Skip to main content

Advertisement

Log in

Effect of physical exercise on changes in activities of creatine kinase, cytochrome c oxidase and ATP levels caused by ovariectomy

  • Research Article
  • Published:
Metabolic Brain Disease Aims and scope Submit manuscript

Abstract

The reduction in the secretion of ovarian hormones, principally estrogen, is a consequence of menopause. Estrogens act primarily as female sex hormones, but also exert effects on different physiological systems including the central nervous system. The treatment normally used to reduce the symptoms of menopause is the hormone therapy, which seems to be effective in treating symptoms, but it may be responsible for adverse effects. Based on this, there is an increasing demand for alternative therapies that minimize signs and symptoms of menopause. In the present study we investigated the effect of ovariectomy and/or physical exercise on the activities of energy metabolism enzymes, such as creatine kinase (cytosolic and mitochondrial fractions), pyruvate kinase, succinate dehydrogenase, complex II, cytochrome c oxidase, as well as on ATP levels in the hippocampus of adult rats. Adult female Wistar rats with 90 days of age were subjected to ovariectomy (an animal model widely used to mimic the postmenopausal changes). Thirty days after the procedure, the rats were submitted to the exercise protocol, which was performed three times a week for 30 days. Twelve hours after the last training session, the rats were decapitated for subsequent biochemical analyzes. Results showed that ovariectomy did not affect the activities of pyruvate kinase, succinate dehydrogenase and complex II, but decreased the activities of creatine kinase (cytosolic and mitochondrial fractions) and cytochrome c oxidase. ATP levels were also reduced. Exercise did not produce the expected results since it was only able to partially reverse the activity of creatine kinase cytosolic fraction. The results of this study suggest that estrogen deficiency, which occurs as a result of ovariectomy, affects generation systems and energy homeostasis, reducing ATP levels in hippocampus of adult female rats.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ADP:

Adenosine diphosphate

ATP:

Adenosine triphosphate

B-CK:

Brain creatine kinase

CK:

Creatine kinase

CNS:

Central nervous system

COX:

Cytochrome c oxidase

ER:

Estrogen receptor

HT:

Hormone therapy

M-CK:

Muscle creatine kinase

Mi-CK:

Mitochondrial creatine kinase

OVX:

Ovariectomy

PK:

Pyruvate kinase

References

  • Acin-Perez R, Enriquez JA (2013) The function of the respiratory supercomplexes: the plasticity model. Biochim Biophys Acta. doi:10.1016/j.bbabio.2013.12.009

    PubMed  Google Scholar 

  • Aksenov M, Aksenova M, Butterfield DA, Markesbery WR (2000) Oxidative modification of creatine kinase BB in Alzheimer’s disease brain. J Neurochem 74:2520–2527

    Article  CAS  PubMed  Google Scholar 

  • Arida RM, Scorza FA, dos Santos NF, Peres CA, Cavalheiro EA (1999) Effect of physical exercise on seizure occurrence in a model of temporal lobe epilepsy in rats. Epilepsy Res 37:45–52

    Article  CAS  PubMed  Google Scholar 

  • Behr GA, Schnorr CE, Simoes-Pires A, da Motta LL, Frey BN, Moreira JC (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. doi:10.1007/s10565-012-9226-x

    Article  CAS  PubMed  Google Scholar 

  • Ben J, Soares FM, Cechetti F, Vuaden FC, Bonan CD, Netto CA, Wyse AT (2009) Exercise effects on activities of Na(+), K(+)-ATPase, acetylcholinesterase and adenine nucleotides hydrolysis in ovariectomized rats. Brain Res 1302:248–255

    CAS  PubMed  Google Scholar 

  • Ben J, Soares FM, Scherer EB, Cechetti F, Netto CA, Wyse AT (2010) Running exercise effects on spatial and avoidance tasks in ovariectomized rats. Neurobiol Learn Mem 94:312–317. doi:10.1016/j.nlm.2010.07.003

    Article  PubMed  Google Scholar 

  • Berchtold NC, Kesslak JP, Pike CJ, Adlard PA, Cotman CW (2001) Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus. Eur J Neurosci 14:1992–2002

    Article  CAS  PubMed  Google Scholar 

  • Bergen HT, Pentecost BT, Dickerman HW, Pfaff DW (1993) In situ hybridization for creatine kinase-B messenger RNA in rat uterus and brain. Mol Cell Endocrinol 92:111–119. doi:10.1016/0303-7207(93)90081-T

    Article  CAS  PubMed  Google Scholar 

  • Bigl M, Bruckner MK, Arendt T, Bigl V, Eschrich K (1999) Activities of key glycolytic enzymes in the brains of patients with Alzheimer’s disease. J Neural Transm 106:499–511

    Article  CAS  PubMed  Google Scholar 

  • Bloomer RJ, Fisher-Wellman K (2009) The role of exercise in minimizing postprandial oxidative stress in cigarette smokers. Nicotine Tob Res 11:3–11. doi:10.1093/ntr/ntn005

    CAS  PubMed  Google Scholar 

  • Brinton RD (2008) The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 31:529–537. doi:10.1016/j.tins.2008.07.003

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29:222–230

    Article  CAS  PubMed  Google Scholar 

  • Cechetti F, Rhod A, Simao F, Santin K, Salbego C, Netto CA, Siqueira IR (2007) Effect of treadmill exercise on cell damage in rat hippocampal slices submitted to oxygen and glucose deprivation. Brain Res 1157:121–125

    CAS  PubMed  Google Scholar 

  • Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301

    Article  CAS  PubMed  Google Scholar 

  • da Cunha MJ, da Cunha AA, Ferreira AG, Machado FR, Schmitz F, Lima DD, Delwing D, Mussulini BH, Wofchuk S, Netto CA, Wyse AT (2012) Physical exercise reverses glutamate uptake and oxidative stress effects of chronic homocysteine administration in the rat. Int J Dev Neurosci 30:69–74. doi:10.1016/j.ijdevneu.2012.01.001

    Article  PubMed  Google Scholar 

  • da Silva CG, Bueno AR, Schuck PF, Leipnitz G, Ribeiro CA, Wannmacher CM, Wyse AT, Wajner M (2003) D-2-hydroxyglutaric acid inhibits creatine kinase activity from cardiac and skeletal muscle of young rats. Eur J Clin Investig 33:840–847

    Article  Google Scholar 

  • Daniel JM, Dohanich GP (2001) Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21:6949–6956

    CAS  PubMed  Google Scholar 

  • de Azevedo Guimaraes AC, Baptista F (2011) Influence of habitual physical activity on the symptoms of climacterium/menopause and the quality of life of middle-aged women. Int J Womens Health 3:319–328. doi:10.2147/ijwh.s24822

    Article  PubMed Central  PubMed  Google Scholar 

  • Ding F, Yao J, Zhao L, Mao Z, Chen S, Brinton RD (2013) Ovariectomy induces a shift in fuel availability and metabolism in the hippocampus of the female transgenic model of familial Alzheimer’s. PLoS One 8:e59825. doi:10.1371/journal.pone.0059825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Edwards BJ, Li J (2013) Endocrinology of menopause. Periodontol 2000(61):177–194. doi:10.1111/j.1600-0757.2011.00407.x

    Article  Google Scholar 

  • Erecinska M, Silver IA (1994) Ions and energy in mammalian brain. Prog Neurobiol 43:37–71

    Article  CAS  PubMed  Google Scholar 

  • Ferreira AG, da Cunha AA, Scherer EB, Machado FR, da Cunha MJ, Braga A, Mussulini BH, Moreira JD, Wofchuk S, Souza DO, Wyse AT (2012) Evidence that hyperprolinemia alters glutamatergic homeostasis in rat brain: neuroprotector effect of guanosine. Neurochem Res 37:205–213. doi:10.1007/s11064-011-0604-1

    Article  CAS  PubMed  Google Scholar 

  • Fischer JC, Ruitenbeek W, Berden JA, Trijbels JM, Veerkamp JH, Stadhouders AM, Sengers RC, Janssen AJ (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 153:23–36

    Article  CAS  PubMed  Google Scholar 

  • Freitas TP, Scaini G, Correa C, Santos PM, Ferreira GK, Rezin GT, Moretti M, Valvassori SS, Quevedo J, Streck EL (2010) Evaluation of brain creatine kinase activity in an animal model of mania induced by ouabain. J Neural Transm 117:149–153. doi:10.1007/s00702-009-0337-3

    Article  PubMed  Google Scholar 

  • Gomes EC, Silva AN, de Oliveira MR (2012) Oxidants, antioxidants, and the beneficial roles of exercise-induced production of reactive species. Oxidative Med Cell Longev 2012:756132. doi:10.1155/2012/756132

    Article  Google Scholar 

  • Henderson VW (2013) Alzheimer’s disease: review of hormone therapy trials and implications for treatment and prevention after menopause. J Steroid Biochem Mol Biol. doi:10.1016/j.jsbmb.2013.05.010

    PubMed  Google Scholar 

  • Hughes BP (1962) A method for the estimation of serum creatine kinase and its use in comparing creatine kinase and aldolase activity in normal and pathological sera. Clin Chim Acta 7:597–603

    Article  CAS  PubMed  Google Scholar 

  • Huttemann M, Helling S, Sanderson TH, Sinkler C, Samavati L, Mahapatra G, Varughese A, Lu G, Liu J, Ramzan R, Vogt S, Grossman LI, Doan JW, Marcus K, Lee I (2012) Regulation of mitochondrial respiration and apoptosis through cell signaling: cytochrome c oxidase and cytochrome c in ischemia/reperfusion injury and inflammation. Biochim Biophys Acta 1817:598–609. doi:10.1016/j.bbabio.2011.07.001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ji LL, Gomez-Cabrera MC, Vina J (2006) Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann N Y Acad Sci 1067:425–435. doi:10.1196/annals.1354.061

    Article  CAS  PubMed  Google Scholar 

  • Klein AM, Ferrante RJ (2007) The neuroprotective role of creatine. Subcell Biochem 46:205–243

    Article  PubMed  Google Scholar 

  • Konorev EA, Hogg N, Kalyanaraman B (1998) Rapid and irreversible inhibition of creatine kinase by peroxynitrite. FEBS Lett 427:171–174

    Article  CAS  PubMed  Google Scholar 

  • Koufen P, Stark G (2000) Free radical induced inactivation of creatine kinase: sites of interaction, protection, and recovery. Biochim Biophys Acta 1501:44–50

    Article  CAS  PubMed  Google Scholar 

  • Kramer AF, Colcombe SJ, McAuley E, Scalf PE, Erickson KI (2005) Fitness, aging and neurocognitive function. Neurobiol Aging 26(Suppl 1):124–127

    Article  PubMed  Google Scholar 

  • Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863–870

    CAS  PubMed  Google Scholar 

  • Kume-Kick J, Ferris DC, Russo-Menna I, Rice ME (1996) Enhanced oxidative stress in female rat brain after gonadectomy. Brain Res 738:8–14

    CAS  PubMed  Google Scholar 

  • Leong SF, Lai JC, Lim L, Clark JB (1981) Energy-metabolizing enzymes in brain regions of adult and aging rats. J Neurochem 37:1548–1556

    Article  CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Mackedanz V, Mattos CB, Feksa LR, Wannmacher CM, Wyse AT (2011) Ovariectomy alters energy metabolism in rat striatum: effect of supplementation with soy diet rich in isoflavones. Metab Brain Dis 26:97–105. doi:10.1007/s11011-010-9216-8

    Article  CAS  PubMed  Google Scholar 

  • Marcondes FK, Bianchi FJ, Tanno AP (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62:609–614

    Article  CAS  PubMed  Google Scholar 

  • Martins DB, Mazzanti CM, Franca RT, Pagnoncelli M, Costa MM, de Souza EM, Goncalves J, Spanevello R, Schmatz R, da Costa P, Mazzanti A, Beckmann DV, Cecim Mda S, Schetinger MR, Lopes ST (2012) 17-beta estradiol in the acetylcholinesterase activity and lipid peroxidation in the brain and blood of ovariectomized adult and middle-aged rats. Life Sci 90:351–359. doi:10.1016/j.lfs.2011.12.006

    Article  CAS  PubMed  Google Scholar 

  • McAndrew LM, Napolitano MA, Albrecht A, Farrell NC, Marcus BH, Whiteley JA (2009) When, why and for whom there is a relationship between physical activity and menopause symptoms. Maturitas 64:119–125. doi:10.1016/j.maturitas.2009.08.009

    Article  PubMed  Google Scholar 

  • Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055–2067

    Article  CAS  PubMed  Google Scholar 

  • Monteiro SC, Matte C, Delwing D, Wyse AT (2005) Ovariectomy increases Na+, K+−ATPase, acetylcholinesterase and catalase in rat hippocampus. Mol Cell Endocrinol 236:9–16

    Article  CAS  PubMed  Google Scholar 

  • Monteiro SC, Mattos CB, Scherer EB, Wyse AT (2007) Supplementation with vitamins E plus C or soy isoflavones in ovariectomized rats: effect on the activities of Na(+), K (+)-ATPase and cholinesterases. Metab Brain Dis 22:156–171. doi:10.1007/s11011-007-9051-8

    Article  CAS  PubMed  Google Scholar 

  • Moran M, Moreno-Lastres D, Marin-Buera L, Arenas J, Martin MA, Ugalde C (2012) Mitochondrial respiratory chain dysfunction: implications in neurodegeneration. Free Radic Biol Med 53:595–609. doi:10.1016/j.freeradbiomed.2012.05.009

    Article  CAS  PubMed  Google Scholar 

  • Moseley AE, Williams MT, Schaefer TL, Bohanan CS, Neumann JC, Behbehani MM, Vorhees CV, Lingrel JB (2007) Deficiency in Na,K-ATPase alpha isoform genes alters spatial learning, motor activity, and anxiety in mice. J Neurosci 27:616–626. doi:10.1523/jneurosci.4464-06.2007

    Article  CAS  PubMed  Google Scholar 

  • Ostlund H, Keller E, Hurd YL (2003) Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann N Y Acad Sci 1007:54–63

    Article  PubMed  Google Scholar 

  • Owen L, Sunram-Lea SI (2011) Metabolic agents that enhance ATP can improve cognitive functioning: a review of the evidence for glucose, oxygen, pyruvate, creatine, and L-carnitine. Nutrients 3:735–755. doi:10.3390/nu3080735

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pacelli C, Latorre D, Cocco T, Capuano F, Kukat C, Seibel P, Villani G (2011) Tight control of mitochondrial membrane potential by cytochrome c oxidase. Mitochondrion 11:334–341. doi:10.1016/j.mito.2010.12.004

    Article  CAS  PubMed  Google Scholar 

  • Pentecost BT, Mattheiss L, Dickerman HW, Kumar SA (1990) Estrogen regulation of creatine kinase-B in the rat uterus. Mol Endocrinol 4:1000–1010

    Article  CAS  PubMed  Google Scholar 

  • Poomalar GK, Arounassalame B (2013) The quality of life during and after menopause among rural women. J Clin Diagn Res 7:135–139. doi:10.7860/JCDR/2012/4910.2688

    Article  Google Scholar 

  • Powers SK, Lennon SL (1999) Analysis of cellular responses to free radicals: focus on exercise and skeletal muscle. Proc Nutr Soc 58:1025–1033

    Article  CAS  PubMed  Google Scholar 

  • Powers SK, Talbert EE, Adhihetty PJ (2011) Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol 589:2129–2138. doi:10.1113/jphysiol.2010.201327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Radak Z, Kaneko T, Tahara S, Nakamoto H, Ohno H, Sasvari M, Nyakas C, Goto S (1999) 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 27:69–74

    Article  CAS  PubMed  Google Scholar 

  • Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44:153–159. doi:10.1016/j.freeradbiomed.2007.01.029

    Article  CAS  PubMed  Google Scholar 

  • Rettberg JR, Yao J, Brinton RD (2013) Estrogen: a master regulator of bioenergetic systems in the brain and body. Front Neuroendocrinol 35:8–30

    Article  PubMed  Google Scholar 

  • Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women’s Health Initiative randomized controlled trial. JAMA 288:321–333

    Article  CAS  PubMed  Google Scholar 

  • Rustin P, Chretien D, Bourgeron T, Gerard B, Rotig A, Saudubray JM, Munnich A (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35–51

    Article  CAS  PubMed  Google Scholar 

  • Savonenko AV, Markowska AL (2003) The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 119:821–830

    Article  CAS  PubMed  Google Scholar 

  • Scopel D, Fochesatto C, Cimarosti H, Rabbo M, Bello-Klein A, Salbego C, Netto CA, Siqueira IR (2006) Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 71:155–159

    Article  CAS  PubMed  Google Scholar 

  • Shangold MM (1990) Exercise in the menopausal woman. Obstet Gynecol 75:53S–58S, discussion 81S–83S

    CAS  PubMed  Google Scholar 

  • Sharpe MA, Cooper CE (1998) Interaction of peroxynitrite with mitochondrial cytochrome oxidase. Catalytic production of nitric oxide and irreversible inhibition of enzyme activity. J Biol Chem 273:30961–30972

    Article  CAS  PubMed  Google Scholar 

  • Shi C, Xu J (2008) Increased vulnerability of brain to estrogen withdrawal-induced mitochondrial dysfunction with aging. J Bioenerg Biomembr 40:625–630. doi:10.1007/s10863-008-9195-1

    Article  CAS  PubMed  Google Scholar 

  • Shi C, Zou J, Li G, Ge Z, Yao Z, Xu J (2011) Bilobalide protects mitochondrial function in ovariectomized rats by up-regulation of mRNA and protein expression of cytochrome c oxidase subunit I. J Mol Neurosci 45:69–75. doi:10.1007/s12031-010-9388-z

    Article  CAS  PubMed  Google Scholar 

  • Shughrue PJ, Lane MV, Merchenthaler I (1997) Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388:507–525

    Article  CAS  PubMed  Google Scholar 

  • Shughrue PJ, Scrimo PJ, Merchenthaler I (2000) Estrogen binding and estrogen receptor characterization (ERalpha and ERbeta) in the cholinergic neurons of the rat basal forebrain. Neuroscience 96:41–49

    Article  CAS  PubMed  Google Scholar 

  • Soane L, Kahraman S, Kristian T, Fiskum G (2007) Mechanisms of impaired mitochondrial energy metabolism in acute and chronic neurodegenerative disorders. J Neurosci Res 85:3407–3415. doi:10.1002/jnr.21498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soules MR, Sherman S, Parrott E, Rebar R, Santoro N, Utian W, Woods N (2001) Executive summary: stages of reproductive aging workshop (STRAW). Fertil Steril 76:874–878

    Article  CAS  PubMed  Google Scholar 

  • Stachowiak O, Dolder M, Wallimann T, Richter C (1998) Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J Biol Chem 273:16694–16699

    Article  CAS  PubMed  Google Scholar 

  • Tomimoto H, Yamamoto K, Homburger HA, Yanagihara T (1993) Immunoelectron microscopic investigation of creatine kinase BB-isoenzyme after cerebral ischemia in gerbils. Acta Neuropathol 86:447–455

    CAS  PubMed  Google Scholar 

  • Valentini G, Chiarelli L, Fortin R, Speranza ML, Galizzi A, Mattevi A (2000) The allosteric regulation of pyruvate kinase. J Biol Chem 275:18145–18152. doi:10.1074/jbc.M001870200

    Article  CAS  PubMed  Google Scholar 

  • Vest RS, Pike CJ (2013) Gender, sex steroid hormones, and Alzheimer’s disease. Horm Behav 63:301–307. doi:10.1016/j.yhbeh.2012.04.006

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vollaard NB, Shearman JP, Cooper CE (2005) Exercise-induced oxidative stress:myths, realities and physiological relevance. Sports Med 35:1045–1062

    Article  PubMed  Google Scholar 

  • Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133–134:193–220

    Article  PubMed  Google Scholar 

  • Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochem J 281(Pt 1):21–40

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waynforth H, Flecknell P (1992) Experimental and surgical technique in the rat, 2nd edn, Academic, London, p 276–278

  • Whelan TJ, Goss PE, Ingle JN, Pater JL, Tu D, Pritchard K, Liu S, Shepherd LE, Palmer M, Robert NJ, Martino S, Muss HB (2005) Assessment of quality of life in MA.17: a randomized, placebo-controlled trial of letrozole after 5 years of tamoxifen in postmenopausal women. J Clin Oncol 23:6931–6940

    Article  CAS  PubMed  Google Scholar 

  • Whittingham TS, Lipton P (1981) Cerebral synaptic transmission during anoxia is protected by creatine. J Neurochem 37:1618–1621

    Article  CAS  PubMed  Google Scholar 

  • Wise PM (2001) The ‘menopause’ and the aging brain: causes and repercussions of hypoestrogenicity. Biogerontology 2:113–115

    Article  CAS  PubMed  Google Scholar 

  • Witt KA, Mark KS, Hom S, Davis TP (2003) Effects of hypoxia-reoxygenation on rat blood–brain barrier permeability and tight junctional protein expression. Am J Physiol Heart Circ Physiol 285:H2820–H2831. doi:10.1152/ajpheart.00589.2003

    CAS  PubMed  Google Scholar 

  • World Helth Organization Scientific Group (1996) Report of WHO scientific group: research on the menopause in the 1990's. Geneva, Switzerland, World Health Organization, v866, p 1-79

  • Xu XW, Shi C, He ZQ, Ma CM, Chen WH, Shen YP, Guo Q, Shen CJ, Xu J (2008) Effects of phytoestrogen on mitochondrial structure and function of hippocampal CA1 region of ovariectomized rats. Cell Mol Neurobiol 28:875–886. doi:10.1007/s10571-008-9265-2

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq–Brazil), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS).

Conflict of interest

All authors declare that no financial/commercial conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Angela T. S. Wyse.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Siebert, C., Kolling, J., Scherer, E.B.S. et al. Effect of physical exercise on changes in activities of creatine kinase, cytochrome c oxidase and ATP levels caused by ovariectomy. Metab Brain Dis 29, 825–835 (2014). https://doi.org/10.1007/s11011-014-9564-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11011-014-9564-x

Keywords

Navigation