Effect of treadmill running on the expression of genes that are involved in neuronal differentiation in the hippocampus of adult male rats

Cell Biology International

Volumn 37, Issue 4, 2013, Pages 276/a-283/a

  Mojtahedi, Shima ^a   Kordi, Mohammad Reza ^a   Hosseini, Seyed Ebrahim ^b   Omran, Simin Fallah ^a   Soleimani, Masoud ^c,d  

^a UNIVERSITY OF TEHRAN   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c TARBIAT MODARES UNIVERSITY   (Iran)

^d STEM CELL TECHNOLOGY RESEARCH CENTER   (Iran)

Author keywords

BDNF; Hippocampus; miR 124; NRSF REST; Treadmill running; TrkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MICRORNA 124; NEURON RESTRICTIVE SILENCER FACTOR; RE1 SILENCING TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MICRORNA; MIRN124 MICRORNA, RAT; RE1-SILENCING TRANSCRIPTION FACTOR; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXERCISE INTENSITY; GENE EXPRESSION; HIPPOCAMPUS; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; REST GENE; RPL26 GENE; TREADMILL EXERCISE; ANIMAL; ANIMAL EXPERIMENT; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; RUNNING; WISTAR RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; GENE EXPRESSION; HIPPOCAMPUS; MALE; MICRORNAS; NEURONS; PHYSICAL CONDITIONING, ANIMAL; RATS, WISTAR; RECEPTOR, TRKB; REPRESSOR PROTEINS; RUNNING;

EID: 84875328174     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1002/cbin.10022     Document Type: Article

References (64)

1. Aoki C,Wu K, Elste A, Len G, Lin S, McAuliffe G, Black IB (2000) Localization of brain-derived neurotrophic factor and TrkB receptors to postsynaptic densities of adult rat cerebral cortex. J Neurosci Res 59: 454-63.
2. Balkowiec A, Katz DM (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22: 10399-407.
3. Béquet F, Gomez-Merino D, Berthelot M, Guezennec CY (2001) Exercise induced changes in brain glucose and serotonin revealed by microdialysis in rat hippocampus: effect of glucose supplementation. Acta Physiol Scand 173: 223-30.
4. Briones TL, Suh E, Hattar H, Wadowska M (2005) Dentate gyrus neurogenesis after cerebral ischemia and behavioral training. Biol Res Nurs 6: 167-79.
5. Calderone A, Jover T, Noh KM, Tanaka H, Yokota H, Lin Y, Grooms SY, Regis R, Bennett MV, Zukin RS (2003) Ischemic insults derepress the gene silencer REST in neurons destined to die. J Neurosci 23: 2112-21.
6. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DW, Yong D, During MJ (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827-35.
7. Chandrasekar V, Dreyer JL (2009) microRNAsmiR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol Cell Neurosci 42: 350-62.
8. Chandrasekar V, Dreyer JL (2011) Regulation of MiR-124, Let-7d, and MiR-181a in the accumbens affects the expression, extinction, and reinstatement of cocaine-induced conditioned place preference. Neuropsychopharmacology 36: 1149-64.
9. Chen MJ, Russo-Neustadt AA (2009) Running exercise-induced up-regulation of hippocampal brain-derived neurotrophic factor is CREB-dependent. Hippocampus 19: 962-72.
10. Cheng L, Pastrana E, Tavazoie M, Doetsch D (2009) miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12: 399-408.
11. Chong JA, Tapia-Ramirez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80: 949-57.
12. Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103: 2422-7.
13. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30: 464-72.
14. Dash PK, Mach SA, Moore AN (2001) Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J Neurosci Res 63: 313-9.
15. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, Palmer TD (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18: 2803-12.
16. Fabel K, Wolf SA, Ehninger D, Babu H, Leal-Galiciaand P, Kempermann G (2009) Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurogenesis 10: 30-50.
17. Fayard B, Loeffler S, Weis J, Vögelin E, Krüttgen A (2005) The secreted brain-derived neurotrophic factor precursor pro-BDNF binds to TrkB and p75NTR but not to TrkA or TrkC. J Neurosci Res 80: 18-28.
18. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST, Ray J (1995) Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci 92: 11879-83.
19. Gomez-Merino D, B́quet F, Berthelot M, Chennaoui M, Guezennec CY (2001) Site-dependent effects of an acute intensive exercise on extracellular 5-HTand 5-HIAA levels in rat brain. Neurosci Lett 301: 143-6.
20. Greenway DJ, Street M, Jeffries A, Buckley NJ (2007) RE1 silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells. Stem Cells 25: 354-63.
21. Grimes JA, Nielsen SJ, Battaglioli E, Miska EA, Speh JC, Berry DL, Atouf F, Holdener BC, Mandel G, Kouzarides T (2000) The corepressor mSin3A is a functional component of the RESTCoREST repressor complex. J Biol Chem 275: 9461-7.
22. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after-high-frequency stimulation of glutamatergic synapses. EMBO J 20: 5887-97.
23. Hennigan A, O'Callaghan RM, Kelly AM (2007) Neurotrophins and their receptors: roles in plasticity, neurodegeneration and neuroprotection. Biochem Soc Trans 35: 424-7.
24. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Ann Rev Neurosci 24: 677-736.
25. Huang AM, Jen CJ, Chen HF, Yu L, Kuo YM, Chen HI (2006) Compulsive exercise acutely upregulates rat hippocampal brainderived neurotrophic factor. J Neural Transm 113: 803-11.
26. Itoh T, Imano M, Nishida S, Tsubaki M, Hashimoto S, Ito A, Satou T (2010) Exercise inhibits neuronal apoptosis and improves cerebral function following rat traumatic brain injury. J Neural Transm 118: 1263-72.
27. Kapsimali M, Kloosterman WP, de Bruijn E, Rosa F, Plasterk RHA, Wilson SW (2007) MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol 8: R173.
28. Ke Z, Yip SP, Li L, Zheng XX, Tong KY (2011) The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia mode. PLoS ONE 6: e16643.
29. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-5.
30. Kerniea SG, Parent JM (2010) Forebrain neurogenesis after focal ischemic and traumatic brain injury. Neurobiol Dis 37: 267-74.
31. Khabour OF, Alzoubi KH, Alomari MA, Alzubi MA (2009) Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus 20: 637-45.
32. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9: 1274-81.
33. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS (2006) Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24: 857-64.
34. Kronenberg G, Bick-Sander A, Bunk E, Wolf C, Ehninger D, Kempermann G (2006) Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol Aging 27: 1505-13.
35. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-33.
36. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12: 735-9.
37. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
38. Lin SY, Wu K, Levine ES, Mount HTJ, Suen PC, Black IB (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Mol Brain Res 55: 20-7.
39. Liu YF, Chen HI, Wu CL, Kuo YM, Yu L, Huang AM, Wu FS, Chuang JI, Jen CJ (2009) Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol 587: 3221-31.
40. Llorens-Martín M, Torres-Alemán I, Trejo JL (2006) Pronounced individual variation in the response to the stimulatory action of exercise on immature hippocampal neurons. Hippocampus 16: 480-90.
41. 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.
42. Makeyev EV, Zhang JW, Carrasco MA, Maniatis T (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27: 435-48.
43. Mehler MF (2008) Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol 86: 305-41.
44. Mulligan P,Westbrook TF, Ottinger M, Pavlova N, Chang B, Macia E, Shi YJ, Barretina J, Liu J, Howley PM, Elledge SJ, Shi Y (2008) CDYL bridges REST and histone methyltransferases for gene repression and suppression of cellular transformation. Mol Cell 32: 718-26.
45. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726: 49-56.
46. Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntingtons disease. J Neurosci 28: 14341-6.
47. Ramsbottom R, Currie J, Gilder M (2010) Relationships between components of physical activity, cardiorespiratory fitness, cardiac autonomic health, and brain-derived neurotrophic factor. J Sports Sci 28: 843-9.
48. Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V (2004) Expression profiling of mammalian micro-RNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5: R13.
49. Shimojo M, Hersh LB (2004) Regulation of the cholinergic gene locus by the repressor element-1 silencing transcription factor/ neuron restrictive silencer factor (REST/NRSF). Life Sci 74: 2213-25.
50. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wul-czyn FG (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21: 1469-77.
51. Soya H, Nakamura T, Deocaris CC, Kimpara A, Iimura M, Fujikawa T, Chang H, McEwen BS, Nishijima T (2007) BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 358: 961-7.
52. Suen PC, Wu K, Levine ES, Mount HTJ, Xu JL, Lin SY, Black IB (1997) Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-D-aspartate receptor subunit 1. Proc Natl Acad Sci USA 94: 8191-5.
53. Uda M, Ishido M, Kami K, Masuhara M (2006) Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain Res 1104: 64-72.
54. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20: 515-24.
55. Van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266-70.
56. Van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25: 8680-5.
57. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20: 2580-90.
58. Vaynman S, Ying Z, Yin D, Gomez-Pinilla F (2006) Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res 1070: 124-30.
59. Widenfalk J, Olson L, Thoŕn P (1999) Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain. Neurosci Res 34: 125-32.
60. Wu K, Xu JL, Suen PC, Levine ES, Huang Y, Mount HTJ, Lin SY, Black IB (1996) Functional trkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density. Mol Brain Res 4: 286-90.
61. Wu CW, Chang YT, Yu L, Chen H, Jen CJ,Wu SY, Lo CP, Kuo YM (2008) Exercise enhances the proliferation of neural stem cells and neurite growth and survival of neuronal progenitor cells in dentate gyrus of middle-aged mice. J Appl Physiol 105: 1585-94.
62. Yoon BC, Kim MY, Byun YG, Ha SY, Han BS, You JH, Kim CJ (2009) Long-term treadmill exercise-induced neuroplasticity and associated memory recovery of streptozotocin-induced diabetic rats: an experimenter blind, randomized controlled study. NeuroRehabilitation 24: 291-7.
63. Zuccato C, Tartari M, Crotti A, Goffredo D, Valenza M, Conti L, Cataudella T, Leavitt BR, Hayden MR, Timmusk T, Rigamonti D, Cattaneo E (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat Genet 35: 76-83.
64. Zuccato C, Belyaev N, Conforti P, Ooi L, Tartari M, Papadimou E, MacDonald M, Fossale E, Zeitlin S, Buckley N, Cattaneo E (2007) Widespread disruption of repressor element-1silencing transcription factor/neuron-restrictive silencer factor occupancy at its target genes inHuntingtons disease. JNeurosci 27: 6972-83.