Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray

European Journal of Neuroscience

Volumn 16, Issue 6, 2002, Pages 1107-1116

  Molteni, Raffaella ^b   Ying, Zhe ^b   Gómez Pinilla, Fernando ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain derived neurotrophic factor; Exercise; Hippocampus; Microarray; Neuronal plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; COMPLEMENTARY DNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GLUTAMATE DECARBOXYLASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE (CALCIUM,CALMODULIN) II; RNA; SYNAPSIN I; SYNAPTOTAGMIN; SYNTAXIN;

ARTICLE; CONTROLLED STUDY; EXERCISE; GENE EXPRESSION; GENETIC ASSOCIATION; HIPPOCAMPUS; MALE; MOLECULAR BIOLOGY; NERVE CELL PLASTICITY; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBONUCLEASE PROTECTION ASSAY; RNA ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION; GENES, REGULATOR; HIPPOCAMPUS; MALE; MAP KINASE SIGNALING SYSTEM; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYSICAL CONDITIONING, ANIMAL; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SYNAPTIC VESICLES; UP-REGULATION;

EID: 1442316352     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.02158.x     Document Type: Article

References (52)

1. Augustine, G.J. (2001) How does calcium trigger neurotransmitter release? Curr. Opin. Neurobiol., 11, 320-326.
2. Benraiss, A., Chmielnicki, E., Lerner, K., Roh, D. & Goldman, S.A. (2001) Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J. Neurosci., 21, 6718-6731.
3. Black, I.B. (1999) Trophic regulation of synaptic plasticity. J. Neurobiol., 41, 108-118.
4. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G. & Silva, A.J. (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell, 79, 59-68.
5. Corbit, K.C., Foster, D.A. & Rosner, M.R. (1999) Protein kinase C-δ mediates neurogenic but not mitogenic activation of mitogen-activated protein kinase in neuronal cells. Mol. Cell. Biol., 19, 4209-4218.
6. Esclapez, M., Tillakaratne, N.J., Kaufman, D.L., Tobin, A.J. & Houser, C.R. (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci., 14, 1834-1855.
7. Figurov, A., Pozzo-Miller, L.D., Olafsson, P., Wang, T. & Lu, B. (1996) Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature, 381, 706-709.
8. Finkbeiner, S. (2000a) Calcium regulation of the brain-derived neurotrophic factor gene. Cell. Mol. Life Sci., 57, 394-401.
9. Finkbeiner, S. (2000b) CREB couples neurotrophin signals to survival messages. Neuron, 25, 11-14.
10. Finkbeiner, S., Tavazoie, S.F., Maloratsky, A., Jacobs, K.M., Harris, K.M. & Greenberg, M.E. (1997) CREB: A major mediator of neuronal neurotrophin responses. Neuron, 19, 1031-1047.
11. Fordyce, D.E. & Farrar, R.P. (1991) Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav. Brain Res., 46, 123-133.
12. Fukunaga, K. & Miyamoto, E. (2000) A working model of CaM kinase II activity in hippocampal long-term potentiation and memory. Neurosci. Res., 38, 3-17.
13. Gadea, A. & Lopez-Colome', A.M. (2001) Glial transporters for glutamate, glycine and GABA I. Glutamate transporters. J. Neurosci. Res., 63, 453-460.
14. Gomez-Pinilla, F., Dao, L. & So, V. (1997) Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res., 764, 1-8.
15. Grewal, S.S., York, R.D. & Stork, P.J. (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol., 9, 544-553.
16. Gross, C.G. (2000) Neurogenesis in the adult brain: Death of a dogma. Nature Rev. Neurosci., 1, 67-73.
17. Isackson, P.J., Huntsman, M.M., Murray, K.D. & Gall, C.M. (1991) BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: Temporal patterns of induction distinct from NGF. Neuron, 6, 937-948.
18. Jovanovic, J.N., Czernik, A.J., Fienberg, A.A., Greengard, P. & Sihra, T.S. (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nature Neurosci., 3, 323-329.
19. Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H. & Bonhoeffer, T. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA, 92, 8856-8860.
20. Kramer, A.F., Hahn, S., Cohen, N.J., Banich, M.T., McAuley, E., Harrison, C.R., Chason, J., Vakil, E., Bardell, L., Boileau, R.A. & Colcombe, A. (1999) Ageing, fitness and neurocognitive function. Nature, 400, 418-419.
21. Larsson, E., Nanobashvili, A., Kokaia, Z. & Lindvall, O. (1999) Evidence for neuroprotective effects of endogenous brain-derived neurotrophic factor after global forebrain ischemia in rats. J. Cereb. Blood Flow Metab., 19, 1220-1228.
22. Laurin, D., Verreault, R., Lindsay, J., MacPherson, K. & Rockwood, K. (2001) Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch. Neurol., 58, 498-504.
23. Levine, E.S. & Kolb, J.E. (2000) Brain-derived neurotrophic factor increases activity of NR2B-containing N-methyl-D-aspartate receptors in excised patches from hippocampal neurons. J. Neurosci. Res., 62, 357-362.
24. Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K. & Taniguchi, H. (1996) Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem., 271, 21108-21113.
25. Mattson, M.P. (2000) Neuroprotective signaling and the aging brain: Take away my food and let me run. Brain Res., 886, 47-53.
26. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B. & Seeburg, P.H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron, 12, 529-540.
27. Neeper, S.A., Gomez-Pinilla, F., Choi, J. & Cotman, C. (1995) Exercise and brain neurotrophin. Nature, 373, 109.
28. Neeper, S.A., Gomez-Pinilla, F. & Cotman, C. (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res., 726, 49-56.
29. Nguyen, P. & Kandel, E.R. (1996) A macromolecular synthesis-dependent late phase of long-term potentiation required cAMP in the medial perforant pathway of rat hippocampal slices. J. Neurosci., 16, 3189-3198.
30. Norman, K.E., Pepin, A. & Barbeau, H. (1998) Effects of drugs on walking after spinal cord injury. Spinal Cord, 36, 699-715.
31. Patterson, S.L., Abel, T., Deuel, T.A.S., Martin, K.C., Rose, J.C. & Kandel, E.R. (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knock-out mice. Neuron, 16, 1137-1145.
32. Pencea, V., Bingaman, K.D., Wiegand, S.J. & Luskin, M.B. (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci., 21, 6706-6717.
33. Poo, M.-M. (2001) Neurotrophins as a synaptic modulators. Nature Rev. Neurosci., 2, 24-32.
34. Poots, J.T. (2001) Exercise and sensory integration. Role of the nucleus tractus solitarius. Ann. NY Acad. Sci., 940, 221-236.
35. Pozzo-Miller, L.D., Gottschalk, W., Zhang, L., Du McDermott, K.J., Gopalakrishnan, R., Oho, C., Sheng, Z.H. & Lu, B. (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci., 19, 4972-4983.
36. van Praag, H., Kempermann, G. & Gage, F.H. (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci., 2, 266-270.
37. Raineteau, O. & Schwab, M.E. (2001) Plasticity of motor systems after incomplete spinal cord injury. Nature Rev. Neurosci., 2, 263-273.
38. Riva, M.A., Tascedda, F., Lovati, E. & Racagni, G. (1997) Regulation of NMDA receptor subunit messenger RNA levels in the rat brain following acute and chronic exposure to antipsychotic drugs. Brain Res. Mol. Brain Res., 50, 136-142.
39. Riva, M.A., Tascedda, F., Molteni, R. & Racagni, G. (1994) Regulation of NMDA receptor subunit mRNA expression in the rat brain during postnatal development. Brain Res. Mol. Brain Res., 25, 209-216.
40. Rossi, D.J., Oshima, T. & Attwell, D. (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature, 403, 316-321.
41. Rudolph, U., Crestani, F. & Mohler, H. (2001) GABA (A) receptor subtypes: Dissecting their pharmacological functions. Trends Pharmacol. Sci., 22, 188-194.
42. Scheetz, A.J., Nairn, A.C. & Constantine-Paton, M. (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nature Neurosci., 3, 211-216.
43. Segal, R.A. & Greenberg, M.E. (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci., 19, 463-489.
44. Selcher, J.C., Nekrasova, T., Paylor, R., Landreth, G.E. & Sweatt, J. (2001) Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn. Mem., 8, 11-19.
45. Shaywitz, A.J. & Greenberg, M.E. (1999) CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem., 68, 821-861.
46. Silva, A.J., Kogan, J.H., Frankland, P.W. & Kida, S. (1998) CREB and memory. Annu. Rev. Neurosci., 21, 127-148.
47. Soderling, T.R. (2000) CaM-kinases: Modulators of synaptic plasticity. Curr. Opin. Neurobiol., 10, 375-380.
48. Sprengel, R., Suchanek, B., Amico, C., Brusa, R., Burnashev, N., Rozov, A., Hvalby, O., Jensen, V., Paulsen, O., Andersen, P., Kim, J.J., Thompson, R.F., Sun, W., Webster, L.C., Grant, S.G., Eilers, J., Konnerth, A., Li, J., McNamara, J.O. & Seeburg, P.H. (1998) Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell, 92, 279-289.
49. Sweatt, J.D. (2001) The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 76, 1-10.
50. Vaynman, S., Ying, Z. & Gomez-Pinilla, F. (2001) Changes in synaptic plasticity in the hippocampus associated to the action of neurotrophins and exercise. Soc. Neurosci. Abstr., 3, 906.2404.
51. Walton, M., Conno, B., Lawlor, P., Young, D., Sirimanne, E., Gluckman, P., Cole, G. & Dragunow, M. (1999) Neuronal death and survival in two models of hypoxic-ischemic brain damage. Brain Res. Brain Res. Rev., 29, 137-168.
52. Zafra, F., Castren, E., Thoenen, H. & Lindholm, D. (1991) Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl. Acad. Sci. USA, 88, 10037-10041.