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Dietary nitrate attenuates oxidative stress, prevents cardiac and renal injuries, and reduces blood pressure in salt-induced hypertension
Abstract
AIMS: Reduced bioavailability of endogenous nitric oxide (NO) is a central pathophysiological event in hypertension and other cardiovascular diseases. Recently, it was demonstrated that inorganic nitrate from dietary sources is converted in vivo to form nitrite, NO, and other bioactive nitrogen oxides. We tested the hypothesis that dietary inorganic nitrate supplementation may have therapeutic effects in a model of renal and cardiovascular disease. METHODS AND RESULTS: Sprague-Dawley rats subjected to unilateral nephrectomy and chronic high-salt diet from 3 weeks of age developed hypertension, cardiac hypertrophy and fibrosis, proteinuria, and histological as well as biochemical signs of renal damage and oxidative stress. Simultaneous nitrate treatment (0.1 or 1 mmol nitrate kg⁻¹ day⁻¹), with the lower dose resembling the nitrate content of a diet rich in vegetables, attenuated hypertension dose-dependently with no signs of tolerance. Nitrate treatment almost completely prevented proteinuria and histological signs of renal injury, and the cardiac hypertrophy and fibrosis were attenuated. Mechanistically, dietary nitrate restored the tissue levels of bioactive nitrogen oxides and reduced the levels of oxidative stress markers in plasma (malondialdehyde) and urine (Class VI F2-isoprostanes and 8-hydroxy-2-deoxyguanosine). In addition, the increased circulating and urinary levels of dimethylarginines (ADMA and SDMA) in the hypertensive rats were normalized by nitrate supplementation. CONCLUSION: Dietary inorganic nitrate is strongly protective in this model of renal and cardiovascular disease. Future studies will reveal if nitrate contributes to the well-known cardioprotective effects of a diet rich in vegetables.
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“Carlström et al., showed that dietary nitrate increased the tissue levels of nitrite and S-nitrosothiols in the heart, and attenuated oxidative stress and prevented cardiac injury in Sprague-Dawley rats subjected to unilateral nephrectomy and a high-salt diet [37].”
From NO-Rich Diet for Lifestyle-Related Diseases (2015) · cites this paper as [37]
In the citing paper
“In addition, nitrate supplementation offered cardioprotection against doxorubicin-induced cardiomyopathy 37 and prevented oxidative stress and cardiovascular and renal injury in salt-induced hypertension.39”
From Dietary nitrate supplementation improves revascularization in chronic ischemia (2012) · cites this paper as [39]
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Pinheiro, L. C., Ferreira, G. C., Amaral, J. H., Portella, R. L., Conde-Tella, S. O., Passos, M. A., & Tanus-Santos, J. E. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.10.013 · Cited by 53
Nitrate transport in salivary glands with implications for NO homeostasis
Lundberg, J. O. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210412109 · Cited by 49
“These effects include vasodilation (14, 15), reduction in blood pressure (16), protection against experimental ischemia reperfusion injury (17), reduction in cellular oxygen consumption (18, 19), reversal of metabolic syndrome (20), reduction in oxidative stress (21), stimulation of mucosal blood flow and mucus format…”
BackgroundSelf-citationHow May Proton Pump Inhibitors Impair Cardiovascular Health?
Sukhovershin, R. A., & Cooke, J. P. (2016) · American Journal of Cardiovascular Drugs · doi:10.1007/s40256-016-0160-9 · Cited by 50
“Of note, dietary supplementation with nitrate prevented ADMA accumulation in a rodent model of chronic cardiovascular disease, likely, by protecting DDAH from oxidative stress [72].”
Peleli, M., Hezel, M. P., Zollbrecht, C., Persson, A. E. G., Lundberg, J. O., Weitzberg, E., Fredholm, B. B., & Carlström, M. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00222 · Cited by 47
Self-citationDietary inorganic nitrate alleviates doxorubicin cardiotoxicity: Mechanisms and implications
Xi, L., Zhu, S., Das, A., Chen, Q., Durrant, D., Hobbs, D. C., Lesnefsky, E. J., & Kukreja, R. C. (2012) · Nitric Oxide · doi:10.1016/j.niox.2012.03.006 · Cited by 47
“[53] Rat (SHBP) High salt-induced hypertension; NaNO3 (1 mmol/kg/day); myocardial infarct size MAP ↓ cardiac hypertrophy ↓ cardiac fibrosis ↓ Blood lipid peroxidation ↓”
BackgroundSchiffer, T. A., Lundberg, J. O., Weitzberg, E., & Carlström, M. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165811 · Cited by 49
Self-citationThe oral microbiome, nitric oxide and exercise performance
Bryan, N. S., Burleigh, M. C., & Easton, C. (2022) · Nitric Oxide · doi:10.1016/j.niox.2022.05.004 · Cited by 46
Tain, Y., & Huang, L. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150711773 · Cited by 45
“Our data are in agreement with a previous study showing that inorganic nitrate can lower BP in a hypertensive model [34].”
ResultEssick, E. E., & Sam, F. (2011) · International Journal of Hypertension · doi:10.4061/2011/346985 · Cited by 45
“Furthermore, decreased endothelial NOS-derived NO has been shown previously to be central in the development of cardiovascular disorders [128] and LVH [129].”
BackgroundDietary nitrite supplementation attenuates cardiac remodeling in l -NAME-induced hypertensive rats
Sonoda, K., Ohtake, K., Uchida, H., Ito, J., Uchida, M., Natsume, H., Tamada, H., & Kobayashi, J. (2017) · Nitric Oxide · doi:10.1016/j.niox.2017.04.009 · Cited by 44
Jones, L., Bailey, S. J., Rowland, S. N., Alsharif, N. S., Shannon, O. M., & Clifford, T. (2021) · Journal of Dietary Supplements · doi:10.1080/19390211.2021.1939472 · Cited by 46
Ling, W. C., Murugan, D. D., Lau, Y. S., Vanhoutte, P. M., & Mustafa, M. R. (2016) · Scientific Reports · doi:10.1038/srep33048 · Cited by 44
Lara, J., Ogbonmwan, I., Oggioni, C., Zheng, D., Qadir, O., Ashor, A. W., Brandt, K., Mathers, J. C., & Siervo, M. (2015) · Maturitas · doi:10.1016/j.maturitas.2015.07.028 · Cited by 44
Nieder, R., Benbi, D. K., & Reichl, F. (2018) · Springer eBooks · doi:10.1007/978-94-024-1222-2_5 · Cited by 46
Kurtz, T. W., DiCarlo, S. E., Pravenec, M., & Morris, R. C. (2017) · Journal of Hypertension · doi:10.1097/hjh.0000000000001458 · Cited by 42
Montenegro, M. F., Pinheiro, L. C., Amaral, J. H., Ferreira, G. C., Portella, R. L., & Tanus-Santos, J. E. (2014) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-014-0970-8 · Cited by 41
“reported similar findings using nitrate instead of nitrite in a saltinduced hypertension model (Carlström et al. 2011).”
Zollbrecht, C., Persson, A. E. G., Lundberg, J. O., Weitzberg, E., & Carlström, M. (2016) · Redox Biology · doi:10.1016/j.redox.2016.09.015 · Cited by 41
Self-citationBahadoran, Z., Mirmiran, P., Ghasemi, A., Carlström, M., Azizi, F., & Hadaegh, F. (2016) · Nutrients · doi:10.3390/nu8120811 · Cited by 41
“Most recent findings imply beneficial cardio-renal protective and antihypertensive outcomes following short-term administration of inorganic NO3 [16,19,24,47].”
BackgroundSelf-citationMabeku, L. B. K., Nana, B. N., Bille, B. E., Tchuenguem, R. T., & Nguepi, E. Z. (2017) · Pharmaceutical Biology · doi:10.1080/13880209.2017.1285326 · Cited by 41
“…since NO is known to play a role in maintaining gastric integrity by increasing mucosal blood flow and mucus secretion (Bjorne et al. 2004), cytoprotection (Duranski et al. 2005; Shiva et al. 2007) as well as anti-inflammatory and antioxidant effects (Stokes et al. 2009; Carlstrom et al. 2011).”
BackgroundHuang, J., Lee, Y., Chuang, L., Guh, J., & Hwang, J. (2015) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25058 · Cited by 38
“Recently, it was demonstrated that nitrate treatment almost completely prevented proteinuria and histological signs of renal injury, and the cardiac hypertrophy and fibrosis were attenuated [Carlström et al., 2011].”
BackgroundLing, W. C., Mustafa, M. R., Vanhoutte, P. M., & Murugan, D. D. (2017) · Vascular Pharmacology · doi:10.1016/j.vph.2017.05.003 · Cited by 40
El-Nabarawy, N. A., Gouda, A. S., Khattab, M. A., & Rashed, L. A. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-07901-6 · Cited by 41
Singh, M., Arya, A., Kumar, R., Bhargava, K., & Sethy, N. K. (2012) · Nitric Oxide · doi:10.1016/j.niox.2011.12.002 · Cited by 38
Guimarães, D. D., Cruz, J. C., Carvalho‐Galvão, A., Zhuge, Z., Marques, S. M., Naves, L. M., Persson, A. E. G., Weitzberg, E., Lundberg, J. O., Balarini, C. M., et al. (2019) · Hypertension · doi:10.1161/hypertensionaha.118.12425 · Cited by 38
Self-citationSalloum, F. N., Sturz, G. R., Yin, C., Rehman, S., Hoke, N. N., Kukreja, R. C., & Xi, L. (2014) · Experimental Biology and Medicine · doi:10.1177/1535370214558024 · Cited by 39
“1 mmol/kg/day) in rats, which led to significant cardiorenal protective effects against the pathological changes caused by salt-induced hypertension.(45) There is a high probability that such a low dose of sodium nitrate may protect against I/R injury as well.”
BackgroundThe role of inorganic nitrate and nitrite in CVD
Jackson, J. K., Patterson, A. J., MacDonald‐Wicks, L. K., & McEvoy, M. (2017) · Nutrition Research Reviews · doi:10.1017/s0954422417000105 · Cited by 37
“found that dietary nitrate supplementation can partly prevent the development of cardiac hypertrophy and high nitrate doses significantly reduced the fibrotic changes which were observed in the high-salt group, two factors which are major predictors of heart failure((152)).”
InfluentialPotential Therapeutic Strategies for Hypertension‐Exacerbated Cardiotoxicity of Anticancer Drugs
Kuriakose, R. K., Kukreja, R. C., & Xi, L. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/8139861 · Cited by 38
Yang, T., Zollbrecht, C., Winerdal, M. E., Zhuge, Z., Zhang, X., Terrando, N., Checa, A., Sällström, J., Wheelock, C. E., Winqvist, O., et al. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.116.003868 · Cited by 35
“combination with HS (UNX-HS) were accompanied with increased preglomerular reactivity and abnormal renal autoregulation and are associated with increased oxidative stress, nitric oxide deficiency, and infiltration of inflammatory cells in the kidney.(5,6) Similar findings regarding nitric oxide deficiency and vascular…”
InfluentialSelf-citationVascular function in rats with adenine-induced chronic renal failure
Nguy, L., Nilsson, H., Lundgren, J., Johansson, M. E., Teerlink, T., Scheffer, P. G., & Guron, G. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00696.2011 · Cited by 34
“The analytes were then extracted using Oasis Mixed-Mode Anion Exchange cartridges (3 cc/60 mg; Waters, Milford, MA), as described before (2).”
MethodSelf-citationPinheiro, L. C., Oliveira‐Paula, G. H., Ferreira, G. C., de Paula, T. D., Duarte, D. Â., Costa-Neto, C. M., & Tanus-Santos, J. E. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101769 · Cited by 35
Metadata
- Authors
- Carlström, M., Persson, A. E. G., Larsson, E., Hezel, M., Scheffer, P. G., Teerlink, T., Weitzberg, E., & Lundberg, J. O.
- Affiliations
- Uppsala University (SE)
- Karolinska Institutet (SE)
- Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
- Corresponding author
- Carlström, Mattias
- Weitzberg, Eddie
- Lundberg, Jon O.
- ORCID
- Venue
- Cardiovascular Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-11-19
- Volume
- 89
- Issue
- 3
- Pages
- 574-585
- ISSN
- 0008-6363 (ISSN-L)
- 1755-3245
- OpenAlex
- W1974569195
- Semantic Scholar
- b3bf26b82cdbdf00b0fade39de86bb83ed79872b
- Cited by
- 261
- References
- 55
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 12 · 2023: 11 · 2022: 10 · 2021: 11 · 2020: 16 · 2019: 13 · 2018: 25 · 2017: 31 · 2016: 22 · 2015: 23 · 2014: 22 · 2013: 20 · 2012: 20
- FWCI
- 11.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cardiovascular Research (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Wenner-Gren Foundation
- Massachusetts General Hospital
- Vrije Universiteit Amsterdam
- Svenska Sällskapet för Medicinsk Forskning
- Karolinska Institutet
- Vetenskapsrådet
- Magnus Bergvalls Stiftelse
- Svenska Läkaresällskapet
- Topics
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Health Sciences › Nursing › Nutrition and Dietetics › Sodium Intake and Health
- Keywords
- dietary nitrate, nitric oxide bioavailability, salt-induced hypertension, oxidative stress, kidney injury, cardiac hypertrophy, myocardial fibrosis, proteinuria, dimethylarginines, asymmetric dimethylarginine, SDMA, malondialdehyde, F2-isoprostanes, 8-hydroxy-2'-deoxyguanosine, high-salt diet, cardioprotection
- MeSH terms
- Animals, Arginine, Blood Pressure, Disease Models, Animal, Cardiomegaly, Hypertension, Renal, Kidney, Male, Nephrectomy, Nitrates, Nitric Oxide, Nitrogen, Proteinuria, Rats, Sprague-Dawley, Sodium Chloride, Dietary, Oxidative Stress, Rats
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