• Users Online: 598
  • Home
  • Print this page
  • Email this page

 Table of Contents  
REVIEW
Year : 2020  |  Volume : 15  |  Issue : 11  |  Page : 1981-1985

The role of exercise in brain DNA damage


1 Laboratory of Translational Biomedicine, Graduate Program of Health Sciences, University of Southern Santa Catarina – UNESC, Criciúma, SC, Brazil
2 Research Institute of Sport Science, University of Physical Education, Budapest, Hungary
3 Laboratory of Exercise Biochemistry in Health, Graduate Program in Health Sciences, School of Medicine, Pontifícia Universidade Católica do Paraná, Curitiba, PR, Brazil

Date of Submission03-Jan-2020
Date of Decision14-Jan-2020
Date of Acceptance04-Mar-2020
Date of Web Publication11-May-2020

Correspondence Address:
Ricardo Aurino de Pinho
Laboratory of Exercise Biochemistry in Health, Graduate Program in Health Sciences, School of Medicine, Pontifícia Universidade Católica do Paraná, Curitiba, PR
Brazil
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1673-5374.282237

Rights and Permissions
  Abstract 


Cells are constantly subjected to cytotoxic and genotoxic insults resulting in the accumulation of unrepaired damaged DNA, which leads to neuronal death. In this way, DNA damage has been implicated in the pathogenesis of neurological disorders, cancer, and aging. Lifestyle factors, such as physical exercise, are neuroprotective and increase brain function by improving cognition, learning, and memory, in addition to regulating the cellular redox milieu. Several mechanisms are associated with the effects of exercise in the brain, such as reduced production of oxidants, up-regulation of antioxidant capacity, and a consequent decrease in nuclear DNA damage. Furthermore, physical exercise is a potential strategy for further DNA damage repair. However, the neuroplasticity molecules that respond to different aspects of physical exercise remain unknown. In this review, we discuss the influence of exercise on DNA damage and adjacent mechanisms in the brain. We discuss the results of several studies that focus on the effects of physical exercise on brain DNA damage.

Keywords: aerobic exercise; apoptosis; brain-derived neurotrophic factor; brain; DNA damage; DNA repair; neurodegenerative disease; oxidative stress; physical exercise; strength exercise


How to cite this article:
Vilela TC, de Andrade VM, Radak Z, de Pinho RA. The role of exercise in brain DNA damage. Neural Regen Res 2020;15:1981-5

How to cite this URL:
Vilela TC, de Andrade VM, Radak Z, de Pinho RA. The role of exercise in brain DNA damage. Neural Regen Res [serial online] 2020 [cited 2021 Oct 17];15:1981-5. Available from: http://www.nrronline.org/text.asp?2020/15/11/1981/282237




  Introduction Top


Cells are often subject to endogenous (metabolic intermediate products), and exogenous (like radiation and chemical substances), insults that result in genetic and epigenetic alterations (Gluckman et al., 2009; Hoeijmakers, 2009) and the accumulation of unrepaired damaged DNA. In this way, the epigenetic changes include aberrant DNA methylation, microRNA (miRNA) and noncoding RNA deregulation and alterations in histone modification states (Dumitrescu, 2018). The common forms of DNA damage, in turn, include single and double-stranded breaks, interstrand DNA crosslink, DNA protein-crosslink, single or multiple base damage and chromosomal damage (Klages and Li, 2017). The DNA damage is a threat to cell viability, compromising the integrity of the genome and the epigenome (Dabin et al., 2016).

The DNA damage, also, leads to neuronal death and is associated with memory impairments and neural deterioration (Bird, 2002). Significant DNA damage activates specific signaling pathways, such as pro-apoptotic or DNA repair proteins. Cells either die or survive depending on the dimension of the damage and the outcome of repair (Rass et al., 2007; Yang et al., 2014). Therefore, DNA damage is associated with the pathogenesis of neurological disorders (like Parkinson and Alzheimer’s diseases), cancer, and aging (Hoeijmakers 2009; Lovell and Markesbery 2017; Poewe et al., 2017).

Exogenous stimuli have been implicated in the protection and/or delay of DNA damage, including physical exercise (Soares et al., 2015). Several studies have reported that physical exercise is neuroprotective and increases brain function by improving plasticity, cognition, learning, and memory (Van Praag et al., 2005; Tuon et al., 2015; Baek, 2016; Vilela et al., 2016), in addition to regulating the cellular redox milieu (Pinho et al., 2019). This regulation induces antioxidant production, which is associated with a reduction in reactive oxygen species and damage to lipids, protein, and DNA (Radak et al., 2013, 2016). Physical exercise alters the cerebral redox state in a type-dependent manner; acute and regular exercise exerts different effects on redox state (Shahandeh et al., 2013). For example, the adaptive response is impaired following acute exercise, whereas regular exercise induces an adaptation on redox signaling that is associated with a wide range of physiological processes (Radak et al., 2016).

Genetic mechanisms, such as DNA methylation, oxidation, and damage are important in the development of different brain diseases and neurodegeneration (Madabhushi et al., 2014). Studies have shown that this can be minimized with adequate doses of lifelong physical exercise (Yang et al., 2014; Fernandes et al., 2017); however, the mechanisms underlying the long-lasting effects of regular exercise on the brain DNA are not fully understood. Most studies have focused on cellular and molecular changes in skeletal muscle. In this review, we discuss the influence of the exercise on DNA damage and their adjacent mechanisms in the brain.


  Search Strategy and Selection Criteria Top


Systematic database searches of PubMed, Web of Science, Scopus, and MEDLINE were performed to identify peer-reviewed studies from the 2000s. Combinations of keywords related to brain disease, aerobic/resistance or strength physical exercise, and DNA damage were used. Other variables were not addressed in this review but should be considered to gain a complete understanding of the effects of physical exercise on brain DNA damage.


  Effect of Different Models of Physical Exercise on Brain Top


There is little evidence addressing the influence of exercise training itself on the brain and the findings are conflicting due to the use of different exercise models (aerobic, strength, combined) and protocols (duration and intensity; Kim et al., 2005; Ogonovszky et al., 2005; Alghadir et al., 2015; Aguiar et al., 2016). Most research assessing the neuroprotective effects of the exercise focuses on aerobic training alone; therefore, the benefits of other exercise protocols, such as strength training, remain unknown. Most experimental studies have used an treadmill- (Speck et al., 2011; Chen et al., 2012; Yang et al., 2014; Vilela et al., 2016) or swimming pool- (Souza et al., 2009; Nonato et al., 2016) based aerobic training program. However, recent studies have revealed some positive effects of resistance training (Vilela et al., 2016).

Regardless of the type or method of exercise, it is clear that physical exercise improves oxidative status and memory, and prevents neurodegenerative disease progression (Patki et al., 2014; Yau et al., 2015; Vilela et al., 2016). This may occur because physical training increases the level of neurotrophic factors in the brain, which induce neurogenesis, synaptogenesis, neuroplasticity, and angiogenesis (Aguiar et al., 2011; Portugal et al., 2015; Kim et al., 2016; Radak et al., 2016). We have observed that treadmill exercise ameliorates spatial memory in aging rats through brain-derived neurotrophic factor (BDNF) signaling, which regulates proteins of the glutamatergic system (Vilela et al., 2016). Previous studies have reported that swimming training attenuates oxidative damage, increases enzymatic antioxidants in the rat brain, and improves depressive-like behavior in chronically stressed rats (Liu et al., 2013; Nonato et al., 2016). Hsu et al. (2018) have shown that aerobic training in older adults with mild subcortical ischemia can improve executive function and the neural efficiency of associated brain areas. Furthermore, treadmill exercise improves motor function via the preservation of nigrostriatal dopaminergic neurons and fibers and in rats with rotenone-induced Parkinson’s disease (Manoharan et al., 2016; Shin et al., 2017). Aerobic training improves brain energy metabolism by increasing ketone uptake and utilization while maintaining brain glucose uptake in Alzheimer’s disease. This may be associated with some cognitive improvement (Castellano et al., 2017).

Resistance exercise confers cognitive and mental health benefits in humans (Mavros et al., 2017; Gordon et al., 2018); therefore, it is critical that animal models are developed and evaluated to examine the underlying neurobiological systems. Hornberger and Farrar (2004) have described an experimental model of progressive resistance exercise in the rat. This is a practical application of the overload principle and forms the basis of most human resistance training programs. Previously, we have reported that this experimental model improved spatial memory possibly via protein kinase C activation, which activates signaling pathways that are crucial for the formation of many distinct types of memory (Vilela et al., 2016). Furthermore, Tuon et al. (2014) have demonstrated that treadmill and strength training prevent depressive-like behavior and promote neuroprotection. This may, in turn, regulate both mitochondrial function and neuroinflammation in an experimental model of Parkinson’s disease. Another study from our group has shown that strength and endurance training attenuates the progression and pathological hallmarks of experimental autoimmune encephalomyelitis, thereby representing an important non-pharmacological intervention for the improvement of immune-mediated diseases, such as multiple sclerosis (Souza et al., 2017). Interestingly, Özbeyli et al. (2017) have shown that aerobic, resistance and combined exercise is protective against the development of Alzheimer’s Disease by reducing oxidative stress and improving the antioxidant system and brain plasticity. However, the specific molecular mechanisms of neuroplasticity that respond to strength training or other models remain undetermined.


  Effect of Physical Exercise on DNA Damage Top


The DNA damage is dependent on cellular repair capacity, which can reverse DNA failure. Previous research has suggested that it may be possible to increase the DNA repair ability of neurons via BDNF regulation (Yang et al., 2014). The neuroprotective effects of exercise are mediated by BDNF (Marais et al., 2009; Aguiar et al., 2011), which binds to the tropomyosin receptor kinase B receptor and activates intracellular signaling pathways (Yang et al., 2014). BDNF increases neuronal DNA repair via activation of cyclic AMP response element-binding protein (CREB), which mediates expression of APE1, a key enzyme for base excision in the DNA repair pathway (Marais et al., 2009).

Previous results from our group have shown that aerobic and strength training improves spatial memory in aging rats via different mechanisms (Vilela et al., 2016). Interestingly, we observed a reduction in DNA damage after treadmill training alone, as previously reported (Yang et al., 2014; Soares et al., 2015; Vilela et al., 2016). We found an increase in BDNF and CREB; however, there were no significant alterations in the expression of APE1. This suggested that other mechanisms are involved in the reduction of DNA damage [Figure 1].
Figure 1 Explanatory scheme of the effect of two physical training models on neurochemical parameters in the hippocampus of old rats.
Both aerobic and strength training improves spatial memory in aging rats by inducing different mechanisms. BDNF: Brain-derived neurotrophic factor; CREB: cyclic AMP response element binding; IL1β: interleukin 1 beta; p75NTR: neurotrophin receptor p75; PKCα: protein kinase C alpha; pNMDA: N-methyl-D-aspartate phosphorylate; PSD 95: postsynaptic density protein-95; TNFα: tumor necrosis factor alpha.


Click here to view


Enzymes such as 8-oxoguanine DNA glycosylase-1, which is primarily responsible for removing 8-hydroxy-2′-deoxyguanosine from DNA, plays a central role in the base excision repair system (Iida et al., 2002; de Souza-Pinto et al., 2008). In addition, the gene expression of 8-oxoguanine DNA glycosylase-1 is upregulated by redox state alterations (Adaikalakoteswari et al., 2007). Several studies have observed that exercise can increase the activity of base excision repair enzymes in human and animal models (Radak et al., 2009; Koltai et al., 2010; Siu et al., 2011). However, few studies have investigated the effects of exercise training on DNA damage and repair in the brain [Table 1].
Table 1 Effects of exercise training on DNA damage and repair in human and animal models

Click here to view


Soares et al. (2015) have shown that the decrease in oxidative damage associated with exercise training may be explained by an increase in antioxidant and metabolic efficiency. Further, Radak et al. (2002) have shown that regular exercise-induced adaptation attenuates the age-associated increase in 8-hydroxy-2′-deoxyguanosine levels and increases DNA repair activity and resistance against oxidative stress in proteins. Interestingly, similar results were observed in a human study using a single-bout of physical exercise; they found increases in the activity of the 8-oxoG repair enzyme in skeletal muscle (Radák et al., 2003). Human models have argued that a reduction in DNA damage after training is related to a decrease in prooxidant cellular conditions (Siu et al., 2011; Pittaluga et al., 2015; Soares et al., 2015). However, strenuous endurance exercise can cause muscle and lymphocyte DNA damage and the extent of this damage increases as running distance increases (Ryu et al., 2016).

Results are scarce and conflicting for the effects of exercise on DNA in the brain. Ogonovszky et al. (2005) have shown that exercise training, even with a very severe protocol, is unlikely to cause significant oxidative damage to brain DNA. Other studies have shown that regular aerobic exercise decreases the accumulation of DNA damage (Kim et al., 2010; Yang et al., 2014; Vilela et al., 2016). Importantly, the brain is susceptible to the damaging effects of reactive oxygen species due to a very high rate of metabolism and oxygen consumption, and specific biochemical reactions that generate free radicals (Manoharan et al., 2016). Therefore, several mechanisms may be related to the effects of exercise in the brain, such as reduced production of oxidants, up-regulation of antioxidant capacity, and consequent decrease of nuclear DNA damage (Soares et al., 2015; [Figure 2]). Furthermore, chronic exercise has a positive response to the brain, which is a different effect when compared with other organs (Liu et al., 2000). Therefore, we can understand its role in novel therapeutic and rehabilitation strategies by further elucidating exercise-induced mechanisms in the brain.
Figure 2 Explanatory scheme of the effect of exercise on DNA damage.
The exercise leads to the up-regulation of antioxidant capacity, increases DNA repair, and consequently reduces nuclear DNA damage. ROS: Reactive oxygen species.


Click here to view



  Conclusion Top


The DNA damage is a common feature of neurodegenerative illnesses and the ability to repair this damage is crucial for neuronal survival. Data from previous studies have revealed clear evidence that physical exercise induces profound genetic alterations that regulate synaptic and brain plasticity. Furthermore, exercise may be fundamental in the control of the neurological disease; however, a better understanding of the effects of different types of exercise is required. Future studies in animals and humans may address these gaps in knowledge and contribute to understanding the effects of physical exercise on the brain.

Acknowledgments: We thank the National Counsel of Technological and Scientific Development-CNPq/Brazil, Coordination for the Improvement of Higher Education Personnel-CAPES/Brazil, and Research Fund of the Pontifícia Universidade Católica do Paraná for contributing to research activities.

Author contributions: TCV, VMA, ZR and RAP contributed to literature searching and the manuscript writing. All authors have read and approved the final version of the manuscript, and agree with the order of presentation of the authors.

Conflicts of interest: The authors declare no conflicts of interest.

Financial support: None.

Copyright license agreement: The Copyright License Agreement has been signed by all authors before publication.

Plagiarism check: Checked twice by iThenticate.

Peer review: Externally peer reviewed.



 
  References Top

1.
Adaikalakoteswari A, Rema M, Mohan V, Balasubramanyam M (2007) Oxidative DNA damage and augmentation of poly(ADP-ribose) polymerase/nuclear factor-kappa B signaling in patients with Type 2 diabetes and microangiopathy. Int J Biochem Cell Biol 39:1673-1684.  Back to cited text no. 1
    
2.
Aguiar AS, Castro AA, Moreira EL, Glaser V, Santos ARS, Tasca CI, Latini A, Prediger RDS (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: Involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 132:560-567.   Back to cited text no. 2
    
3.
Aguiar AS, Duzzioni M, Remor AP, Tristão FSM, Matheus FC, Raisman-Vozari R, Latini A, Prediger RD (2016) Moderate-intensity physical exercise protects against experimental 6-hydroxydopamine-induced hemiparkinsonism through Nrf2-antioxidant response element pathway. Neurochem Res 41:64-72.   Back to cited text no. 3
    
4.
Alghadir AH, Gabr SA, Aly FA (2015) The effects of four weeks aerobic training on saliva cortisol and testosterone in young healthy persons. J Phys Ther Sci 227:2029-2033.   Back to cited text no. 4
    
5.
Baek SS (2016) Role of exercise on the brain. J Exerc Rehabil 12:380-385.   Back to cited text no. 5
    
6.
Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6-21.   Back to cited text no. 6
    
7.
Castellano CA, Paquet N, Dionne IJ, Imbeault H, Langlois F, Croteau E, Tremblay S, Fortier M, Matte JJ, Lacombe G, Fülöp T, Bocti C, Cunnane SC (2017) A 3-month aerobic training program improves brain energy metabolism in mild Alzheimer’s disease: preliminary results from a neuroimaging study. J Alzheimers Dis 56:1459-1468.   Back to cited text no. 7
    
8.
Chen J, Qin J, Su Q, Liu Z, Yang J (2012) Treadmill rehabilitation treatment enhanced BDNF-TrkB but not NGF-TrkA signaling in a mouse intracerebral hemorrhage model. Neurosci Lett 529:28-32.   Back to cited text no. 8
    
9.
Dabin J, Fortuny A, Pollo SE (2016) Epigenome maintenance in response to DNA damage. Mol Cell 62:712-727.   Back to cited text no. 9
    
10.
de Souza-Pinto NC, Wilson DM, Stevnsner TV, Bohr VA (2008) Mitochondrial DNA, base excision repair and neurodegeneration. DNA Repair (Amst) 7:1098-1109.   Back to cited text no. 10
    
11.
Dumitrescu RG (2018) Early epigenetic markers for precision medicine. Methods Mol Biol 1856:3-17.   Back to cited text no. 11
    
12.
Fernandes J, Arida RM, Gomez-Pinilla F (2017) Physical exercise as an epigenetic modulator of brain plasticity and cognition. Neurosci Biobehav Rev 80:443-456.   Back to cited text no. 12
    
13.
Gluckman PD, Hanson MA, Buklijas T, Low FM, Beedle AS (2009) Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol 5:401-408.   Back to cited text no. 13
    
14.
Gordon BR, McDowell CP, Hallgren M, Meyer JD, Lyons M, Herring MP (2018) Association of efficacy of resistance exercise training with depressive symptoms meta-analysis and meta-regression: Analysis of randomized clinical trials. JAMA Psychiatry 75:566-576.   Back to cited text no. 14
    
15.
Hoeijmakers JHJ (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475-1485.   Back to cited text no. 15
    
16.
Hornberger TA, Farrar RP (2004) Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can J Appl Physiol 29:16-31.   Back to cited text no. 16
    
17.
Hsu CL, Best JR, Davis JC, Nagamatsu LS, Wang S, Boyd LA, Hsiung GR, Voss MW, Eng JJ, Liu-Ambrose T (2018) Aerobic exercise promotes executive functions and impacts functional neural activity among older adults with vascular cognitive impairment. Br J Sports Med 52:184-191.   Back to cited text no. 17
    
18.
Iida T, Furuta A, Nishioka K, Nakabeppu Y, Iwaki T (2002) Expression of 8-oxoguanine DNA glycosylase is reduced and associated with neurofibrillary tangles in Alzheimer’s disease brain. Acta Neuropathol 103:20-25.  Back to cited text no. 18
    
19.
Kim DH, Ko IG, Kim BK, Kim TW, Kim SE, Shin MS, Kim CJ, Kim H, Kim KM, Baek SS (2010) Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav 101:660-665.   Back to cited text no. 19
    
20.
Kim MW, Bang MS, Han TR, Ko YJ, Yoon BW, Kim JH, Kang LM, Lee KM, Kim MH (2005) Exercise increased BDNF and trkB in the contralateral hemisphere of the ischemic rat brain. Brain Res 1052:16-21.   Back to cited text no. 20
    
21.
Kim TW, Choi HH, Chung YR (2016) Treadmill exercise alleviates impairment of cognitive function by enhancing hippocampal neuroplasticity in the high-fat diet-induced obese mice. J Exerc Rehabil 12:156-162.  Back to cited text no. 21
    
22.
Klages-Mundt NL, Li L (2017) Formation and repair of DNA-protein crosslink damage. Sci China Life Sci 60:1065-1076.   Back to cited text no. 22
    
23.
Koltai E, Szabo Z, Atalay M, Boldogh I, Naito H, Goto S, Nyakas C, Radak Z (2010) Exercise alters SIRT1, SIRT6, NAD and NAMPT levels in skeletal muscle of aged rats. Mech Ageing Dev 131:21-28.   Back to cited text no. 23
    
24.
Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, Brooks GA, Ames BN (2000) Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89:21-28.   Back to cited text no. 24
    
25.
Liu W, Sheng H, Xu Y, Liu Y, Lu J, Ni X (2013) Swimming exercise ameliorates depression-like behavior in chronically stressed rats: relevant to proinflammatory cytokines and IDO activation. Behav Brain Res 242:110-116.   Back to cited text no. 25
    
26.
Lovell MA, Markesbery WR (2007) Oxidative DNA damage in mild cognitive impairment and late-stage Alzheimer’s disease. Nucleic Acids Res 35:7497-504.   Back to cited text no. 26
    
27.
Madabhushi R, Pan L, Tsai LH (2014) DNA damage and its links to neurodegeneration. Neuron 83:266-282.   Back to cited text no. 27
    
28.
Manoharan S, Guillemin GJ, Abiramasundari RS, Essa MM, Akbar M, Akbar MD (2016) The role of reactive oxygen species in the pathogenesis of Alzheimer’s disease, Parkinson’s disease, and Huntington’s disease: a mini review. Oxid Med Cell Longev 2016:8590578.  Back to cited text no. 28
    
29.
Marais L, Stein DJ, Daniels WMU (2009) Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 224:587-597.   Back to cited text no. 29
    
30.
Mavros Y, Gates N, Wilson GC, Jain N, Meiklejohn J, Brodaty H, Wen W, Singh N, Baune BT, Suo C, Baker MK, Foroughi N, Wang Y, Sachdev PS, Valenzuela M, Fiatarone Singh MA (2017) Mediation of cognitive function improvements by strength gains after resistance training in older adults with mild cognitive impairment: outcomes of the study of mental and resistance training. J Am Geriatr Soc 65:550-559.   Back to cited text no. 30
    
31.
Nonato LF, Rocha-Vieira E, Tossige-Gomes R, Soares AA, Soares BA, Freitas DA, Oliveira MX, Mendonça VA, Lacerda AC, Massensini AR, Leite HR (2016) Swimming training attenuates oxidative damage and increases enzymatic but not non-enzymatic antioxidant defenses in the rat brain. Braz J Med Biol Res 49:e5310.  Back to cited text no. 31
    
32.
Ogonovszky H, Berkes I, Kumagai S, Kaneko T, Tahara S, Goto S, Radák Z (2005) The effects of moderate-, strenuous- and over-training on oxidative stress markers, DNA repair, and memory, in rat brain. Neurochem Int 46:635-640.   Back to cited text no. 32
    
33.
Özbeyli D, Sarı G, Özkan N, Karademir B, Yüksel M, Çilingir Kaya ÖT, Kasımay Çakır Ö (2017) Protective effects of different exercise modalities in an Alzheimer’s disease-like model. Behav Brain Res 328:159-177.   Back to cited text no. 33
    
34.
Patki G, Solanki N, Atrooz F, Ansari A, Allam F, Jannise B, Maturi J, Salim S (2014) Novel mechanistic insights into treadmill exercise based rescue of social defeat-induced anxiety-like behavior and memory impairment in rats. Physiol Behav 130:135-144.   Back to cited text no. 34
    
35.
Pinho RA, Aguiar AS, Radák Z (2019) Effects of resistance exercise on cerebral redox regulation and cognition: an interplay between muscle and brain. Antioxidants 8:E529.   Back to cited text no. 35
    
36.
Pittaluga M, Sgadari A, Dimauro I, Tavazzi B, Parisi P, Caporossi D (2015) Physical exercise and redox balance in type 2 diabetics: effects of moderate training on biomarkers of oxidative stress and DNA damage evaluated through comet assay. Oxid Med Cell Longev 2015:981242.  Back to cited text no. 36
    
37.
Poewe W, Seppi K, Tanner CM, Halliday GM, Brundin P, Volkmann J, Schrag AE, Lang AE (2017) Parkinson disease. Nat Rev Dis Prim 3:17013.  Back to cited text no. 37
    
38.
Portugal E, Vasconcelos P, Souza R, Lattari E, Monteiro-Junior R, Machado S, Deslandes A (2015) Aging process, cognitive decline and Alzheimer's disease: can strength training modulate these responses? CNS Neurol Disord Drug Targets 14:1209-1213.   Back to cited text no. 38
    
39.
Radák Z, Apor P, Pucsok J, Berkes I, Ogonovszky H, Pavlik G, Nakamoto H, Goto S (2003) Marathon running alters the DNA base excision repair in human skeletal muscle. Life Sci 72:1627-1633.   Back to cited text no. 39
    
40.
Radak Z, Atalay M, Jakus J, Boldogh I, Davies K, Goto S (2009) Exercise improves import of 8-oxoguanine DNA glycosylase into the mitochondrial matrix of skeletal muscle and enhances the relative activity. Free Radic Biol Med 46:238-243.   Back to cited text no. 40
    
41.
Radák Z, Naito H, Kaneko T, Tahara S, Nakamoto H, Takahashi R, Cardozo-Pelaez F, Goto S (2002) Exercise training decreases DNA damage and increases DNA repair and resistance against oxidative stress of proteins in aged rat skeletal muscle. Pflugers Arch 445:273-278.   Back to cited text no. 41
    
42.
Radak Z, Suzuki K, Higuchi M, Balogh L, Boldogh I, Koltai E (2016) Physical exercise, reactive oxygen species and neuroprotection. Free Radic Biol Med 98:187-196.   Back to cited text no. 42
    
43.
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 18:1208-1246.   Back to cited text no. 43
    
44.
Rass U, Ahel I, West SC (2007) Defective DNA repair and neurodegenerative disease. Cell 130:991-1004.   Back to cited text no. 44
    
45.
Ryu JH, Paik IY, Woo JH, Shin KO, Cho SY, Roh HT (2016) Impact of different running distances on muscle and lymphocyte DNA damage in amateur marathon runners. J Phys Ther Sci 28:450-455.   Back to cited text no. 45
    
46.
Shahandeh M, Roshan VD, Hosseinzadeh S, Mahjoub S, Sarkisian V (2013) Chronic exercise training versus acute endurance exercise in reducing neurotoxicity in rats exposed to lead acetate. Neural Regen Res 8:714-722.   Back to cited text no. 46
    
47.
Shin MS, Kim TW, Lee JM, Ji ES, Lim BV (2017) Treadmill exercise alleviates nigrostriatal dopaminergic loss of neurons and fibers in rotenone-induced Parkinson rats. J Exerc Rehabil 13:30-35.   Back to cited text no. 47
    
48.
Siu PM, Pei XM, Teng BT, Benzie IF, Ying M, Wong SH (2011) Habitual exercise increases resistance of lymphocytes to oxidant-induced DNA damage by upregulating expression of antioxidant and DNA repairing enzymes. Exp Physiol 96:889-906.   Back to cited text no. 48
    
49.
Soares JP, Silva AI, Silva AM, Almeida V, Teixeira JP, Matos M, Gaivão I, Mota MP (2015) Effects of physical exercise training in DNA damage and repair activity in humans with different genetic polymorphisms of hOGG1 (Ser326Cys). Cell Biochem Funct 33:519-524.   Back to cited text no. 49
    
50.
Souza MA, Oliveira MS, Furian AF, Rambo LM, Ribeiro LR, Lima FD, Dalla Corte LC, Silva LFA, Retamoso LT, Dalla Corte CL, Puntel GO, de Avila DS, Soares FAA, Fighera MR, de Mello CF, Royes LFF (2009) Swimming training prevents pentylenetetrazol-induced inhibition of Na+, K+-ATPase activity, seizures, and oxidative stress. Epilepsia 50:811-823.   Back to cited text no. 50
    
51.
Souza PS, Gonçalves ED, Pedroso GS, Farias HR, Junqueira SC, Marcon R, Tuon T, Cola M, Silveira PCL, Santos AR, Calixto JB, Souza CT, de Pinho RA, Dutra RC (2017) Physical exercise attenuates experimental autoimmune encephalomyelitis by inhibiting peripheral immune response and blood-brain barrier disruption. Mol Neurobiol 54:4723-4737.   Back to cited text no. 51
    
52.
Speck AE, Fraga D, Soares P, Scheffer DL, Silva LA, Aguiar AS Jr, Estreck EL, Pinho RA (2011) Cigarette smoke inhibits brain mitochondrial adaptations of exercised mice. Neurochem Res 36:1056-1061.   Back to cited text no. 52
    
53.
Tuon T, Souza PS, Santos MF, Pereira FT, Pedroso GS, Luciano TF, Souza CT De, Dutra RC, Silveira PCL, Pinho RA (2015) Physical training regulates mitochondrial parameters and neuroinflammatory mechanisms in an experimental model of Parkinson’s disease. Oxid Med Cell Longev 2015:261809.   Back to cited text no. 53
    
54.
Tuon T, Valvassori SS, Dal Pont GC, Paganini CS, Pozzi BG, Luciano TF, Souza PS, Quevedo J, Souza CT, Pinho RA (2014) Physical training prevents depressive symptoms and a decrease in brain-derived neurotrophic factor in Parkinson’s disease. Brain Res Bull 108:106-112.   Back to cited text no. 54
    
55.
Van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680-8685.   Back to cited text no. 55
    
56.
Vilela TC, Muller AP, Damiani AP, Macan TP, da Silva S, Canteiro PB, de Sena Casagrande A, Pedroso GDS, Nesi RT, de Andrade VM, de Pinho RA (2016) Strength and aerobic exercises improve spatial memory in aging rats through stimulating distinct neuroplasticity mechanisms. Mol Neurobiol 54:7928-7937.  Back to cited text no. 56
    
57.
Yang JL, Lin YT, Chuang PC, Bohr VA, Mattson MP (2014) BDNF and exercise enhance neuronal DNA repair by stimulating CREB-mediated production of apurinic/apyrimidinic endonuclease 1. Neuromolecular Med 16:161-174.   Back to cited text no. 57
    
58.
Yau SY, Li A, Xu A, So KF (2015) Fat cell-secreted adiponectin mediates physical exercise-induced hippocampal neurogenesis: an alternative anti-depressive treatment? Neural Regen Res 10:7-9.  Back to cited text no. 58
    

C-Editors: Zhao M, Li JY; T-Editor: Jia Y


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1]


This article has been cited by
1 Physical Activity and Redox Balance in the Elderly: Signal Transduction Mechanisms
Daniela Galli,Cecilia Carubbi,Elena Masselli,Mauro Vaccarezza,Valentina Presta,Giulia Pozzi,Luca Ambrosini,Giuliana Gobbi,Marco Vitale,Prisco Mirandola
Applied Sciences. 2021; 11(5): 2228
[Pubmed] | [DOI]
2 Cognitive reserve and Alzheimerćs biological continuum: clues for prediction and prevention of dementia
Alessandro MARTORANA,Martina ASSOGNA,Vincenzo DE LUCIA,Caterina MOTTA,Chiara G. BONOMI,Francesca BERNOCCHI,Martina G. DI DONNA,Giacomo KOCH
Minerva Medica. 2021; 112(4)
[Pubmed] | [DOI]
3 The Effect of Eight Weeks of Training on Positive and Negative Slopes with Royal Jelly Consumption on MGMT and ATPase Gene Expression Levels in the Hippocampus Tissue of Trimethyltin-Induced Alzheimer’s Rats
Zahra Giti,Abdolali Banaeifar,Sajad Arshadi,Mohammad Ali Azarbayjani
Gene, Cell and Tissue. 2021; In Press(In Press)
[Pubmed] | [DOI]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  Search Strategy ...Effect of Differ...Effect of Physic...
  In this article
Abstract
Introduction
Conclusion
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed2947    
    Printed161    
    Emailed0    
    PDF Downloaded553    
    Comments [Add]    
    Cited by others 3    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]