Incubation with sodium nitrite attenuates fatigue development in intact single mouse fibres at physiological
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Key points Dietary nitrate supplementation increases plasma nitrite concentration, which provides an oxygen‐independent source of nitric oxide and can delay skeletal muscle fatigue. Nitrate supplementation has been shown to increase myofibre calcium release and force production in mouse skeletal muscle during contractions at a supra‐physiological oxygen tension, but it is unclear whether nitrite exposure can delay fatigue development and improve myofibre calcium handling at a near‐physiological oxygen tension. Single mouse muscle fibres acutely treated with nitrite had a lower force and cytosolic calcium concentration during single non‐fatiguing contractions at a near‐physiological oxygen tension. Nitrite treatment delayed fatigue development during repeated fatiguing isometric contractions at near‐physiological, but not at supra‐physiological, oxygen tension in combination with better maintenance of myofilament calcium sensitivity and sarcoplasmic reticulum calcium pumping. These findings improve understanding of the mechanisms by which increased skeletal muscle nitrite exposure might be ergogenic and imply that this is related to improved calcium handling. Abstract Dietary nitrate (NO3−) supplementation, which increases plasma nitrite (NO2−) concentration, has been reported to attenuate skeletal muscle fatigue development. Sarcoplasmic reticulum (SR) calcium (Ca2+) release is enhanced in isolated single skeletal muscle fibres following NO3− supplementation or NO2− incubation at a supra‐physiological but it is unclear whether NO2− incubation can alter Ca2+ handling and fatigue development at a near‐physiological . We hypothesised that NO2− treatment would improve Ca2+ handling and delay fatigue at a physiological in intact single mouse skeletal muscle fibres. Each muscle fibre was perfused with Tyrode solution pre‐equilibrated with either 20% ( ∼150 Torr) or 2% O2 ( = 15.6 Torr) in the absence and presence of 100 µM NaNO2. At supra‐physiological (i.e. 20% O2), time to fatigue was lowered by 34% with NaNO2 (control: 257 ± 94 vs. NaNO2: 159 ± 46 s, Cohen's d = 1.63, P < 0.05), but extended by 21% with NaNO2 at 2% O2 (control: 308 ± 217 vs. NaNO2: 368 ± 242 s, d = 1.14, P < 0.01). During the fatiguing contraction protocol completed with NaNO2 at 2% O2, peak cytosolic Ca2+ concentration ([Ca2+]c) was not different (P > 0.05) but [Ca2+]c accumulation between contractions was lower, concomitant with a greater SR Ca2+ pumping rate (P < 0.05) compared to the control condition. These results demonstrate that increased exposure to NO2− blunts fatigue development at near‐physiological, but not at supra‐physiological, through enhancing SR Ca2+ pumping rate in single skeletal muscle fibres. These findings extend our understanding of the mechanisms by which increased NO2− exposure can mitigate skeletal muscle fatigue development.
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During a repeated, fatigue-inducing contraction protocol, NaNO2 administration increased time to task failure by offsetting reductions in Ca2+ pumping rate and Ca2+ sensitivity.
“However, during a repeated, fatigue-inducing contraction protocol, NaNO2 administration increased time to task failure by offsetting the reductions in Ca2+ pumping rate and Ca2+ sensitivity [135].”
From Effects of Dietary Nitrate Supplementation on Weightlifting Exercise Performance in Healthy Adults: A Systematic Review (2020) · cites this paper as [135]
The potential candidate mechanisms for improved weightlifting exercise performance after NO3− supplementation include enhanced excitation-contraction coupling via modulation of Ca2+-handling and contractile proteins; improved skeletal muscle metabolic control via lowering the high-energy phosphate cost of contraction and fatigue-related metabolite accumulation; and improved skeletal muscle PerfUSI
“The potential candidate mechanisms for improved weightlifting exercise performance after NO3− supplementation include enhanced excitation–contraction coupling, via modulation of Ca2+-handling and contractile proteins [98,134,135,139]; improved skeletal muscle metabolic control, via lowering the high-energy phosphate cost of contraction and fatigue-related metabolite accumulation [51,94]; and”
From Effects of Dietary Nitrate Supplementation on Weightlifting Exercise Performance in Healthy Adults: A Systematic Review (2020) · cites this paper as [135]
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Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide.
Ignarro, L. J., Buga, G. M., Wood, K. S., Byrns, R. E., & Chaudhuri, G. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.24.9265 · Cited by 5,074 · see citing works
Skeletal muscle fatigue: cellular mechanisms
Allen, D. G., Lamb, G. D., & Westerblad, H. (2008) · Physiological Reviews · doi:10.1152/physrev.00015.2007 · Cited by 2,495 · see citing works
Fabiato, A., & Fabiato, F. (1978) · Journal of Physiology · doi:10.1113/jphysiol.1978.sp012231 · Cited by 1,168 · see citing works
Physiology of Nitric Oxide in Skeletal Muscle
Stamler, J. S., & Meissner, G. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.1.209 · Cited by 1,080 · see citing works
Peroxynitrite, a Stealthy Biological Oxidant
Radí, R. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.r113.472936 · Cited by 891 · see citing works
Endogenous nitric oxide: physiology, pathology and clinical relevance
Moncada, S., & Higgs, E. A. (1991) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1991.tb01383.x · Cited by 760 · see citing works
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
Self-citationDietary Inorganic Nitrate Improves Mitochondrial Efficiency in Humans
Larsen, F. J., Schiffer, T. A., Borniquel, S., Sahlin, K., Ekblom, B., Lundberg, J. O., & Weitzberg, E. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.004 · Cited by 689 · cited 5× · see citing works
“For example, short-term NO3− supplementation has been reported to improve exercise economy in association with (Larsen et al. 2011), or independently of (Whitfield et al. 2016), improved efficiency of mitochondrial oxidative phosphorylation (i.e. a higher P/O ratio).”
BackgroundInfluentialMyoglobin O2 desaturation during exercise. Evidence of limited O2 transport.
Richardson, R. S., Noyszewski, E. A., Kendrick, K. F., Leigh, J. S., & Wagner, P. D. (1995) · Journal of Clinical Investigation · doi:10.1172/jci118237 · Cited by 647 · 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
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
Self-citationReporting ethical matters in The Journal of Physiology: standards and advice
Drummond, G. B. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.167387 · Cited by 570 · 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
Self-citationCastello, P. R., David, P. S., McClure, T., Crook, Z., & Poyton, R. O. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.02.011 · Cited by 495 · see citing works
Murad, F., Mittal, C. K., Arnold, W. P., Katsuki, S., & Kimura, H. (1978) · PubMed · Cited by 446 · 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
Self-citationAndrade, F. H., Reid, M. B., Allen, D. G., & Westerblad, H. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.565bn.x · Cited by 438 · see citing works
Hypoxia-induced reactive oxygen species formation in skeletal muscle
Clanton, T. L. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01298.2006 · Cited by 401 · see citing works
Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers.
Westerblad, H., & Allen, D. G. (1991) · The Journal of General Physiology · doi:10.1085/jgp.98.3.615 · Cited by 385 · see citing works
Nitrite‐derived nitric oxide: a possible mediator of ‘acidic–metabolic’ vasodilation
Modin, A., Björne, H., Herulf, M., Alving, K., Weitzberg, E., & Lundberg, J. O. N. (2001) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2001.00771.x · Cited by 346 · see citing works
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
Self-citationHernández, A., Schiffer, T. A., Ivarsson, N., Cheng, A. J., Bruton, J. D., Lundberg, J. O., Weitzberg, E., & Westerblad, H. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.232777 · Cited by 319 · see citing works
Effect of Inorganic Nitrate on Exercise Capacity in Heart Failure With Preserved Ejection Fraction
Zamani, P., Rawat, D., Shiva-Kumar, P., Geraci, S., Bhuva, R., Konda, P., Doulias, P.-T., Ischiropoulos, H., Townsend, R. R., Margulies, K. B., et al. (2015) · Circulation · doi:10.1161/circulationaha.114.012957 · Cited by 307 · see citing works
Mohr, S., Stamler, J. S., & Brüne, B. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.8.4209 · Cited by 251 · see citing works
Dietary nitrate reduces muscle metabolic perturbation and improves exercise tolerance in hypoxia
Vanhatalo, A., Fulford, J., Bailey, S. J., Blackwell, J. R., Winyard, P. G., & Jones, A. M. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.216341 · Cited by 233 · see citing works
Self-citationControl of microvascular oxygen pressures in rat muscles comprised of different fibre types
McDonough, P., Behnke, B. J., Padilla, D. J., Musch, T. I., & Poole, D. C. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.079533 · Cited by 228 · see citing works
Tocchetti, C. G., Wang, W., Froehlich, J. P., Huke, S., Aon, M. A., Wilson, G. M., Benedetto, G. D., O'Rourke, B. P., Gao, W. D., Wink, D. A., et al. (2006) · Circulation Research · doi:10.1161/01.res.0000253904.53601.c9 · Cited by 216 · see citing works
The medical use of oxygen: a time for critical reappraisal
Sjöberg, F., & Singer, M. (2013) · Journal of Internal Medicine · doi:10.1111/joim.12139 · Cited by 214 · 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
NO-synthase independent NO generation in mammals
Lundberg, J. O., & Weitzberg, E. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.02.136 · Cited by 172 · 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
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
NO generation from inorganic nitrate and nitrite: Role in physiology, nutrition and therapeutics
Lundberg, J. O., & Weitzberg, E. (2009) · Archives of Pharmacal Research · doi:10.1007/s12272-009-1803-z · Cited by 153 · see citing works
Coggan, A. R., Leibowitz, J. L., Spearie, C. A., Kadkhodayan, A., Thomas, D. P., Ramamurthy, S., Mahmood, K., Park, S., Waller, S., Farmer, M., et al. (2015) · Circulation Heart Failure · doi:10.1161/circheartfailure.115.002141 · Cited by 136 · see citing works
Effects of nitric oxide on the contraction of skeletal muscle
Maréchal, G., & Gailly, P. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050359 · Cited by 135 · see citing works
Effect of nitric oxide on single skeletal muscle fibres from the mouse
Andrade, F. H., Reid, M. B., Allen, D. G., & Westerblad, H. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.577bn.x · Cited by 133 · see citing works
Sarcolipin: A Key Thermogenic and Metabolic Regulator in Skeletal Muscle
Pant, M., Bal, N. C., & Periasamy, M. (2016) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2016.08.006 · Cited by 133 · see citing works
Ferguson, S. K., Holdsworth, C. T., Wright, J. L., Fees, A. J., Allen, J. D., Jones, A. M., Musch, T. I., & Poole, D. C. (2015) · Nitric Oxide · doi:10.1016/j.niox.2014.09.157 · Cited by 120 · see citing works
Self-citationFulford, J., Winyard, P. G., Vanhatalo, A., Bailey, S. J., Blackwell, J. R., & Jones, A. M. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1220-5 · Cited by 118 · see citing works
Self-citationHuman 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
Self-citationWhitfield, J., Ludzki, A., Heigenhauser, G. J. F., Senden, J. M. G., Verdijk, L. B., van Loon, L. J. C., Spriet, L. L., & Holloway, G. P. (2016) · The Journal of Physiology · doi:10.1113/jp270844 · Cited by 115 · see citing works
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
Self-citationWesterblad, H., & Allen, D. G. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020022 · Cited by 104 · see citing works
Westerblad, H., & Allen, D. G. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019074 · Cited by 92 · see citing works
Barclay, C. J. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140038 · Cited by 91 · see citing works
METABOLISM OF INORGANIC NITRITE AND NITRATE ESTERS
HEPPEL, L. A., & Hilmoe, R. J. (1950) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)56450-4 · Cited by 90 · see citing works
Ca2+ levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice.
Bakker, A. J., Head, S. I., Williams, D. A., & Stephenson, D. G. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019455 · Cited by 89 · see citing works
Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide
Eu, J. P., Hare, J. M., Hess, D. T., Skaf, M. W., Sun, J., Cardenas-Navina, I., Sun, Q.-A., Dewhirst, M. W., Meissner, G., & Stamler, J. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2433468100 · Cited by 89 · see citing works
Yang, T., Peleli, M., Zollbrecht, C., Giulietti, A., Terrando, N., Lundberg, J. O., Weitzberg, E., & Carlström, M. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.02.016 · Cited by 88 · see citing works
Beetroot Juice Increases Human Muscle Force without Changing Ca2+-Handling Proteins
WHITFIELD, J., GAMU, D., HEIGENHAUSER, G. J. F., VAN LOON, L. J. C., SPRIET, L. L., TUPLING, A. R., & HOLLOWAY, G. P. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001321 · Cited by 83 · see citing works
Peroxynitrite induces contractile dysfunction and lipid peroxidation in the diaphragm
Supinski, G. S., Stofan, D. A., Callahan, L. A., Nethery, D. E., Nosek, T. M., & DiMarco, A. F. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.87.2.783 · Cited by 79 · see citing works
Skeletal Muscle Function during Exercise—Fine-Tuning of Diverse Subsystems by Nitric Oxide
Suhr, F., Gehlert, S., Grau, M., & Bloch, W. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14047109 · Cited by 78 · see citing works
Direct Regulation of Striated Muscle Myosins by Nitric Oxide and Endogenous Nitrosothiols
Evangelista, A. M., Rao, V. S., Filo, A. R., Marozkina, N. V., Doctor, A., Jones, D. R., Gaston, B., & Guilford, W. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011209 · Cited by 69 · see citing works
Moopanar, T. R., & Allen, D. G. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.101105 · Cited by 68 · 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
Self-citationMETABOLISM OF INORGANIC NITRITE AND NITRATE ESTERS
HEPPEL, L. A., & Porterfield, V. T. (1949) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)56874-5 · Cited by 64 · see citing works
Effect of dietary nitrate levels on nitrate fluxes in rat skeletal muscle and liver
Gilliard, C. N., Lam, J. K., Cassel, K. S., Park, J. W., Schechter, A. N., & Piknova, B. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.01.010 · Cited by 63 · see citing works
Skeletal muscle microvascular and interstitial from rest to contractions
Hirai, D. M., Craig, J. C., Colburn, T. D., Eshima, H., Kano, Y., Sexton, W. L., Musch, T. I., & Poole, D. C. (2017) · The Journal of Physiology · doi:10.1113/jp275170 · Cited by 60 · see citing works
Kinetic analysis of DAF-FM activation by NO: Toward calibration of a NO-sensitive fluorescent dye
Namin, S. M., Nofallah, S., Joshi, M. S., Kavallieratos, K., & Tsoukias, N. M. (2012) · Nitric Oxide · doi:10.1016/j.niox.2012.10.001 · Cited by 59 · see citing works
Sarco/endoplasmic reticulum Ca2+-ATPase isoforms: diverse responses to acidosis
Wolosker, H., da Rocha, J. B. T., Engelender, S., Panizzutti, R., Miranda, J. D., & MEIS, L. D. (1997) · Biochemical Journal · doi:10.1042/bj3210545 · Cited by 55 · see citing works
Coggan, A. R., Broadstreet, S. R., Mahmood, K., Mikhalkova, D., Madigan, M., Bole, I., Park, S., Leibowitz, J. L., Kadkhodayan, A., Thomas, D. P., et al. (2017) · Journal of Cardiac Failure · doi:10.1016/j.cardfail.2017.09.004 · Cited by 52 · see citing works
Nogueira, L., Trisko, B. M., Lima‐Rosa, F. L., Jackson, J., Lund‐Palau, H., Yamaguchi, M., & Breen, E. C. (2018) · The Journal of Physiology · doi:10.1113/jp275888 · Cited by 44 · see citing works
Self-citationDutka, T. L., Verburg, E., Larkins, N. T., Hortemo, K. H., Lunde, P., Sejersted, O. M., & Lamb, G. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035226 · Cited by 37 · see citing works
Walsh, B. J., Howlett, R. A., Stary, C. M., Kindig, C. A., & Hogan, M. C. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00687.2005 · Cited by 37 · see citing works
Self-citationManaging the power grid: how myoglobin can regulate PO2 and energy distribution in skeletal muscle
Clanton, T. L. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00614.2018 · Cited by 33 · see citing works
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
Kovács, M., Kiss, A., Gönczi, M., Miskolczi, G., Seprényi, G., Kaszaki, J., Kohr, M. J., Murphy, E., & Végh, Á. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122243 · Cited by 30 · see citing works
Tupling, A. R. (2009) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h09-033 · Cited by 30 · see citing works
Dietary nitrate improves cardiac contractility via enhanced cellular Ca2+ signaling
Pironti, G., Ivarsson, N., Yang, J., Farinotti, A. B., Jonsson, W. O., Zhang, S., Bas, D. B., Svensson, C. I., Westerblad, H., Weitzberg, E., et al. (2016) · Basic Research in Cardiology · doi:10.1007/s00395-016-0551-8 · Cited by 30 · see citing works
Dietary nitrate markedly improves voluntary running in mice
Ivarsson, N., Schiffer, T. A., Hernández, A., Lanner, J. T., Weitzberg, E., Lundberg, J. O., & Westerblad, H. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.10.018 · Cited by 25 · see citing works
Nogueira, L., Shiah, A. A., Gandra, P. G., & Hogan, M. C. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00178.2013 · Cited by 24 · see citing works
Self-citationSpencer, T., & Posterino, G. S. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00251.2008 · Cited by 22 · see citing works
Gandra, P. G., Shiah, A. A., Nogueira, L., & Hogan, M. C. (2018) · The Journal of Physiology · doi:10.1113/jp275470 · Cited by 20 · see citing works
Self-citationTanaka, Y., Poole, D. C., & Kano, Y. (2016) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026616666160413130221 · Cited by 8 · see citing works
Huang, Y., He, Q., Zhan, L., & Yang, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0082552 · Cited by 2 · see citing works
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Self-citationKadach, S., Park, J. W., Stoyanov, Z., Black, M. I., Vanhatalo, A., Burnley, M., Walter, P. J., Cai, H., Schechter, A. N., Piknova, B., et al. (2023) · Acta Physiologica · doi:10.1111/apha.13924 · Cited by 38 · see citing works
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Apte, M., Nadavade, N., & Sheikh, S. S. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.11.003 · Cited by 35 · see citing works
Tan, R., Cano, L., Lago-Rodríguez, Á., & Domínguez, R. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19020762 · Cited by 37 · see citing works
Alsharif, N. S., Clifford, T., Alhebshi, A., Rowland, S. N., & Bailey, S. J. (2023) · Antioxidants · doi:10.3390/antiox12061194 · Cited by 33 · see citing works
Self-citationNyberg, M., Christensen, P. M., Blackwell, J. R., Hostrup, M., Jones, A. M., & Bangsbo, J. (2021) · The Journal of Physiology · doi:10.1113/jp281995 · Cited by 23 · see citing works
Self-citationCocksedge, S. P., Breese, B. C., Morgan, P. T., Nogueira, L., Thompson, C., Wylie, L. J., JONES, A. M., & Bailey, S. J. (2020) · Nitric Oxide · doi:10.1016/j.niox.2020.03.007 · Cited by 23 · see citing works
Self-citationEsen, Ö., Dobbin, N., & Callaghan, M. J. (2022) · Journal of the American Nutrition Association · doi:10.1080/07315724.2022.2037475 · Cited by 24 · see citing works
Tan, R., Pennell, A., Price, K. M., Karl, S. T., Seekamp-Hicks, N. G., Paniagua, K. K., Weiderman, G. D., Powell, J. P., Sharabidze, L. K., Lincoln, I. G., et al. (2022) · Nutrients · doi:10.3390/nu14183703 · Cited by 21 · see citing works
Self-citationTan, R., Pennell, A., Karl, S. T., Cass, J. K., Go, K., Clifford, T., Bailey, S. J., & Storm, C. P. (2023) · Nutrients · doi:10.3390/nu15112493 · Cited by 23 · see citing works
Self-citationde Zevallos, J. O., Hogwood, A. C., Kruse, K., Guzman, J. D., Buckley, M., WELTMAN, A. L., & Allen, J. D. (2023) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00220.2023 · Cited by 20 · see citing works
Esen, Ö., Domínguez, R., & Karayiğit, R. (2022) · Nutrients · doi:10.3390/nu14142839 · Cited by 20 · see citing works
Petrick, H. L., Brownell, S., Vachon, B., Brunetta, H. S., Handy, R. M., van Loon, L. J. C., Murrant, C. L., & Holloway, G. P. (2022) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00371.2021 · Cited by 19 · see citing works
Hogwood, A. C., de Zevallos, J. O., Kruse, K., Guzman, J. C. D., Buckley, M., WELTMAN, A. L., & Allen, J. D. (2023) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00221.2023 · Cited by 14 · see citing works
Dietary nitrate supplementation increases diaphragm peak power in old mice
Kumar, R. A., Kelley, R. C., Hahn, D., & Ferreira, L. F. (2020) · The Journal of Physiology · doi:10.1113/jp280027 · Cited by 12 · see citing works
Nitrate and Nitrite Metabolism in Aging Rats: A Comparative Study
Piknova, B., Park, J. W., Thomas, S. M., Tunau-Spencer, K. J., & Schechter, A. N. (2023) · Nutrients · doi:10.3390/nu15112490 · Cited by 11 · see citing works
Evangelista, J. F., Meirelles, C., Aguiar, G. S., Alves, R., & Matsuura, C. (2023) · Journal of the American Nutrition Association · doi:10.1080/27697061.2023.2211318 · Cited by 11 · see citing works
Evidence-based sports supplements: A redox analysis
Margaritelis, N. V., Cobley, J. N., Nastos, G. G., Παπανικολάου, Κ., Bailey, S. J., Kritsiligkou, P., & Nikolaidis, M. G. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.08.012 · Cited by 10 · see citing works
Self-citationWei, C., Vanhatalo, A., Black, M. I., Rajaram, R., Massey, G. J., & JONES, A. M. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.01.048 · Cited by 10 · see citing works
Self-citationNogueira, L., Gilmore, N. K., & Hogan, M. C. (2022) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00861.2021 · Cited by 10 · see citing works
Self-citationTan, R., Cass, J. K., Lincoln, I. G., Wideen, L. E., Nicholl, M. J., Molnar, T. J., Gough, L. A., Bailey, S. J., & Pennell, A. (2024) · Nutrients · doi:10.3390/nu16162764 · Cited by 10 · see citing works
Self-citationMcIlvenna, L. C., Muggeridge, D. J., & Whitfield, J. (2019) · The Journal of Physiology · doi:10.1113/jp279118 · Cited by 9 · see citing works
Rowland, S. N., Boit, M. D., Tan, R., Robinson, G. P., O’Donnell, E., James, L. J., & Bailey, S. J. (2022) · Antioxidants · doi:10.3390/antiox12010025 · Cited by 8 · see citing works
Self-citationTan, R., Price, K. M., Wideen, L. E., Lincoln, I. G., Karl, S. T., Seals, J. P., Paniagua, K. K., Hagen, D. W., Tchaprazian, I., Bailey, S. J., et al. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1217192 · Cited by 7 · see citing works
Self-citationRasica, L., Colosio, M., Ferri, A., Baldassarre, G., Easton, C., Burleigh, M. C., Vernillo, G., Bottinelli, R., Marzorati, M., & Porcelli, S. (2025) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000003708 · Cited by 6 · see citing works
Role of nitric oxide in convective and diffusive skeletal muscle microvascular oxygen kinetics
Poole, D. C., Ferguson, S. K., Musch, T. I., & Porcelli, S. (2022) · Nitric Oxide · doi:10.1016/j.niox.2022.01.005 · Cited by 6 · see citing works
Metabolic Factors in Skeletal Muscle Fatigue
Place, N., & Westerblad, H. (2022) · Physiology in health and disease · doi:10.1007/978-3-030-94305-9_17 · Cited by 6 · see citing works
Tan, R., Baranauskas, M. N., Karl, S. T., de Zevallos, J. O., Shei, R., Paris, H. L. R., Wiggins, C. C., & Bailey, S. J. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.05.003 · Cited by 7 · see citing works
Self-citationHogwood, A. C., de Zevallos, J. O., Kruse, K., Buckley, M., Guzman, J. C. D., Lempke, A. F. D., WELTMAN, A. L., & Allen, J. D. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00323.2024 · Cited by 5 · see citing works
de Zevallos, J. O., Hogwood, A. C., Kruse, K., Guzman, J. D., Buckley, M., Lempke, A. F. D., WELTMAN, A. L., & Allen, J. D. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00321.2024 · Cited by 5 · see citing works
Porcelli, S., Rasica, L., Ferguson, B. S., Kavazis, A. N., McDonald, J. R., Hogan, M. C., Grassi, B., & Gladden, L. B. (2020) · The Journal of Physiology · doi:10.1113/jp279789 · Cited by 5 · see citing works
Self-citationSadler, D. G., Draijer, R., Stewart, C. E., Jones, H., Marwood, S., & Thijssen, D. H. J. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04682-9 · Cited by 5 · see citing works
Wang, L., Zhao, R., Yan, Y., Zhang, H., Yan, R., Zhu, Y., Han, Z., Qu, Y., Wang, R., Li, Y., et al. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1576712 · Cited by 4 · see citing works
Tan, R., Baranauskas, M. N., Karl, S. T., de Zevallos, J. O., Shei, R., Paris, H. L. R., Wiggins, C. C., & Bailey, S. J. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.06.004 · Cited by 2 · see citing works
Self-citationEffect of nitrite on Ca2+ movements and fatigue in muscle
Lamb, G. D., & Stephenson, D. G. (2020) · The Journal of Physiology · doi:10.1113/jp279529 · Cited by 2 · see citing works
The Popeye mythology may be true: eating spinach can make you fatigue resistant!
Mosely, S., & Landberg, C. (2019) · The Journal of Physiology · doi:10.1113/jp279264 · Cited by 1 · see citing works
Nitric oxide as a mediator of exercise performance: NO pain NO gain
Allen, J. D. (2023) · Nitric Oxide · doi:10.1016/j.niox.2023.04.006 · Cited by 1 · see citing works
Nie, R., Zhang, G., Kong, J., Wang, X., Xie, Z., Lin, L., Li, T., & Liang, Y. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1699766 · Cited by 1 · see citing works
Bailey, S. J., Gandra, P. G., JONES, A. M., Hogan, M. C., & Nogueira, L. (2020) · The Journal of Physiology · doi:10.1113/jp279621
Self-citationKirsh, A. J., Juracic, E. S., Petrick, H. L., Monaco, C. M. F., Barbeau, P., Tupling, A. R., & Holloway, G. P. (2020) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2020-0078
Wei, C., Vanhatalo, A., Black, M. I., Rajaram, R., Massey, G. J., & JONES, A. M. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.5051285
Self-citationLobina, C., Carai, M. A. M., & Colombo, G. (2026) · Natural Product Communications · doi:10.1177/1934578x261434480
Xu, Z., Sun, J., Xu, S., Gu, J., Jiang, S., Guo, J., Lin, J., & Yu, L. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1823053
- Authors
- Bailey, S. J., Gandra, P. G., Jones, A. M., Hogan, M. C., & Nogueira, L.
- Affiliations
- Loughborough University (GB)
- Universidade Estadual de Campinas (UNICAMP) (BR)
- University of Exeter (GB)
- University of California San Diego (US)
- Universidade Federal do Rio de Janeiro (BR)
- Corresponding author
- Nogueira, Leonardo
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2019-10-30
- Volume
- 597
- Issue
- 22
- Pages
- 5429-5443
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC6938685
- OpenAlex
- W2974403411
- Cited by
- 51
- References
- 75
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 13 · 2022: 10 · 2021: 6 · 2020: 9 · 2019: 2
- FWCI
- 2.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Open Research Exeter (University of Exeter) (acceptedVersion)
- Figshare (submittedVersion)
- Figshare (submittedVersion, cc-by-nc-nd)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Funders
- University of Exeter
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR, ‐, 069577)
- Ministério da Ciência, Tecnologia e Inovação
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- sodium nitrite, nitrate supplementation, skeletal muscle fatigue, sarcoplasmic reticulum calcium handling, myofilament calcium sensitivity, oxygen partial pressure, nitric oxide, single muscle fibers, ergogenic effects, sarcopenia prevention, sarcopenic obesity
- MeSH terms
- Animals, Calcium, Male, Mice, Inbred C57BL, Muscle Contraction, Myofibrils, Nitric Oxide, Oxygen, Sarcoplasmic Reticulum, Sodium Nitrite, Muscle Fibers, Skeletal, Muscle Fatigue, Mice, Sarcoplasmic Reticulum Calcium-Transporting ATPases
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