Spatial memory training modifies the expression of brain-derived neurotrophic factor tyrosine kinase receptors in young and aged rats

Neuroscience

Volumn 146, Issue 3, 2007, Pages 962-973

  Silhol, M ^a,b,c   Arancibia, S ^a,b,c   Maurice, T ^a,b,c   Tapia Arancibia, L ^a,b,c  

^a UNIV MONTPELLIER   (France)

^b INSERM   (France)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

hippocampus; Morris water maze; proBDNF; trkB.FL mRNA; trkB.T1 mRNA; Wistar rats

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR FULL LENGTH CATALYTIC RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; MESSENGER RNA; PROTEIN PRECURSOR; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; IN SITU HYBRIDIZATION; LATENT PERIOD; LEARNING; MALE; MAZE TEST; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN MODIFICATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPATIAL MEMORY; TRAINING;

AGING; ANIMALS; BLOTTING, WESTERN; DNA; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIPPOCAMPUS; IMMUNOASSAY; IN SITU HYBRIDIZATION; MAZE LEARNING; RATS; RATS, WISTAR; RECEPTOR, TRKB; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 34247892268     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.02.013     Document Type: Article

References (78)

1. Adlard P.A., Perreau V.M., and Cotman C.W. The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol Aging 26 (2005) 511-520
2. Agirregoitia N., Irazusta A., Ruiz F., Irazusta J., and Gil J. Ontogeny of soluble and particulate prolyl endopeptidase activity in several areas of the rat brain and in the pituitary gland. Dev Neurosci 25 (2003) 316-323
3. Armanini M.P., McMahon S.B., Sutherland J., Shelton D.L., and Phillips H.S. Truncated and catalytic isoforms of trkB are co-expressed in neurons of rat and mouse CNS. Eur J Neurosci 7 (1995) 1403-1409
4. Barnes C.A. Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17 (1994) 13-18
5. Baxter G.T., Radeke M.J., Kuo R.C., Makrides V., Hinkle B., Hoang R., Medina-Selby A., Coit D., Valenzuela P., and Feinstein S.C. Signal transduction mediated by the truncated trkB receptor isoforms, trkB. T1 and trkB.T2. J Neurosci 17: (1997) 2683-2690
6. Baynes J.W. The role of AGEs in aging: causation or correlation. Exp Gerontol 36 (2001) 1527-1537
7. Beal M.F. Oxidatively modified proteins in aging and disease. Free Radic Biol Med 32 (2002) 797-803
8. Bernath E., Kupina N., Liu M.C., Hayes R.L., Meegan C., and Wang K.K. Elevation of cytoskeletal protein breakdown in aged Wistar rat brain. Neurobiol Aging 27 (2006) 624-632
9. Biffo S., Offenhauser N., Carter B.D., and Barde Y.A. Selective binding and internalisation by truncated receptors restrict availability of BDNF during development. Development 121 (1995) 2461-2470
10. Burke S.N., and Barnes C.A. Neural plasticity in the ageing brain. Nat Rev Neurosci 7 (2006) 30-40
11. Cirulli F., Berry A., Chiarotti F., and 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 14 (2004) 802-807
12. Connor B., and Dragunow M. The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res Rev 27 (1998) 1-39
13. Cotman C.W., and Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25 (2002) 295-301
14. Croll S.D., Ip N.Y., Lindsay R.M., and Wiegand S.J. Expression of BDNF and trkB as a function of age and cognitive performance. Brain Res 812 (1998) 200-208
15. Eide F.F., Vining E.R., Eide B.L., Zang K.L., Wang X.Y., and Reichardt L.F. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16 (1996) 3123-3129
16. Elgersma Y., and Silva A.J. Molecular mechanisms of synaptic plasticity and memory. Curr Opin Neurobiol 9 (1999) 209-213
17. Erickson C.A., and Barnes C.A. The neurobiology of memory changes in normal aging. Exp Gerontol 38 (2003) 61-69
18. Fayard B., Loeffler S., Weis J., Vogelin E., and Kruttgen A. The secreted brain-derived neurotrophic factor precursor pro-BDNF binds to TrkB and p75NTR but not to TrkA or TrkC. J Neurosci Res 80 (2005) 18-28
19. Fischer W., Sirevaag A., Wiegand S.J., Lindsay R.M., and Bjorklund A. Reversal of spatial memory impairments in aged rats by nerve growth factor and neurotrophins 3 and 4/5 but not by brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 91 (1994) 8607-8611
20. Fryer R.H., Kaplan D.R., and Kromer L.F. Truncated trkB receptors on nonneuronal cells inhibit BDNF-induced neurite outgrowth in vitro. Exp Neurol 148 (1997) 616-627
21. Gicquiaux H., Lecat S., Gaire M., Dieterlen A., Mely Y., Takeda K., Bucher B., and Galzi J.L. Rapid internalization and recycling of the human neuropeptide Y Y(1) receptor. J Biol Chem 277 (2002) 6645-6655
22. Gooney M., Messaoudi E., Maher F.O., Bramham C.R., and Lynch M.A. BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol Aging 25 (2004) 1323-1331
23. Gorski J.A., Balogh S.A., Wehner J.M., and Jones K.R. Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 121 (2003) 341-354
24. Goutan E., Marti E., and Ferrer I. BDNF, and full length and truncated TrkB expression in the hippocampus of the rat following kainic acid excitotoxic damage. Evidence of complex time-dependent and cell-specific responses. Mol Brain Res 59 (1998) 154-164
25. Haapasalo A., Koponen E., Hoppe E., Wong G., and Castren E. Truncated trkB.T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival. Biochem Biophys Res Commun 280 (2001) 1352-1358
26. Haapasalo A., Sipola L., Larsson K., Akerman K.E.O., Stoilov P., Stamm S., Wong G., and Castren E. Regulation of TrkB surface expression by brain-derived neurotrophic factor and truncated TrkB isoforms. J Biol Chem 277 (2002) 43160-43167
27. Hall J., Thomas K.L., and Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3 (2000) 533-535
28. Jarrard L.E. What does the hippocampus really do?. Behav Brain Res 71 (1995) 1-10
29. Katoh-Semba R., Takeuchi I.K., Semba R., and Kato K. Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 69 (1997) 34-42
30. Klein R., Conway D., Parada L.F., and Barbacid M. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61 (1990) 647-656
31. Klein R., Parada L.F., Coulier F., and Barbacid M. trkB, A novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J 8 (1989) 3701-3709
32. Koponen E., Lakso M., and Castren E. Overexpression of the full-length neurotrophin receptor trkB regulates the expression of plasticity-related genes in mouse brain. Mol Brain Res 130 (2004) 81-94
33. Koponen E., Voikar V., Riekki R., Saarelainen T., Rauramaa T., Rauvala H., Taira T., and Castren E. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLC gamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 26 (2004) 166-181
34. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., and Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92 (1995) 8856-8860
35. Korte M., Staiger V., Griesbeck O., Thoenen H., and Bonhoeffer T. The involvement of brain-derived neurotrophic factor in hippocampal long-term potentiation revealed by gene targeting experiments. J Physiol (Lond) 90 (1996) 157-164
36. Kovalchuk Y., Hanse E., Kafitz K.W., and Konnerth A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295 (2002) 1729-1734
37. Lapchak P.A., Araujo D.M., Beck K.D., Finch C.E., Johnson S.A., and Hefti F. BDNF and trkB mRNA expression in the hippocampal formation of aging rats. Neurobiol Aging 14 (1993) 121-126
38. Levine R.L. Carbonyl modified proteins in cellular regulation, aging, and disease. Free Radic Biol Med 32 (2002) 790-796
39. Lewin G.R., and Barde Y.A. Physiology of the neurotrophins. Annu Rev Neurosci 19 (1996) 289-317
40. Lindvall O., Kokaia Z., Bengzon J., Elmér E., and Kokaia M. Neurotrophins and brain insults. Trends Neurosci 17 (1994) 490-496
41. Ma Y.L., Wang H.L., Wu H.C., Wei C.L., and Lee E.H.Y. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82 (1998) 957-967
42. McAllister A.K., Katz L.C., and Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22 (1999) 295-318
43. Michalski B., and Fahnestock M. Pro-brain-derived neurotrophic factor is decreased in parietal cortex in Alzheimer's disease. Mol Brain Res 111 (2003) 148-154
44. Middlemas D.S., Lindberg R.A., and Hunter T. trkB, A neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol Cell Biol 11 (1991) 143-153
45. Minichiello L., Korte M., Wolfer D., Kühn R., Unsicker K., Cestari V., Rossi-Arnaud C., Lipp H.P., Bonhoeffer T., and Klein R. Essential role for trkB receptors in hippocampus-mediated learning. Neuron 24 (1999) 401-414
46. Mowla S.J., Farhadi H.F., Pareek S., Atwal J.K., Morris S.J., Seidah N.G., and Murphy R.A. Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor. J Biol Chem 276 (2001) 12660-12666
47. Mu J.S., Li W.P., Yao Z.B., and Zhou X.F. Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res 835 (1999) 259-265
48. Murer M.G., Yan Q., and Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63 (2001) 71-124
49. Nibuya M., Takahashi M., Russell D.S., and Duman R.S. Repeated stress increases catalytic TrkB mRNA in rat hippocampus. Neurosci Lett 267 (1999) 81-84
50. Ninkina N., Adu J., Fischer A., Pinon L.G.P., Buchman V.L., and Davies A.M. Expression and function of TrkB variants in developing sensory neurons. EMBO J 15 (1996) 6385-6393
51. Offenhauser N., Muzio V., and Biffo S. BDNF binding to truncated trkB. T1 does not affect gene expression. Neuroreport 13 (2002) 1189-1193
52. Patterson S.L., Abel T., Deuel T.A.S., Martin K.C., Rose J.C., and Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16 (1996) 1137-1145
53. Poo M.M. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2 (2001) 24-32
54. Rose C.R., Blum R., Pichler B., Lepier A., Kafitz K.W., and Konnerth A. Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 426 (2003) 74-78
55. Rosenzweig E.S., and Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69 (2003) 143-179
56. Rozen S., and Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 (2000) 365-386
57. Rudge J.S., Li Y., Pasnikowski E.M., Mattsson K., Pan L., Yancopoulos D., Wiegand S.J., Lindsay R.M., and Ip N.Y. Neurotrophic factor receptors and their signal transduction capabilities in rat astrocytes. Eur J Neurosci 6 (1994) 693-705
58. Russo-Neustadt A.A., Beard R.C., Huang Y.M., and Cotman C.W. Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101 (2000) 305-312
59. Saarelainen T., Lukkarinen J.A., Koponen S., Grohn O.H.J., Jolkkonen J., Koponen E., Haapasalo A., Alhonen L., Wong G., Koistinaho J., Kauppinen R.A., and Castren E. Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons show increased susceptibility to cortical injury after focal cerebral ischemia. Mol Cell Neurosci 16 (2000) 87-96
60. Saarelainen T., Pussinen R., Koponen E., Alhonen L., Wong G., Sirvio J., and Castren E. Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons have impaired long-term spatial memory but normal hippocampal LTP. Synapse 38 (2000) 102-104
61. Schaaf M.J., Sibug R.M., Duurland R., Fluttert M.F., Oitzl M.S., De Kloet E.R., and Vreugdenhil E. Corticosterone effects on BDNF mRNA expression in the rat hippocampus during Morris water maze training. Stress 3 (1999) 173-183
62. Schaaf M.J.M., Workel J.O., Lesscher H.M., Vreugdenhil E., Oitzl M.S., and de Kloet E.R. Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915 (2001) 227-233
63. Schafer M.K., Day R., Cullinan W.E., Chretien M., Seidah N.G., and Watson S.J. Gene expression of prohormone and proprotein convertases in the rat CNS: a comparative in situ hybridization analysis. J Neurosci 13 (1993) 1258-1279
64. Schuman E. Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 9 (1999) 105-109
65. Seidah N.G., Hamelin J., Mamarbachi M., Dong W., Tardos H., Mbikay M., Chretien M., and Day R. cDNA structure, tissue distribution, and chromosomal localization of rat PC7, a novel mammalian proprotein convertase closest to yeast kexin-like proteinases. Proc Natl Acad Sci U S A 93 (1996) 3388-3393
66. Silhol M., Bonnichon V., Rage F., and Tapia-Arancibia L. Age-related changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 132 (2005) 613-624
67. Smith T.D., Adams M.M., Gallagher M., Morrison J.H., and Rapp P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J Neurosci 20 (2000) 6587-6593
68. Sommerfeld M.T., Schweigreiter R., Barde Y.A., and Hoppe E. Down-regulation of the neurotrophin receptor TrkB following ligand binding: Evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J Biol Chem 275 (2000) 8982-8990
69. Soppet D., Escandon E., Maragos J., Middlemas D.S., Reid S.W., Blair J., Burton L.E., Stanton B.R., Kaplan D.R., Hunter T., Nikolics K., and Parada L.F. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65 (1991) 895-903
70. Tapia-Arancibia L., Rage F., Givalois L., and Arancibia S. Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol 25 (2004) 77-107
71. Thoenen H. Neurotrophins and neuronal plasticity. Science 270 (1995) 593-598
72. Thoenen H. Neurotrophins and activity-dependent plasticity. Prog Brain Res 128 (2000) 183-191
73. Venero J.L., and Hefti F. Regionally specific induction of BDNF and truncated trkB. T1 receptors in the hippocampal formation after intraseptal injection of kainic acid. Brain Res 790 (1998) 270-277
74. Wetmore C., and Olson L. Neuronal and nonneuronal expression of neurotrophins and their receptors in sensory and sympathetic ganglia suggest new intercellular trophic interactions. J Comp Neurol 353 (1995) 143-159
75. Whitaker J.R., and Granum P.E. An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal Biochem 109 (1980) 156-159
76. Yacoubian T.A., and Lo D.C. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 3 (2000) 342-349
77. Yamada K., Mizuno M., and Nabeshima T. Role for brain-derived neurotrophic factor in learning and memory. Life Sci 70 (2002) 735-744
78. Zhou X.F., Song X.Y., Zhong J.H., Barati S., Zhou F.H., and Johnson S.M. Distribution and localization of pro-brain-derived neurotrophic factor-like immunoreactivity in the peripheral and central nervous system of the adult rat. J Neurochem 91 (2004) 704-715