(6878), 337-339. https://doi.org/10.1038/416337a
Berk, B. C., Fujiwara, K., & Lehoux, S. (2007). ECM remodeling in hypertensive heart disease. The Journal of Clinical Investigation, 117(3), 568-575. https://doi.org/10.1172/JCI31044
Berry, C. E., & Hare, J. M. (2004). Xanthine oxidoreductase and cardiovascular disease: Molecular mechanisms and pathophysiological implications. The Journal of Physiology, 555(Pt 3), 589-606. https://doi.org/10.1113/jphysiol.2003.055913
Bhushan, S., Kondo, K., Polhemus, D. J., Otsuka, H., Nicholson, C. K., Tao, Y.-X., Huang, H., Georgiopoulou, V. V., Murohara, T., Calvert, J. W., Butler, J., & Lefer, D. J. (2014). Nitrite therapy improves left ventricular function during heart failure via restoration of nitric oxide-mediated cytoprotective signaling. Circulation Research, 114(8), 1281-1291. https://doi.org/10.1161/CIRCRESAHA.114.301475
Bondonno, C. P., Liu, A. H., Croft, K. D., Ward, N. C., Shinde, S., Moodley, Y., Lundberg, J. O., Puddey, I. B., Woodman, R. J., & Hodgson, J. M. (2015). Absence of an effect of high nitrate intake from beetroot juice on blood pressure in treated hypertensive individuals: A randomized controlled trial. The American Journal of Clinical Nutrition, 102(2), 368-375. https://doi.org/10.3945/ajcn.114.101188
Borlaug, B. A., Anstrom, K. J., Lewis, G. D., Shah, S. J., Levine, J. A., Koepp, G. A., Givertz, M. M., Felker, G. M., LeWinter, M. M., Mann, D. L., Margulies, K. B., Smith, A. L., Tang, W. H. W., Whellan, D. J., Chen, H. H., Davila-Roman, V. G., McNulty, S., Desvigne-Nickens, P., Hernandez, A. F., … Blood Institute Heart Failure Clinical Research Network. (2018). Effect of inorganic nitrite vs placebo on exercise capacity among patients with heart failure with preserved ejection fraction: The INDIE-HFpEF randomized clinical trial. JAMA, 320(17), 1764-1773.
Borlaug, B. A., Melenovsky, V., & Koepp, K. E. (2016). Inhaled sodium nitrite improves rest and exercise hemodynamics in heart failure with preserved ejection fraction. Circulation Research, 119, 880-886. https://doi.org/10.1161/CIRCRESAHA.116.309184
Broekmans, K., Giesen, J., Menges, L., Koesling, D., & Russwurm, M. (2020). Angiotensin II-induced cardiovascular fibrosis is attenuated by NO-sensitive guanylyl cyclase1. Cell, 9(11), 2436-2447. https://doi.org/10.3390/cells9112436
Brunner, H., Cockcroft, J. R., Deanfield, J., Donald, A., Ferrannini, E., Halcox, J., Kiowski, W., Lüscher, T. F., Mancia, G., Natali, A., Oliver, J. J., Pessina, A. C., Rizzoni, D., Rossi, G. P., Salvetti, A., Spieker, L. E., Taddei, S., & Webb, D. J. (2005). Endothelial function and dysfunction. Part II: Association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension*. Journal of Hypertension, 23(2), 233-246. https://doi.org/10.1097/00004872-200502000-00001
Cai, H., & Harrison, D. G. (2000). Endothelial dysfunction in cardiovascular diseases: The role of oxidant stress. Circulation Research, 87, 840-844. https://doi.org/10.1161/01.RES.87.10.840
Chang, H.-R., Wu, C. Y., Hsu, Y.-H., & Chen, H. I. (2005). Reduction of ventricular hypertrophy and fibrosis in spontaneously hypertensive rats by l-arginine. The Chinese Journal of Physiology, 48(1), 15-22.
Chang, S. C., Ren, S., Rau, C. D., & Wang, J. J. (2018). Isoproterenol-induced heart failure mouse model using osmotic pump implantation. Methods in Molecular Biology (Clifton, N.J.), 1816, 207-220.
Chen, H.-H., Chu, Y.-S., Hu, Y.-C., & Lin, R.-T. (2012). An occupational hazard emergency that presented as methemoglobinemia. Journal of Acute Medicine, 2(2), 58-61. https://doi.org/10.1016/j.jacme.2012.05.001
Chidambaram, V. A., Tun, N. L., Haque, W. Z., Majella, M. A.-O., Sivakumar, R. K., Kumar, A., Hsu, A. T., Ishak, I. A., Nur, A. A., Ayeh, S. K., Salia, E. L., Zil-E-Ali, A., Saeed, M. A., Sarena, A. P. B., Seth, B., Ahmadzada, M., Haque, E. F., Neupane, P., Wang, K. H., … Galiatsatos, P. (2020). Factors associated with disease severity and mortality among patients with COVID-19: A systematic review and meta-analysis. PLoS ONE, 15(1932-6203), e0241541. https://doi.org/10.1371/journal.pone.0241541
Chirinos, J. A., & Zamani, P. (2016). The nitrate-nitrite-NO pathway and its implications for heart failure and preserved ejection fraction. Current Heart Failure Reports, 13(1), 47-59. https://doi.org/10.1007/s11897-016-0277-9
Coggan, A. R., Leibowitz, J. L., Anderson Spearie, C., Kadkhodayan, A., Thomas, D. P., Ramamurthy, S., Mahmood, K., Park, S., Waller, S., Farmer, M., & Peterson, L. R. (2015). Acute dietary nitrate intake improves muscle contractile function in patients with heart failure: A double-blind, placebo-controlled, randomized trial. Circulation Heart Failure, 8, 914-920. https://doi.org/10.1161/CIRCHEARTFAILURE.115.002141
Curtis, M. J., Alexander, S., Cirino, G., Docherty, J. R., George, C. H., Giembycz, M. A., Hoyer, D., Insel, P. A., Izzo, A. A., Ji, Y., MacEwan, D. J., Sobey, C. G., Stanford, S. C., Teixeira, M. M., Wonnacott, S., & Ahluwalia, A. (2018). Experimental design and analysis and their reporting II: Updated and simplified guidance for authors and peer reviewers. British Journal of Pharmacology, 175(7), 987-993. https://doi.org/10.1111/bph.14153
de Simone, G. (2004). Concentric or eccentric hypertrophy: How clinically relevant is the difference? Hypertension, 43(4), 714-715. https://doi.org/10.1161/01.HYP.0000121363.08252.a7
Drexler, H., Hayoz, D., Munzel, T., Hornig, B., Just, H., Brunner, H. R., & Zelis, R. (1992). Endothelial function in chronic congestive heart failure. The American Journal of Cardiology, 69(19), 1596-1601. https://doi.org/10.1016/0002-9149(92)90710-G
Eggebeen, J., Kim-Shapiro, D. B., Haykowsky, M., Morgan, T. M., Basu, S., Brubaker, P., Rejeski, J., & Kitzman, D. W. (2016). One week of daily dosing with beetroot juice improves submaximal endurance and blood pressure in older patients with heart failure and preserved ejection fraction. JACC. Heart Failure, 4, 428-437. https://doi.org/10.1016/j.jchf.2015.12.013
Ekelund, U. E., Harrison, R. W., Shokek, O., Thakkar, R. N., Tunin, R. S., Senzaki, H., … Hare, J. M. (1999). Intravenous allopurinol decreases myocardial oxygen consumption and increases mechanical efficiency in dogs with pacing-induced heart failure. Circulation Research, 85(5), 437-445. https://doi.org/10.1161/01.RES.85.5.437
Feig, D. I., Madero, M., Jalal, D. I., Sanchez-Lozada, L. G., & Johnson, R. J. (2013). Uric acid and the origins of hypertension. The Journal of Pediatrics, 162(5), 896-902. https://doi.org/10.1016/j.jpeds.2012.12.078
Feig, D. I., Soletsky, B., & Johnson, R. J. (2008). Effect of allopurinol on blood pressure of adolescents with newly diagnosed essential hypertension: A randomized trial. JAMA, 300(8), 924-932. https://doi.org/10.1001/jama.300.8.924
Ferguson, S. K., Hirai, D. M., Copp, S. W., Holdsworth, C. T., Allen, J. D., Jones, A. M., Musch, T. I., & Poole, D. C. (2013). Effects of nitrate supplementation via beetroot juice on contracting rat skeletal muscle microvascular oxygen pressure dynamics. Respiratory Physiology & Neurobiology, 187(3), 250-255. https://doi.org/10.1016/j.resp.2013.04.001
Ferguson, S. K., Holdsworth, C. T., Colburn, T. D., Wright, J. L., Craig, J. C., Fees, A., Jones, A. M., Allen, J. D., Musch, T. I., & Poole, D. C. (2016). Dietary nitrate supplementation: Impact on skeletal muscle vascular control in exercising rats with chronic heart failure. Journal of Applied Physiology, 121(3), 661-669. https://doi.org/10.1152/japplphysiol.00014.2016
Fraccarollo, D., Widder, J. D., Galuppo, P., Thum, T., Tsikas, D., Hoffmann, M., Ruetten, H., Ertl, G., & Bauersachs, J. (2008). Improvement in left ventricular remodeling by the endothelial nitric oxide synthase enhancer AVE9488 after experimental myocardial infarction. Circulation, 118(8), 818-827. https://doi.org/10.1161/CIRCULATIONAHA.107.717702
Franssen, C., Chen, S., Unger, A., Korkmaz, H. I., De Keulenaer, G. W., Tschöpe, C., Leite-Moreira, A. F., Musters, R., Niessen, H. W., Linke, W. A., Paulus, W. J., & Hamdani, N. (2016). Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC: Heart Failure, 4(4), 312-324. https://doi.org/10.1016/j.jchf.2015.10.007
Gaasch, W. H., & Zile, M. R. (2011). Left ventricular structural remodeling in health and disease: With special emphasis on volume, mass, and geometry. Journal of the American College of Cardiology, 58(17), 1733-1740. https://doi.org/10.1016/j.jacc.2011.07.022
Ghosh, S. M., Kapil, V., Fuentes-Calvo, I., Bubb, K. J., Pearl, V., Milsom, A. B., Khambata, R., Maleki-Toyserkani, S., Yousuf, M., Benjamin, N., Webb, A. J., Caulfield, M. J., Hobbs, A. J., & Ahluwalia, A. (2013). Enhanced Vasodilator Activity of Nitrite in Hypertension: Critical Role for Erythrocytic Xanthine Oxidoreductase and Translational Potential. Hypertension, 61, 1091-1102.
Hernández, A., Schiffer, T. A., Ivarsson, N., Cheng, A. J., Bruton, J. D., Lundberg, J. O., Weitzberg, E., & Westerblad, H. (2012). Dietary nitrate increases tetanic [Ca2+]i and contractile force in mouse fast-twitch muscle. The Journal of Physiology, 590(15), 3575-3583. https://doi.org/10.1113/jphysiol.2012.232777
Hirai, D. M., Zelt, J. T., Jones, J. H., Castanhas, L. G., Bentley, R. F., Earle, W., Staples, P., Tschakovsky, M. E., McCans, J., O'Donnell, D. E., & Neder, J. A. (2017). Dietary nitrate supplementation and exercise tolerance in patients with heart failure with reduced ejection fraction. Am J Physiol Reg Integr Comp Physiol, 312(1), R13-R22. https://doi.org/10.1152/ajpregu.00263.2016
Hou, J., Kato, H., Cohen, R. A., Chobanian, A. V., & Brecher, P. (1995). Angiotensin II-induced cardiac fibrosis in the rat is increased by chronic inhibition of nitric oxide synthase. Journal of Clinical Investigation, 96(5), 2469-2477. https://doi.org/10.1172/JCI118305
Hunault, C. C., van Velzen, A. G., Sips, A. J. A. M., Schothorst, R. C., & Meulenbelt, J. (2009). Bioavailability of sodium nitrite from an aqueous solution in healthy adults. Toxicology Letters, 190(1), 48-53. https://doi.org/10.1016/j.toxlet.2009.06.865
Hunter, J. J., & Chien, K. R. (1999). Signaling pathways for cardiac hypertrophy and failure. New England Journal of Medicine, 341(17), 1276-1283. https://doi.org/10.1056/NEJM199910213411706
Ignarro, L. J., Fukuto, J. M., Griscavage, J. M., Rogers, N. E., & Byrns, R. E. (1993). Oxidation of nitric oxide in aqueous solution to nitrite but not nitrate: comparison with enzymatically formed nitric oxide from L-arginine. Proceedings of the National Academy of Sciences, 90, 8103-8107.
Kapil, V., Haydar, S. M. A., Pearl, V., Lundberg, J. O., Weitzberg, E., & Ahluwalia, A. (2013). Physiological role for nitrate-reducing oral bacteria in blood pressure control. Free Radical Biology & Medicine, 55, 93-100. https://doi.org/10.1016/j.freeradbiomed.2012.11.013
Kapil, V., Khambata, R. S., Jones, D. A., Rathod, K., Primus, C., Massimo, G., Fukuto, J. M., & Ahluwalia, A. (2020). The noncanonical pathway for in vivo nitric oxide generation: The nitrate-nitrite-nitric oxide pathway. Pharmacological Reviews, 72(3), 692-766. https://doi.org/10.1124/pr.120.019240
Kapil, V., Khambata, R. S., Robertson, A., Caulfield, M. J., & Ahluwalia, A. (2015). Dietary nitrate provides sustained blood pressure lowering in hypertensive patients: A randomized phase 2, double-blind, placebo-controlled study. Hypertension, 65, 320-327. https://doi.org/10.1161/HYPERTENSIONAHA.114.04675
Kapil, V., Milsom, A. B., Okorie, M., Maleki-Toyserkani, S., Akram, F., Rehman, F., Arghandawi, S., Pearl, V., Benjamin, N., & Loukogeorgakis, S. (2010). Inorganic nitrate supplementation lowers blood pressure in humans: Role for nitrite-derived NO. Hypertension, 56, 274-281. https://doi.org/10.1161/HYPERTENSIONAHA.110.153536
Katholi, R. E., & Couri, D. M. (2011). Left ventricular hypertrophy: Major risk factor in patients with hypertension: Update and practical clinical applications. International Journal of Hypertension, 2011(1), 495349-495310.
Katz Stuart, D., Khan, T., Zeballos Guillermo, A., Mathew, L., Potharlanka, P., Knecht, M., & Whelan, J. (1999). Decreased activity of the l-arginine-nitric oxide metabolic pathway in patients with congestive heart failure. Circulation, 99(16), 2113-2117. https://doi.org/10.1161/01.CIR.99.16.2113
Kelley, E. E., Hock, T., Khoo, N. K. H., Richardson, G. R., Johnson, K. K., Powell, P. C., Giles, G. I., Agarwal, A., Lancaster, J. R. Jr., & Tarpey, M. M. (2006). Moderate hypoxia induces xanthine oxidoreductase activity in arterial endothelial cells. Free Radical Biology and Medicine, 40, 952-959. https://doi.org/10.1016/j.freeradbiomed.2005.11.008
Khambata, R. S., Ghosh, S. M., & Ahluwalia, A. (2015). “Repurposing” of xanthine oxidoreductase as a nitrite reductase: A new paradigm for therapeutic targeting in hypertension. Antioxidants & Redox Signaling, 23(4), 340-353. https://doi.org/10.1089/ars.2015.6254
Khambata, R. S., Ghosh, S. M., Rathod, K. S., Thevathasan, T., Filomena, F., Xiao, Q., & Ahluwalia, A. (2017). Antiinflammatory actions of inorganic nitrate stabilize the atherosclerotic plaque. Proceedings of the National Academy of Sciences of the United States of America, 114(4), E550-E559. https://doi.org/10.1073/pnas.1613063114
Kleinbongard, P., Dejam, A., Lauer, T., Rassaf, T., Schindler, A., Picker, O., Scheeren, T., Gödecke, A., Schrader, J., Schulz, R., Heusch, G., Schaub, G. A., Bryan, N. S., Feelisch, M., & Kelm, M. (2003). Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radical Biology & Medicine, 35(7), 790-796. https://doi.org/10.1016/S0891-5849(03)00406-4
Kubo, S. H., Rector, T. S., Bank, A. J., Williams, R. E., & Heifetz, S. M. (1991). Endothelium-dependent vasodilation is attenuated in patients with heart failure. Circulation, 84(4), 1589-1596. https://doi.org/10.1161/01.CIR.84.4.1589
Laakso, J., Mervaala, E., Himberg, J.-J., Teräväinen, T.-L., Karppanen, H., Vapaatalo, H., & Lapatto, R. (1998). Increased kidney xanthine oxidoreductase activity in salt-induced experimental hypertension. Hypertension, 32(5), 902-906.
Laakso, J. T., Teravainen, T. L., Martelin, E., Vaskonen, T., & Lapatto, R. (2004). Renal xanthine oxidoreductase activity during development of hypertension in spontaneously hypertensive rats. Journal of Hypertension, 22(7), 1333-1340. https://doi.org/10.1097/01.hjh.0000125441.28861.9f
Lam, C. S. P., & Brutsaert, D. L. (2012). Endothelial dysfunction: A pathophysiologic factor in heart failure with preserved ejection fraction. Journal of the American College of Cardiology, 60(18), 1787-1789. https://doi.org/10.1016/j.jacc.2012.08.004
Larsen, F. J., Schiffer, T. A., Borniquel, S., Sahlin, K., Ekblom, B., Lundberg, J. O., & Weitzberg, E. (2011). Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metabolism, 13(2), 149-159. https://doi.org/10.1016/j.cmet.2011.01.004
Lauer, T., Preik, M., Rassaf, T., Strauer, B. E., Deussen, A., Feelisch, M., & Kelm, M. (2001). Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proceedings of the National Academy of Sciences of the United State of America, 98(22), 12814-12819.
Laursen, J. B., Somers, M., Kurz, S., McCann, L., Warnholtz, A., Freeman, B., Tarpey, M., Fukai, T., & Harrison, D. G. (2001). Endothelial regulation of vasomotion in apoE-deficient mice: Implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation, 103(1524-4539), 1282-1288.
Lee, R., Margaritis, M., Channon, K. M., & Antoniades, C. (2012). Evaluating oxidative stress in human cardiovascular disease: Methodological aspects and considerations. Current Medicinal Chemistry, 19(16), 2504-2520. https://doi.org/10.2174/092986712800493057
Li, H., Samouilov, A., Liu, X., & Zweier, J. L. (2001). Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrite reduction: Evaluation of its role in nitric oxide generation in anoxic tissues. Journal of Biological Chemistry, 276(27), 24482-24489. https://doi.org/10.1074/jbc.M011648200
Lilley, E., Stanford, S. C., Kendall, D. E., Alexander, S. P., Cirino, G., Docherty, J. R., George, C. H., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Sobey, C. G., Stefanska, B., Stephens, G., Teixeira, M., & Ahluwalia, A. (2020). ARRIVE 2.0 and the British Journal of Pharmacology: Updated guidance for 2020. British Journal of Pharmacology, 177, 3611-3616. https://doi.org/10.1111/bph.15178
Linschoten, M., Peters, S., van Smeden, M., Jewbali, L. S., Schaap, J., Siebelink, H. M., Smits, P. C., Tieleman, R. G., van der Harst, P., van Gilst, W. H., & Asselbergs, F. W. (2020). Cardiac complications in patients hospitalised with COVID-19. European Heart Journal Acute Cardiovascular Care, 9(2048-8734), 817-823. https://doi.org/10.1177/2048872620974605
McNamara Dennis, M., Holubkov, R., Postava, L., Ramani, R., Janosko, K., Mathier, M., MacGowan, G. A., Murali, S., Feldman, A. M., & London, B. (2003). Effect of the Asp298 variant of endothelial nitric oxide synthase on survival for patients with congestive heart failure. Circulation, 107(12), 1598-1602. https://doi.org/10.1161/01.CIR.0000060540.93836.AA
Menges, L., Krawutschke, C., Füchtbauer, E.-M., Füchtbauer, A., Sandner, P., Koesling, D., & Russwurm, M. (2019). Mind the gap (junction): cGMP induced by nitric oxide in cardiac myocytes originates from cardiac fibroblasts. British Journal of Pharmacology, 176(24), 4696-4707. https://doi.org/10.1111/bph.14835
Millar, T. M., Stevens, C. R., Benjamin, N., Eisenthal, R., Harrison, R., & Blake, D. R. (1998). Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Letters, 427(2), 225-228. https://doi.org/10.1016/S0014-5793(98)00430-X
Miyai, N., Arita, M., Kazuhisa, M., Ikuharu, M., Shiraishi, T., & Nishio, I. (2002). Blood pressure response to heart rate during exercise test and risk of future hypertension. Hypertension, 39(1524-4563 [Electronic]), 761-766.
Miyai, N., Shiozaki, M., Terada, K., Takeshita, T., Utsumi, M., Miyashita, K., & Arita, M. (2021). Exaggerated blood pressure response to exercise is associated with subclinical vascular impairment in healthy normotensive individuals. Clinical and Experimental Hypertension, 43(1525-6006 [Electronic]), 56-62.
Montenegro, M. F., Amaral, J. H., Pinheiro, L. C., Sakamoto, E. K., Ferreira, G. C., Reis, R. I., Marçal, D. M. O., Pereira, R. P., & Tanus-Santos, J. E. (2011). Sodium nitrite downregulates vascular NADPH oxidase and exerts antihypertensive effects in hypertension. Free Radical Biology and Medicine, 51, 144-152. https://doi.org/10.1016/j.freeradbiomed.2011.04.005
Muiesan, M. L., Salvetti, M., Monteduro, C., Bonzi, B., Paini, A., Viola, S., Poisa, P., Rizzoni, D., Castellano, M., & Agabiti-Rosei, E. (2004). Left ventricular concentric geometry during treatment adversely affects cardiovascular prognosis in hypertensive patients. Hypertension, 43(4), 731-738. https://doi.org/10.1161/01.HYP.0000121223.44837.de
Muller-Brunotte, R., Kahan, T., Lopez, B., Edner, M., Gonzalez, A., Diez, J., & Malmqvist, K. (2007). Myocardial fibrosis and diastolic dysfunction in patients with hypertension: Results from the Swedish Irbesartan Left Ventricular Hypertrophy Investigation versus Atenolol (SILVHIA). Journal of Hypertension, 25(9), 1958-1966. https://doi.org/10.1097/HJH.0b013e3282170ada
Münzel, T., Gori, T., Keaney, J. F., Maack, C., & Daiber, A. (2015). Pathophysiological role of oxidative stress in systolic and diastolic heart failure and its therapeutic implications. European Heart Journal, 36, 2555-2564. https://doi.org/10.1093/eurheartj/ehv305
Münzel, T., Steven, S., & Daiber, A. (2014). Organic nitrates: Update on mechanisms underlying vasodilation, tolerance and endothelial dysfunction. Vascular Pharmacology, 63(3), 105-113. https://doi.org/10.1016/j.vph.2014.09.002
Panza, J. A., Quyyumi, A. A., & Brush, J. E. Jr. (1990). Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. New England Journal of Medicine, 323(1), 22-27. https://doi.org/10.1056/NEJM199007053230105
Parks, D. A., & Granger, D. N. (1986). Xanthine oxidase: Biochemistry, distribution and physiology. Acta Physiologica Scandinavica. Supplementum, 548, 87-99.
Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Würbel, H. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biology, 18(7), e3000410. https://doi.org/10.1371/journal.pbio.3000410
Pironti, G., Ivarsson, N., Yang, J., Farinotti, A. B., Jonsson, W., Zhang, S.-J., Bas, D., Svensson, C. I., Westerblad, H., Weitzberg, E., Lundberg, J. O., Pernow, J., Lanner, J., & Andersson, D. C. (2016). Dietary nitrate improves cardiac contractility via enhanced cellular Ca2+ signaling. Basic Research in Cardiology, 111(3), 34. https://doi.org/10.1007/s00395-016-0551-8
Ponikowski, P., Voors, A. A., Anker, S. D., Bueno, H., Cleland, J. G. F., Coats, A. J. S., Falk, V., González-Juanatey, J. R., Harjola, V. P., Jankowska, E. A., Jessup, M., Linde, C., Nihoyannopoulos, P., Parissis, J. T., Pieske, B., Riley, J. P., Rosano, G. M., Ruilope, L. M., Ruschitzka, F., … ESC Scientific Document Group. (2016). 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure of the European Society of Cardiology (ESC). Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. European Heart Journal, 37(27), 2129-2200.
Rammos, C., Hendgen-Cotta, U. B., Sobierajski, J., Bernard, A., Kelm, M., & Rassaf, T. (2014). Dietary nitrate reverses vascular dysfunction in older adults with moderately increased cardiovascular risk. Journal of the American College of Cardiology, 63(15), 1584-1585. https://doi.org/10.1016/j.jacc.2013.08.691
Rodrigues, J. C. L., Amadu, A. M., Dastidar, A. G., Szantho, G. V., Lyen, S. M., Godsave, C., Ratcliffe, L. E. K., Burchell, A. E., Hart, E. C., Hamilton, M. C. K., Nightingale, A. K., Paton, J. F. R., Manghat, N. E., & Bucciarelli-Ducci, C. (2016). Comprehensive characterisation of hypertensive heart disease left ventricular phenotypes. Heart, 102(20), 1671-1679. https://doi.org/10.1136/heartjnl-2016-309576
Rowland, N. E., & Fregly, M. J. (1988). Characteristics of thirst and sodium appetite in mice (Mus musculus). Behavioral Neuroscience, 102(6), 969-974. https://doi.org/10.1037/0735-7044.102.6.969
Sandner, P., & Stasch, J. P. (2017). Anti-fibrotic effects of soluble guanylate cyclase stimulators and activators: A review of the preclinical evidence. Respiratory Medicine, 122, S1-S9. https://doi.org/10.1016/j.rmed.2016.08.022
Saura, M., Zaragoza, C., Herranz, B., Griera, M., Diez-Marqués, L., Rodriguez-Puyol, D., & Rodriguez-Puyol, M. (2005). Nitric oxide regulates transforming growth factor-β signaling in endothelial cells. Circulation Research, 97(11), 1115-1123. https://doi.org/10.1161/01.RES.0000191538.76771.66
Simon, M. A., Vanderpool, R. R., Nouraie, M., Bachman, T. N., White, P. M., Sugahara, M., Gorcsan, J. 3rd, Parsley, E. L., & Gladwin, M. T. (2016). Acute hemodynamic effects of inhaled sodium nitrite in pulmonary hypertension associated with heart failure with preserved ejection fraction. JCI Insight, 1(18), e89620. https://doi.org/10.1172/jci.insight.89620
Smith Carolyn, J., Sun, D., Hoegler, C., Roth Barrie, S., Zhang, X., Zhao, G., Xu, X. B., Kobari, Y., Pritchard, K. Jr., Sessa, W. C., & Hintze Thomas, H. (1996). Reduced gene expression of vascular endothelial NO synthase and cyclooxygenase-1 in heart failure. Circulation Research, 78(1), 58-64. https://doi.org/10.1161/01.RES.78.1.58
Sonoda, K., Ohtake, K., Uchida, H., Ito, J., Uchida, M., Natsume, H., Tamada, H., & Kobayashi, J. (2017). Dietary nitrite supplementation attenuates cardiac remodeling in l-NAME-induced hypertensive rats. Nitric Oxide, 67, 1-9. https://doi.org/10.1016/j.niox.2017.04.009
Stuehr, D. J., Wei, C.-C., Wang, Z., & Hille, R. (2005). Exploring the redox reactions between heme and tetrahydrobiopterin in the nitric oxide synthases. Dalton Transactions (Cambridge, England: 2003), 212(21), 3427-3435.
Treasure, C. B., Klein, J. L., Vita, J. A., Manoukian, S. V., Renwick, G. H., Selwyn, A. P., Ganz, P., & Alexander, R. W. (1993). Hypertension and left ventricular hypertrophy are associated with impaired endothelium-mediated relaxation in human coronary resistance vessels. Circulation, 87(1), 86-93. https://doi.org/10.1161/01.CIR.87.1.86
Treibel, T. A., Zemrak, F., Sado, D. M., Banypersad, S. M., White, S. K., Maestrini, V., Barison, A., Patel, V., Herrey, A. S., Davies, C., Caulfield, M. J., Petersen, S. E., & Moon, J. C. (2015). Extracellular volume quantification in isolated hypertension-Changes at the detectable limits? Journal of Cardiovascular Magnetic Resonance, 17(1), 74. https://doi.org/10.1186/s12968-015-0176-3
Tripatara, P., Patel, N. S. A., Webb, A., Rathod, K., Lecomte, F. M. J., Mazzon, E., Cuzzocrea, S., Yaqoob, M. M., Ahluwalia, A., & Thiemermann, C. (2007). Nitrite-derived nitric oxide protects the rat kidney against ischemia/reperfusion injury in vivo: Role for xanthine oxidoreductase. Journal of the American Society of Nephrology, 18(2), 570-580. https://doi.org/10.1681/ASN.2006050450
van Heerebeek, L., Hamdani, N., Falcão-Pires, I., Leite-Moreira, A. F., Begieneman, M. P. V., Bronzwaer, J. G. F., van der Velden, J., Stienen, G. J. M., Laarman, G. J., Somsen, A., Verheugt, F. W. A., Niessen, H. W. M., & Paulus, W. J. (2012). Low myocardial protein kinase G activity in heart failure with preserved ejection fraction. Circulation, 126(7), 830-839. https://doi.org/10.1161/CIRCULATIONAHA.111.076075
Velmurugan, S., Kapil, V., Ghosh, S. M., Davies, S., McKnight, A., Aboud, Z., Khambata, R. S., Webb, A. J., Poole, A., & Ahluwalia, A. (2013). Antiplatelet effects of dietary nitrate in healthy volunteers: Involvement of cGMP and influence of sex. Free Radical Biology and Medicine, 65, 1521-1532. https://doi.org/10.1016/j.freeradbiomed.2013.06.031
Webb, A. J., Patel, N., Loukogeorgakis, S., Okorie, M., Aboud, Z., Misra, S., Rashid, R., Miall, P., Deanfield, J., Benjamin, N., MacAllister, R., Hobbs, A. J., & Ahluwalia, A. (2008). Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension, 51(3), 784-790. https://doi.org/10.1161/HYPERTENSIONAHA.107.103523
Zamani, P., Rawat, D., Shiva-Kumar, P., Geraci, S., Bhuva, R., Konda, P., Doulias, P. T., Ischiropoulos, H., Townsend, R. R., Margulies, K. B., Cappola, T. P., Poole, D. C., & Chirinos, J. A. (2015). The effect of inorganic nitrate on exercise capacity in heart failure with preserved ejection fraction. Circulation, 131, 371-385.
Zamani, P., Tan, V., Soto-Calderon, H., Beraun, M., Brandimarto, J. A., Trieu, L., Varakantam, S., Doulias, P. T., Townsend, R. R., Chittams, J., Margulies, K. B., Cappola, T. P., Poole, D. C., Ischiropoulos, H., & Chirinos, J. A. (2017). Pharmacokinetics and pharmacodynamics of inorganic nitrate in heart failure with preserved ejection fraction. Circulation Research, 120(7), 1151-1161. https://doi.org/10.1161/CIRCRESAHA.116.309832
Zollbrecht, C., Persson, A. E. G., Lundberg, J. O., Weitzberg, E., & Carlström, M. (2016). Nitrite-mediated reduction of macrophage NADPH oxidase activity is dependent on xanthine oxidoreductase-derived nitric oxide but independent of S-nitrosation. Redox Biology, 10, 119-127. https://doi.org/10.1016/j.redox.2016.09.015