Physiology of Nitric Oxide in Skeletal Muscle

Stamler, Jonathan S.; Meissner, Gerhard

doi:10.1152/physrev.2001.81.1.209

Cited by 1,080Nitric Oxide and Endothelin EffectsMuscle Physiology and DisordersCardiovascular and exercise physiology

Physiology of Nitric Oxide in Skeletal Muscle

Stamler, Jonathan S., Meissner, Gerhard·2001·Physiological Reviews

DOI 10.1152/physrev.2001.81.1.209

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Abstract

In the past five years, skeletal muscle has emerged as a paradigm of "nitric oxide" (NO) function and redox-related signaling in biology. All major nitric oxide synthase (NOS) isoforms, including a muscle-specific splice variant of neuronal-type (n) NOS, are expressed in skeletal muscles of all mammals. Expression and localization of NOS isoforms are dependent on age and developmental stage, innervation and activity, history of exposure to cytokines and growth factors, and muscle fiber type and species. nNOS in particular may show a fast-twitch muscle predominance. Muscle NOS localization and activity are regulated by a number of protein-protein interactions and co- and/or posttranslational modifications. Subcellular compartmentalization of the NOSs enables distinct functions that are mediated by increases in cGMP and by S-nitrosylation of proteins such as the ryanodine receptor-calcium release channel. Skeletal muscle functions regulated by NO or related molecules include force production (excitation-contraction coupling), autoregulation of blood flow, myocyte differentiation, respiration, and glucose homeostasis. These studies provide new insights into fundamental aspects of muscle physiology, cell biology, ion channel physiology, calcium homeostasis, signal transduction, and the biochemistry of redox-related systems.

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The physiological responder status of caffeine may have a greater implication on caffeine efficacy, with a dose-response relationship relative to body weight needed to invoke effectiveness.
“It may be that the physiological responder status of caffeine has a greater implication on caffeine efficacy [298]; with a dose–response relationship relative to body weight needed to invoke effectiveness [291].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [298]
NO can modulate skeletal muscle function through regulation of blood flow, contractility, glucose and calcium homeostasis, and mitochondrial respiration and biogenesis.
“NO can modulate skeletal muscle function through its role in the regulation of blood flow, contractility, glucose and calcium homeostasis, and mitochondrial respiration and biogenesis [19].”
From Dietary Nitrate Supplementation and Exercise Performance (2014) · cites this paper as [19]
Nitric oxide plays important roles in vascular and metabolic control.
“In conditions of low oxygen availability, nitrite can be converted into nitric oxide, which is known to play a number of important roles in vascular and metabolic control.”
From Dietary Nitrate Supplementation and Exercise Performance (2014) · cites this paper as [19]
NO can react with protein thiols to form RSNO groups in a reversible process termed S-nitrosylation.
“Indeed, NO can react with protein thiols (i.e., moieties containing sulfhydryl groups, RSH or RS−) to form RSNO groups in a reversible process termed S-nitrosylation [137].”
From Effects of Dietary Nitrate Supplementation on Weightlifting Exercise Performance in Healthy Adults: A Systematic Review (2020) · cites this paper as [137]

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Hussain, S. N. A., Giaid, A., Dawiri, Q. E., Sakkal, D., Hattori, R., & Guo, Y. (1997) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.17.2.2612 · Cited by 53 · see citing works
Leukocyte adhesion induced by inhibition of nitric oxide production in skeletal muscle
Akimitsu, T., Gute, D. C., & Korthuis, R. J. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.5.1725 · Cited by 53 · see citing works
Nitroprusside inhibits neurotransmitter release at the frog neuromuscular junction
Lindgren, C. A., & Laird, M. V. (1994) · Neuroreport · doi:10.1097/00001756-199410270-00054 · Cited by 52 · see citing works
Sulfhydryl-Disulfide Modulation and the Role of Disulfide Oxidoreductases in Regulation of the Catalytic Activity of Nitric Oxide Synthase in Pulmonary Artery Endothelial Cells
Patel, J. M., & Block, E. R. (1995) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.13.3.7544597 · Cited by 52 · see citing works
Kinetics of NO Ligation with Nitric-oxide Synthase by Flash Photolysis and Stopped-flow Spectrophotometry
Scheele, J. S., Bruner, E. L., Kharitonov, V. G., Pavel Martasek, E., Roman, L. J., Masters, B. S. S., Sharma, V. S., & Magde, D. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.19.13105 · Cited by 52 · see citing works
Resistance responses in proximal arterial vessels, arterioles and veins during reactive hyperaemia in skeletal muscle and their underlying regulatory mechanisms
Björnberg, J., ALBERT, U., & Mellander, S. (1990) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1990.tb08957.x · Cited by 51 · see citing works
Increase of Neuronal Nitric Oxide Synthase in Rat Skeletal Muscle during Ageing
Capanni, C., Squarzoni, S., Petrini, S., Villanova, M., Muscari, C., Maraldi, N. M., Guarnieri, C., & Caldarera, C. M. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.8404 · Cited by 48 · see citing works
NO synthase II in mouse skeletal muscle is associated with caveolin 3
Gath, I., Ebert, J. G., Gödtel‐Armbrust, U., Ross, R., Reske‐Kunz, A. B., & Förstermann, U. (1999) · Biochemical Journal · doi:10.1042/bj3400723 · Cited by 47 · see citing works
Neurogenically derived nitrosyl factors mediate sympathetic vasodilation in the hindlimb of the rat
Davisson, R. L., Possas, O. S., Murphy, S. P., et al. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.272.5.h2369 · Cited by 44 · see citing works
Dystrophin is phosphorylated by endogenous protein kinases
Luise, M., Presotto, C., Senter, L., et al. (1993) · Biochemical Journal · doi:10.1042/bj2930243 · Cited by 44 · see citing works
Muscle NMDA receptors regulate the resting membrane potential through NO-synthase.
Ak, U., St, M., Gi, P., et al. (1995) · PubMed · Cited by 44 · see citing works
Effect of nitric oxide on the maximal velocity of shortening of a mouse skeletal muscle
Maréchal, G., & Beckersbleukx, G. (1998) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050722 · Cited by 43 · see citing works
Overexpression of fragile X gene (FMR-1) transcripts increases cAMP production in neural cells.
Berry‐Kravis, E. (1998) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19980101)51:1 · Cited by 42 · see citing works
Regulation of inducible nitric oxide synthase expression in L6 rat skeletal muscle cells
Okuda, S., Kanda, F., Kawahara, Y., et al. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.1.c35 · Cited by 41 · see citing works
Expression of Different Isoforms of Nitric Oxide Synthase in Experimentally Denervated and Reinnervated Skeletal Muscle
Tews, D. S., Goebel, H. H., Schneider, I., Gunkel, A. R., Stennert, E., & Neiss, W. F. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199712000-00003 · Cited by 41 · see citing works
Cyclic GMP is a Second Messenger by which Nitric Oxide Inhibits Diaphragm Contraction
Abraham, R. Z., Kobzik, L., Moody, M. R., Reid, M. B., & Stamler, J. S. (1998) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(97)00421-2 · Cited by 39 · see citing works
Self-citation
Effect of nitroprusside and endothelium-derived products on slow-twitch skeletal muscle function in vitro
Murrant, C. L., Woodley, N. E., & Barclay, J. K. (1994) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y94-152 · Cited by 38 · see citing works
Nitric oxide synthase (NOS) in mouse skeletal muscle development and differentiated myoblasts
Blottner, D., & L�ck, G. (1998) · Cell and Tissue Research · doi:10.1007/s004410051060 · Cited by 38 · see citing works
Ontogenesis of Nitric Oxide Synthases in the Ventilatory Muscles
DWAIRI, Q. E., Guo, Y., Comtois, A. S., Zhu, E., Greenwood, M. T., Bredt, D. S., & Hussain, S. N. A. (1998) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.18.6.3109 · Cited by 37 · see citing works
Accumulation of NO synthase (type-I) at the neuromuscular junctions in adult mice
Oliver, L., Goureau, O., Courtois, Y., et al. (1996) · Neuroreport · doi:10.1097/00001756-199603220-00019 · Cited by 35 · see citing works
Immunolocalization of Nitric Oxide Synthases at the Postsynaptic Domain of Human and Rat Neuromuscular Junctions—Light and Electron Microscopic Studies
Yang, C., Alvarez, R. B., Engel, W. K., et al. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6663 · Cited by 35 · see citing works
Effects ofS-nitroso-N-acetylcysteine on contractile function of reperfused skeletal muscle
Chen, L., Seaber, A. V., Nasser, R. M., Stamler, J. S., & Urbaniak, J. R. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.274.3.r822 · Cited by 34 · see citing works
Self-citation
Activation and inhibition of purified skeletal muscle calcium release channel by NO donors in single channel current recordings
Josef, S. U. K. O., Drobny, H., & Hellmann, G. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(99)00098-1 · Cited by 32 · see citing works
Ultrastructural localization of α1-syntrophin and neuronal nitric oxide synthase in normal skeletal myofiber, and their relation to each other and to dystrophin
Wakayama, Y., Inoue, M., Murahashi, M., Shibuya, S., Jimi, T., Kojima, H., & Oniki, H. (1997) · Acta Neuropathologica · doi:10.1007/s004010050733 · Cited by 32 · see citing works
The effect of nitric oxide and endothelin on skeletal muscle contractility changes when stimulation is altered
Murrant, C. L., Frisbee, J. C., & Barclay, J. K. (1997) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y97-096 · Cited by 32 · see citing works
Regulation of nitric oxide production in response to skeletal muscle activation
Fujii, Y., Guo, Y. E., & Hussain, S. N. A. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.6.2330 · Cited by 32 · see citing works
Role of endothelial factors in active hyperemic responses in contracting canine muscle
King‐VanVlack, C. E., Curtis, S. E., Mewburn, J. D., et al. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.79.1.107 · Cited by 31 · see citing works

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Exercise-Induced Oxidative Stress: Cellular Mechanisms and Impact on Muscle Force Production
Powers, S. K., & Jackson, M. J. (2008) · Physiological Reviews · doi:10.1152/physrev.00031.2007 · Cited by 2,459 · see citing works
Satellite Cells and the Muscle Stem Cell Niche
Yin, H., Price, F., & Rudnicki, M. A. (2013) · Physiological Reviews · doi:10.1152/physrev.00043.2011 · Cited by 2,166 · see citing works
Dietary nitrate supplementation reduces the O 2 cost of low-intensity exercise and enhances tolerance to high-intensity exercise in humans
Bailey, S. J., Winyard, P., Vanhatalo, A., Blackwell, J. R., DiMenna, F. J., Wilkerson, D. P., Tarr, J., Benjamin, N., & Jones, A. M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00722.2009 · Cited by 759 · 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
Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans
Bailey, S. J., Fulford, J., Vanhatalo, A., Winyard, P. G., Blackwell, J. R., DiMenna, F. J., Wilkerson, D. P., Benjamin, N., & Jones, A. M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00046.2010 · Cited by 607 · see citing works
Acute and chronic effects of dietary nitrate supplementation on blood pressure and the physiological responses to moderate-intensity and incremental exercise
Vanhatalo, A., Bailey, S. J., Blackwell, J. R., DiMenna, F. J., Pavey, T. G., Wilkerson, D. P., Benjamin, N., Winyard, P. G., & Jones, A. M. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00206.2010 · Cited by 529 · see citing works
Systemic AAV Micro-dystrophin Gene Therapy for Duchenne Muscular Dystrophy
Duan, D. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2018.07.011 · Cited by 489 · see citing works
Beetroot juice and exercise: pharmacodynamic and dose-response relationships
Wylie, L. J., Kelly, J., Bailey, S. J., Blackwell, J. R., Skiba, P. F., Winyard, P. G., Jeukendrup, A. E., Vanhatalo, A., & Jones, A. M. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00372.2013 · Cited by 500 · see citing works
Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals
Nisoli, E., Falcone, S., Tonello, C., Cozzi, V., Palomba, L., Fiorani, M., Pisconti, A., Brunelli, S., Cardile, A., Francolini, M., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405432101 · Cited by 495 · see citing works
Dietary Nitrate Supplementation and Exercise Performance
Jones, A. M. (2014) · Sports Medicine · doi:10.1007/s40279-014-0149-y · Cited by 442 · see citing works
Oxidative Stress, Chronic Disease, and Muscle Wasting
Moylan, J. S., & Reid, M. B. (2007) · Muscle & Nerve · doi:10.1002/mus.20743 · Cited by 416 · see citing works
Mechanisms of disuse muscle atrophy: role of oxidative stress
Powers, S. K., Kavazis, A. N., & DeRuisseau, K. C. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00469.2004 · Cited by 368 · see citing works
Impact of dietary nitrate supplementation via beetroot juice on exercising muscle vascular control in rats
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) · The Journal of Physiology · doi:10.1113/jphysiol.2012.243121 · Cited by 333 · see citing works
Free radicals and muscle fatigue: of ROS, canaries, and the IOC
Reid, M. B. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.03.002 · Cited by 329 · see citing works
The chemistry of nitrosative stress induced by nitric oxide and reactive nitrogen oxide species. Putting perspective on stressful biological situations
Ridnour, L. A., Thomas, D. D., Mancardi, D., Espey, M. G., Miranda, K. M., Paolocci, N., Feelisch, M., Fukuto, J., & Wink, D. A. (2004) · Biological Chemistry · doi:10.1515/bc.2004.001 · Cited by 312 · see citing works
Studies of Mitochondrial and Nonmitochondrial Sources Implicate Nicotinamide Adenine Dinucleotide Phosphate Oxidase(s) in the Increased Skeletal Muscle Superoxide Generation That Occurs During Contractile Activity
Sakellariou, G. K., Vasilaki, A., Palomero, J., Kayani, A., Zibrik, L., McArdle, A., & Jackson, M. J. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4623 · Cited by 276 · see citing works
The Noncanonical Pathway for In Vivo Nitric Oxide Generation: The Nitrate-Nitrite-Nitric Oxide Pathway
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
The many roads to mitochondrial dysfunction in neuroimmune and neuropsychiatric disorders
Morris, G., & Berk, M. (2015) · BMC Medicine · doi:10.1186/s12916-015-0310-y · Cited by 245 · see citing works
Effects of short-term dietary nitrate supplementation on blood pressure, O2uptake kinetics, and muscle and cognitive function in older adults
Kelly, J., Fulford, J., Vanhatalo, A., Blackwell, J. R., French, O., Bailey, S. J., Gilchrist, M., Winyard, P. G., & Jones, A. M. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00406.2012 · Cited by 232 · see citing works
Effects of Beetroot Juice Supplementation on Cardiorespiratory Endurance in Athletes. A Systematic Review
Domínguez, R., Cuenca, E., Maté-Muñoz, J., García-Fernández, P., Serra-Paya, N., Estevan, M., Herreros, P., & Garnacho-Castaño, M. (2017) · Nutrients · doi:10.3390/nu9010043 · Cited by 227 · see citing works
Skeletal muscle dysfunction in patients with chronic obstructive pulmonary disease
Hussain, S., Cheol, K., & Mofarrahi, M. (2008) · International Journal of Chronic Obstructive Pulmonary Disease · doi:10.2147/copd.s4480 · Cited by 224 · see citing works
The Effect of Dietary Nitrate Supplementation on Endurance Exercise Performance in Healthy Adults: A Systematic Review and Meta-Analysis
McMahon, N. F., Leveritt, M. D., & Pavey, T. G. (2017) · Sports Medicine · doi:10.1007/s40279-016-0617-7 · Cited by 221 · see citing works
Dietary nitrate supplementation improves team sport-specific intense intermittent exercise performance
Wylie, L. J., Mohr, M., Krustrup, P., Jackman, S. R., Ermιdis, G., Kelly, J., Black, M. I., Bailey, S. J., Vanhatalo, A., & Jones, A. M. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2589-8 · Cited by 220 · see citing works
Dietary Nitrate and Physical Performance
Jones, A. M., Thompson, C., Wylie, L. J., & Vanhatalo, A. (2018) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-082117-051622 · Cited by 206 · see citing works
Aerobic Fitness Affects the Exercise Performance Responses to Nitrate Supplementation
PORCELLI, S., RAMAGLIA, M., BELLISTRI, G., PAVEI, G., PUGLIESE, L., MONTORSI, M., RASICA, L., & MARZORATI, M. (2015) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000577 · Cited by 187 · see citing works
Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases
Sakellariou, G. K., Jackson, M. J., & Vasilaki, A. (2014) · Free Radical Research · doi:10.3109/10715762.2013.830718 · Cited by 184 · see citing works
Nitrate-rich vegetables increase plasma nitrate and nitrite concentrations and lower blood pressure in healthy adults
Jonvik, K. L., Nyakayiru, J., Pinckaers, P. J., Senden, J. M., van Loon, L. J., & Verdijk, L. B. (2016) · The Journal of Nutrition · doi:10.3945/jn.116.229807 · Cited by 172 · see citing works
Age-induced oxidative stress: how does it influence skeletal muscle quantity and quality?
Baumann, C. W., Kwak, D., Liu, H. M., & Thompson, L. V. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00321.2016 · Cited by 169 · see citing works
Nitrate Supplementation Enhances the Contractile Properties of Human Skeletal Muscle
HAIDER, G., & FOLLAND, J. P. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000351 · Cited by 166 · see citing works
Effects of beetroot juice supplementation on intermittent high-intensity exercise efforts
Domínguez, R., Maté-Muñoz, J. L., Cuenca, E., García-Fernández, P., Mata-Ordoñez, F., Lozano-Estevan, M. C., Veiga-Herreros, P., da Silva, S. F., & Garnacho-Castaño, M. V. (2018) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-017-0204-9 · Cited by 164 · see citing works
Effect of acute dietary nitrate intake on maximal knee extensor speed and power in healthy men and women
Coggan, A. R., Leibowitz, J. L., Kadkhodayan, A., Thomas, D. P., Ramamurthy, S., Spearie, C. A., Waller, S., Farmer, M., & Peterson, L. R. (2015) · Nitric Oxide · doi:10.1016/j.niox.2014.08.014 · Cited by 159 · see citing works
Dietary Nitrate and Nitric Oxide Metabolism: Mouth, Circulation, Skeletal Muscle, and Exercise Performance
Jones, A. M., Vanhatalo, A., Seals, D. R., Rossman, M. J., Piknova, B., & Jonvik, K. L. (2021) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002470 · Cited by 156 · see citing works
Dietary nitrate improves muscle but not cerebral oxygenation status during exercise in hypoxia
Masschelein, E., Van Thienen, R., Wang, X., Van Schepdael, A., Thomis, M., & Hespel, P. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01253.2011 · Cited by 152 · see citing works
A Single Dose of Beetroot Juice Enhances Cycling Performance in Simulated Altitude
Muggeridge, D. J., Howe, C. C. F., Spendiff, O., Pedlar, C., James, P. E., & Easton, C. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3182a1dc51 · Cited by 150 · see citing works
Influence of dietary nitrate on the physiological determinants of exercise performance: a critical review
Jones, A. M. (2014) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2014-0036 · Cited by 144 · see citing works
Dietary Nitrate, Nitric Oxide, and Cardiovascular Health
Bondonno, C. P., Croft, K. D., & Hodgson, J. M. (2016) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2013.811212 · Cited by 141 · see citing works
L-Arginine as a Potential Ergogenic Aid in Healthy Subjects
Álvares, T. S., Meirelles, C. M., Bhambhani, Y. N., Paschoalin, V. M. F., & Gomes, P. S. C. (2011) · Sports Medicine · doi:10.2165/11538590-000000000-00000 · Cited by 138 · see citing works
<scp>l</scp>-Citrulline supplementation improves O2 uptake kinetics and high-intensity exercise performance in humans
Bailey, S. J., Blackwell, J. R., Lord, T., Vanhatalo, A., Winyard, P. G., & Jones, A. M. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00192.2014 · Cited by 136 · see citing works
Influence of beetroot juice supplementation on intermittent exercise performance
Wylie, L. J., Bailey, S. J., Kelly, J., Blackwell, J. R., Vanhatalo, A., & Jones, A. M. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-015-3296-4 · Cited by 133 · see citing works
Acute <scp>l</scp>-arginine supplementation reduces the O2 cost of moderate-intensity exercise and enhances high-intensity exercise tolerance
Bailey, S. J., Winyard, P. G., Vanhatalo, A., Blackwell, J. R., DiMenna, F. J., Wilkerson, D. P., & Jones, A. M. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00503.2010 · Cited by 132 · see citing works
Dietary nitrate supplementation improves sprint and high-intensity intermittent running performance
Thompson, C., Vanhatalo, A., Jell, H., Fulford, J., Carter, J., Nyman, L., Bailey, S. J., & Jones, A. M. (2016) · Nitric Oxide · doi:10.1016/j.niox.2016.10.006 · Cited by 130 · see citing works
Nitric Oxide in Skeletal Muscle: Role on Mitochondrial Biogenesis and Function
Tengan, C., Rodrigues, G., & Godinho, R. (2012) · International Journal of Molecular Sciences · doi:10.3390/ijms131217160 · Cited by 123 · see citing works
Influence of vitamin C and vitamin E on redox signaling: implications for exercise adaptations
Cobley, J. N., McHardy, H., Morton, J. P., Nikolaidis, M. G., & Close, G. L. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.03.018 · Cited by 118 · see citing works
Human skeletal muscle nitrate store: Influence of dietary nitrate supplementation and exercise
Wylie, L. J., Park, J. W., Vanhatalo, A., Kadach, S., Black, M. I., Stoyanov, Z., Schechter, A. N., Jones, A. M., & Piknova, B. (2019) · The Journal of Physiology · doi:10.1113/jp278076 · Cited by 116 · see citing works
Dietary nitrate supplementation: effects on plasma nitrite and pulmonary O2 uptake dynamics during exercise in hypoxia and normoxia
Kelly, J., Vanhatalo, A., Bailey, S. J., Wylie, L. J., Tucker, C., List, S., Winyard, P. G., & Jones, A. M. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00068.2014 · Cited by 113 · see citing works
Skeletal Muscle Contractions Induce Acute Changes in Cytosolic Superoxide, but Slower Responses in Mitochondrial Superoxide and Cellular Hydrogen Peroxide
Pearson, T., Kabayo, T., Ng, R., Chamberlain, J., McArdle, A., & Jackson, M. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096378 · Cited by 107 · see citing works
Skeletal muscle as an endogenous nitrate reservoir
Piknova, B., Park, J. W., Swanson, K. M., Dey, S., Noguchi, C. T., & Schechter, A. N. (2015) · Nitric Oxide · doi:10.1016/j.niox.2015.02.145 · Cited by 108 · see citing works
The Effects of a Single Dose of Concentrated Beetroot Juice on Performance in Trained Flatwater Kayakers
Muggeridge, D. J., Howe, C. C. F., Spendiff, O., Pedlar, C., James, P. E., & Easton, C. (2013) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.23.5.498 · Cited by 108 · see citing works
International society of sports nutrition position stand: nutritional concerns of the female athlete
Sims, S. T., Kerksick, C. M., Smith-Ryan, A. E., Janse de Jonge, X. A. K., Hirsch, K. R., Arent, S. M., Hewlings, S. J., Kleiner, S. M., Bustillo, E., Tartar, J. L., et al. (2023) · Journal of the International Society of Sports Nutrition · doi:10.1080/15502783.2023.2204066 · Cited by 91 · see citing works
“be converted into nitric oxide, which is known to play a number of important roles in vascular and metabolic control [299].”
Background
Ingestion of a Nitric Oxide Enhancing Supplement Improves Resistance Exercise Performance
Mosher, S. L., Sparks, S. A., Williams, E. L., Bentley, D. J., & Mc Naughton, L. R. (2016) · Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000001437 · Cited by 82 · see citing works
Current Knowledge on Beetroot Bioactive Compounds: Role of Nitrate and Betalains in Health and Disease
Milton-Laskibar, I., Martínez, J. A., & Portillo, M. P. (2021) · Foods · doi:10.3390/foods10061314 · Cited by 77 · see citing works
Microalgae Produce Antioxidant Molecules with Potential Preventive Effects on Mitochondrial Functions and Skeletal Muscular Oxidative Stress
Vignaud, J., Loiseau, C., Hérault, J., Mayer, C., Côme, M., Martin, I., & Ulmann, L. (2023) · Antioxidants · doi:10.3390/antiox12051050 · Cited by 72 · see citing works
Effects of dietary nitrate supplementation on the oxygen cost of exercise and walking performance in individuals with type 2 diabetes: a randomized, double-blind, placebo-controlled crossover trial
Shepherd, A. I., Gilchrist, M., Winyard, P. G., Jones, A. M., Hallmann, E., Kazimierczak, R., Rembialkowska, E., Benjamin, N., Shore, A. C., & Wilkerson, D. P. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.05.014 · Cited by 69 · see citing works
Beetroot juice does not enhance altitude running performance in well-trained athletes
Arnold, J. T., Oliver, S. J., Lewis-Jones, T. M., Wylie, L. J., & Macdonald, J. H. (2015) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2014-0470 · Cited by 66 · see citing works
Myosin is reversibly inhibited by S-nitrosylation
Nogueira, L., Figueiredo-Freitas, C., Casimiro-Lopes, G., Magdesian, M. H., Assreuy, J., & Sorenson, M. M. (2009) · Biochemical Journal · doi:10.1042/bj20091144 · Cited by 67 · see citing works
Effects of acute supplementation of L-arginine and nitrate on endurance and sprint performance in elite athletes
Sandbakk, S. B., Sandbakk, Ø., Peacock, O., James, P., Welde, B., Stokes, K., Böhlke, N., & Tjønna, A. E. (2015) · Nitric Oxide · doi:10.1016/j.niox.2014.10.006 · Cited by 66 · see citing works
Redox Characterization of Functioning Skeletal Muscle
Zuo, L., & Pannell, B. K. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00338 · Cited by 60 · see citing works
Inorganic Nitrate Mimics Exercise-Stimulated Muscular Fiber-Type Switching and Myokine and γ-Aminobutyric Acid Release
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Authors: Stamler, J. S., & Meissner, G.
Affiliations: University of North Carolina at Chapel Hill (US)
ORCID: Stamler, Jonathan S.
Meissner, Gerhard
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2001-01-01
Volume: 81
Issue: 1
Pages: 209-237
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.2001.81.1.209
OpenAlex: W1957992664
Cited by: 1,080
References: 228
Citations by year: 2026: 21 · 2025: 20 · 2024: 35 · 2023: 42 · 2022: 46 · 2021: 52 · 2020: 49 · 2019: 43 · 2018: 66 · 2017: 44 · 2016: 40 · 2015: 56 · 2014: 41 · 2013: 69 · 2012: 46
FWCI: 4.90
Type: journal article
Language: en
Open access: closed
Locations: Physiological Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01hl052529-05)
National Heart, Lung, and Blood Institute (HL 52529, R01HL059130, HL 59130)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR18687)
Topics: Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
Keywords: nitric oxide, skeletal muscle, nitric oxide synthase, redox signaling, S-nitrosylation, ryanodine receptor, cGMP signaling, excitation-contraction coupling, myocyte differentiation, muscle respiration, glucose homeostasis, fast-twitch muscle, calcium homeostasis, post-translational modification
MeSH terms: Animals, Carrier Proteins, Cell Differentiation, Dyneins, Physical Exertion, Glucose, Humans, Isoenzymes, Mammals, Membrane Potentials, Muscle Contraction, Nitric Oxide, Regional Blood Flow, Muscle, Skeletal, Nitric Oxide Synthase, Cell Respiration, Ryanodine Receptor Calcium Release Channel, Muscular Dystrophy, Duchenne, Caveolins, Drosophila Proteins, Caveolin 3

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Physiology of Nitric Oxide in Skeletal Muscle

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