BDNF-stimulated intracellular signalling mechanisms underlie exercise-induced improvement in spatial memory in the male Wistar rat

Behavioural Brain Research

Volumn 275, Issue , 2014, Pages 297-306

  Bechara, Ranya G ^a,b   Lyne, Ronan ^a   Kelly, Áine M ^a,b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Brain derived neurotrophic factor; Dentate gyrus; Exercise; Spatial learning; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; SYNAPSIN I; BROXURIDINE; MESSENGER RNA; POTASSIUM CHLORIDE; SYNAPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIVISION; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVATION; EXERCISE; INTRACELLULAR SIGNALING; MALE; MENTAL PERFORMANCE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; SITTING; SPATIAL LEARNING; SPATIAL MEMORY; TASK PERFORMANCE; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELL DIVISION; DENTATE GYRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; PHYSICAL CONDITIONING, ANIMAL; POTASSIUM CHLORIDE; RATS; RATS, WISTAR; RECEPTOR, TRKB; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; SYNAPSINS;

EID: 84908207390     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.11.015     Document Type: Article

References (50)

1. Pang T.Y., Hannan A.J. Enhancement of cognitive function in models of brain disease through environmental enrichment and physical activity. Neuropharmacology 2013, 64:515-528.
2. Vaynman S., Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair 2005, 19:283-295.
3. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
4. Gomez-Pinilla F., Vaynman S., Ying Z. Brain-derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition. Eur J Neurosci 2008, 28:2278-2287.
5. Farmer J., Zhao X., van Praag H., Wodtke K., Gage F.H., Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004, 124:71-79.
6. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20:2580-2590.
7. Bekinschtein P., Oomen C.A., Saksida L.M., Bussey T.J. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable. Semin Cell Dev Biol 2011, 22:536-542.
8. Alonso M., Bekinschtein P., Cammarota M., Vianna M.R., Izquierdo I., Medina J.H. Endogenous BDNF is required for long-term memory formation in the rat parietal cortex. Learn Mem 2005, 12:504-510.
9. Bekinschtein P., Cammarota M., Katche C., Slipczuk L., Rossato J.I., Goldin A., et al. BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A 2008, 105:2711-2716.
10. Hall J., Thomas K.L., Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 2000, 3:533-535.
11. Bramham C.R., Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 2005, 76:99-125.
12. Cunha C., Brambilla R., Thomas K.L. A simple role for BDNF in learning and memory?. Front Mol Neurosci 2010, 3:1.
13. Sweatt J.D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 2001, 76:1-10.
14. Davis S., Laroche S. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes Brain Behav 2006, 5(Suppl 2):61-72.
15. Peng S., Zhang Y., Zhang J., Wang H., Ren B. ERK in learning and memory: a review of recent research. Int J Mol Sci 2010, 11:222-232.
16. Griffin E.W., Bechara R.G., Birch A.M., Kelly A.M. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus 2009, 19:973-980.
17. Bechara R.G., Kelly A.M. Exercise improves object recognition memory and induces BDNF expression and cell proliferation in cognitively enriched rats. Behav Brain Res 2013.
18. van Praag H. Neurogenesis and exercise: past and future directions. Neuromolecular Med 2008, 10:128-140.
19. Paxinos G, Watson C. The Rat Brain in Stereotactic Coordinates 2004.
20. Margoliash E. Primary structure and evolution of cytochrome C. Proc Natl Acad Sci U S A 1963, 50:672-679.
21. Gooney M., Messaoudi E., Maher F.O., Bramham C.R., Lynch M.A. BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol Aging 2004, 25:1323-1331.
22. Messaoudi E., Ying S.W., Kanhema T., Croll S.D., Bramham C.R. Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 2002, 22:7453-7461.
23. Haan E.A., Bowen D.M. Protection of neocortical tissue prisms from freeze-thaw injury by dimethyl sulphoxide. J Neurochem 1981, 37:243-246.
24. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
25. Gobbo O.L., O'Mara S.M. Exercise, but not environmental enrichment, improves learning after kainic acid-induced hippocampal neurodegeneration in association with an increase in brain-derived neurotrophic factor. Behav Brain Res 2005, 159:21-26.
26. Christie B.R., Swann S.E., Fox C.J., Froc D., Lieblich S.E., Redila V., et al. Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci 2005, 21:1719-1726.
27. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007, 30:464-472.
28. Soya H., Nakamura T., Deocaris C.C., Kimpara A., Iimura M., Fujikawa T., et al. BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 2007, 358:961-967.
29. Groves-Chapman J.L., Murray P.S., Stevens K.L., Monroe D.C., Koch L.G., Britton S.L., et al. Changes in mRNA levels for brain-derived neurotrophic factor after wheel running in rats selectively bred for high- and low-aerobic capacity. Brain Res 2011, 1425:90-97.
30. Russo-Neustadt A.A., Beard R.C., Huang Y.M., Cotman C.W. Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 2000, 101:305-312.
31. Neeper S.A., Gomez-Pinilla F., Choi J., Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 1996, 726:49-56.
32. Thomas K., Davies A. Neurotrophins: a ticket to ride for BDNF. Curr Biol 2005, 15:R262-R264.
33. Jovanovic J.N., Czernik A.J., Fienberg A.A., Greengard P., Sihra T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 2000, 3:323-329.
34. Bergami M., Santi S., Formaggio E., Cagnoli C., Verderio C., Blum R., et al. Uptake and recycling of pro-BDNF for transmitter-induced secretion by cortical astrocytes. J Cell Biol 2008, 183:213-221.
35. Matsumoto T., Rauskolb S., Polack M., Klose J., Kolbeck R., Korte M., et al. Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 2008, 11:131-133.
36. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003, 72:609-642.
37. Minichiello L. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 2009, 10:850-860.
38. Murer M.G., Yan Q., Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 2001, 63:71-124.
39. Zheng F., Luo Y., Wang H. Regulation of brain-derived neurotrophic factor-mediated transcription of the immediate early gene Arc by intracellular calcium and calmodulin. J Neurosci Res 2009, 87:380-392.
40. Saarelainen T., Vaittinen S., Castren E. trkB-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell Mol Neurobiol 2001, 21:429-435.
41. Kelly A., Laroche S., Davis S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 2003, 23:5354-5360.
42. Shupliakov O., Haucke V., Pechstein A. How synapsin I may cluster synaptic vesicles. Semin Cell Dev Biol 2011, 22:393-399.
43. Kim S.H., Kim H.B., Jang M.H., Lim B.V., Kim Y.J., Kim Y.P., et al. Treadmill exercise increases cell proliferation without altering of apoptosis in dentate gyrus of Sprague-Dawley rats. Life Sci 2002, 71:1331-1340.
44. Uda M., Ishido M., Kami K., Masuhara M. Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat. Brain Res 2006, 1104:64-72.
45. Van der Borght K., Kobor-Nyakas D.E., Klauke K., Eggen B.J., Nyakas C., Van der Zee E.A., et al. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009, 19:928-936.
46. Snyder J.S., Choe J.S., Clifford M.A., Jeurling S.I., Hurley P., Brown A., et al. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 2009, 29:14484-14495.
47. Ehninger D., Kempermann G. Neurogenesis in the adult hippocampus. Cell Tissue Res 2008, 331:243-250.
48. Cirulli F., Berry A., Chiarotti F., Alleva E. Intrahippocampal administration of BDNF in adult rats affects short-term behavioral plasticity in the Morris water maze and performance in the elevated plus-maze. Hippocampus 2004, 14:802-807.
49. Yan Q., Rosenfeld R.D., Matheson C.R., Hawkins N., Lopez O.T., Bennett L., et al. Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 1997, 78:431-448.
50. Bekinschtein P., Cammarota M., Izquierdo I., Medina J.H. BDNF and memory formation and storage. Neuroscientist 2008, 14:147-156.