The Journal of Physiological Sciences

, Volume 67, Issue 3, pp 387–394 | Cite as

Differential effect of treadmill exercise on histone deacetylase activity in rat striatum at different stages of development

  • Viviane Rostirola Elsner
  • Carla Basso
  • Karine Bertoldi
  • Louisiana Carolina Ferreira de Meireles
  • Laura Reck Cechinel
  • Ionara Rodrigues Siqueira
Original Paper

Abstract

The study described herein aimed to evaluate the impact of exercise on histone acetylation markers in striatum from Wistar rats at different stages of development. Male Wistar rats were submitted to two different exercise protocols: a single session of treadmill (running 20 min) or a moderate daily exercise protocol (running 20 min for 2 weeks). Striata of rats aged 39 days postnatal (adolescents), 3 months (young adults), and 20 months (aged) were used. The single exercise session induced persistent effects on global HDAC activity only in the adolescent group, given that exercised rats showed decreased HDAC activity 1 and 18 h after training, without effect on histone H4 acetylation levels. However, the moderate daily exercise did not alter any histone acetylation marker in adolescent and mature groups in any time point evaluated after training. In sum, our data suggest that exercise impacts striatal HDAC activity in an age- and protocol-dependent manner. Specifically, this response seems to be more evident during the adolescent period and might suffer a molecular adaptation in response to chronic training.

Keywords

Wistar rats Forced exercise Histone deacetylases Striatum Stage of development 

Notes

Acknowledgments

This work was supported, in part, by Grant 476634/2013-0 from Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq/Brazil. CNPq fellowships (Dr. I.R. Siqueira; V.R. Elsner; K. Bertoldi); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES fellowships (L.C. Meireles); Programa de Bolsas de Iniciação Científica—UFRGS (L.R. Cechinel; C.Basso).

References

  1. 1.
    Abel JL, Rissman EF (2013) Running-induced epigenetic and gene expression changes in the adolescent brain. Int J Dev Neurosci 31(6):382–390CrossRefPubMedGoogle Scholar
  2. 2.
    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 72:218–254CrossRefGoogle Scholar
  3. 3.
    Broadbent NJ, Squire LR, Clark RE (2007) Rats depend on habit memory for discrimination learning and retention. Learn Mem 14:145–151CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Brooks GA, White TP (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J App Physiol 45:1009–1015Google Scholar
  5. 5.
    Chandramohan Y, Droste SK, Arthur JS, Reul JM (2008) The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-d-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signalling pathway. Eur J Neurosci 27(10):2701–2713CrossRefPubMedGoogle Scholar
  6. 6.
    de Almeida AA, Gomes da Silva S, Fernandes J, Peixinho-Pena LF, Scorza FA, Cavalheiro EA, Arida RM (2013) Differential effects of exercise intensities in hippocampal BDNF, inflammatory cytokines and cell proliferation in rats during the postnatal brain development. Neurosci Lett 553:1–6CrossRefPubMedGoogle Scholar
  7. 7.
    De Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475CrossRefPubMedGoogle Scholar
  8. 8.
    de Meireles LC, Bertoldi K, Elsner VR, dos Moysés SF, Siqueira IR (2014) Treadmill exercise alters histone acetylation differently in rats exposed or not exposed to aversive learning context. Neurobiol Learn Mem 116:193–196CrossRefPubMedGoogle Scholar
  9. 9.
    Darlington TM, McCarthy RD, Cox RJ, Miyamoto-Ditmon J, Gallego X, Ehringer MA (2016) Voluntary wheel running reduces voluntary consumption of ethanol in mice: identification of candidate genes through striatal gene expression profiling. Genes Brain Behav. 15(5):474–490CrossRefPubMedGoogle Scholar
  10. 10.
    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 192:580–587CrossRefPubMedGoogle Scholar
  11. 11.
    Elsner VR, Lovatel GA, Moysés F, Bertoldi K, Spindler C, Cechinel LR, Muotri AR, Siqueira IR (2013) Exercise induces age-dependent changes on epigenetic parameters in rat hippocampus: a preliminary study. Exp Gerontol 48(2):136–139CrossRefPubMedGoogle Scholar
  12. 12.
    Ferreira AF, Real CC, Rodrigues AC, Alves AS, Britto LR (2010) Moderate exercise changes synaptic and cytoskeletal proteins in motor regions of the rat brain. Brain Res 1361:31–42CrossRefPubMedGoogle Scholar
  13. 13.
    Gaglio D, Capitano F, Mastrodonato A, Minicocci E, Deiana C, Fragapane P et al (2014) Learning induced epigenetic modifications in the ventral striatum are necessary for long-term memory. Behav Brain Res 265:61–68CrossRefPubMedGoogle Scholar
  14. 14.
    Handel AE, Ebers GC, Ramagopalan SV (2010) Epigenetics: molecular mechanisms and implications for disease. Trends Mol Med 16:7–16CrossRefPubMedGoogle Scholar
  15. 15.
    Horn K, Dino G, Branstetter SA, Zhang J, Noerachmanto N, Jarrett T, Taylor M (2011) Effects of physical activity on teen smoking cessation. J Dev Neurosci 31:382–390Google Scholar
  16. 16.
    Kennedy PJ, Robison AJ, Maze I, Feng J, Badimon A, Bassel-Duby R, Olson EN, Nestler EJ (2013) HDAC1 inhibition blocks cocaine-induced plasticity through targeted changes in histone methylation. Nat Neurosci 16:434–440CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, Neve RL, Self DW, Nestler EJ (2008) Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48:303–314CrossRefGoogle Scholar
  18. 18.
    Lovatel GA, Bertoldi K, Elsner VR, Piazza FV, Basso CG et al (2014) Long-term effects of pre and post-ischemic exercise following global cerebral ischemia on astrocyte and microglia functions in hippocampus from Wistar rats. Brain Res 1587:119–126CrossRefPubMedGoogle Scholar
  19. 19.
    Lovatel GA, Elsner VR, Bertoldi K, Vanzella C, dos Moysés SF, Vizuete A, Spindler C, Cechinel LR, Netto CA, Muotri AR, Siqueira IR (2013) Treadmill exercise induces age-related changes in aversive memory, neuroinflammatory and epigenetic processes in the rat hippocampus. Neurobiol Learn Mem 101:94–102CrossRefPubMedGoogle Scholar
  20. 20.
    Monchi O, Petrides M, Petre V, Worsley K, Dagher A (2001) Wisconsin Card Sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. J Neurosci 21:7733–7741PubMedGoogle Scholar
  21. 21.
    Monchi O, Petrides M, Strafella AP, Worsley KJ, Doyon J (2006) Functional role of the basal ganglia in the planning and execution of actions. Ann Neurol 59:257–264CrossRefPubMedGoogle Scholar
  22. 22.
    Owen AM (2004) Cognitive dysfunction in Parkinson’s disease: the role of frontostriatal circuitry. Neuroscientist 10:525–537CrossRefPubMedGoogle Scholar
  23. 23.
    Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65–72CrossRefPubMedGoogle Scholar
  24. 24.
    Pascual M, Do Couto BR, Alfonso-Loeches S, Aguilar MA, Rodriguez-Arias M, Guerri C (2012) Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rat are associated with ethanol-induced place conditioning. Neuropharmacol 62:2309–2319CrossRefGoogle Scholar
  25. 25.
    Saha RN, Pahan K (2006) HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ 13(4):539–550CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Sant’ Anna G, Elsner VR, Moysés F, Cechinel LR, Agustini GL, Siqueira IR (2013) Histone deacetylase activity is altered in brain areas from aged rats. Neurosci Lett 556:152–154CrossRefGoogle Scholar
  27. 27.
    Schilling EA, Aseltine RH Jr, Gore S (2007) Adverse childhood experiences and mental health in young adults: a longitudinal survey. BMC Public Health 7:30CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Shen S, Casaccia-Bonnefil P (2008) Post-translational modifications of nucleosomal histones in oligodendrocyte lineage cells in development and disease. J Mol Neurosci 35:13–22CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Smith MA, Lynch WJ (2011) Exercise as a potential treatment for drug abuse: evidence from preclinical studies. Front Psychiatry 2:82CrossRefPubMedGoogle Scholar
  30. 30.
    Spindler C, Cechinel LR, Basso C, Moysés F, Bertoldi K, Roesler R, Lovatel GA, Elsner VR, Siqueira IR (2014) Treadmill exercise alters histone acetyltransferases and histone deacetylases activities in frontal cortices from wistar rats. Cell Mol Neurobiol 34(8):1097–1101CrossRefPubMedGoogle Scholar
  31. 31.
    Motoike T, Long JM, Tanaka H, Sinton CM, Skach A, Williams SC, Hammer RE, Sakurai T, Yanagisawa M (2016) Mesolimbic neuropeptide W coordinates stress responses under novel environments. Proc Natl Acad Sci USA 113(21):6023–6028CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Physiological Society of Japan and Springer Japan 2016

Authors and Affiliations

  • Viviane Rostirola Elsner
    • 1
    • 2
  • Carla Basso
    • 1
  • Karine Bertoldi
    • 1
  • Louisiana Carolina Ferreira de Meireles
    • 1
  • Laura Reck Cechinel
    • 1
  • Ionara Rodrigues Siqueira
    • 1
    • 3
  1. 1.Programa de Pós-Graduação em Ciências Biológicas: Fisiologia, Universidade Federal do Rio Grande do Sul Porto AlegreBrasil
  2. 2.Programa de Pós Graduação em Biociências e ReabilitaçãoCentro Universitário Metodista-IPAPorto AlegreBrasil
  3. 3.Laboratório de Neuropsicofarmacologia, Departamento de Farmacologia, Instituto de Ciências Básicas da SaúdeUniversidade Federal do Rio Grande do SulPorto AlegreBrasil

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