Skip to main content
SpringerLink
Log in

Treadmill Exercise Alters Histone Acetyltransferases and Histone Deacetylases Activities in Frontal Cortices from Wistar Rats

  • Short Communication
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Studies have pointed out the relationship between neuroprotective exercise effects and epigenetic mechanisms on the hippocampus. Considering the role of frontal cortex on brain functions, we investigated the impact of different exercise protocols on enzymatic system involved with histone acetylation status, histone acetyltransferases (HATs), and histone desacetylases (HDACs) in frontal cortices from Wistar rats. Male Wistar rats aged 3 months were submitted to a single session or a daily running protocol during 2 weeks. The single session enhanced HAT activity, while the moderate daily exercise protocol reduced the HDAC activity. Our results indicate that frontal cortex is susceptible to epigenetic modulation following exercise and that both exercise protocols seem to induce a histone hyperacetylation condition in this brain area.

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

References

  • Abel JL, Rissman EF (2013) Running-induced epigenetic and gene expression changes in the adolescent brain. Int J Dev Neurosci 31(6):382–390

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:218–254

    Article  Google Scholar 

  • Brooks GA, White TP (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J App Physiol 45:1009–1015

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cechetti F, Fochesatto C, Scopel D, Nardin P, Goncalves CA, Netto CA et al (2008) Effect of a neuroprotective exercise protocol on oxidative state and BDNF levels in the rat hippocampus. Brain Res 1188:182–188

    Article  PubMed  CAS  Google Scholar 

  • Choi JK, Howe LJ (2009) Histone acetylation: truth of consequences? Biochem Cell Biol 87:139–150

    Article  PubMed  CAS  Google Scholar 

  • Collins A, Hill LE, Chandramohan Y, Whitcomb D, Droste SK, Reul JMHM (2009) Exercise improves cognitive responses to psychological stress through enhancement of epigenetic mechanisms and gene expression in the dentate gyrus. PLoS One 4:e4330

    Article  PubMed  PubMed Central  Google Scholar 

  • Elsner VR, Lovatel GA, Bertoldi K, Vanzella C, Santos FM, Spindler C, de Almeida EF, Nardin P, Siqueira IR (2011) Effect of different exercise protocols on histone acetyltransferases and histone deacetylases activities in rat hippocampus. Neuroscience 192:580–587

    Article  PubMed  CAS  Google Scholar 

  • Feng J, Fouse S, Fan G (2007) Epigenetic regulation of neural gene expression and neuronal function. Pediatr Res 61(5 Pt 2):58R–63R

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Pinilla F, Zhuang Y, Feng J, Ying Z, Fan G (2011) Exercise impacts brain derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci 33:383–390

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459:55–60

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hopkins ME, Nitecki R, Bucci DJ (2011) Physical exercise during adolescence versus adulthood: differential effects on object recognition memory and brain-derived neurotrophic fator. Neuroscience 194:84–94

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Huang TY, Lin LS, Cho KC, Chen SJ, Kuo YM, Yu L, Wu FS, Chuang JI, Chen HI, Jen CJ (2012) Chronic treadmill exercise in rats delicately alters the Purkinje cell structure to improve motor performance and toxin resistance in the cerebellum. J Appl Physiol 1136:889–895

    Article  Google Scholar 

  • Jiang H, Nucifora FC Jr, Ross CA, DeFranco DB (2003) Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Hum Mol Genet 12:1–12

    Article  PubMed  Google Scholar 

  • Kimura A, Matsubara K, Horikoshi M (2005) A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J Biochem 138:647–662

    Article  PubMed  CAS  Google Scholar 

  • Korzus E, Rosenfeld MG, Mayford M (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42:961–972

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 4:693–705

    Article  Google Scholar 

  • Levenson JM, Sweatt J (2005) Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6:108–118

    Article  PubMed  CAS  Google Scholar 

  • Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26(30):7870–7874

    Article  PubMed  CAS  Google Scholar 

  • Lou SJ, Liu JY, Chang H, Chen PJ (2008) Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats. Brain Res 1210:48–55

    Article  PubMed  CAS  Google Scholar 

  • Lovatel G, Elsner V, Bertoldi K, Vanzella C, Moysés F, Vizuete A, Spindler C, Cechinel L, Netto CA, Muotri A, Siqueira IR (2013) Treadmill exercise induces age-related changes on aversive memory, neuroinflammatory and epigenetic parameters in rat hippocampus. Neurobiol Learn Mem 101:94–102

    Article  PubMed  CAS  Google Scholar 

  • Magistretti PJ, Pellerin L (1996) Cellular bases of brain energy metabolism and their relevance to functional brain imaging: evidence for a prominent role of astrocytes. Cereb Cortex 1:50–61

    Article  Google Scholar 

  • McKinsey TA, Zhang CL, Olson EN (2001) Control of muscle developmentby dueling HATs and HDACs. Curr Opin Genet Dev. 5:497–504

    Article  Google Scholar 

  • McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, Alenghat T (2011) HDAC3 is a critical negative regulator of long-term memory formation. J Neurosci 31(2):764–774

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Miller CA, Sweatt JD (2008) Covalent modification of DNA regulates memory formation. Neuron 59:1051

    Article  CAS  Google Scholar 

  • Ntanasis-Stathopoulos J, Tzanninis JG, Philippou A, Koutsilieris M (2013) Epigenetic regulation on gene expression induced by physical exercise. J Musculoskelet Neuronal Interact 13:133–146

    PubMed  CAS  Google Scholar 

  • Pareja-Galeano H, Sanchis-Gomar F, Garcia-Gimenez JL (2014) Physical exercise and epigenetic modulation: elucidating intricate mechanisms. Sports Med 44:429–436

    Article  PubMed  Google Scholar 

  • Radák Z, Goto S, Tahara S, Kaneco T, Kumagai S, Berkes I, Ogonovszky H (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

    Article  PubMed  Google Scholar 

  • Rando TA, Chang HY (2012) Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148:46–57

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rouaux C, Jokic N, Mbebi C, Boutillier S, Loeffler JP, Boutillier AL (2003) Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J 22:6537–6549

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ryu H, Lee J, Olofsson BA, Mwidau A, Dedeoglu A, Escudero M, Flemington E, Azizkhan-Clifford J, Ferrante RJ, Ratan RR (2003) Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci U S A 100:4281–4286

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Saha RN, Pahan K (2006) HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ 13:539–550

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stankiewicz AM, Swiergiel AH, Lisowski P (2013) Epigenetics of stress adaptations in the brain. Brain Res Bull 98:76–92

    Article  PubMed  CAS  Google Scholar 

  • Stilling RM, Fischer A (2011) The role of histone acetylation in age-associated memory impairment and alzheimer’s disease. Neurobiol Learn Mem 96:19–26

    Article  PubMed  CAS  Google Scholar 

  • Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45

    Article  PubMed  CAS  Google Scholar 

  • Szyf M, McGowan P, Meaney MJ (2008) The social environment and the epigenome. Environ Mol Mutagen 49:46–60

    Article  PubMed  CAS  Google Scholar 

  • Takamatsu Y, Ishida A, Hamakawa M, Tamakoshi k, Jung C, Ishida K (2010) Treadmill running improves motor function and alters dendritic morphology in the striatum after collagenase-induced intracerebral hemorrhage in rats. Brain Res 1355:165–173

    Article  PubMed  CAS  Google Scholar 

  • Vissing J, Andersen M, Diemer NH (1996) Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 4:729–736

    Article  Google Scholar 

  • Wade PA (2001) Methyl CpG-binding proteins and transcriptional repression. Bioessays 23:1131–1137

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Brazilian funding agencies: Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (Dr. I.R. Siqueira; V.R. Elsner; C. Spindler); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES (K. Bertoldi; G.A. Lovatel; F. Moysés); Programa Institucional de Bolsas de Iniciação Científica–PIBIC CNPq-UFRGS (L.R. Cechinel; C.Basso).

Conflict of interest

The authors declare no conflicts of interest.

Limitations

The current study has an important limitation. It was the small sample size, what can difficult extrapolation of the results. Further studies with larger sample sizes could be done to better understand these results.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação Em Ciências Biológicas: Fisiologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil

    Christiano Spindler, Felipe Moysés, Karine Bertoldi, Viviane Rostirola Elsner & Ionara Rodrigues Siqueira

  2. Departamento de Farmacologia, Instituto de Ciências Básicas Da Saúde, Universidade Federal Do Rio Grande Do Sul, Rua Sarmento Leite, 500, Porto Alegre, Rio Grande do Sul, 90050-170, Brazil

    Laura Reck Cechinel, Carla Basso, Rafael Roesler & Ionara Rodrigues Siqueira

  3. Curso de Fisioterapia, Universidade Federal de Santa Catarina, Campus Araranguá, Santa Catarina, Brazil

    Gisele Agustini Lovatel

  4. Programa de Pós Graduação Em Biociências E Reabilitação Do Centro Universitário Metodista Do IPA, Porto Alegre, Rio Grande do Sul, Brazil

    Viviane Rostirola Elsner

  5. Universidade Regional Integrada do Alto Uruguai e das Missões, Campus Erechim, Erechim , Rio Grande do Sul, Brazil

    Felipe Moysés

Authors
  1. Christiano Spindler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Reck Cechinel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carla Basso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Felipe Moysés
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Karine Bertoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rafael Roesler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gisele Agustini Lovatel
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Viviane Rostirola Elsner
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ionara Rodrigues Siqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ionara Rodrigues Siqueira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spindler, C., Cechinel, L.R., Basso, C. et al. Treadmill Exercise Alters Histone Acetyltransferases and Histone Deacetylases Activities in Frontal Cortices from Wistar Rats. Cell Mol Neurobiol 34, 1097–1101 (2014). https://doi.org/10.1007/s10571-014-0096-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-014-0096-z

Keywords

Search

Navigation