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Oxidative stress and sport performance.

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D’Angelo, S., et al.: Oxidative stress and sport performance Sport Science 13 (2020) Suppl 1: 18-22

OXIDATIVE STRESS AND SPORT PERFORMANCE

Stefania D’Angelo1 and Roberta Rosa2

1
Department of Movement Sciences and Wellbeing, University of Naples “Parthenope”, Naples, Italy
2
IUL Telematic University, Rome, Italy

Review paper

Abstract
During physical activity, the demand for oxygen increases, particularly in skeletal muscle, causing a drastic
change in blood flow to the various organs. In addition, exercise-induced micro muscle trauma promotes
infiltration of phagocytes (i.e. neutrophils and macrophages) at the injury site. These physiological changes
that occur during acute exercise increase the production of free radicals, inducing oxidative damage to
biomolecules. Recent molecular and biological studies have allowed the observation of events at the cellular
level and have shown, in an increasingly evident way that free radicals play a role in physiological
adjustments that take place after training. The increase in the rate of oxygen consumption during exercise
generates greater production of reactive oxygen species, in relation to incomplete reduction of the oxygen
itself. A correct physical activity program or rational muscle training generates the moderate and short-term
increase in free radicals, which can activate molecular mechanisms useful for the cell to adapt and protect
itself from states of oxidative stress: not only, but also to improve the immunological defenses of the
organism.

Key words: athletic performance, oxidative stress, ROS, physical exercise, sports.

Introduction

Both the free radical theory and oxidative stress habits, UV rays, ionizing radiation and
are of the hypotheses associated with ageing, psychophysical stress resulting from intense
suggesting that oxygen-free radicals are formed physical activity. Although the free radicals have
endogenously from normal oxygen-utilizing positive effects in immune reactions and cellular
metabolic processes and play an essential role in signaling, they are also known to have negative
this process. The ageing process is one of the main effects, such as oxidative damage of lipids, proteins
un-modifiable risk factors for life-threatening and nucleic acids (Gutteridge & Halliwell, 2000).
conditions, reducing immunity and common
diseases, including type 2 diabetes, cardiovascular Discussion
and respiratory diseases, neurodegenerative
disease, and cancer. As ageing progresses, lipid Oxidative stress
and protein oxidation and unrepaired damage to Reactive oxygen species (ROS), including free
DNA accumulated over a lifetime may cause cellular radicals, play important roles in cellular signaling,
senescence, which is postulated as a theory of being an important element of organismal
ageing. The irradiation of living things, known to homeostasis. On the other hand, ROS are
induce the formation of free radicals, shorten their implicated in the pathogenesis of many human
lifespan and produce changes that resemble diseases, and, in fact, it is not easy to find a
ageing. Involvement of free radicals in ageing has disorder without ROS in its pathogenesis. Moreover,
increased progressively and is becoming one of the ROS are directly or indirectly implicated in both
more plausible theories of the ageing process, even normal (physiological) and accelerated aging.
considering how is believed that the antioxidant Therefore, it is not surprising that ROS are reported
defense is generally weakened in old age (Galletti to play an important role in the etiology of several
et al.,2007; D’Angelo et al., 2012a; D’Angelo et al., age-related diseases (Davalli et al., 2016).
2013;Davalli et al., 2016; Ingrosso et al., 2000).
Free radicals and reactive oxygen species are the The ROS is a family of highly reactive molecules
main oxidizing agents in cellular systems, and are which includes free oxygen radicals, like superoxide
involved in aging and the onset of many types of anion (O2•−), hydroxyl radical (OH•), and non-
diseases (Ingrosso et al., 1995; Ingrosso et al., radical oxygen derivatives, like the stable hydrogen
1996; Ingrosso et al., 2002). They are peroxide (H2O2). The superoxide radicals react to
physiologically produced in different cellular form other ROS, namely, hydrogen peroxides and
biochemical reactions occurring in the body, such hydroxyl radicals, and interconvert with reactive
as in mitochondria for aerobic oxygen production, nitrogen species (RNS), which generate effects
in fatty acid metabolism, in drug metabolism and similar to ROS. The inefficient electron transfer in
during activity of the immune system. On the other mitochondrial respiratory chain is believed to be a
hand, free radicals can also be produced by main ROS source, among diverse possible
exogenous factors such as pollution, bad lifestyle enzymatic and non-enzymatic sources.

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D’Angelo, S., et al.: Oxidative stress and sport performance Sport Science 13 (2020) Suppl 1: 18-22

Increased expression of catalase and Therefore, free radicals generated by exercise are
peroxiredoxin-1 molecules are considered as considered to have both positive and negative
oxidative markers. The family comprises seven physiological effects (Malaguti et al., 2013;
trans-membrane members, namely, Nox1–5 and Mankowski et al., 2015). Exercise-induced oxidative
Duox1-2. ROS are generated by oxygen stress associated with increased free radical
metabolism (i.e., cellular respiration) in all the cells production has been studied for 40 years, since it
that utilize oxygen, as inevitable consequence of was first reported in 1978. In the study had
aerobic life, and may derive from exogenous subjects perform a 60-min cycle ergometer
metals, recycling of redox compounds, radiation, exercise at 50% VO2 max intensity, and reported
chemotherapeutic agents, carcinogens (estrogenic increased levels of expired pentane, an index of
molecules), and other dietary and environmental lipid peroxidation. Subsequently, in 1987, in a
means. Generally, the ROS increasing levels cause study on six young men, who performed an
nonlinear cellular responses. A fine balance incremental load exercise on a cycle ergometer to
between oxidant-antioxidant mechanisms leads to exhaustion, the blood levels of thiobarbituric acid
continuous modulation of ROS production, location, reactive substances, another marker of lipid
and inactivation, in both physiological and peroxidation, increased. In another study, in 1988,
pathological conditions. Endogenous antioxidants, in which eight highly trained young men performed
like the enzymes of catalase family, glutathione cycle ergometer exercise for 90 min at 65%
group, thioredoxin-related group, and superoxide VO2peak intensity, the levels of GSH, a non-
dismutase, together with exogenous antioxidant as enzymatic antioxidant, decreased, whereas the
reduced glutathione, carotenoids, and vitamins C GSSG levels conversely increased (Mankowski et al,
and E, constitute the indispensable ROS detoxifying 2015).
system. Nevertheless, imbalance of redox
homeostasis may occur, usually in favor of Because prolonged exercise results in an increased
oxidants, so that ROS shift from physiological to production of oxidants in skeletal muscle, and
potentially harmful levels, named oxidative and hence regular activation of enzymatic antioxidant-
nitrosative stress (Gutteridge & Halliwell, 2000) using mechanisms, endurance exercise training
(Figure 1). induces adaptations resulting in up-regulation of
antioxidant enzyme activity in skeletal muscle, i.e.,
superoxide dismutase (SOD1 and SOD2)GPx, and
CAT. It has been well documented that endurance
exercise training increases total SOD activity in
highly oxidative type I (the soleus) and IIa (red
gastrocnemius) skeletal muscle fibers. Longer and
more intensive endurance training promotes a
greater increase in both cytosolic and mitochondrial
GPx activity in oxidative skeletal muscle (type I and
IIa) fibers. Endurance training, also, up regulates
CAT activity in peroxisomes and mitochondria, in
highly oxidative muscles (Radak et al., 2013;
Mankowski et al., 2015) (Figure 2).

Figure 1. Antioxidants and oxidative stress.

Oxidative stress and training

There is a consensus that a single session of
exercise induces oxidative stress and that the free
radicals produced during exercise are important
modulators of muscle and systemic adaptations to
physical activity. This is based on the results of
exercise studies over the past three decades.
During exercise, oxygen demand increases, Figure 2. Physiological adaptations to endurance
particularly in skeletal muscle, causing a dramatic training.
change in the blood flow to various organs.
Furthermore, exercise-induced muscle damage Exercise-induced oxidative stress and the
promotes infiltration of phagocytes (i.e., mitochondrial biogenesis
neutrophils and macrophages) at the site of injury. ROSs stimulate the mitochondrial biogenesis
These physiological changes that occur during cascade in response to endurance exercise training,
acute exercise increase free radical production, i.e., chronic muscle contractions. The newly formed
leading to oxidative damage to biomolecules. mitochondria are known to be highly efficient and
Recent developments in biochemical and molecular produce fewer ROSs for the same amount of
biological techniques have enabled observation of produced adenosine triphosphate (ATP). Regular
events at the cellular level, and have increasingly exercise training increases expression of proteins
demonstrated that free radicals play at least some involved in mitochondrial biogenesis, i.e., PGC-1α,
role in physiological adaptations after exercise nuclear respiratory factor 1 (NRF-1), and
training. mitochondrial transcription factor A (Tfam).

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D’Angelo, S., et al.: Oxidative stress and sport performance Sport Science 13 (2020) Suppl 1: 18-22

PGC-1α is an important transcriptional co-activator Antioxidant supplementation may be an effective

of nuclear genes encoding mitochondrial proteins, strategy, considering the reactive oxygen species
whilst Tfam regulates the expression of scavenging effects that could lead to a reduction in
mitochondrial DNA. For example, expression of muscle damage caused by prolonged exercise
PGC-1α in skeletal muscle was significantly (Sies, 2015).
increased following 4 weeks of endurance exercise
training, indicating a skeletal muscle contraction- Antioxidants and training
stimulated mechanism of mitochondrial biogenesis. Undoubtedly, the harmful effects of high
Mitochondria are also one of the main sources of concentrations of ROS can include a decrease in
ROSs, which are products of oxidative lipid and muscle function, histological changes and muscle
glucose metabolism during muscle contraction. soreness, and a reduction in sports performance.
These are some of the reasons why it is
However, the mitochondria are not the only sources recommended to consume quantities of non-
of ROS during muscle contraction. For example, it enzymatic antioxidant supplements, such as
has recently been shown that muscle contraction vitamins C and E and -lipoic acid. Research has
increases superoxide activity in cytosol, with a been conducted to ascertain whether non-
delayed increase in mitochondria. It has been enzymatic antioxidant supplementation could
proposed that nicotinamide adenine dinucleotide prevent the harmful effects of ROS during exercise
phosphate-oxidase (NADPH) oxidases are the and thus improve the performance of resistance
potential sources for superoxide generation. exercises in humans. Contrary to the initial
Accordingly, ROS production (level of H2O2) was hypothesis of protection, preclinical studies and
previously shown to increase in isolated some recent human studies have shown
mitochondria after acute muscle contraction in controversial results on the blunt effect of the
comparison with rested skeletal muscle biopsy integration of non-enzymatic antioxidants on
sample (Mankowski et al, 2015). training with resistance exercises.

Skeletal muscle contractions at high intensity There is still an active debate on the effect of
increase the AMP/ATP ratio and the Ca2+ flux, thus integrating antioxidants on exercise-induced
causing up-regulation of the gene expression and oxidative stress. As for endpoints, the antioxidant
post-translational modification of PGC-1α by the could be effective in particular conditions in terms
activation of AMPK, Ca2+/calmodulin-dependent of training and training, such as a type of sport
kinase (CaMK), and calcineurin A. Co-activation of versus another (e.g. aerobic vs. anaerobic) or
PGC-1α activates nuclear respiratory factors (NRF-1 specific time of training (e.g. before or after the
and -2), which promote the expression of Tfam that race). Therefore, the selection and detailed
directly stimulates mitochondrial DNA replication description of the appropriate training stimulus
and transcription. This consequently enhances and/or monitoring of the athlete during the training
mitochondrial biogenesis, which results in greater phases is required (Kawamura & Muraoka, 2013;
oxygen consumption (Mankowski et al., 2015; Simioni et al., 2018).
Webb et al., 2017).
Several studies report the negative effects of
It has been shown that moderate ROS levels are antioxidants. One of the explanations for the
crucial for signaling pathways of mitochondrial controversy is the different population used. Most
biogenesis. Decreased expression of PGC-1α, studies that report a benefit of antioxidant
therefore, is associated with reduced ROS- supplementation in alleviating muscle damage and
stimulated mitochondrial biogenesis. oxidative stress following endurance exercise have
Supplementation with vitamin C decreased ROS included sedentary and non-resistance subjects. In
levels, preventing enzymatic antioxidant activity. trained subjects, endogenous antioxidant defenses
Moreover, some studies are in agreement with the can be excessively regulated and therefore these
statement associating blunted expression of PGC- subjects may not benefit greatly from taking
1α with decreased activity of antioxidant enzymes exogenous antioxidants in order to reduce muscle
(SOD, GPx, CAT), the primary endogenic injuries. In addition, studies on the use of
antioxidant defense system (Mankowski et al, antioxidants during exercise have used different
2015). types of exercise, ranging from long-term
resistance exercise to short-term resistance
ROS production leads to muscle fiber damage, exercise. The aerobic endurance exercise tends to
which eventually results in muscle fatigue. induce a different radical flow than the anaerobic
However, there is growing evidence suggesting that endurance exercise (Muñoz Marín et al., 2018).
the presence of a small stimulus, like low
concentration of ROS, is able to express the Therefore, efforts have been made to develop
transcription of major antioxidant genes. Enzymes dietary strategies against oxidative stress and
like SOD and glutathione are important antioxidant recently there has been a growing interest in
defenses that protect cells from ROS-induced studying the potential of polyphenols to modulate
oxidative stress. The correlation between oxidative physical performance and prevent oxidative stress
damage and muscle fatigue could be an important induced by it (Myburgh, 2014; D’Angelo &
strategy for nutritional interventions to increase Sammartino, 2015; Motti et al., 2018; D’Angelo et
exercise performance. al, 2017).

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D’Angelo, S., et al.: Oxidative stress and sport performance Sport Science 13 (2020) Suppl 1: 18-22

Recently a large number of scientific articles have Conclusion

highlighted a potential relationship between the
bioactive compounds of plant foods and oxidative Many reports confirm that exercises cause oxidative
stress and attention has been shifted to the effects stress through free radical generation and a
of nutraceutical bioactive compounds such as decrease in the levels of antioxidant enzymes in
polyphenols. In fact, human diets are rich in different tissues and organs, but different
polyphenols; Western populations consume about intensities and forms of exercise result in different
1-2 g/day of polyphenols. The most important levels of biological stress. The production of free
polyphenols food sources are fruit and vegetables, radicals increases with the increase in oxygen
green and black tea, red wine, coffee, chocolate consumption and oxidative phosphorylation.
and extra virgin olive oil; apples, grapes, pears and
berries generally contain high amounts of In conclusion, in animal and human studies there is
polyphenols (200-300 mg per 100 g). evidence that exercise-induced ROS play a crucial
role in stimulating signaling pathways for the
Polyphenols have various biological activities enzymatic activity of antioxidants (SOD, GPx and
(D’Angelo et al., 2012b; D’Angelo et al., 2017; CAT), mitochondrial biogenesis (expression PGC-
D’Angelo et al., 2019a; Martino et al., 2019; 1α) and glucose metabolism and absorption (insulin
D’Angelo et al., 2019b) and in particular, they are sensitivity, expression of GLUT4).
antioxidants (Zappia et al., 2010;
D’Angelo&Sammartino, 2015) and they can be Furthermore, adaptation to the ROS normal
considered a valid nutritional support against moderate production during physical activity allows
oxidative stress caused by physical activity. In their more effective enzymatic elimination increases
fact, to date, the effects of different polyphenols the mitochondrial oxidative capacity and its
have been studied in a wide range of operating efficiency (new more efficient mitochondria) and,
conditions, using a variety of integration, timing therefore, prevents the deleterious ROS
and dosage strategies (D’Angelo, 2019; Somerville overproduction.
et al., 2017; Malaguti et al., 2013).

References

Galletti, P., De Bonis, M.L., Sorrentino, A., Raimo, M., D'Angelo, S., Scala, I., Andria, G., D'Aniello, A.,
Ingrosso, D., & Zappia V. (2007). Accumulation of altered aspartyl residues in erythrocyte proteins from
patients with Down's syndrome. FEBS Journal, 274(20), 5263-5277.
D'Angelo, S., Lembo, S., Flora, F., De Bonis, M.L., Balato, A., Ayala, F., Balato, N., Galletti, P., & Zappia, V.
(2012)a. Abnormal isoaspartyl residues in erythrocyte membranes from psoriatic patients.Archives of
DermatologicalResearch, 304(6), 475-479.
D'Angelo, S., La Porta, R., Napolitano, M., Galletti, P., Quagliuolo, L., & Boccellino, M.R. (2012b). Effect of
Annurca apple polyphenols on human HaCaT keratinocytes proliferation. Journal of Medicinal Food,
15(11), 1024-1031.
D’Angelo, S., Trojsi, F., Salvatore, A., Daniele, L., Raimo, M., Galletti, P., & Monsurrò, M.R. (2013).
Accumulation of altered aspartyl residues in erythrocyte membraneproteins from patients with sporadic
amyotrophic lateral sclerosis. Neurochemistry International, 63 (6), 626-34.
D’Angelo, S., & Sammartino, D. (2015). Protective effect of Annurcaapple extract against oxidative damage
in human erythrocytes. Current Nutrition & Food Science, 11 (4), 248-256.
D'Angelo, S., Martino, E., Ilisso, C.P., Bagarolo, M.L., Porcelli, M. &Cacciapuoti, G. (2017). Pro-oxidant and
pro-apoptotic activity of polyphenol extract from Annurca apple and its underlying mechanisms in human
breast cancer cells. International Journal of Oncology, 51, 939-948.
D’Angelo, S., Scafuro, M., & Meccariello, R. (2019a). BPA and Nutraceuticals, Simultaneous Effects on
Endocrine Functions. Endocrine, Metabolic& Immune Disorders- Drug Targets, 19(5), 594-604.
D'Angelo, S., Martino E., & Cacciapuoti, G. (2019b). Effects of Annurca Apple (Maluspumila cv Annurca)
Polyphenols on Breast Cancer Cells. Current Nutrition & Food Science, 15(7), 745-751.
D’Angelo S. (2019). Polyphenols and athletic performance: a review on human data. Plant Physiological
Aspects of Phenolic Compounds. 1-24
Davalli, P., Mitic, T., Caporali, A., Lauriola, A., Arca, D., & Arca, D. (2016). ROS, Cell Senescence, and Novel
Molecular Mechanisms in Aging and Age-Related Diseases. Oxidative Medicine and Cellular Longevity, 1–
18.
Gutteridge, J.M., & Halliwell, B. (2000). Free radicals and antioxidants in the year 2000. A historical look to
the future. Annals of the New York Academy of Sciences. 899, 136–147
Ingrosso, D., D’Angelo, S., Perna, A.F., Iolascon, A., Miraglia del Giudice, E. Perrotta, S., Zappia, V., &
Galletti P. (1995). Increased membrane-protein methylation in hereditary spherocytosis. A marker of
cytoskeletal disarray. European Journal of Biochemistry (The FEBS Journal), 228, 894-898.
Ingrosso, D., D'Angelo, S., Perrotta, S., d'Urzo, G., Iolascon, A., Perna, A.F., Galletti, P., Zappia, V. &
Miraglia del Giudice, E. (1996). Cytoskeletal behaviour in Spectrin and Band 3 deficient spherocytic red
cells: evidence for a differentiated splenic conditioning role. British Journal of Haematology, 93, 38-41.

21
D’Angelo, S., et al.: Oxidative stress and sport performance Sport Science 13 (2020) Suppl 1: 18-22

Ingrosso, D., D'Angelo, S., di Carlo, E., Perna, A.F., Zappia, V., & Galletti, P. (2000). Increased methyl
esterification of altered aspartyl residues in erythrocyte membrane proteins in response to oxidative
stress. European Journal of Biochemistry, 267, 1-10.
Ingrosso, D., Cimmino, A., D'Angelo, S., Zappia, V., & Galletti, P. (2002). Protein methylation as a marker of
aspartyl damage in G6PD-deficient erythrocytes: role of oxidative stress. European Journal of
Biochemistry, 269, 2032-2039
Kawamura, T., & Muraoka, I. (2018). Exercise-induced oxidative stress and the effects of antioxidant intake
from a physiological viewpoint. Antioxidants (Basel), 7(9).
Malaguti, M., Angeloni, C., & Hrelia, S. (2013). Polyphenols in exercise performance and prevention of
exercise-induced muscle damage. Oxidative Medicine and Cellular Longevity, 2013, 825928.
Mankowski, R.T., Anton, S.D., Buford, T.W., & Leeuwenburgh C. (2015). Dietary Antioxidants as Modifiers of
Physiologic Adaptations to Exercise. Med Sci Sports Exerc. 47(9), 1857–1868.
Martino, E., Vuoso, D.C., D'Angelo, S., Mele, L., D'Onofrio, N., Porcelli, M., & Cacciapuoti, G. (2019).
Annurca apple polyphenol extract selectively kills MDA-MB-231 cells through ROS generation, sustained
JNK activation and cell growth and survival inhibition. Scientific Reports, 10(1), 13045.
Myburgh, K.H. (2014). Polyphenol supplementation: benefits for exercise performance or oxidative stress?
Sports Medicine. S1. 57-70.
Motti, M.L., D’Angelo, S., & Rosaria, M. (2018). MicroRNAs, Cancer and Diet: Facts and New Exciting
Perspectives. Current Molecular Pharmacology, 11, 90-96.
Muñoz Marín, D., Barrientos, G., Alves, J., Grijota, F.J., Robles, M.C,. & Maynar, M. (2018). Oxidative stress,
lipid peroxidation indexes and antioxidant vitamins in long and middle distance athletes during a sport
season. The Journal of Sports Medicine and Physical Fitness, 58(12), 1713-1719.
Radak, Z., Zhao, Z., Koltai, E., Ohno, H., & Atalay M. (2013). Oxygen consumption and usage during
physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid
Redox Signal, 18(10), 1208–1246.
Sies, H. (2015). Oxidative stress: a concept in redox biology and medicine. Redox Biology, 4, 180-183.
Simioni, C., Giorgio Zauli, G., Martelli, A.M., Marco Vitale, M., Gianni Sacchetti, G., Arianna Gonelli, A., Neri
L.M. (2018). Oxidative stress: role of physical exercise and antioxidant nutraceuticals in adulthood and
aging. Oncotarget, 9(24), 17181-17198.
Webb, R., Hughes, M.G., Thomas, A.W., & Morris, K. (2017). The ability of exercise-associated oxidative
stress to trigger redox-sensitive signaling responses. Antioxidants (Basel). 6(3).

Received: March 3, 2019

Accepted: March 18, 2019
Correspondence to:
Stefania D’Angelo
Department of Movement Sciences and Wellbeing,
University of Naples “Parthenope”, Naples, Italy
E-mail: [email protected]

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