Uremic myopathy: is oxidative stress implicated in muscle dysfunction in uremia?

Antonia Kaltsatou, Giorgos K Sakkas, Konstantina P Poulianiti, Yiannis Koutedakis, Konstantinos Tepetes, Grigorios Christodoulidis, Ioannis Stefanidis, Christina Karatzaferi, Antonia Kaltsatou, Giorgos K Sakkas, Konstantina P Poulianiti, Yiannis Koutedakis, Konstantinos Tepetes, Grigorios Christodoulidis, Ioannis Stefanidis, Christina Karatzaferi

Abstract

Renal failure is accompanied by progressive muscle weakness and premature fatigue, in part linked to hypokinesis and in part to uremic toxicity. These changes are associated with various detrimental biochemical and morphological alterations. All of these pathological parameters are collectively termed uremic myopathy. Various interventions while helpful can't fully remedy the pathological phenotype. Complex mechanisms that stimulate muscle dysfunction in uremia have been proposed, and oxidative stress could be implicated. Skeletal muscles continuously produce reactive oxygen species (ROS) and reactive nitrogen species (RNS) at rest and more so during contraction. The aim of this mini review is to provide an update on recent advances in our understanding of how ROS and RNS generation might contribute to muscle dysfunction in uremia. Thus, a systematic review was conducted searching PubMed and Scopus by using the Cochrane and PRISMA guidelines. While few studies met our criteria their findings are discussed making reference to other available literature data. Oxidative stress can direct muscle cells into a catabolic state and chronic exposure to it leads to wasting. Moreover, redox disturbances can significantly affect force production per se. We conclude that oxidative stress can be in part responsible for some aspects of uremic myopathy. Further research is needed to discern clear mechanisms and to help efforts to counteract muscle weakness and exercise intolerance in uremic patients.

Keywords: muscle dysfunction; muscle weakness; oxidative stress; premature fatigue; uremia; uremic myopathy.

Figures

Figure 1
Figure 1
The multifactorial nature of uremic myopathy. Many specific disease-related but also lifestyle factors (e.g., physical inactivity) contribute to the pathological muscle state. Exactly when one factor reaches critical importance cannot be surmised so far. The results of this systematic mini review do point to oxidative stress as a contributor to the development of uremic myopathy. MDA, malondialdehyde; PC, protein carbonyls.

References

    1. Allen D. G., Lamb G. D., Westerblad H. (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol. Rev. 88, 287–332. 10.1152/physrev.00015.2007
    1. Anderson E. J., Neufer P. D. (2006). Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. Am. J. Physiol. Cell Physiol. 290, C844–C851. 10.1152/ajpcell.00402.2005
    1. Bhattacharya A., Muller F. L., Liu Y., Sabia M., Liang H., Song W., et al. . (2009). Denervation induces cytosolic phospholipase A2-mediated fatty acid hydroperoxide generation by muscle mitochondria. J. Biol. Chem. 284, 46–55. 10.1074/jbc.M806311200
    1. Campistol J. M. (2002). Uremic myopathy. Kidney Int. 62, 1901–1913. 10.1046/j.1523-1755.2002.00614.x
    1. Carrero J. J., Chmielewski M., Axelsson J., Snaedal S., Heimburger O., Barany P., et al. . (2008). Muscle atrophy, inflammation and clinical outcome in incident and prevalent dialysis patients. Clin. Nutr. 27, 557–564. 10.1016/j.clnu.2008.04.007
    1. Chen X., Mori T., Guo Q., Hu C., Ohsaki Y., Yoneki Y., et al. . (2013). Carbonyl stress induces hypertension and cardio-renal vascular injury in Dahl salt-sensitive rats. Hypertens. Res. 36, 361–367. 10.1038/hr.2012.204
    1. Cheung W. W., Paik K. H., Mak R. H. (2010). Inflammation and cachexia in chronic kidney disease. Pediatr. Nephrol. 25, 711–724. 10.1007/s00467-009-1427-z
    1. Clyne N., Ekholm J., Jogestrand T., Lins L. E., Pehrsson S. K. (1991). Effects of exercise training in predialytic uremic patients. Nephron 59, 84–89. 10.1159/000186524
    1. Clyne N., Jogestrand T., Lins L. E., Pehrsson S. K. (1994). Progressive decline in renal function induces a gradual decrease in total hemoglobin and exercise capacity. Nephron 67, 322–326. 10.1159/000187987
    1. Clyne N., Jogestrand T., Lins L. E., Pehrsson S. K., Ekelund L. G. (1987). Factors limiting physical working capacity in predialytic uraemic patients. Acta Med. Scand. 222, 183–190. 10.1111/j.0954-6820.1987.tb10657.x
    1. Crowe A. V., McArdle A., McArdle F., Pattwell D. M., Bell G. M., Kemp G. J., et al. . (2007). Markers of oxidative stress in the skeletal muscle of patients on haemodialysis. Nephrol. Dial. Transplant. 22, 1177–1183. 10.1093/ndt/gfl721
    1. Davies K. J., Quintanilha A. T., Brooks G. A., Packer L. (1982). Free radicals and tissue damage produced by exercise. Biochem. Biophys. Res. Commun. 107, 1198–1205. 10.1016/S0006-291X(82)80124-1
    1. Filiopoulos V., Hadjiyannakos D., Takouli L., Metaxaki P., Sideris V., Vlassopoulos D. (2009). Inflammation and oxidative stress in end-stage renal disease patients treated with hemodialysis or peritoneal dialysis. Int. J. Artif. Organs 32, 872–882.
    1. Giannaki C. D., Stefanidis I., Karatzaferi C., Liakos N., Roka V., Ntente I., et al. . (2011). The effect of prolonged intradialytic exercise in hemodialysis efficiency indices. ASAIO J. 57, 213–218. 10.1097/MAT.0b013e318215dc9e
    1. Gordon P. L., Sakkas G. K., Doyle J. W., Shubert T., Johansen K. L. (2007). Relationship between vitamin D and muscle size and strength in patients on hemodialysis. J. Ren. Nutr. 17, 397–407. 10.1053/j.jrn.2007.06.001
    1. Gouspillou G., Bourdel-Marchasson I., Rouland R., Calmettes G., Biran M., Deschodt-Arsac V., et al. . (2014). Mitochondrial energetics is impaired in vivo in aged skeletal muscle. Aging Cell 13, 39–48. 10.1111/acel.12147
    1. Grams M. E., Chow E. K. H., Segev D. L., Coresh J. (2013). Lifetime Incidence of CKD Stages 3-5 in the United States. Am. J. Kidney Dis. 62, 245–252. 10.1053/j.ajkd.2013.03.009
    1. Griffiths R. D. (1996). Muscle mass, survival, and the elderly ICU patient. Nutrition 12, 456–458. 10.1016/S0899-9007(96)00141-4
    1. Hu W. T., Shelnutt M., Wilson A., Yarab N., Kelly C., Grossman M., et al. . (2013). Behavior Matters-Cognitive Predictors of Survival in Amyotrophic Lateral Sclerosis. PLoS ONE 8:e57584. 10.1371/journal.pone.0057584
    1. Ikizler T. A., Pupim L. B., Brouillette J. R., Levenhagen D. K., Farmer K., Hakim R. M., et al. . (2002). Hemodialysis stimulates muscle and whole body protein loss and alters substrate oxidation. Am. J. Physiol. Endocrinol. Metab. 282, E107–E116.
    1. Jackson M. J. (2009). Redox regulation of adaptive responses in skeletal muscle to contractile activity. Free Radic. Biol. Med. 47, 1267–1275. 10.1016/j.freeradbiomed.2009.09.005
    1. Johansen K. L., Doyle J., Sakkas G. K., Kent-Braun J. A. (2005). Neural and metabolic mechanisms of excessive muscle fatigue in maintenance hemodialysis patients. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R805–R813. 10.1152/ajpregu.00187.2005
    1. Johansen K. L., Painter P. L., Sakkas G. K., Gordon P., Doyle J., Shubert T. (2006). Effects of resistance exercise training and nandrolone decanoate on body composition and muscle function among patients who receive hemodialysis: a randomized, controlled trial. J. Am. Soc. Nephrol. 17, 2307–2314. 10.1681/ASN.2006010034
    1. Johansen K. L., Shubert T., Doyle J., Soher B., Sakkas G. K., Kent-Braun J. A. (2003). Muscle atrophy in patients receiving hemodialysis: effects on muscle strength, muscle quality, and physical function. Kidney Int. 63, 291–297. 10.1046/j.1523-1755.2003.00704.x
    1. Kaysen G. A., Dubin J. A., Muller H. G., Rosales L., Levin N. W., Mitch W. E. (2004). Inflammation and reduced albumin synthesis associated with stable decline in serum albumin in hemodialysis patients. Kidney Int. 65, 1408–1415. 10.1111/j.1523-1755.2004.00520.x
    1. Klein J. C., Moen R. J., Smith E. A., Titus M. A., Thomas D. D. (2011). Structural and functional impact of site-directed methionine oxidation in myosin. Biochemistry 50, 10318–10327. 10.1021/bi201279u
    1. Kouidi E., Albani M., Natsis K., Megalopoulos A., Gigis P., Guiba-Tziampiri O., et al. . (1998). The effects of exercise training on muscle atrophy in haemodialysis patients. Nephrol. Dial. Transplant. 13, 685–699. 10.1093/ndt/13.3.685
    1. Laganiere S., Yu B. P. (1993). Modulation of membrane phospholipid fatty acid composition by age and food restriction. Gerontology 39, 7–18. 10.1159/000213509
    1. Lamb G. D., Westerblad H. (2011). Acute effects of reactive oxygen and nitrogen species on the contractile function of skeletal muscle. J. Physiol. 589, 2119–2127. 10.1113/jphysiol.2010.199059
    1. Lim P. S., Cheng Y. M., Wei Y. H. (2000). Large-scale mitochondrial DNA deletions in skeletal muscle of patients with end-stage renal disease. Free Radic. Biol. Med. 29, 454–463. 10.1016/S0891-5849(00)00334-8
    1. Lim P. S., Cheng Y. M., Wei Y. H. (2002a). Increase in oxidative damage to lipids and proteins in skeletal muscle of uremic patients. Free Radic. Res. 36, 295–301. 10.1080/10715760290019318
    1. Lim P. S., Ma Y. S., Cheng Y. M., Chai H., Lee C. F., Chen T. L., et al. . (2002b). Mitochondrial DNA mutations and oxidative damage in skeletal muscle of patients with chronic uremia. J. Biomed. Sci. 9, 549–560. 10.1007/BF02254982
    1. Lowrie E. G., Lew N. L. (1990). Death risk in hemodialysis patients: the predictive value of commonly measured variables and an evaluation of death rate differences between facilities. Am. J. Kidney Dis. 15, 458–482. 10.1016/S0272-6386(12)70364-5
    1. McArdle A., Pattwell D., Vasilaki A., Griffiths R. D., Jackson M. J. (2001). Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am. J. Physiol. Cell Physiol. 280, C621–C627.
    1. Moylan J. S., Reid M. B. (2007). Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35, 411–429. 10.1002/mus.20743
    1. Porter M. M., Vandervoort A. A., Lexell J. (1995). Aging of human muscle: structure, function and adaptability. Scand. J. Med. Sci. Sports 5, 129–142. 10.1111/j.1600-0838.1995.tb00026.x
    1. Powers S. K., Ji L. L., Kavazis A. N., Jackson M. J. (2011). Reactive oxygen species: impact on skeletal muscle. Compr. Physiol. 1, 941–969. 10.1002/cphy.c100054
    1. Prochniewicz E., Lowe D. A., Spakowicz D. J., Higgins L., O'conor K., Thompson L. V., et al. . (2008a). Functional, structural, and chemical changes in myosin associated with hydrogen peroxide treatment of skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 294, C613–C626. 10.1152/ajpcell.00232.2007
    1. Prochniewicz E., Spakowicz D., Thomas D. D. (2008b). Changes in actin structural transitions associated with oxidative inhibition of muscle contraction. Biochemistry 47, 11811–11817. 10.1021/bi801080x
    1. Reardon T. F., Allen D. G. (2009). Time to fatigue is increased in mouse muscle at 37 degrees C; the role of iron and reactive oxygen species. J. Physiol. 587, 4705–4716. 10.1113/jphysiol.2009.173005
    1. Sakkas G. K., Ball D., Mercer T. H., Sargeant A. J., Tolfrey K., Naish P. F. (2003a). Atrophy of non-locomotor muscle in patients with end-stage renal failure. Nephrol. Dial. Transplant. 18, 2074–2081. 10.1093/ndt/gfg325
    1. Sakkas G. K., Hadjigeorgiou G. M., Karatzaferi C., Maridaki M. D., Giannaki C. D., Mertens P. R., et al. . (2008a). Intradialytic aerobic exercise training ameliorates symptoms of restless legs syndrome and improves functional capacity in patients on hemodialysis. ASAIO J. 54, 185–190. 10.1097/MAT.0b013e3181641b07
    1. Sakkas G. K., Karatzaferi C., Zintzaras E., Giannaki C. D., Liakopoulos V., Lavdas E., et al. . (2008b). Liver fat, visceral adiposity, and sleep disturbances contribute to the development of insulin resistance and glucose intolerance in nondiabetic dialysis patients. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1721–R1729. 10.1152/ajpregu.00935.2007
    1. Sakkas G. K., Liakopoulos V., Karatzaferi C., Stefanidis I. (2008c). Sleep quality and dialysis efficacy affect functional capacity in patients receiving haemodialysis therapy. Nephrol. Dial. Transplant. 23, 2703–2704. 10.1093/ndt/gfn048
    1. Sakkas G. K., Sargeant A. J., Mercer T. H., Ball D., Koufaki P., Karatzaferi C., et al. . (2003b). Changes in muscle morphology in dialysis patients after 6 months of aerobic exercise training. Nephrol. Dial. Transplant. 18, 1854–1861. 10.1093/ndt/gfg237
    1. Samouilidou E., Grapsa E. (2003). Effect of dialysis on plasma total antioxidant capacity and lipid peroxidation products in patients with end-stage renal failure. Blood Purif. 21, 209–212. 10.1159/000070691
    1. Spencer T., Posterino G. S. (2009). Sequential effects of GSNO and H2O2 on the Ca2+ sensitivity of the contractile apparatus of fast- and slow-twitch skeletal muscle fibers from the rat. Am. J. Physiol. Cell Physiol. 296, C1015–C1023. 10.1152/ajpcell.00251.2008
    1. Taes Y. E. C., Speeckaert M., Bauwens E., De Buyzere M. R., Libbrecht J., Lameire N. H., et al. . (2004). Effect of dietary creatine on skeletal muscle myosin heavy chain isoform expression in an animal model of uremia. Nephron Exp. Nephrol. 96, E103–E110. 10.1159/000077376
    1. Topp K. S., Painter P. L., Walcott S., Krasnoff J. B., Adey D., Sakkas G. K., et al. . (2003). Alterations in skeletal muscle structure are minimized with steroid withdrawal after renal transplantation. Transplantation 76, 667–673. 10.1097/01.TP.0000076096.45542.1B
    1. Varan H. I., Dursun B., Dursun E., Ozben T., Suleymanlar G. (2010). Acute effects of hemodialysis on oxidative stress parameters in chronic uremic patients: comparison of two dialysis membranes. Int. J. Nephrol. Renovasc. Dis. 3, 39–45.
    1. Wang X. H., Mitch W. E. (2013). Muscle wasting from kidney failure-a model for catabolic conditions. Int. J. Biochem. Cell Biol. 45, 2230–2238. 10.1016/j.biocel.2013.06.027
    1. Yazdi P. G., Moradi H., Yang J. Y., Wang P. H., Vaziri N. D. (2013). Skeletal muscle mitochondrial depletion and dysfunction in chronic kidney disease. Int. J. Clin. Exp. Med. 6, 532–539.
    1. Zhang L., Du J., Hu Z., Han G., Delafontaine P., Garcia G., et al. . (2009). IL-6 and serum amyloid A synergy mediates angiotensin II-induced muscle wasting. J. Am. Soc. Nephrol. 20, 604–612. 10.1681/ASN.2008060628
    1. Zhang L., Rajan V., Lin E., Hu Z., Han H. Q., Zhou X., et al. . (2011). Pharmacological inhibition of myostatin suppresses systemic inflammation and muscle atrophy in mice with chronic kidney disease. FASEB J. 25, 1653–1663. 10.1096/fj.10-176917
    1. Zhang L., Wang X. H., Wang H., Du J., Mitch W. E. (2010). Satellite cell dysfunction and impaired IGF-1 signaling cause CKD-induced muscle atrophy. J. Am. Soc. Nephrol. 21, 419–427. 10.1681/ASN.2009060571
    1. Zoccali C., Kramer A., Jager K. J. (2010). Epidemiology of CKD in Europe: an uncertain scenario. Nephrol. Dial. Transplant. 25, 1731–1733. 10.1093/ndt/gfq250

Source: PubMed

3
Abonneren