Alteration of synaptic activity-regulating genes underlying functional improvement by long-term exposure to an enriched environment in the adult brain

Neurorehabilitation and Neural Repair

Volumn 27, Issue 6, 2013, Pages 561-574

  Lee, Min Young ^a   Yu, Ji Hea ^a,b   Kim, Ji Yeon ^a   Seo, Jung Hwa ^a,b   Park, Eun Sook ^a   Kim, Chul Hoon ^a,b   Kim, Hyongbum ^c   Cho, Sung Rae ^a,b  

^a Yonsei University College of Medicine   (South Korea)

^b Yonsei University   (South Korea)

^c Hanyang University   (South Korea)

Author keywords

enriched environment; gene expression; gene set enrichment analysis; synaptic activity

Indexed keywords

CHLORIDE; DOPAMINE TRANSPORTER; DRD1A PROTEIN; NEUROTRANSMITTER RECEPTOR; OPIATE; P2RY12 PROTEIN; PDYN PROTEIN; PPP1R1B PROTEIN; PROTEIN; SLC6A3 PROTEIN; SODIUM ION; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; BRAIN REGION; COGNITION; CONTROLLED STUDY; DOWN REGULATION; ENVIRONMENTAL ENRICHMENT; GENE CONTROL; GENE EXPRESSION; GENETIC ASSOCIATION; GLOBAL CHANGE; HEMISPHERE; LONG TERM EXPOSURE; MICROARRAY ANALYSIS; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PASSIVE AVOIDANCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAROD TEST; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; STANDARD; SYNAPTIC TRANSMISSION; TASK PERFORMANCE; TREADMILL ERGOMETRY; UPREGULATION; VALIDATION PROCESS; WESTERN BLOTTING; WORKING MEMORY;

ENRICHED ENVIRONMENT; GENE EXPRESSION; GENE SET ENRICHMENT ANALYSIS; SYNAPTIC ACTIVITY;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BRAIN; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ENKEPHALINS; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INTERPERSONAL RELATIONS; MEMORY, SHORT-TERM; MICE; MICE, INBRED ICR; MOTOR ACTIVITY; NEURONAL PLASTICITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN PRECURSORS; RECEPTORS, DOPAMINE D1; RECEPTORS, PURINERGIC P2Y12;

EID: 84878844562     PISSN: 15459683     EISSN: 15526844     Source Type: Journal    
DOI: 10.1177/1545968313481277     Document Type: Article

References (45)

1. Rosenzweig MR, Bennett EL, Hebert M, Morimoto H. Social grouping cannot account for cerebral effects of enriched environments. Brain Res. 1978 ; 153: 563-576
2. Will B, Galani R, Kelche C, Rosenzweig MR. Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol. 2004 ; 72: 167-182
3. Cummins RA, Walsh R, Budtz-Olsen OE, Konstantinos T, Horsfall CR. Environmentally-induced changes in the brains of elderly rats. Nature. 1973 ; 243: 516-518
4. Holloway RL. Dendritic branching: some preliminary results of training and complexity in rat visual cortex. Brain Res. 1966 ; 2: 393-396
5. Branchi I, D'Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psychiatry. 2006 ; 60: 690-696
6. Zhu SW, Yee BK, Nyffeler M, Winblad B, Feldon J, Mohammed AH. Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav Brain Res. 2006 ; 169: 10-20
7. Rossi C, Angelucci A, Costantin L, et al. Brain-derived neurotrophicfactor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci. 2006 ; 24: 1850-1856
8. Staiger JF, Masanneck C, Bisler S, Schleicher A, Zuschratter W, Zilles K. Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of 1a novel environment. Neuroscience. 2002 ; 109: 687-699
9. Mlynarik M, Johansson BB, Jezova D. Enriched environment influences adrenocortical response to immune challenge and glutamate receptor gene expression in rat hippocampus. Ann N Y Acad Sci. 2004 ; 1018: 273-280
10. Williams BM, Luo Y, Ward C, et al. Environmental enrichment: Effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav. 2001 ; 73: 649-658
11. Rosenzweig MR, Beneett EL. Psychobiology of plasticity: Effects of training and experience on brain and behaviour. Behav Brain Res. 1996 ; 78: 57-65
12. Van Praag H, Kempermann G, Gage FH. Neural consequences of environmental enrichment. Nat Rev Neurosci. 2000 ; 1: 191-198
13. Will B, Kelche C. Environmental approaches to recovery of function from brain damage: a review of animal studies (1981-1991). Adv Exp Med Biol. 1992 ; 325: 79-103
14. Stranahan AM, Lee K, Becker KG, et al. Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiol Aging. 2010 ; 31: 1937-1949
15. Rampon C, Jiang CH, Dong H, et al. Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci U S A. 2000 ; 97: 12880-12884
16. Li C, Niu W, Jiang CH, Hu Y. Effects of enriched environment on gene expression and signal pathways in cortex of hippocampal CA1 specific NMDAR1 knockout mice. Brain Res Bull. 2007 ; 71: 568-577
17. Jiwa NS, Garrard P, Hainsworth AH. Experimental models of vascular dementia and vascular cognitive impairment: a systematic review. J Neurochem. 2010 ; 115: 814-828
18. Yamamoto Y, Shioda N, Han F, et al. Nobiletin improves brain ischemia-induced learning and memory deficits through stimulation of CaMKII and CREB phosphorylation. Brain Res. 2009 ; 27: 218-229
19. Na HN, Kim H, Nam JH. Novel genes and cellular pathways related to infection and adenovirus-36 as an obesity agent in human mesenchymal stem cells. Int J Obes (Lond). 2012 ; 36: 195-200
20. Kim H, Cho HJ, Kim SW, et al. CD31+ cells represent highly angiogenic and vasculogenic cells in bone marrow: novel role of nonendothelial CD31+ cells in neovascularization and their therapeutic effects on ischemic vascular disease. Circ Res. 2010 ; 107: 602-614
21. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005 ; 102: 15545-15550
22. Werme M, Thorén P, Olson L, Brené S. Running and cocaine both upregulate dynorphin mRNA in medial caudate putamen. Eur J Neurosci. 2000 ; 12: 2967-2974
23. Stagg NJ, Mata HP, Ibrahim MM, et al. Regular exercise reverses sensory hypersensitivity in a rat neuropathic pain model: role of endogenous opioids. Anesthesiology. 2011 ; 114: 940-948
24. Boecker H, Sprenger T, Spilker ME, et al. The runner's high: opioidergic mechanisms in the human brain. Cereb Cortex. 2008 ; 18: 2523-2531
25. Neves SR, Ram PT, Iyenger R. G protein pathways. Science. 2002 ; 31: 1636-1639
26. Contractor A, Swanson GT, Sailer A, O'Gorman S, Heinemann SF. Identification of the kainite receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci. 2000 ; 15: 8269-8278
27. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience. 2002 ; 111: 815-835
28. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1998 ; 386: 493-495
29. Ueda S, Sakakibara S, Yoshimoto K. Effect of long-lasting serotonin depletion on environmental enrichment-induced neurogenesis in adult rat hippocampus and spatial learning. Neuroscience. 2005 ; 135: 395-402
30. Page G, Peeters M, Najimi M, Maloteaux JM, Hermans E. Modulation of the neuronal dopamine transporter activity by the metabotropic glutamate receptor mGluR5 in rat striatal synaptosomes through phosphorylation mediated processes. J Neurochem. 2001 ; 76: 1282-1290
31. Jaber M, Dumartin B, Sagne C, et al. Differential regulation of tyrosine hydroxylase in the basal ganglia of mice lacking the dopamine transporter. Eur J Neurosci. 1999 ; 11: 3499-3511
32. Fauchey V, Jaber M, Caron MG, Bloch B, Le Moine C. Differential regulation of the dopamine D1, D2 and D3 receptor gene expression and changes in the phenotype of the striatal neurons in mice lacking the dopamine transporter. Eur J Neurosci. 2000 ; 12: 19-26
33. Konradi C, Cole RL, Heckers S, Hyman SE. Amphetamine regulates gene expression in rat striatum via transcription factor CREB. Neuroscience. 1994 ; 14: 5623-5634
34. Kempermann G, Kuhn HG, Gage FH. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci. 1998 ; 18: 3206-3212
35. Vivar C, Potter MC, van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci. :
36. Johansson BB, Ohlsson AL. Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Exp Neurol. 1996 ; 139: 322-327
37. Fernandez E, Schiappa R, Girault JA, Le Novère N. DARPP-32 is a robust integrator of dopamine and glutamate signals. PLoS Comput Biol. 2006 ; 2: 1619-1633
38. Meyer-Lindenberg A, Straub RE, Lipska BK, et al. Genetic evidence implicating DARPP-32 in human frontostriatal structure, function, and cognition. J Clin Invest. 2007 ; 111: 672-682
39. Burnstock G. Potential therapeutic targets in the rapidly expanding field of purinergic signaling. Clin Med. 2002 ; 2: 45-53
40. Sasaki Y, Hoshi M, Akazawa C, et al. Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia. 2003 ; 44: 242-250
41. Rometo AM, Rance NE. Changes in prodynorphin gene expression and neuronal morphology in the hypothalamus of postmenopausal women. J Neuroendocrinol. 2008 ; 20: 1376-1381
42. Candeletti S, Lopetuso G, Cannarsa R, Cavina C, Romualdi P. Effects of prolonged treatment with the opiate tramadol on prodynorphin gene expression in rat CNS. J Mol Neurosci. 2006 ; 30: 341-347
43. Romualdi P, Donatini A, Capobianco A, Ferri S. Methamphetamine alters prodynorphin gene expression and dynorphin A levels in rat hypothalamus. Eur J Pharmacol. 1999 ; 365: 183-186
44. Nader J, Claudia C, Rawas RE, et al. Loss of environmental enrichment increases vulnerability to cocaine addiction. Neuropsychopharmacology. 2012 ; 37: 1579-1587
45. Puhl MD, Blum JS, Acosta-Torres S, Grigson PS. Environmental enrichment protects against the acquisition of cocaine self-administration in adult male rats, but does not eliminate avoidance of a drug-associated saccharin cue. Behav Pharmacol. 2012 ; 23: 43-53