Abstract
Objectives
The aim of the present study was to investigate the effects of moderate- or high-intensity intermittent exercise (MIIE/HIIE) on the oxidative status of the prefrontal cortex and cerebellum, locomotor activities, as well as working memory performances of rats.
Materials and Methods
Twenty female rats were divided into four groups: (1) sham-operated (Sham), (2) ovariectomy (OVX), (3) OVX + MIIE, and (4) OVX + HIIE groups. The OVX + MIIE and OVX + HIIE groups exercised on a rat treadmill for 7 weeks. The assessment on the working memory performances and locomotor activities were conducted on the last day of the exercise period. Levels of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX) enzyme activities, as well as levels of hydrogen peroxidase (H2O2), and malondialdehyde (MDA) in the prefrontal cortex and cerebellum were determined using a spectrophotometer.
Results
Ovariectomy depressed the working memory, locomotor activities, the levels of SOD, CAT, and GPX enzyme activities, and elevated the levels of H2O2, and MDA in the prefrontal cortex and cerebellum.
Conclusion
MIIE and HIIE exert their neuroprotective effects by reducing oxidative stress in the brain of ovariectomized rats. HIIE has more potent effects than MIIE in suppressing the levels of oxidants in the prefrontal cortex and cerebellum by increasing the levels of SOD and CAT activities more than MIIE.
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References
Genazzani A, Pluchino N, Luisi S, Luisi L (2007) Estrogen, cognition and female ageing. Hum Reprod Update 13:175–187
World Health Organization (2007) Women, ageing and health: a framework for action focus on gender. WHO Press, Geneva
Parker WH, Broder MS, Liu Z, Shoupe D, Farquhar C, Berek JS (2005) Ovarian conservation at the time of hysterectomy for benign disease. Obstet Gynecol 2005 106:219–226
Petrovska S, Dejanova B, Jurisic V (2012) Estrogens: mechanisms of neuroprotective effects J Physiol Biochem 68:455–460
McEwen BS, Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20:279–307
de Chaves G, Moretti M, Castro AA et al (2009) Effects of long-term ovariectomy on anxiety and behavioral despair in rats. Physiol Behav 97:420–425
Baeza I, De Castro NM, Giménez-Llort L, De la Fuente M (2010) Ovariectomy, a model of menopause in rodents, causes a premature aging of the nervous and immune systems. J Neuroimmunol 219:90–99
Signorelli SS, Neri S, Sciacchitano S et al (2006) Behaviour of some indicators of oxidative stress in postmenopausal and fertile women. Maturitas 53:77–82
Tan MN, Kartal M, Guldal D (2014) The effect of physical activity and body mass index on menopausal symptoms in Turkish women: a cross-sectional study in primary care. BMC Womens Health 14:38
Kaidah S, Soejono SK, Partadiredja G (2016) Exercise improves hippocampal estrogen and spatial memory of ovariectomized rats. Bratisl Med J 117:94–99
Mishr N, Mishra VN, Devanshi (2011) Exercise beyond menopause: dos and don’ts. J Midlife Health 2:51–56
Justine M, Azizan A, Hassan V, Salleh Z, Manaf H (2013) Barriers to participation in physical activity and exercise among middle-aged and elderly individuals. Singap Med J 54:581–586
Coquart JBJ, Lemaire C, Dubart AE, Luttembacher DP, Douillard C, Garcin M (2008) Intermittent versus continuous exercise: effects of perceptually lower exercise in obese women. Med Sci Sports Exerc 40:1546–1553
Gibala MJ, McGee SL (2008) Metabolic adaptations to short-term high-intensity interval training: a little pain for a lot of gain? Exerc Sport Sci Rev 36:58–63
Racil G, Ounis OB, Hammouda O et al (2013) Effects of high vs. moderate exercise intensity during interval training on lipids and adiponectin levels in obese young females. Eur J Appl Physiol 113:2531–2540
Delwing-de Lima D, Ulbricht ASSF., Werlang-Coelho C et al (2017) Effects of two aerobic exercise training protocols on parameters of oxidative stress in the blood and liver of obese rats. J Physiol Sci. https://doi.org/10.1007/s12576-017-0584-2
Afzalpour ME, Chadorneshin HT, Foadoddini M, Eivari HA (2015) Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain. Physiol Behav 147:78–83
Agustiningsih D, Soejono SK, Soesatyo MHNE., Prakosa D (2015) Exercise induces the synthesis of estrogen in ovariectomized Sprague–Dawley rats ventricular myocardium trough increase expression of CYP19 aromatase. Sport Sci Health 11:337–343
Brooks GA, White TP (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol Respir Environ Exerc Physiol 45:1009–1015
Hritcu L, Stefan M, Brandsch R, Mihasan M (2013) 6-Hydroxy-l-nicotine from arthrobacter nicotinovorans sustain spatial memory formation by decreasing brain oxidative stress in rats. J Physiol Biochem 69:25–34
Marques-Aleixo I, Santos-Alves E, Balca MM et al (2015) Physical exercise improves brain cortex and cerebellum mitochondrial bioenergetics and alters apoptotic, dynamic and auto(mito)phagy markers. Neuroscience 301:480–495
Iwai K, Nakaya N, Kawasaki Y, Matsue H (2002) Antioxidative functions of natto, a kind of fermented soybeans: effect on LDL oxidation and lipid metabolism in cholesterol-fed rats. J Agric Food Chem 50:3597–3601
Gülçin I, Küfrevioǧlu ÖI, Oktay M, Büyükokuroǧlu ME (2004) Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urtica dioica L.). J Ethnopharmacol 90:205–215
Singh RP, Murthy KNC, Jayaprakasha GK (2002) Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 50:81–86
Rauf S, Soejono SK, Partadiredja G (2015) Effects of treadmill exercise training on cerebellar estrogen and estrogen receptors, serum estrogen, and motor coordination performance of ovariectomized rats. Iran J Basic Med Sci 18:587–592
Behr GA, Schnorr CE, Simoes-Pires A, Motta LLD, Frey BN, Moreira JCF (2012) Increased cerebral oxidative damage and decreased antioxidant defenses in ovariectomized and sham-operated rats supplemented with vitamin A. Cell Biol Toxicol 28:317–330
Ciobica A, Olteanu Z, Padurariu M, Hritcu L (2012) The effects of pergolide on memory and oxidative stress in a rat model of Parkinson’s disease. J Physiol Biochem 68:59–69
Borrás C, Gambini J, Gómez-Cabrera MC et al (2005) 17β-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFЌB cascade. Aging Cell 4:113–118
Vina J, Gambini J, Lopez-GruesoR (2011) Females live longer than males: role of oxidative stress. Curr Pharm Des 17:3959–3965
Evsen MS, Ozler A, Gocmez C et al (2013) Effects of estrogen, estrogen/progesteron combination and genistein treatments on oxidant/antioxidant status in the brain of ovariectomized rats. Eur Rev Med Pharmacol Sci 17:1869–1873
Aksu I, Topcu A, Camsari UM, Acikgoz O (2009) Effect of acute and chronic exercise on oxidant–antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 452:281–285
Oliveira PJ, Moreira PI (2012) Physical exercise as a possible strategy for brain protection: evidence from mitochondrial-mediated mechanisms. Prog Neurobiol 99:149–162
Pingitore A, Lima GPP, Mastorci F, Quinones A, Iervasi G, Vassalle C (2015) Exercise and oxidative stress: potential effects of antioxidant dietary strategies in sports. Nutrition 31:916–922
Rattan SI (2004) Aging, anti-aging, and hormesis. Mech Ageing Dev 125:285–289
Radak Z, Marton O, Nagy E, Koltai E, Goto S (2013) The complex role of physical exercise and reactive oxygen species on brain. J Sport Helath Sci 2:87–93
Daud DM, Karim AAH, Mohammad M, Hamid NAA, Ngah WZW (2006) Effect of exercise intensity on antioxidant enzymatic activities in sedentary adults. Malay J Biochem Mol Biol 13:37–47
Radak Z, Ishihara K, Tekus E et al (2017) Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biol 12:285–290
Melisa A, Bradley-Whitman MA, Timmons MD (2014) Nucleic acid oxidation: an early feature of Alzheimer’s disease. J Neurochem 128:294–304
Liu J, Head E, Gharib AM (2002) Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-l-carnitine and/or R-α-lipoic acid. PNAS 99:2356–2361
Liu R, Liu IY, Bi X (2003) Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. PNAS 100:8526–8531
Garcia PC, Real CC, Ferreira AFB, Alouche SR, Britto LRG, Pires RS (2012) Different protocols of physical exercise produce different effects on synaptic and structural proteins in motor areas of the rat brain. Brain Res 1456:36–48
Acknowledgements
This study was funded by a grant from the Indonesia Endowment Fund for Education, Ministry of Finance, the Republic of Indonesia (Grant number: PRJ-956/LPDP/2014). The authors would like to thank Suparno (Department of Physiology, Faculty of Medicine, Universitas Gadjah Mada) and Yulianto (Department of PAU, Universitas Gadjah Mada) for their technical assistance, as well as Erik C Hookom for the language editing.
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All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The Ethics Committee of the Faculty of Medicine, Universitas Gadjah Mada has approved all experimental procedures in this study (approval number: KE/FK/217/EC/2016).
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Rauf, S., Soesatyo, M., Agustiningsih, D. et al. Intermittent exercise improves working memory and locomotor activity by attenuating oxidative stress in the prefrontal cortex and cerebellum of ovariectomized rats. Sport Sci Health 14, 615–624 (2018). https://doi.org/10.1007/s11332-018-0470-1
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DOI: https://doi.org/10.1007/s11332-018-0470-1