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Int J Sports Med 2014; 35(13): 1072-1077
DOI: 10.1055/s-0034-1371834
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Influence of Acute Exercise on the Osmotic Stability of the Human Erythrocyte Membrane

L. F. Paraiso
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
M. V. de Freitas
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
A. F. M. Gonçalves-e-Oliveira
2   Faculty of Medicine, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
O.P. de Almeida Neto
2   Faculty of Medicine, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
E. A. Pereira
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
R. C. Mascarenhas Netto
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
L. M. Cunha
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
M. Bernardino Neto
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
G. G. de Agostini
3   Faculty of Physical Education, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
E. S. Resende
3   Faculty of Physical Education, Federal University of Uberlândia, Uberlândia, MG, Brazil
,
N. Penha-Silva
1   Institute of Genetics and Biochemisty, Federal University of Uberlândia, Uberlândia, MG, Brazil
› Author Affiliations
Further Information

Publication History



accepted after revision 04 February 2014

Publication Date:
21 August 2014 (online)

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Abstract

This study evaluated the effects of 2 different types of acute aerobic exercise on the osmotic stability of human erythrocyte membrane and on different hematological and biochemical variables that are associated with this membrane property. The study population consisted of 20 healthy and active men. Participants performed single sessions of 2 types of exercise. The first session consisted of 60 min of moderate-intensity continuous exercise (MICE). The second session, executed a week later, consisted of high-intensity interval exercise (HIIE) until exhaustion. The osmotic stability of the erythrocyte membrane was represented by the inverse of the salt concentration (1/H50) at the midpoint of the sigmoidal curve of dependence between the absorbance of hemoglobin and the NaCl concentration. The values of 1/H50 changed from 2.29±0.1 to 2.33±0.09 after MICE and from 2.30±0.08 to 2.23±0.12 after HIIE. During MICE mean corpuscular volume increased, probably due to in vivo lysis of older erythrocytes, with preservation of cells that were larger and more resistant to in vitro lysis. The study showed that a single bout of acute exercise affected erythrocyte stability, which increased after MICE and decreased after HIIE.

Key words

acute exercise - erythrocyte - membrane - hemolysis - osmotic stability
 

  • References

  • 1 Alessio HM. Exercise-induced oxidative stress. Med Sci Sports Exerc 1993; 25: 218-224
    PubMedSearch in Google Scholar
  • 2 An WS, Lee SM, Son YK, Kim SE, Kim KH, Han JY, Bae HR, Park Y. Effect of omega-3 fatty acids on the modification of erythrocyte membrane fatty acid content including oleic acid in peritoneal dialysis patients. Prostaglandins Leukot Essent Fatty Acids 2012; 86: 29-34
    CrossrefPubMedSearch in Google Scholar
  • 3 Austin AW, Patterson SM, von Kanel R. Hemoconcentration and hemostasis during acute stress: interacting and independent effects. Ann Behav Med 2011; 42: 153-173
    CrossrefPubMedSearch in Google Scholar
  • 4 Baird MF, Graham SM, Baker JS, Bickerstaff GF. Creatine-kinase- and exercise-related muscle damage implications for muscle performance and recovery. J Nutr Metab 2012; 2012: 960363
    PubMed
  • 5 Berlin E, Bhathena SJ, Judd JT, Nair PP, Peters RC, Bhagavan HN, Ballardbarbash R, Taylor PR. Effects of omega-3-fatty-acid and vitamin-e supplementation on erythrocyte-membrane fluidity, tocopherols, insulin binding, and lipid-composition in adult men. J Nutr Biochem 1992; 3: 392-400
    CrossrefPubMedSearch in Google Scholar
  • 6 Berthon P, Fellmann N, Bedu M, Beaune B, Dabonneville M, Coudert J, Chamoux A. A 5-min running field test as a measurement of maximal aerobic velocity. Eur J Appl Physiol 1997; 75: 233-238
    CrossrefPubMedSearch in Google Scholar
  • 7 Berzosa C, Gomez-Trullen EM, Piedrafita E, Cebrian I, Martinez-Ballarin E, Miana-Mena FJ, Fuentes-Broto L, Garcia JJ. Erythrocyte membrane fluidity and indices of plasmatic oxidative damage after acute physical exercise in humans. Eur J Appl Physiol 2011; 111: 1127-1133
    CrossrefPubMedSearch in Google Scholar
  • 8 Brancaccio P, Maffulli N, Buonauro R, Limongelli FM. Serum enzyme monitoring in sports medicine. Clin Sports Med 2008; 27: 1-18
    CrossrefPubMedSearch in Google Scholar
  • 9 Brancaccio P, Maffulli N, Limongelli FM. Creatine kinase monitoring in sport medicine. Br Med Bull 2007; 81-82: 209-230
    CrossrefPubMedSearch in Google Scholar
  • 10 Brites FD, Evelson PA, Christiansen MG, Nicol MF, Basilico MJ, Wikinski RW, Llesuy SF. Soccer players under regular training show oxidative stress but an improved plasma antioxidant status. Clin Sci (Lond) 1999; 96: 381-385
    CrossrefPubMedSearch in Google Scholar
  • 11 Brun JF. Exercise hemorheology as a three acts play with metabolic actors: Is it of clinical relevance?. Clin Hemorheol Microcirc 2002; 26: 155-174
    PubMedSearch in Google Scholar
  • 12 Brun JF, Connes P, Varlet-Marie E. Alterations of blood rheology during and after exercise are both consequences and modifiers of body’s adaptation to muscular activity. Science & Sports 2007; 22: 251-266
    CrossrefPubMedSearch in Google Scholar
  • 13 Brun JF, Khaled S, Raynaud E, Bouix D, Micallef JP, Orsetti A. The triphasic effects of exercise on blood rheology: which relevance to physiology and pathophysiology?. Clin Hemorheol Microcirc 1998; 19: 89-104
    PubMedSearch in Google Scholar
  • 14 Brzeszczynska J, Pieniazek A, Gwozdzinski L, Gwozdzinski K, Jegier A. Structural alterations of erythrocyte membrane components induced by exhaustive exercise. Appl Physiol Nutr Metab 2008; 33: 1223-1231
    CrossrefPubMedSearch in Google Scholar
  • 15 Cartwright IJ, Pockley AG, Galloway JH, Greaves M, Preston FE. The effects of dietary omega-3 polyunsaturated fatty acids on erythrocyte membrane phospholipids, erythrocyte deformability and blood viscosity in healthy volunteers. Atherosclerosis 1985; 55: 267-281
    CrossrefPubMedSearch in Google Scholar
  • 16 Cazzola R, Russo-Volpe S, Cervato G, Cestaro B. Biochemical assessments of oxidative stress, erythrocyte membrane fluidity and antioxidant status in professional soccer players and sedentary controls. Eur J Clin Invest 2003; 33: 924-930
    CrossrefPubMedSearch in Google Scholar
  • 17 Cunha CC, Arvelos LR, Costa JO, Penha-Silva N. Effects of glycerol on the thermal dependence of the stability of human erythrocytes. J Bioenerg Biomembr 2007; 39: 341-347
    CrossrefPubMedSearch in Google Scholar
  • 18 de Arvelos LR, Rocha VC, Felix GP, da Cunha CC, Bernardino Neto M, da Silva Garrote Filho M, de Fatima Pinheiro C, Resende ES, Penha-Silva N. Bivariate and multivariate analyses of the influence of blood variables of patients submitted to Roux-en-Y gastric bypass on the stability of erythrocyte membrane against the chaotropic action of ethanol. J Membr Biol 2013; 246: 231-242
    CrossrefPubMedSearch in Google Scholar
  • 19 de Freitas MV, de Oliveira MR, dos Santos DF, de Cassia Mascarenhas Netto R, Fenelon SB, Penha-Silva N. Influence of the use of statin on the stability of erythrocyte membranes in multiple sclerosis. J Membr Biol 2010; 233: 127-134
    CrossrefPubMedSearch in Google Scholar
  • 20 de Freitas MV, Netto Rde C, da Costa Huss JC, de Souza TM, Costa JO, Firmino CB, Penha-Silva N. Influence of aqueous crude extracts of medicinal plants on the osmotic stability of human erythrocytes. Toxicol In Vitro 2008; 22: 219-224
    CrossrefPubMedSearch in Google Scholar
  • 21 De Moffarts B, Portier K, Kirschvink N, Coudert J, Fellmann N, van Erck E, Letellier C, Motta C, Pincemail J, Art T, Lekeux P. Effects of exercise and oral antioxidant supplementation enriched in (n-3) fatty acids on blood oxidant markers and erythrocyte membrane fluidity in horses. Vet J 2007; 174: 113-121
    CrossrefPubMedSearch in Google Scholar
  • 22 Derby MC, Gleeson PA. New insights into membrane trafficking and protein sorting. Int Rev Cytol 2007; 261: 47-116
    PubMedSearch in Google Scholar
  • 23 Finaud J, Lac G, Filaire E. Oxidative stress: relationship with exercise and training. Sports Med 2006; 36: 327-358
    CrossrefPubMedSearch in Google Scholar
  • 24 Fonseca LC, Arvelos LR, Netto RC, Lins AB, Garrote-Filho MS, Penha-Silva N. Influence of the albumin concentration and temperature on the lysis of human erythrocytes by sodium dodecyl sulfate. J Bioenerg Biomembr 2010; 42: 413-418
    CrossrefPubMedSearch in Google Scholar
  • 25 Garcia JJ, Martinez-Ballarin E, Millan-Plano S, Allue JL, Albendea C, Fuentes L, Escanero JF. Effects of trace elements on membrane fluidity. J Trace Elem Med Biol 2005; 19: 19-22
    CrossrefPubMedSearch in Google Scholar
  • 26 Garcia JJ, Reiter RJ, Guerrero JM, Escames G, Yu BP, Oh CS, Munoz-Hoyos A. Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett 1997; 408: 297-300
    CrossrefPubMedSearch in Google Scholar
  • 27 Gonsette RE. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J Neurol Sci 2008; 274: 48-53
    CrossrefPubMedSearch in Google Scholar
  • 28 Harriss DJ, Atkinson G. Ethical Standards in Sport and Exercise Science Research: 2014 Update. Int J Sports Med. 2013 34. 1025-1028
    PubMedSearch in Google Scholar
  • 29 Hensley K, Robinson KA, Gabbita SP, Salsman S, Floyd RA. Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med 2000; 28: 1456-1462
    CrossrefPubMedSearch in Google Scholar
  • 30 Kamada T, Tokuda S, Aozaki S, Otsuji S. Higher levels of erythrocyte membrane fluidity in sprinters and long-distance runners. J Appl Physiol 1993; 74: 354-358
    PubMedSearch in Google Scholar
  • 31 Kato GJ, McGowan V, Machado RF, Little JA, Taylor Jt, Morris CR, Nichols JS, Wang X, Poljakovic M, Morris SMJ, Gladwin MT. Lactate dehydrogenase as a biomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood 2006; 107: 2279-2285
    CrossrefPubMedSearch in Google Scholar
  • 32 Lemos GSD, Marquez-Bernardes LF, Arvelos LR, Paraíso LF, Penha-Silva N. Influence of glucose concentration on the membrane stability of human erythrocytes. Cell Biochem Biophys 2011; 61: 531-537
    CrossrefPubMedSearch in Google Scholar
  • 33 Li JX, Tong CW, Xu DQ, Chan KM. Changes in membrane fluidity and lipid peroxidation of skeletal muscle mitochondria after exhausting exercise in rats. Eur J Appl Physiol 1999; 80: 113-117
    CrossrefPubMedSearch in Google Scholar
  • 34 Marks PA, Johnson AB. Relationship between the age of human erythrocytes and their osmotic resistance – basis for separating young and old erythrocytes. J Clin Invest 1958; 37: 1542-1548
    CrossrefPubMedSearch in Google Scholar
  • 35 Myhre E, Rasmussen K. Serum-lactic-dehydrogenase activity and intravascular haemolysis. Lancet 1970; 1: 355
    PubMedSearch in Google Scholar
  • 36 Myhre E, Rasmussen K, Andersen A. Serum lactic dehydrogenase activity in patients with prosthetic heart valves: a parameter of intravascular hemolysis. Am Heart J 1970; 80: 463-468
    CrossrefPubMedSearch in Google Scholar
  • 37 Penha-Silva N, Arvelos LR, Cunha CC, Aversi-Ferreira TA, Gouvea-e-Silva LF, Garrote-Filho MS, Finotti CJ, Bernardino-Neto M, de Freitas Reis FG. Effects of glycerol and sorbitol on the thermal dependence of the lysis of human erythrocytes by ethanol. Bioelectrochemistry 2008; 73: 23-29
    CrossrefPubMedSearch in Google Scholar
  • 38 Penha-Silva N, Firmino CB, Reis FGD, Huss JCD, de Souza TMT, de Freitas MV, Netto RDM. Influence of age on the stability of human erythrocyte membranes. Mech Ageing Dev 2007; 128: 444-449
    CrossrefPubMedSearch in Google Scholar
  • 39 Radak Z, Kaneko T, Tahara S, Nakamoto H, Ohno H, Sasvari M, Nyakas C, Goto S. The effect of exercise training on oxidative damage of lipids, proteins, and DNA in rat skeletal muscle: evidence for beneficial outcomes. Free Radic Biol Med 1999; 27: 69-74
    CrossrefPubMedSearch in Google Scholar
  • 40 Santos-Silva A, Rebelo MI, Castro EM, Belo L, Guerra A, Rego C, Quintanilha A. Leukocyte activation, erythrocyte damage, lipid profile and oxidative stress imposed by high competition physical exercise in adolescents. Clin Chim Acta 2001; 306: 119-126
    CrossrefPubMedSearch in Google Scholar
  • 41 Schmidt W, Maassen N, Trost F, Boning D. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur J Appl Physiol 1988; 57: 490-498
    CrossrefPubMedSearch in Google Scholar
  • 42 Senturk UK, Gunduz F, Kuru O, Kocer G, Ozkaya YG, Yesilkaya A, Bor-Kucukatay M, Uyuklu M, Yalcin O, Baskurt OK. Exercise-induced oxidative stress leads hemolysis in sedentary but not trained humans. J Appl Physiol 2005; 99: 1434-1441
    CrossrefPubMedSearch in Google Scholar
  • 43 Sinensky M. Homeoviscous adaptation – A homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 1974; 71: 522-525
    CrossrefPubMedSearch in Google Scholar
  • 44 Soffler C. Oxidative stress. Vet Clin North Am Equine Pract 2007; 23: 135-157
    CrossrefPubMedSearch in Google Scholar
  • 45 Spodaryk K, Berger L, Hauke S. Influences of physical training on the functional changes of young and old red blood cells. Mech Ageing Dev 1990; 55: 199-206
    CrossrefPubMedSearch in Google Scholar
  • 46 Steck TL. Organization of proteins in human red blood-cell membrane – review. J Cell Biol 1974; 62: 1-19
    CrossrefPubMedSearch in Google Scholar
  • 47 Stubbs CD, Smith AD. The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 1984; 779: 89-137
    CrossrefPubMedSearch in Google Scholar
  • 48 Tavazzi B, Di Pierro D, Amorini AM, Fazzina G, Tuttobene M, Giardina B, Lazzarino G. Energy metabolism and lipid peroxidation of human erythrocytes as a function of increased oxidative stress. Eur J Biochem 2000; 267: 684-689
    CrossrefPubMedSearch in Google Scholar
  • 49 Telford RD, Sly GJ, Hahn AG, Cunningham RB, Bryant C, Smith JA. Footstrike is the major cause of hemolysis during running. J Appl Physiol 2003; 94: 38-42
    CrossrefPubMedSearch in Google Scholar
  • 50 Tsuda K, Yoshikawa A, Kimura K, Nishio I. Effects of mild aerobic physical exercise on membrane fluidity of erythrocytes in essential hypertension. Clin Exp Pharmacol Physiol 2003; 30: 382-386
    CrossrefPubMedSearch in Google Scholar
  • 51 Yalcin O, Erman A, Muratli S, Bor-Kucukatay M, Baskurt OK. Time course of hemorheological alterations after heavy anaerobic exercise in untrained human subjects. J Appl Physiol 2003; 94: 997-1002
    CrossrefPubMedSearch in Google Scholar
  • 52 Yatvin MB. The influence of membrane lipid composition and procaine on hyperthermic death of cells. Int J Radiat Biol 1977; 32: 513-521
    CrossrefPubMedSearch in Google Scholar