Skip to main content
SpringerLink
Log in

Erythrocyte membrane fluidity and indices of plasmatic oxidative damage after acute physical exercise in humans

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Optimal levels of membrane fluidity are essential for numerous cell functions including cell growth, solute transport and signal transduction. Since exercise enhances free radical production, our aim was to evaluate in healthy male subjects the effects of an acute bout of maximal and submaximal exercise on the erythrocyte membrane fluidity and its possible relation to the oxidative damage overproduction due to exercise. Subjects (n = 34) performed three cycloergometric tests: a continuous progressive exercise, a strenuous exercise until exhaustion and an acute bout of exercise at an intensity corresponding to 70% of maximal work capacity for 30 min. Venous blood samples were collected before and immediately after these exercises. Erythrocyte membrane fluidity was assessed by fluorescence spectroscopy. Plasma malondialdehyde (MDA) and 4-hydroxyalkenals (4-HDA) concentrations and carbonyl content of plasmatic proteins were used as an index of lipid and protein oxidation, respectively. Exercise produced a dramatic drop in the erythrocyte membrane fluidity as compared to resting time, but this was not accompanied by significant changes in the plasmatic MDA and 4-HDA concentrations. The highest erythrocyte membrane rigidity was detected immediately after strenuous exercise until exhaustion was performed. Protein carbonyl levels were higher after exhaustive exercises than at rest. Continuous progressive and strenuous exercises until exhaustion, but not submaximal workload, resulted in a significant enhanced accumulation of carbonylated proteins in the plasma. These findings are consistent with the idea that exercise exaggerates oxidative damage, which may contribute, at least partially, to explain the rigidity in the membrane of the erythrocytes due to acute exercise.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alessio HM, Hagerman AE, Fulkerson BK, Ambrose J, Rice RE, Wiley RL (2000) Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Med Sci Sports Exerc 32:1576–1581

    Article  PubMed  CAS  Google Scholar 

  • Ashton T, Rowlands CC, Jones E, Young IS, Jackson SK, Davies B, Peters JR (1998) Electron spin resonance spectroscopic detection of oxygen-centred radicals in human serum following exhaustive exercise. Eur J Appl Physiol Occup Physiol 77:498–502

    Article  PubMed  CAS  Google Scholar 

  • Asmussen E, Christensen EH, Nielsen M (1939) Die O2-Aufnahme der Ruhenden und der Arbeitenden Skelettmuskein. Skan Arch Physiol 82:212

    CAS  Google Scholar 

  • Bloomer RJ, Fisher-Wellman KH (2008) Blood oxidative stress biomarkers: influence of sex, exercise training status, and dietary intake. Gend Med 5:218–228

    Article  PubMed  Google Scholar 

  • Bloomer RJ, Falvo MJ, Fry AC, Schilling BK, Smith WA, Moore CA (2006) Oxidative stress response in trained men following repeated squats or sprints. Med Sci Sports Exerc 38:1436–1442

    Article  PubMed  CAS  Google Scholar 

  • Bloomer RJ, Davis PG, Consitt LA, Wideman L (2007) Plasma protein carbonyl response to increasing exercise duration in aerobically trained men and women. Int J Sports Med 28:21–25

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Brzeszczynska J, Pieniazek A, Gwozdzinski L, Gwozdzinski K, Jegier A (2008) Structural alterations of erythrocyte membrane components induced by exhaustive exercise. Appl Physiol Nutr Metab 33:1223–1231

    Article  PubMed  CAS  Google Scholar 

  • Caputo F, Denadai BS (2004) Effects of aerobic endurance training status and specificity on oxygen uptake kinetics during maximal exercise. Eur J Appl Physiol 93:87–95

    Article  PubMed  CAS  Google Scholar 

  • Carta P, Aru G, Barbieri MT, Mele M (1991) Bicycle ergometry exercise tests: a comparison between 3 protocols with an increasing load. Med Lav 82:56–64

    PubMed  CAS  Google Scholar 

  • Cazzola R, Russo-Volpe S, Cervato G, Cestaro B (2003) Biochemical assessments of oxidative stress, erythrocyte membrane fluidity and antioxidant status in professional soccer players and sedentary controls. Eur J Clin Invest 33:924–930

    Article  PubMed  CAS  Google Scholar 

  • Chen JJ, Yu BP (1994) Alterations in mitochondrial membrane fluidity by lipid peroxidation products. Free Radic Biol Med 17:411–418

    Article  PubMed  CAS  Google Scholar 

  • Cimen MY (2008) Free radical metabolism in human erythrocytes. Clin Chim Acta 390:1–11

    Article  PubMed  CAS  Google Scholar 

  • Curtis MT, Gilfor D, Farber JL (1984) Lipid peroxidation increases the molecular order of microsomal membranes. Arch Biochem Biophys 235:644–649

    Article  PubMed  CAS  Google Scholar 

  • Davies KJ, Goldberg AL (1987) Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes. J Biol Chem 262:8220–8226

    PubMed  CAS  Google Scholar 

  • Davies KJ, Quintanilha AT, Brooks GA, Packer L (1982) Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107:1198–1205

    Article  PubMed  CAS  Google Scholar 

  • De Moffarts B, Portier K, Kirschvink N, Coudert J, Fellmann N, van Erck E, Letellier C, Motta C, Pincemail J, Art T, Lekeux P (2007) 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 174:113–121

    Article  PubMed  Google Scholar 

  • Derby MC, Gleeson PA (2007) New insights into membrane trafficking and protein sorting. Int Rev Cytol 261:47–116

    Article  PubMed  CAS  Google Scholar 

  • Dumaswala UJ, Zhuo L, Jacobsen DW, Jain SK, Sukalski KA (1999) Protein and lipid oxidation of banked human erythrocytes: role of glutathione. Free Radic Biol Med 27:1041–1049

    Article  PubMed  CAS  Google Scholar 

  • Dutta-Roy AK, Ray TK, Sinha AK (1985) Control of erythrocyte membrane microviscosity by insulin. Biochim Biophys Acta 816:187–190

    Article  PubMed  CAS  Google Scholar 

  • Eichner ER (1985) Runner’s macrocytosis: a clue to footstrike hemolysis. Runner’s anemia as a benefit versus runner’s hemolysis as a detriment. Am J Med 78:321–325

    Article  PubMed  CAS  Google Scholar 

  • García JJ, Reiter RJ, Guerrero JM, Escames G, Yu BP, Oh CS, Muñoz-Hoyos A (1997) Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett 408:297–300

    Article  PubMed  Google Scholar 

  • Groussard C, Rannou-Bekono F, Machefer G, Chevanne M, Vincent S, Sergent O, Cillard J, Gratas-Delamarche A (2003) Changes in blood lipid peroxidation markers and antioxidants after a single sprint anaerobic exercise. Eur J Appl Physiol 89:14–20

    Article  PubMed  CAS  Google Scholar 

  • Gutteridge JM (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828

    PubMed  CAS  Google Scholar 

  • Halliwell B (1991) Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am J Med 91:14S–22S

    Article  PubMed  CAS  Google Scholar 

  • Hanahan DJ, Ekholm JE (1974) The preparation of red cell ghosts (membranes). Methods Enzymol 31:168–172

    Article  PubMed  CAS  Google Scholar 

  • Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 9:515–540

    Article  PubMed  CAS  Google Scholar 

  • Ji LL, Fu R (1992) Responses of glutathione system and antioxidant enzymes to exhaustive exercise and hydroperoxide. J Appl Physiol 72:549–554

    PubMed  CAS  Google Scholar 

  • Kamada T, Tokuda S, Aozaki S, Otsuji S (1993) Higher levels of erythrocyte membrane fluidity in sprinters and long-distance runners. J Appl Physiol 74:354–358

    PubMed  CAS  Google Scholar 

  • Kim JD, Yu BP, McCarter RJ, Lee SY, Herlihy JT (1996) Exercise and diet modulate cardiac lipid peroxidation and antioxidant defenses. Free Radic Biol Med 20:83–88

    Article  PubMed  CAS  Google Scholar 

  • Kuhry JG, Fonteneau P, Duportail G, Maechling C, Laustriat G (1983) TMA-DPH: a suitable fluorescence polarization probe for specific plasma membrane fluidity studies in intact living cells. Cell Biophys 5:129–140

    PubMed  CAS  Google Scholar 

  • Lamprecht M, Greilberger JF, Schwaberger G, Hofmann P, Oettl K (2008) Single bouts of exercise affect albumin redox state and carbonyl groups on plasma protein of trained men in a workload-dependent manner. J Appl Physiol 104:1611–1617

    Article  PubMed  Google Scholar 

  • Leaf DA, Kleinman MT, Hamilton M, Barstow TJ (1997) The effect of exercise intensity on lipid peroxidation. Med Sci Sports Exerc 29:1036–1039

    PubMed  CAS  Google Scholar 

  • Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36:1495–1502

    Article  PubMed  CAS  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  PubMed  CAS  Google Scholar 

  • Li JX, Tong CW, Xu DQ, Chan KM (1999) Changes in membrane fluidity and lipid peroxidation of skeletal muscle mitochondria after exhausting exercise in rats. Eur J Appl Physiol Occup Physiol 80:113–117

    Article  PubMed  CAS  Google Scholar 

  • Motta S, Letellier C, Ropert M, Motta C, Thiebault JJ (2009) Protecting effect of vitamin E supplementation on submaximal exercise-induced oxidative stress in sedentary dogs as assessed by erythrocyte membrane fluidity and paraoxonase-1 activity. Vet J 181:288–295

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa H, Genka C, Fujishima M (1996) Pathological aspects of active oxygens/free radicals. Jpn J Physiol 46:15–32

    Article  PubMed  CAS  Google Scholar 

  • Petibois C, Deleris G (2005) Evidence that erythrocytes are highly susceptible to exercise oxidative stress: FT-IR spectrometric studies at the molecular level. Cell Biol Int 29:709–716

    Article  PubMed  CAS  Google Scholar 

  • Pialoux V, Mounier R, Rock E, Mazur A, Schmitt L, Richalet JP, Robach P, Coudert J, Fellmann N (2009) Effects of acute hypoxic exposure on prooxidant/antioxidant balance in elite endurance athletes. Int J Sports Med 30:87–93

    Article  PubMed  CAS  Google Scholar 

  • Ponizovsky AM, Barshtein G, Bergelson LD (2003) Biochemical alterations of erythrocytes as an indicator of mental disorders: an overview. Harv Rev Psychiatry 11:317–332

    PubMed  Google Scholar 

  • Portier K, de Moffarts B, Fellman N, Kirschvink N, Motta C, Letellierw C, Ruelland A, van Erck E, Lekeux P, Couder J (2006) The effects of dietary N-3 and antioxidant supplementation on erythrocyte membrane fatty acid composition and fluidity in exercising horses. Equine Vet J Suppl: 279–284

  • Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276

    Article  PubMed  CAS  Google Scholar 

  • Prendergast FG, Haugland RP, Callahan PJ (1981) 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1, 3, 5-triene: synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers. Biochemistry 20:7333–7338

    Article  PubMed  CAS  Google Scholar 

  • Shinitzky M (1984) Membrane fluidity in malignancy. Adversative and recuperative. Biochim Biophys Acta 738:251–261

    PubMed  CAS  Google Scholar 

  • Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    Article  PubMed  CAS  Google Scholar 

  • Stubbs CD, Smith AD (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779:89–137

    PubMed  CAS  Google Scholar 

  • Sudhahar CG, Haney RM, Xue Y, Stahelin RV (2008) Cellular membranes and lipid-binding domains as attractive targets for drug development. Curr Drug Targets 9:603–613

    Article  PubMed  CAS  Google Scholar 

  • Szygula Z (1990) Erythrocytic system under the influence of physical exercise and training. Sports Med 10:181–197

    Article  PubMed  CAS  Google Scholar 

  • Tsuda K, Yoshikawa A, Kimura K, Nishio I (2003) Effects of mild aerobic physical exercise on membrane fluidity of erythrocytes in essential hypertension. Clin Exp Pharmacol Physiol 30:382–386

    Article  PubMed  CAS  Google Scholar 

  • Yu BP, Suescun EA, Yang SY (1992) Effect of age-related lipid peroxidation on membrane fluidity and phospholipase A2: modulation by dietary restriction. Mech Ageing Dev 65:17–33

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Gobierno de Aragón (Aging and Oxidative Stress Physiology, Grant No. B40) and by F.I.S. from Instituto de Salud Carlos III (Grant No. RD06/0013/1017).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Aging Physiology and Oxidative Stress (B40), Universidad de Zaragoza, Saragossa, Spain

    C. Berzosa, E. M. Gómez–Trullén, E. Piedrafita, I. Cebrián, E. Martínez–Ballarín, F. J. Miana–Mena, L. Fuentes–Broto & J. J. García

  2. Department of Pharmacology and Physiology, Faculty of Medicine, University of Zaragoza, c) Domingo Miral s/n, 50009, Saragossa, Spain

    J. J. García

Authors
  1. C. Berzosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. M. Gómez–Trullén
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Piedrafita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Cebrián
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Martínez–Ballarín
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. J. Miana–Mena
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L. Fuentes–Broto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J. J. García
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. J. García.

Additional information

Communicated by Susan Ward.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berzosa, C., Gómez–Trullén, E.M., Piedrafita, E. et al. Erythrocyte membrane fluidity and indices of plasmatic oxidative damage after acute physical exercise in humans. Eur J Appl Physiol 111, 1127–1133 (2011). https://doi.org/10.1007/s00421-010-1738-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-010-1738-6

Keywords

Search

Navigation