Dietary nitrite improves insulin signaling through GLUT4 translocation
Abstract
Diabetes mellitus type 2 is a syndrome of disordered metabolism with inappropriate hyperglycemia owing to a reduction in the biological effectiveness of insulin. Type 2 diabetes is associated with an impaired nitric oxide (NO) pathway that probably serves as the key link between metabolic disorders and cardiovascular disease. Insulin-mediated translocation of GLUT4 involves the PI3K/Akt kinase signal cascade that results in activation of endothelial NO synthase (eNOS). eNOS is dysfunctional during diabetes. We hypothesize that loss of eNOS-derived NO terminates the signaling cascade and therefore cannot activate GLUT4 translocation and that dietary nitrite may repair this pathway. In this study, we administered 50mg/L sodium nitrite to db/db diabetic mice for 4 weeks. After 4 weeks treatment, the db/db mice experienced less weight gain, improved fasting glucose levels, and reduced insulin levels. Cell culture experiments using CHO-HIRc-myc-GLUT4eGFP cell lines stably expressing insulin receptor and myc-GLUT4eGFP protein, as well as L6 skeletal muscle cells stably expressing rat GLUT4 with a Myc epitope (L6-GLUT4myc), showed that NO, nitrite, and GSNO stimulate GLUT4 translocation independent of insulin, which is inhibited by NEM. Collectively our data suggest that nitrite improves insulin signaling through restoration of NO-dependent nitrosation of GLUT4 signaling translocation. These data suggest that NO-mediated nitrosation of GLUT4 by nitrite or other nitrosating agents is necessary and sufficient for GLUT4 translocation in target tissue. Description of this pathway may justify a high-nitrate/nitrite diet along with the glycemic index to provide a safe and nutritional regimen for the management and treatment of diabetes.
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Recent studies demonstrate improvements of insulin resistance in humans and animals as a result of dietary nitrate/nitrite enhancing NO availability in plasma and tissues.
“the therapeutic potential of dietary nitrate/nitrite has been supported by recent studies demonstrating the improvements of insulin resistance in humans and animals as a result of its enhancing the NO availability in plasma and tissues [65,66,67,68].”
From NO-Rich Diet for Lifestyle-Related Diseases (2015) · cites this paper as [65]
NO-dependent nitrosylation of GLUT4 facilitates GLUT4 translocation to the membrane for glucose uptake and improves insulin resistance.
“Jiang recently reported that NO-dependent nitrosylation of GLUT4 facilitates GLUT4 translocation to the membrane for glucose uptake, and improves insulin resistance [65].”
From NO-Rich Diet for Lifestyle-Related Diseases (2015) · cites this paper as [65]
Cites
Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation
Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R., & Zeiher, A. M. (1999) · Nature · doi:10.1038/21224 · Cited by 3,591 · see citing works
Steinberg, H. O., Brechtel, G., Johnson, A., Fineberg, N. S., & Baron, A. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117433 · Cited by 1,216 · see citing works
Webb, A. J., Patel, N., Loukogeorgakis, S., Okorie, M., Aboud, Z., Misra, S., Rashid, R., Miall, P., Deanfield, J., Benjamin, N., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.103523 · Cited by 1,078 · see citing works
Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus
Williams, S. B., Cusco, J. A., Roddy, M.-A., Johnstone, M. T., & Creager, M. A. (1996) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(95)00522-6 · Cited by 1,014 · see citing works
de Tejada, I. S., Goldstein, I., Azadzoi, K. M., Krane, R. J., & Cohen, R. A. (1989) · New England Journal of Medicine · doi:10.1056/nejm198904203201601 · Cited by 944 · see citing works
Zeng, G., Nystrom, F. H., Ravichandran, L. V., Cong, L.-N., Kirby, M., Mostowski, H., & Quon, M. J. (2000) · Circulation · doi:10.1161/01.cir.101.13.1539 · Cited by 745 · see citing works
Carter, P., Gray, L. J., Troughton, J., Khunti, K., & Davies, M. J. (2010) · BMJ · doi:10.1136/bmj.c4229 · Cited by 728 · see citing works
Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver
Duranski, M. R., Greer, J. J. M., Dejam, A., Jaganmohan, S., Hogg, N., Langston, W., Patel, R. P., Yet, S.-F., Wang, X., Kevil, C. G., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci22493 · Cited by 674 · see citing works
Effects of dietary nitrate on oxygen cost during exercise
Larsen, F. J., Weitzberg, E., Lundberg, J. O., & Ekblom, B. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01713.x · Cited by 637 · see citing works
Inorganic Nitrate Supplementation Lowers Blood Pressure in Humans: Role for Nitrite-Derived NO
Kapil, V., Milsom, A. B., Okorie, M., Maleki-Toyserkani, S., Akram, F., Rehman, F., Arghandawi, S., Pearl, V., Benjamin, N., Loukogeorgakis, S., et al. (2010) · Hypertension · doi:10.1161/hypertensionaha.110.153536 · Cited by 621 · see citing works
Webb, A., Bond, R., McLean, P., Uppal, R., Benjamin, N., & Ahluwalia, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402927101 · Cited by 608 · see citing works
Nitric oxide and its role in the cardiovascular system
Loscalzo, J., & Welch, G. N. (1995) · Progress in Cardiovascular Diseases · doi:10.1016/s0033-0620(05)80001-5 · Cited by 599 · see citing works
Effects of Dietary Nitrate on Blood Pressure in Healthy Volunteers
Larsen, F. J., Ekblom, B., Sahlin, K., Lundberg, J. O., & Weitzberg, E. (2006) · New England Journal of Medicine · doi:10.1056/nejmc062800 · Cited by 587 · see citing works
Free radicals mediate endothelial cell dysfunction caused by elevated glucose
Tesfamariam, B., & Cohen, R. A. (1992) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1992.263.2.h321 · Cited by 558 · see citing works
Shiva, S., Sack, M. N., Greer, J. J., Duranski, M., Ringwood, L. A., Burwell, L., Wang, X., MacArthur, P. H., Shoja, A., Raghavachari, N., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070198 · Cited by 555 · see citing works
Functional Properties and Genomics of Glucose Transporters
Zhao, F., & Keating, A. F. (2007) · Current Genomics · doi:10.2174/138920207780368187 · Cited by 550 · see citing works
Duplain, H., Burcelin, R., Sartori, C., Cook, S., Egli, M., Lepori, M., Vollenweider, P., Pedrazzini, T., Nicod, P., Thorens, B., et al. (2001) · Circulation · doi:10.1161/01.cir.104.3.342 · Cited by 533 · see citing works
Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues
Bryan, N. S., Fernandez, B. O., Bauer, S. M., Garcia-Saura, M. F., Milsom, A. B., Rassaf, T., Maloney, R. E., Bharti, A., Rodriguez, J., & Feelisch, M. (2005) · Nature Chemical Biology · doi:10.1038/nchembio734 · Cited by 518 · see citing works
Self-citationCarlström, M., Larsen, F. J., Nyström, T., Hezel, M., Borniquel, S., Weitzberg, E., & Lundberg, J. O. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008872107 · Cited by 382 · see citing works
Review of Alterations in Endothelial Nitric Oxide Production in Diabetes
Pieper, G. M. (1998) · Hypertension · doi:10.1161/01.hyp.31.5.1047 · Cited by 353 · see citing works
Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury
Bryan, N. S., Calvert, J. W., Elrod, J. W., Gundewar, S., Ji, S. Y., & Lefer, D. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706579104 · Cited by 347 · see citing works
Self-citationLarsen, F. J., Weitzberg, E., Lundberg, J. O., & Ekblom, B. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.11.006 · Cited by 320 · see citing works
Insulin transport across capillaries is rate limiting for insulin action in dogs.
Yang, Y. J., Hope, I. D., Ader, M., & Bergman, R. N. (1989) · Journal of Clinical Investigation · doi:10.1172/jci114339 · Cited by 303 · see citing works
Pluta, R. M. (2005) · JAMA · doi:10.1001/jama.293.12.1477 · Cited by 261 · see citing works
Jung, K.-H., Chu, K., Ko, S.-Y., Lee, S.-T., Sinn, D.-I., Park, D.-K., Kim, J.-M., Song, E.-C., Kim, M., & Roh, J.-K. (2006) · Stroke · doi:10.1161/01.str.0000245116.40163.1c · Cited by 253 · see citing works
An <i>S</i> -nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate
Angelo, M., Singel, D. J., & Stamler, J. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600942103 · Cited by 233 · see citing works
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) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006050450 · Cited by 226 · see citing works
Bernal‐Mizrachi, E., Fátrai, S., Johnson, J. D., Ohsugi, M., Otani, K., Han, Z., Polonsky, K. S., & Permutt, M. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20016 · Cited by 223 · see citing works
Oxygen free radicals abolish endothelium-dependent relaxation in diabetic rat aorta
Pieper, G. M., & Gross, G. J. (1988) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1988.255.4.h825 · Cited by 192 · see citing works
Bernal‐Mizrachi, E., Fátrai, S., Johnson, J. D., et al. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200420016 · Cited by 191 · see citing works
Chronic sodium nitrite therapy augments ischemia-induced angiogenesis and arteriogenesis
Kumar, D., Branch, B. G., Pattillo, C. B., Hood, J., Thoma, S., Simpson, S., Illum, S., Arora, N., Chidlow, J. H., Langston, W., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711480105 · Cited by 187 · see citing works
Nyström, F. H., & Quon, M. J. (1999) · Cellular Signalling · doi:10.1016/s0898-6568(99)00025-x · Cited by 182 · see citing works
Diabetic-induced endothelial dysfunction in rat aorta: role of hydroxyl radicals
Pieper, G. M., Langenstroer, P., & Siebeneich, W. (1997) · Cardiovascular Research · doi:10.1016/s0008-6363(96)00237-4 · Cited by 179 · see citing works
Lane, P. B., Hao, G., & Gross, S. S. (2001) · Science s STKE · doi:10.1126/stke.2001.86.re1 · Cited by 177 · see citing works
Bryan, N. S., Calvert, J. W., Gundewar, S., & Lefer, D. J. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.04.040 · Cited by 161 · see citing works
Kobayashi, T., Taguchi, K., Takenouchi, Y., Matsumoto, T., & Kamata, K. (2004) · Hypertension · doi:10.1161/01.hyp.0000147559.10261.a7 · Cited by 141 · see citing works
Nitric oxide promotes distant organ protection: evidence for an endocrine role of nitric oxide
Elrod, J. W., Calvert, J. W., Gundewar, S., Bryan, N. S., & Lefer, D. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800700105 · Cited by 137 · see citing works
Self-citationJansson, P., Fowelin, J., von Schenck, H., Smith, U., & Lönnroth, P. (1993) · Diabetes · doi:10.2337/diab.42.10.1469 · Cited by 129 · see citing works
Bioavailability of sodium nitrite from an aqueous solution in healthy adults
Hunault, C. C., van Velzen, A. G., Sips, A. J. A. M., Schothorst, R. C., & Meulenbelt, J. (2009) · Toxicology Letters · doi:10.1016/j.toxlet.2009.06.865 · Cited by 102 · see citing works
Kinetics of Insulin Action In Vivo: Identification of Rate-Limiting Steps
Miles, P. D. G., Levisetti, M. G., Reichart, D. R., Khoursheed, M., Moossa, A. R., & Olefsky, J. M. (1995) · Diabetes · doi:10.2337/diab.44.8.947 · Cited by 101 · see citing works
The Union of Vascular and Metabolic Actions of Insulin in Sickness and in Health
Kim, J., Koh, K. K., & Quon, M. J. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000164044.42910.6b · Cited by 96 · see citing works
(2005) · PubMed · Cited by 88 · see citing works
Endothelial dysfunction in a model of hyperglycemia and hyperinsulinemia
Pieper, G. M., Meier, D. A., & Hager, S. R. (1995) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1995.269.3.h845 · Cited by 83 · see citing works
Posttranslational Modifications of GLUT4 Affect Its Subcellular Localization and Translocation
Sadler, J. B. A., Bryant, N. J., Gould, G. W., & Welburn, C. R. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14059963 · Cited by 44 · see citing works
Cilenšek, I., Mankoč, S., Petrovič, M. G., & Petrovič, D. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1537-8 · Cited by 36 · see citing works
Vijayakumar, M. V., Ajay, A. K., & Bhat, M. K. (2010) · Journal of Biosciences · doi:10.1007/s12038-010-0060-0 · Cited by 21 · see citing works
Flagged first, then by citations
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Sorted by citations
Metabolic Effects of Dietary Nitrate in Health and Disease
Lundberg, J. O., Carlström, M., & Weitzberg, E. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.007 · Cited by 374 · see citing works
Lai, Y.-C., Tabima, D. M., Dube, J. J., Hughan, K. S., Vanderpool, R. R., Goncharov, D. A., St. Croix, C. M., Garcia-Ocaña, A., Goncharova, E. A., Tofovic, S. P., et al. (2016) · Circulation · doi:10.1161/circulationaha.115.018935 · Cited by 270 · see citing works
Kapil, V., Khambata, R. S., Jones, D. A., Rathod, K., Primus, C., Massimo, G., Fukuto, J. M., & Ahluwalia, A. (2020) · Pharmacological Reviews · doi:10.1124/pr.120.019240 · Cited by 248 · see citing works
Therapeutic effects of inorganic nitrate and nitrite in cardiovascular and metabolic diseases
Omar, S. A., Webb, A. J., Lundberg, J. O., & Weitzberg, E. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12441 · Cited by 175 · see citing works
Hypoxia in Obesity and Diabetes: Potential Therapeutic Effects of Hyperoxia and Nitrate
Norouzirad, R., González‐Muniesa, P., & Ghasemi, A. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/5350267 · Cited by 96 · see citing works
Dietary nitrate improves glucose tolerance and lipid profile in an animal model of hyperglycemia
Khalifi, S., Rahimipour, A., Jeddi, S., Ghanbari, M., Kazerouni, F., & Ghasemi, A. (2015) · Nitric Oxide · doi:10.1016/j.niox.2014.11.011 · Cited by 95 · see citing works
NO-Rich Diet for Lifestyle-Related Diseases
Kobayashi, J., Ohtake, K., & Uchida, H. (2015) · Nutrients · doi:10.3390/nu7064911 · Cited by 94 · see citing works
Anti-obesity and anti-diabetic effects of nitrate and nitrite
Ghasemi, A., & Jeddi, S. (2017) · Nitric Oxide · doi:10.1016/j.niox.2017.08.003 · Cited by 89 · see citing works
Gheibi, S., Jeddi, S., Carlström, M., Gholami, H., & Ghasemi, A. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.02.002 · Cited by 90 · see citing works
Xu, L., Li, W., Chen, Z., Guo, Q., Wang, C., Santhanam, R. K., & Chen, H. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.12.064 · Cited by 87 · see citing works
Goh, C. E., Trinh, P., Colombo, P. C., Genkinger, J. M., Mathema, B., Uhlemann, A., LeDuc, C. A., Leibel, R. L., Rosenbaum, M. S., Paster, B. J., et al. (2019) · Journal of the American Heart Association · doi:10.1161/jaha.119.013324 · Cited by 82 · see citing works
Gheibi, S., Bakhtiarzadeh, F., Jeddi, S., Farrokhfall, K., Zardooz, H., & Ghasemi, A. (2017) · Nitric Oxide · doi:10.1016/j.niox.2017.01.003 · Cited by 79 · see citing works
Beneficial effects of inorganic nitrate/nitrite in type 2 diabetes and its complications
Bahadoran, Z., Ghasemi, A., Mirmiran, P., Azizi, F., & Hadaegh, F. (2015) · Nutrition & Metabolism · doi:10.1186/s12986-015-0013-6 · Cited by 82 · see citing works
Mitochondrial involvement in skeletal muscle insulin resistance: A case of imbalanced bioenergetics
Affourtit, C. (2016) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2016.07.008 · Cited by 67 · see citing works
Tan, X., Chua, K. H., Ram, M. R., & Kuppusamy, U. R. (2015) · Food Chemistry · doi:10.1016/j.foodchem.2015.09.042 · Cited by 71 · see citing works
Dietary nitrite supplementation improves insulin resistance in type 2 diabetic KKAy mice
Ohtake, K., Nakano, G., Ehara, N., Sonoda, K., Ito, J., Uchida, H., & Kobayashi, J. (2015) · Nitric Oxide · doi:10.1016/j.niox.2014.11.009 · Cited by 63 · see citing works
Regulation of carbohydrate metabolism by nitric oxide and hydrogen sulfide: Implications in diabetes
Gheibi, S., Samsonov, A. P., Gheibi, S., Vazquez, A. B., & Kashfi, K. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.113819 · Cited by 63 · see citing works
Effects of insulin on wound healing: A review of animal and human evidences
Oryan, A., & Alemzadeh, E. (2017) · Life Sciences · doi:10.1016/j.lfs.2017.02.015 · Cited by 59 · see citing works
On the mechanism by which dietary nitrate improves human skeletal muscle function
Affourtit, C., Bailey, S. J., Jones, A. M., Smallwood, M. J., & Winyard, P. G. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00211 · Cited by 58 · see citing works
From nitrate to NO: potential effects of nitrate-reducing bacteria on systemic health and disease
Liu, H., Huang, Y., Huang, M., Wang, M., Ming, Y., Chen, W., Chen, Y., Tang, Z., & Jia, B. (2023) · European Journal of Medical Research · doi:10.1186/s40001-023-01413-y · Cited by 58 · see citing works
The impact of gut microbiota metabolites on cellular bioenergetics and cardiometabolic health
Tomášová, L., Grman, M., Ondriaš, K., & Ufnal, M. (2021) · Nutrition & Metabolism · doi:10.1186/s12986-021-00598-5 · Cited by 58 · see citing works
Ashor, A. W., Chowdhury, S., Oggioni, C., Qadir, O., Brandt, K., Ishaq, A., Mathers, J. C., Saretzki, G. C., & Siervo, M. (2016) · Journal of Nutrition · doi:10.3945/jn.116.237529 · Cited by 55 · see citing works
Dietary stimulators of GLUT4 expression and translocation in skeletal muscle: A mini‐review
Gannon, N. P., Conn, C. A., & Vaughan, R. A. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400414 · Cited by 53 · see citing works
Dietary nitrate supplementation in cardiovascular health: an ergogenic aid or exercise therapeutic?
Woessner, M. N., McIlvenna, L. C., Ortiz de Zevallos, J., Neil, C. J., & Allen, J. D. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00414.2017 · Cited by 50 · see citing works
Homeostatic medicine: a strategy for exploring health and disease
Wang, S., & Qin, L. (2022) · Current Medicine · doi:10.1007/s44194-022-00016-9 · Cited by 56 · see citing works
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 · see citing works
Schiffer, 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 48 · see citing works
Keyhanmanesh, ., Hamidian, G., Alipour, M. R., Ranjbar, M., & Oghbaei, H. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.09.019 · Cited by 46 · see citing works
Nitrite and myocardial ischaemia reperfusion injury. Where are we now?
Griffiths, K., Lee, J. J., Frenneaux, M. P., Feelisch, M., & Madhani, M. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107819 · Cited by 46 · see citing works
Beals, J. W., Binns, S. E., Davis, J., Giordano, G., Klochak, A. L., Paris, H. L. R., Schweder, M. M., Peltonen, G. L., Scalzo, R. L., & Bell, C. (2017) · Journal of Nutrition and Metabolism · doi:10.1155/2017/6436783 · Cited by 44 · see citing works
Aliahmadi, M., Amiri, F., Bahrami, L. S., Hosseini, A. F., Abiri, B., & Vafa, M. (2021) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-021-00798-z · Cited by 48 · see citing works
Kanuri, B., Kanshana, J. S., Rebello, S. C., Pathak, P., Gupta, A. P., Gayen, J. R., Jagavelu, K., & Dikshit, M. (2017) · Scientific Reports · doi:10.1038/srep41009 · Cited by 40 · see citing works
Role of flavonoids and nitrates in cardiovascular health
Lovegrove, J. A., Stainer, A. R., & Hobbs, D. A. (2017) · Proceedings of The Nutrition Society · doi:10.1017/s0029665116002871 · Cited by 37 · see citing works
Effects of Nitrate Intake on Myocardial Ischemia-Reperfusion Injury in Diabetic Rats
Jeddi, S., Khalifi, S., Ghanbari, M., Bageripour, F., & Ghasemi, A. (2016) · Arquivos Brasileiros de Cardiologia · doi:10.5935/abc.20160137 · Cited by 37 · see citing works
Insulin secretion: The nitric oxide controversy
Gheibi, S., & Ghasemi, A. (2020) · EXCLI journal · doi:10.17179/excli2020-2711 · Cited by 34 · see citing works
Oghbaei, H., Alipour, M. R., Hamidian, G., Ahmadi, M., Ghorbanzadeh, V., & Keyhanmanesh, . (2018) · Experimental Physiology · doi:10.1113/ep087198 · Cited by 31 · see citing works
Hadaegh, F., Asgari, S., Bozorgmanesh, M., Jeddi, S., Azizi, F., & Ghasemi, A. (2016) · Nitric Oxide · doi:10.1016/j.niox.2016.02.004 · Cited by 29 · see citing works
Bhattacharya, S., Maji, U. K., Khan, G. A., Das, R., Sinha, A. K., Ghosh, C., & Maiti, S. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.01.036 · Cited by 29 · see citing works
Bahadoran, Z., Mirmiran, P., Carlström, M., & Ghasemi, A. (2021) · Nitric Oxide · doi:10.1016/j.niox.2021.09.001 · Cited by 26 · see citing works
Ohtake, K., Ehara, N., Chiba, H., Nakano, G., Sonoda, K., Ito, J., Uchida, H., & Kobayashi, J. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00360.2016 · Cited by 26 · see citing works
Cottrell, J. J., Ponnampalam, E. N., Dunshea, F. R., & Warner, R. D. (2015) · Meat Science · doi:10.1016/j.meatsci.2015.02.007 · Cited by 25 · see citing works
Dietary nitrate biochemistry and physiology. An update on clinical benefits and mechanisms of action
Bryan, N. S., Ahmed, S., Lefer, D. J., Hord, N. G., & Schwarz, E. R. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.01.003 · Cited by 26 · see citing works
Keyhanmanesh, ., Hamidian, G., Alipour, M. R., & Oghbaei, H. (2019) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2018.11.027 · Cited by 25 · see citing works
Abbaszadeh, F., Azizi, S., Mobasseri, M., & Ebrahimi‐Mameghani, M. (2021) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-021-00669-w · Cited by 22 · see citing works
Varzandi, T., Abdollahifar, M., Rohani, S. A. H., Piryaei, A., Zadeh–Vakili, A., Jeddi, S., & Ghasemi, A. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.06.012 · Cited by 22 · see citing works
Oghbaei, H., Hamidian, G., Alipour, M. R., Alipour, S., & Keyhanmanesh, . (2020) · Food & Function · doi:10.1039/c9fo00974d · Cited by 22 · see citing works
Afzali, H., Khaksari, M., Norouzirad, R., Jeddi, S., Kashfi, K., & Ghasemi, A. (2020) · Nitric Oxide · doi:10.1016/j.niox.2020.07.001 · Cited by 21 · see citing works
Metabolic effects of L ‐citrulline in type 2 diabetes
Bagheripour, F., Jeddi, S., Kashfi, K., & Ghasemi, A. (2023) · Acta Physiologica · doi:10.1111/apha.13937 · Cited by 23 · see citing works
Gheibi, S., Jeddi, S., Carlström, M., Kashfi, K., & Ghasemi, A. (2019) · Nitric Oxide · doi:10.1016/j.niox.2019.08.006 · Cited by 20 · see citing works
Karimzadeh, L., Sohrab, G., Hedayati, M., Ebrahimof, S., Emami, G., & Razavion, T. (2022) · Irish Journal of Medical Science (1971 -) · doi:10.1007/s11845-022-03090-y · Cited by 21 · see citing works
Yeo, Y. H., & Lai, Y. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.05.003 · Cited by 19 · see citing works
Bahadoran, Z., Mirmiran, P., Kashfi, K., & Ghasemi, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094735 · Cited by 19 · see citing works
Aggarwal, H., Pathak, P., Singh, P., Gayen, J. R., Jagavelu, K., & Dikshit, M. (2020) · Antioxidants · doi:10.3390/antiox9080736 · Cited by 17 · see citing works
Khorasani, V., Jeddi, S., Yaghmaei, P., Tohidi, M., & Ghasemi, A. (2019) · Nitric Oxide · doi:10.1016/j.niox.2019.02.003 · Cited by 19 · see citing works
Yang, Y., Zhao, M., Yu, X., Liu, L., He, X., Deng, J., & Zang, W. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00569.2018 · Cited by 18 · see citing works
Zhou, J., Liu, H., Hu, L., Kagami, H., & Wang, S. (2024) · Medicine Plus · doi:10.1016/j.medp.2023.100003 · Cited by 17 · see citing works
Nitric oxide and insulin resistance
(2015) · Immunoendocrinology · doi:10.14800/ie.657 · Cited by 16 · see citing works
Moon, J., Ha, M. J., Shin, M., Kim, O. Y., Yoo, E. H., Song, J., & Chung, J. H. (2019) · Nutrients · doi:10.3390/nu11123035 · Cited by 15 · see citing works
Ghasemi, A., Afzali, H., & Jeddi, S. (2021) · Biomedical Journal · doi:10.1016/j.bj.2021.04.004 · Cited by 14 · see citing works
Oral nitrite therapy improves vascular function in diabetic mice
Sindler, A. L., Cox‐York, K. A., Reese, L., Bryan, N. S., Seals, D. R., & Gentile, C. L. (2015) · Diabetes and Vascular Disease Research · doi:10.1177/1479164114565628 · Cited by 13 · see citing works
Aggarwal, H., Pathak, P., Kumar, Y., Jagavelu, K., & Dikshit, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010195 · Cited by 13 · see citing works
Nitric Oxide Formation From Inorganic Nitrate
Lundberg, J. O., & Weitzberg, E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804273-1.00012-0 · Cited by 12 · see citing works
The role of Dermcidin isoform-2 in the occurrence and severity of Diabetes
Bhattacharya, S., Khan, M. M., Ghosh, C., Bank, S., & Maiti, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-07958-3 · Cited by 14 · see citing works
Jeddi, S., Yousefzadeh, N., Afzali, H., & Ghasemi, A. (2020) · Gene · doi:10.1016/j.gene.2020.145155 · Cited by 12 · see citing works
Floyd, C. N., Lidder, S., Hunt, J., Omar, S. A., McNeill, K. L., & Webb, A. J. (2019) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.13913 · Cited by 11 · see citing works
Farahani, A., Farahani, A., Kashfi, K., & Ghasemi, A. (2025) · Medical Gas Research · doi:10.4103/mgr.medgasres-d-24-00100 · Cited by 12 · see citing works
Yousefzadeh, N., Jeddi, S., Zarkesh, M., Kashfi, K., & Ghasemi, A. (2023) · Scientific Reports · doi:10.1038/s41598-023-31240-4 · Cited by 12 · see citing works
Anti-oxidant effect of nitrite in the pancreatic islets of type 2 diabetic male rats.
Ghasemi, A., Gheibi, S., Kashfi, K., & Jeddi, S. (2023) · PubMed Central · doi:10.22038/ijbms.2023.68245.14900 · Cited by 11 · see citing works
Jeddi, S., Gheibi, S., Carlström, M., Kashfi, K., & Ghasemi, A. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118770 · Cited by 11 · see citing works
Oral and systemic diseases under the framework of homeostatic medicine
Zhou, J., Li, X., Hu, L., & Wang, S. (2026) · Dental Research · doi:10.1016/j.dtrs.2026.100027 · Cited by 11 · see citing works
Bryan, N. S. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-384947-2.00484-0 · Cited by 10 · see citing works
Glucose Homeostasis Is Dysregulated in Ducks Infected with Duck Hepatitis B Virus
Tan, Y., Liu, J., Qin, Y., Liang, B., Gu, Y., Liang, L., Liu, L., Liu, Y., & Su, H. (2021) · Intervirology · doi:10.1159/000516766 · Cited by 9 · see citing works
Fischer, A., Lüersen, K., Schultheiß, G., de Pascual‐Teresa, S., Mereu, A., Ipharraguerre, I. R., & Rimbach, G. H. (2019) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.19-43 · Cited by 9 · see citing works
Paiva, B., Laranjinha, J. A. N., & Rocha, B. S. (2024) · FEBS Letters · doi:10.1002/1873-3468.14859 · Cited by 11 · see citing works
Gonçalves, J. S., Marçal, A. L., Marques, B. S., Costa, F. D., Laranjinha, J., Rocha, B. S., & Lourenço, C. F. (2024) · Biochemical Society Transactions · doi:10.1042/bst20230491 · Cited by 6 · see citing works
Karimzadeh, L., Behrouz, V., Sohrab, G., Razavion, T., & Haji‐Maghsoudi, S. (2024) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2024.2395817 · Cited by 6 · see citing works
Abianeh, S. H., Bajestani, S. M., Rahmati, J., Shahrbaf, M. A., & Shirzad, N. (2020) · European Journal of Plastic Surgery · doi:10.1007/s00238-020-01683-3 · Cited by 6 · see citing works
Dietary Nitrite: from menace to marvel
Bryan, N. S. (2016) · Functional Foods in Health and Disease · doi:10.31989/ffhd.v6i11.295 · Cited by 6 · see citing works
Oghbaei, H., Alipour, M. R., Mohaddes, G., Hamidian, G., & Keyhanmanesh, . (2019) · Endocrine Regulations · doi:10.2478/enr-2019-0003 · Cited by 5 · see citing works
Donnell, R. A., Carré, J. E., & Affourtit, C. (2022) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2022.101274 · Cited by 5 · see citing works
Sowton, A. P., Holzner, L. M. W., Krause, F. N., Baxter, R. M., Mocciaro, G., Krzyzanska, D., Minnion, M., O’Brien, K. A., Harrop, M. C., Darwin, P. M., et al. (2024) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00256.2024 · Cited by 4 · see citing works
Kramkowski, K., Leszczynska, A., Przyborowski, K., Proniewski, B., Marcińczyk, N., Rykaczewska, U., Jarmoc, D., Chabielska, E., & Chłopicki, S. (2016) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-016-1308-5 · Cited by 4 · see citing works
Shahraki, Z. S., Karbalaei, N., & Nemati, M. (2020) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-020-00516-1 · Cited by 4 · see citing works
Wynne, A. G., & Affourtit, C. (2022) · PLoS ONE · doi:10.1371/journal.pone.0266905 · Cited by 5 · see citing works
Impact of different hormones on the regulation of nitric oxide in diabetes
Gluvic, Z. M., Obradovic, M. M., Manojlovic, M. S., Giglio, R. V., Patti, A. M., Ciaccio, M., Suri, J. S., Rizzo, M., & Isenović, E. R. (2024) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2024.112325 · Cited by 3 · see citing works
El-Nabarawy, N. A., Zohdy, K. M., Medany, S. S., & Fadlallah, S. A. (2019) · Microchemical Journal · doi:10.1016/j.microc.2019.104398 · Cited by 3 · see citing works
Nitric Oxide Bioavailability and Insulin Resistance: An Overview
Kobayashi, J. (2022) · Book Publisher International (a part of SCIENCEDOMAIN International) · doi:10.9734/bpi/capr/v8/4440a · Cited by 2 · see citing works
The organic nitrate NDBP promotes cardiometabolic protection in type 1 diabetic mice
Fernandes-Costa, F., da Silva, R. T. G., Flôr, A. F. D. L., Brandão, M. C. R., de Athayde-Filho, P. F., de França-Falcão, M. D. S., Braga, V. A., dos Santos, G. J., Carlström, M., & Cruz, J. C. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105526 · Cited by 2 · see citing works
Blau, L. S., Gerber, J., Finkel, A., Lützow, M., Maassen, N., Röhrich, M. A., Hanff, E., Tsikas, D., Shushakov, V., & Jantz, M. (2023) · Applied Sciences · doi:10.3390/app13116849 · Cited by 2 · see citing works
Anti‐obesity effects of Beta vulgaris and Eruca sativa‐based extracts
Markou, M. I., Katsouda, A., Papaioannou, V., Argyropoulou, A., Vanioti, Μ., Tamvakopoulos, C., Skaltsounis, A., Halabalaki, M., Mitakou, S., & Papapetropoulos, A. (2024) · Phytotherapy Research · doi:10.1002/ptr.8291 · Cited by 2 · see citing works
Adelu, A. O., Durojaiye, O. K., & Owie, U. C. (2024) · African Journal of Agriculture and Food Science · doi:10.52589/ajafs-ekdavahq · Cited by 1 · see citing works
Mirzababaei, A., Mahmoodi, M., Keshtkar, A., Ashraf, H., Pashayee-Khamene, F., Khalili, P., & Mirzaei, K. (2026) · Scientific Reports · doi:10.1038/s41598-026-37907-y · Cited by 1 · see citing works
Gonçalves, J. S., Marcal, A., Laranjinha, J. A. N., & Lourenço, C. F. (2026) · European Journal of Clinical Investigation · doi:10.1111/eci.70223 · Cited by 1 · see citing works
Epigenetics and the Regulation of Nitric Oxide
Handy, D. E., & Loscalzo, J. (2017) · Springer eBooks · doi:10.1007/978-3-319-46189-2_4 · Cited by 1 · see citing works
Wynne, A. G., & Affourtit, C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.30.486447 · Cited by 1 · see citing works
Shepherd, A. I., Wilkerson, D. P., Dobson, L., Kelly, J., Winyard, P. G., Jones, A. M., Benjamin, N., Shore, A. C., & Gilchrist, M. (2015) · Nitric Oxide · doi:10.1016/j.niox.2015.01.002 · Cited by 88 · see citing works
Effect of Short Term High Dietary Salt on Insulin sensitivity in the Peripheral Tissues.
Abdelsadik, A., & Faisal, M. N. (2018) · Bulletin of Egyptian Society for Physiological Sciences · doi:10.21608/besps.2018.8212
Nitrate, Nitrite and Type 2 Diabetes
Bahadoran, Z., Mirmiran, P., Kashfi, K., & Ghasemi, A. (2022) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/9789815079814122010017
Involvement of Nitric Oxide in Insulin Secretion to Carbohydrate Metabolism
Khatua, S., Bank, S., & Acharya, K. (2023) · Advances in biochemistry in health and disease · doi:10.1007/978-3-031-24778-1_10
- Authors
- Jiang, H., Torregrossa, A. C., Potts, A., Pierini, D., Aranke, M., Garg, H. K., & Bryan, N. S.
- Affiliations
- Brown Foundation Institute of Molecular Medicine for the Prevention of Human Diseases (US)
- California State University, Fullerton (US)
- The University of Texas at Austin (US)
- Corresponding author
- Bryan, Nathan S.
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 67
- Pages
- 51-57
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W2049215298
- Cited by
- 105
- References
- 45
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 8 · 2023: 8 · 2022: 7 · 2021: 9 · 2020: 11 · 2019: 12 · 2018: 7 · 2017: 13 · 2016: 7 · 2015: 11 · 2014: 3
- FWCI
- 4.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Texas Health Science Center at Houston
- Hospital for Sick Children
- Topics
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Natural Antidiabetic Agents Studies
- Keywords
- dietary nitrite, sodium nitrite, insulin signaling, GLUT4 translocation, nitric oxide, type 2 diabetes, endothelial nitric oxide synthase, PI3K/Akt signaling, nitrosation, S-nitrosoglutathione, db/db mice, skeletal muscle, glycemic control
- MeSH terms
- Animals, Diabetes Mellitus, Type 2, Disease Models, Animal, Ethylmaleimide, Gene Expression Regulation, Humans, Male, Mice, Transgenic, Nitric Oxide, Receptor, Insulin, Sodium Nitrite, Signal Transduction, Proto-Oncogene Proteins c-myc, Protein Transport, Glucose Transporter Type 4, Mice, Rats, Nitric Oxide Synthase Type III
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