Effect of citrulline malate supplementation on muscle function and bioenergetics during short-term repeated bouts of fatiguing exercise

References

• Arnold, D. L., Matthews, P. M., & Radda, G. K. (1984). Metabolic recovery after exercise and the assessment of mitochondrial function in vivo in human skeletal muscle by means of 31P NMR. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine, 1(3), 307–315. https://doi.org/10.1002/mrm.1910010303
   PubMed Web of Science ®Google Scholar
• Bendahan, D. (2002). Citrulline/malate promotes aerobic energy production in human exercising muscle. British Journal of Sports Medicine, 36(4), 282–289. https://doi.org/10.1136/bjsm.36.4.282
   PubMed Web of Science ®Google Scholar
• Bessman, S. P., & Geiger, P. J. (1981). Transport of energy in muscle: The phosphorylcreatine shuttle. Science, 211(4481), 448–452. https://doi.org/10.1126/science.6450446
   PubMed Web of Science ®Google Scholar
• Brevetti, L. S., Chang, D. S., Tang, G. L., Sarkar, R., & Messina, L. M. (2003). Overexpression of endothelial nitric oxide synthase increases skeletal muscle blood flow and oxygenation in severe rat hind limb ischemia. Journal of Vascular Surgery, 38(4), 820–826. https://doi.org/10.1016/S0741-5214(03)00555-X
   PubMed Web of Science ®Google Scholar
• Briand, J., Blehaut, H., Calvayrac, R., & Laval-Martin, D. (1992). Use of a microbial model for the determination of drug effects on cell metabolism and energetics: Study of citrulline-malate. Biopharmaceutics & Drug Disposition, 13(1), 1–22. https://doi.org/10.1002/bdd.2510130102
   PubMed Web of Science ®Google Scholar
• Cea, G. (2002). Reduced oxidative phosphorylation and proton efflux suggest reduced capillary blood supply in skeletal muscle of patients with dermatomyositis and polymyositis: A quantitative 31P-magnetic resonance spectroscopy and MRI study. Brain, 125(7), 1635–1645. https://doi.org/10.1093/brain/awf163
   PubMedGoogle Scholar
• Chin, E. R., & Allen, D. G. (1997). Effects of reduced muscle glycogen concentration on force, Ca2+ release and contractile protein function in intact mouse skeletal muscle. J Physiol (Lond), 498(1), 17–29. https://doi.org/10.1113/jphysiol.1997.sp021838
   Google Scholar
• Cook, S. B., Clark, B. C., & Ploutz-Snyder, L. L. (2007). Effects of exercise load and blood-flow restriction on skeletal muscle function. Medicine and Science in Sports and Exercise, 39(10), 1708–1713. https://doi.org/10.1249/mss.0b013e31812383d6
   PubMed Web of Science ®Google Scholar
• Cunniffe, B., Papageorgiou, M., O’Brien, B., Davies, N. A., Grimble, G. K., & Cardinale, M. (2016). Acute citrulline-malate supplementation and high-intensity cycling performance. Journal of Strength and Conditioning Research / National Strength & Conditioning Association, 30(9) , 2638–2647. https://doi.org/10.1519/JSC.0000000000001338
   PubMed Web of Science ®Google Scholar
• Farney, T. M., Bliss, M. V., Hearon, C. M., & Salazar, D. A. (2019). The Effect of Citrulline Malate Supplementation on Muscle Fatigue Among Healthy Participants. Journal of Strength and Conditioning Research / National Strength & Conditioning Association, 33(9), 2464–2470. https://doi.org/10.1519/JSC.0000000000002356
   PubMed Web of Science ®Google Scholar
• Fitts, R. H. (1994). Cellular mechanisms of muscle fatigue. Physiological Reviews, 74(1), 49–94. https://doi.org/10.1152/physrev.1994.74.1.49
   PubMed Web of Science ®Google Scholar
• Giannesini, B., Izquierdo, M., Cozzone, P. J., & Bendahan, D. (2002). Metabolic underpinnings of the paradoxical net phosphocreatine resynthesis in contracting rat gastrocnemius muscle. Biochimica et biophysica acta, 1553(3), 223–231. https://doi.org/10.1016/S0005-2728(01)00243-2
   PubMed Web of Science ®Google Scholar
• Giannesini, B., Izquierdo, M., Le Fur, Y., Cozzone, P. J., Fingerle, J., Himber, J., Kunnecke, B., Von Kienlin, M., & Bendahan, D. (2005). New experimental setup for studying strictly noninvasively skeletal muscle function in rat using 1H-magnetic resonance (MR) imaging and 31P-MR spectroscopy. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine, 54(5), 1058–1064. https://doi.org/10.1002/mrm.20637
   PubMed Web of Science ®Google Scholar
• Giannesini, B., Izquierdo, M., Le Fur, Y., Cozzone, P. J., Verleye, M., Le Guern, M. E., Gillardin, J. M., & Bendahan, D. (2009). Beneficial effects of citrulline malate on skeletal muscle function in endotoxemic rat. European Journal of Pharmacology, 602(1), 143–147. https://doi.org/10.1016/j.ejphar.2008.11.015
   PubMed Web of Science ®Google Scholar
• Giannesini, B., Le Fur, Y., Cozzone, P. J., Verleye, M., Le Guern, M. E., & Bendahan, D. (2011). Citrulline malate supplementation increases muscle efficiency in rat skeletal muscle. European Journal of Pharmacology, 667(1–3), 100–104. https://doi.org/10.1016/j.ejphar.2011.05.068
   PubMed Web of Science ®Google Scholar
• Glenn, J. M., Gray, M., Wethington, L. N., Stone, M. S., Stewart, R. W., Jr., & Moyen, N. E. (2017). Acute citrulline malate supplementation improves upper- and lower-body submaximal weightlifting exercise performance in resistance-trained females. European Journal of Nutrition, 56(2), 775–784. https://doi.org/10.1007/s00394-015-1124-6
   PubMed Web of Science ®Google Scholar
• Gonzalez, A. M., Spitz, R. W., Ghigiarelli, J. J., Sell, K. M., & Mangine, G. T. (2018). Acute effect of citrulline malate supplementation on upper-body resistance exercise performance in recreationally resistance-trained men. Journal of Strength and Conditioning Research / National Strength & Conditioning Association, 32(11), 3088–3094. https://doi.org/10.1519/JSC.0000000000002373
   PubMed Web of Science ®Google Scholar
• Goubel, F., Vanhoutte, C., Allaf, O., Verleye, M., & Gillardin, J. M. (1997). Citrulline malate limits increase in muscle fatigue induced by bacterial endotoxins. Canadian Journal of Physiology and Pharmacology, 75(3), 205–207. https://doi.org/10.1139/Y97-029
   PubMed Web of Science ®Google Scholar
• Gyulai, L., Roth, Z., Leigh, J. S., Jr., & Chance, B. (1985). Bioenergetic studies of mitochondrial oxidative phosphorylation using 31phosphorus NMR. The Journal of Biological Chemistry, 260(7), 3947–3954. https://doi.org/10.1016/S0021-9258(18)89214-6
   PubMed Web of Science ®Google Scholar
• Hochachka, P. W., & Mommsen, T. P. (1983). Protons and anaerobiosis. Science, 219(4591), 1391–1397. https://doi.org/10.1126/science.6298937
   PubMed Web of Science ®Google Scholar
• Juel, C. (1998). Muscle pH regulation: Role of training. Acta Physiologica Scandinavica, 162(3), 359–366. https://doi.org/10.1046/j.1365-201X.1998.0305f.x
   PubMedGoogle Scholar
• Kemp, G. J., Ahmad, R. E., Nicolay, K., & Prompers, J. J. (2015). Quantification of skeletal muscle mitochondrial function by 31P magnetic resonance spectroscopy techniques: A quantitative review. Acta Physiol (Oxf), 213(1), 107–144. https://doi.org/10.1111/apha.12307
   PubMed Web of Science ®Google Scholar
• Kemp, G. J., & Radda, G. K. (1994). Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: An analytical review. Magnetic Resonance Quarterly, 10(1), 43–63.
   PubMedGoogle Scholar
• Kemp, G. J., Taylor, D. J., & Radda, G. K. (1993). Control of phosphocreatine resynthesis during recovery from exercise in human skeletal muscle. NMR in Biomedicine, 6(1), 66–72. https://doi.org/10.1002/nbm.1940060111
   PubMed Web of Science ®Google Scholar
• Kemp, G. J., Thompson, C. H., Sanderson, A. L., & Radda, G. K. (1994). pH control in rat skeletal muscle during exercise, recovery from exercise, and acute respiratory acidosis. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine, 31(2), 103–109. https://doi.org/10.1002/mrm.1910310203
   PubMed Web of Science ®Google Scholar
• Komi, P. V., & Viitasalo, J. T. (1977). Changes in motor unit activity and metabolism in human skeletal muscle during and after repeated eccentric and concentric contractions. Acta Physiologica Scandinavica, 100(2), 246–254. https://doi.org/10.1111/j.1748-1716.1977.tb05943.x
   PubMedGoogle Scholar
• Korzeniewski, B., & Zoladz, J. A. (2004). Factors determining the oxygen consumption rate (VO2) on-kinetics in skeletal muscles. The Biochemical Journal, 379(3), 703–710. https://doi.org/10.1042/bj20031740
   PubMedGoogle Scholar
• Lauretani, F., Russo, C. R., Bandinelli, S., Bartali, B., Cavazzini, C., Di Iorio, A., Corsi, A. M., Rantanen, T., Guralnik, J. M., & Ferrucci, L. Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia. (2003). Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology, 95(5), 1851–1860. 1985. https://doi.org/10.1152/japplphysiol.00246.2003
   PubMed Web of Science ®Google Scholar
• Mainwood, G. W., & Renaud, J. M. (1985). The effect of acid-base balance on fatigue of skeletal muscle. Canadian Journal of Physiology and Pharmacology, 63(5), 403–416. https://doi.org/10.1139/y85-072
   PubMed Web of Science ®Google Scholar
• Meyer, R. A., Sweeney, H. L., & Kushmerick, M. J. (1984). A simple analysis of the “phosphocreatine shuttle”. The American Journal of Physiology, 246(5), C365–377. https://doi.org/10.1152/ajpcell.1984.246.5.C365
   PubMedGoogle Scholar
• Murray, B., & Rosenbloom, C. (2018). Fundamentals of glycogen metabolism for coaches and athletes. Nutrition Reviews, 76(4), 243–259. https://doi.org/10.1093/nutrit/nuy001
   PubMed Web of Science ®Google Scholar
• Newsholme, E. A., & Leech, A. R. (1983). Biochemistry for the medical sciences. John Wiley.
   Google Scholar
• Perez-Guisado, J., & Jakeman, P. M. (2010). Citrulline malate enhances athletic anaerobic performance and relieves muscle soreness. Journal of Strength and Conditioning Research, 24(5), 1215–1222. https://doi.org/10.1519/JSC.0b013e3181cb28e0
   PubMed Web of Science ®Google Scholar
• Roth, K., & Weiner, M. W. (1991). Determination of cytosolic ADP and AMP concentrations and the free energy of ATP hydrolysis in human muscle and brain tissues with 31P NMR spectroscopy. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine, 22(2), 505–511. https://doi.org/10.1002/mrm.1910220258
   PubMed Web of Science ®Google Scholar
• Sahlin, K., Tonkonogi, M., & Soderlund, K. (1998). Energy supply and muscle fatigue in humans. Acta Physiologica Scandinavica, 162(3), 261–266. https://doi.org/10.1046/j.1365-201X.1998.0298f.x
   PubMedGoogle Scholar
• Tevald, M. A., Foulis, S. A., Lanza, I. R., & Kent-Braun, J. A. (2010). Lower energy cost of skeletal muscle contractions in older humans. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 298(3), R729–739. https://doi.org/10.1152/ajpregu.00713.2009
   PubMed Web of Science ®Google Scholar
• Tousoulis, D., Kampoli, A. M., Tentolouris, C., Papageorgiou, N., & Stefanadis, C. (2012). The role of nitric oxide on endothelial function. Current Vascular Pharmacology, 10(1), 4–18. https://doi.org/10.2174/157016112798829760
   PubMed Web of Science ®Google Scholar
• Vanhamme, L., van den Boogaart, A., & Van Huffel, S. (1997). Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. Journal of Magnetic Resonance (San Diego, Calif.: 1997), 129(1), 35–43. https://doi.org/10.1006/jmre.1997.1244
   PubMed Web of Science ®Google Scholar
• Verleye, M., Heulard, I., Stephens, J. R., Levy, R. H., & Gillardin, J. M. (1995). Effects of citrulline malate on bacterial lipopolysaccharide induced endotoxemia in rats. Arzneimittelforschung, 45(6), 712–715.
   PubMed Web of Science ®Google Scholar
• Wagenmakers, A. J. (1998). 11 muscle amino acid metabolism at rest and during exercise. Exercise and Sport Sciences Reviews, 26(1) , 287–314. https://doi.org/10.1249/00003677-199800260-00013
   PubMedGoogle Scholar
• Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., & Eppenberger, H. M. (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: The ‘phosphocreatine circuit’ for cellular energy homeostasis. The Biochemical Journal, 281(1), 21–40. https://doi.org/10.1042/bj2810021
   PubMedGoogle Scholar
• Wax, B., Kavazis, A. N., & Luckett, W. (2016). Effects of supplemental citrulline-malate ingestion on blood lactate, cardiovascular dynamics, and resistance exercise performance in trained males. Journal of Dietary Supplements, 13(3), 269–282. https://doi.org/10.3109/19390211.2015.1008615
   PubMedGoogle Scholar
• Wax, B., Kavazis, A. N., Weldon, K., & Sperlak, J. (2015). Effects of supplemental citrulline malate ingestion during repeated bouts of lower-body exercise in advanced weightlifters. Journal of Strength and Conditioning Research / National Strength & Conditioning Association, 29(3), 786–792. https://doi.org/10.1519/JSC.0000000000000670
   PubMed Web of Science ®Google Scholar
• Willcocks, R. J., Williams, C. A., Barker, A. R., Fulford, J., & Armstrong, N. (2010). Age- and sex-related differences in muscle phosphocreatine and oxygenation kinetics during high-intensity exercise in adolescents and adults. NMR in Biomedicine, 23(6), 569–577. https://doi.org/10.1002/nbm.1495
   PubMed Web of Science ®Google Scholar
• Young, M. E., Radda, G. K., & Leighton, B. (1997). Nitric oxide stimulates glucose transport and metabolism in rat skeletal muscle in vitro. The Biochemical Journal, 322(1), 223–228. https://doi.org/10.1042/bj3220223
   PubMedGoogle Scholar