Hippocampal BDNF mRNA shows a diurnal regulation, primarily in the exon III transcript

Molecular Brain Research

Volumn 71, Issue 1, 1999, Pages 11-22

  Berchtold, Nicole C ^a,b   Oliff, Heather S ^a   Isackson, Paul ^c   Cotman, Carl W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

Brain derived neurotrophic factor; Diurnal; Exon; Hippocampus; Plasticity; Promoter

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; EXON; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0033064504     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(99)00137-0     Document Type: Article

References (57)

1. Beck T., Lindholm D., Castren E., Wree A. Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus. J. Cereb. Blood Flow. Metab. 14:1994;689-692.
2. N.C. Berchtold, H.S. Oliff, P. Isackson, C.W. Cotman, Brain-derived neurotrophic factor (BDNF) shows a circadian pattern of expression in the hippocampal formation, 27th Annual Meeting of the Society for Neurosciences, 1997, p. 27.2.
3. Bishop J.F., Mueller G.P., Mouradian M.M. Alternate 5′ exons in the rat brain-derived neurotrophic factor gene: differential patterns of expression across brain regions. Brain Res. Mol. Brain Res. 26:1994;225-232.
4. Boatell L.L., Lindefors N., Ballarin M., Ernfors P., Mahy N., Persson H. Activation of basal forebrain cholinergic neurons differentially regulates brain-derived neurotrophic factor mRNA expression in different projection areas. Neurosci. Lett. 136:1992;203-208.
5. Bova R., Micheli M.R., Qualadrucci P., Zucconi G.G. BDNF and trkB mRNAs oscillate in rat brain during the light-dark cycle. Brain Res. Mol. Brain Res. 57:1998;321-324.
6. Castren E., Pitkanen M., Sirvio J., Parsadanian A., Lindholm D., Thoenen H., Riekkinen P.J. The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport. 4:1993;895-898.
7. Castren E., Zafra F., Thoenen H., Lindholm D. Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. USA. 89:1992;9444-9448.
8. da Penha Berzaghi M., Cooper J., Castren E., Zafra F., Sofroniew M., Thoenen H., Lindholm D. Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus. J. Neurosci. 13:1993;3818-3826.
9. Dudar J.D., Whishaw I.Q., Szerb J.C. Release of acetylcholine from the hippocampus of freely moving rats during sensory stimulation and running. Neuropharmacology. 18:1979;673-678.
10. Elmer E., Kokaia Z., Kokaia M., Carnahan J., Nawa H., Lindvall O. Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience. 83:1998;351-362.
11. Falkenberg T., Mohammed A.K., Henriksson B., Persson H., Winblad B., Lindefors N. Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci. Lett. 138:1992;153-156.
12. Foyt H.L., LeRoith D., Roberts C.T. Jr. Differential association of insulin-like growth factor I mRNA variants with polysomes in vivo. J. Biol. Chem. 266:1991;7300-7305.
13. Grassi Z.G., Menegazzi M., De P.A., Bassetti A., Montagnese P., Mandile P., Cosi C., Bentivoglio M. c-Fos mRNA is spontaneously induced in the rat brain during the activity period of the circadian cycle. Eur. J. Neurosci. 5:1993;1071-1078.
14. Griesbeck O., Korte M., Staiger V., Gravel C., Carroll P., Bonhoeffer T., Thoenen H. Combination of gene targeting and gene transfer by adenoviral vectors in the analysis of neurotrophin-mediated neuronal plasticity. Cold Spring Harb. Symp. Quant. Biol. 61:1996;77-83.
15. Hayes V.Y., Towner M.D., Isackson P.J. Organization, sequence and functional analysis of a mouse BDNF promoter. Brain Res. Mol. Brain Res. 45:1997;189-198.
16. Jackson R.J., Standart N. Do the poly(A) tail and 3′ untranslated region control mRNA translation? Cell. 62:1990;15-24.
17. Kesslak J.P., So V., Choi J., Cotman C.W., Gomez-Pinilla F. Learning upregulates BDNF mRNA: a mechanism to facilitate encoding and circuit maintenance? Behav. Neurosci. 112:1998;1012-1019.
18. Knusel B., Beck K.D., Winslow J.W., Rosenthal A., Burton L.E., Widmer H.R., Nikolics K., Hefti F. Brain-derived neurotrophic factor administration protects basal forebrain cholinergic but not nigral dopaminergic neurons from degenerative changes after axotomy in the adult rat brain. J. Neurosci. 12:1992;4391-4402.
19. Kokaia Z., Metsis M., Kokaia M., Bengzon J., Elmer E., Smith M.L., Timmusk T., Siesjo B.K., Persson H., Lindvall O. Brain insults in rats induce increased expression of the BDNF gene through differential use of multiple promoters. Eur. J. Neurosci. 6:1994;587-596.
20. Kokaia Z., Nawa H., Uchino H., Elmer E., Kokaia M., Carnahan J., Smith M.L., Siesjo B.K., Lindvall O. Regional brain-derived neurotrophic factor mRNA and protein levels following transient forebrain ischemia in the rat. Brain Res. Mol. Brain Res. 38:1996;139-144.
21. Kononen J., Koistinaho J., Alho H. Circadian rhythm in c-fos-like immunoreactivity in the rat brain. Neurosci. Lett. 120:1990;105-108.
22. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. USA. 92:1995;8856-8860.
23. Korte M., Griesbeck O., Gravel C., Carroll P., Staiger V., Thoenen H., Bonhoeffer T. Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA. 93:1996;12547-12552.
24. Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J. Cell Biol. 115:1991;887-903.
25. Lapchak P.A., Araujo D.M., Hefti F. Cholinergic regulation of hippocampal brain-derived neurotrophic factor mRNA expression: evidence from lesion and chronic cholinergic drug treatment studies. Neuroscience. 52:1993;575-585.
26. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C., Depaulis A. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport. 6:1995;1937-1941.
27. Lauterborn J.C., Rivera S., Stinis C.T., Hayes V.Y., Isackson P.J., Gall C.M. Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J. Neurosci. 16:1996;7428-7436.
28. Lauterborn J.C., Stinis C.T., Wong J.S., Sun Z., Isackson P.J., Gall C.M. Transcript-specific effects of adrenalectomy on seizure-induced BDNF expression in rat hippocampus. Mol. Brain Res. 55:1998;81-91.
29. Levine E.S., Dreyfus C.F., Black I.B., Plummer M.R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA. 92:1995;8074-8077.
30. Liang F.Q., Walline R., Earnest D.J. Circadian rhythm of brain-derived neurotrophic factor in the rat suprachiasmatic nucleus. Neurosci. Lett. 242:1998;89-92.
31. Lindefors N., Ernfors P., Falkenberg T., Persson H. Septal cholinergic afferents regulate expression of brain-derived neurotrophic factor and beta-nerve growth factor mRNA in rat hippocampus. Exp. Brain Res. 88:1992;78-90.
32. Lindholm D., Castren E., Berzaghi M., Blochl A., Thoenen H. Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain-implications for neuronal plasticity. J. Neurobiol. 25:1994;1362-1372.
33. Ma Y.L., Wang H.L., Wu H.C., Wei C.L., 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.
34. Mahy N., Diaz R., Andres N., Fuxe K. Ibotenic acid in the medial septum increased brain-derived neurotrophic factor mRNA levels in the dorsal rat hippocampal formation. Neurosci. Lett. 213:1996;169-172.
35. Mattson M.P., Lovell M.A., Furukawa K., Markesbery W.R. Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular CA2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J. Neurochem. 65:1995;1740-1751.
36. Menegazzi M., Carcereri De., Prati Ac., Zucconi G.G. Differential expression pattern of junB and c-jun in the rat brain during the 24-h cycle. Neurosci. Lett. 182:1994;295-298.
37. Messaoudi E., Bardsen K., Srebro B., Bramham C.R. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J. Neurophysiol. 79:1998;496-499.
38. Mizuno T., Arita J., Kimura F. Spontaneous acetylcholine release in the hippocampus exhibits a diurnal variation in both young and old rats. Neurosci. Lett. 178:1994;271-274.
39. Mizuno T., Endo Y., Arita J., Kimura F. Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience. 44:1991;607-612.
40. Morse J.K., Wiegand S.J., Anderson K., You Y., Cai N., Carnahan J., Miller J., DiStefano P.S., Altar C.A., Lindsay R.M. Brain-derived neurotrophic factor (BDNF) prevents the degeneration of medial septal cholinergic neurons following fimbria transection. J. Neurosci. 13:1993;4146-4156.
41. Nakayama M., Gahara Y., Kitamura T., Ohara O. Distinctive four promoters collectively direct expression of brain-derived neurotrophic factor gene. Brain Res. Mol. Brain Res. 21:1994;206-218.
42. Nawa H., Carnahan J., Gall C. BDNF protein measured by novel enzyme immunoassay in normal brain and after seizure: partial disaccordance with mRNA levels. Eur. J. Neurosci. 7:1995;1527-1535.
43. Neeper S.A., Gomez P.F., Choi J., Cotman C.W. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 726:1996;49-56.
44. Neeper S.A., Gómez-Pinilla F., Choi J., Cotman C.W. Exercise and brain neurotrophins. Nature. 373:1995;109.
45. Nielsen F.C., Gammeltoft S., Christiansen J. Translational discrimination of mRNAs coding for human insulin-like growth factor II. J. Biol. Chem. 265:1990;13431-13434.
46. Nilsson O.G., Kalen P., Rosengren E., Bjorklund A. Acetylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioural activation. Neuroscience. 36:1990;325-338.
47. Oliff H.S., Berchtold N.C., Isackson P., Cotman C.W. Exercise-induced regulation of BDNF transcripts in the rat hippocampus. Mol. Brain Res. 61:1998;147-153.
48. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron. 16:1996;1137-1145.
49. Rocamora N., Welker E., Pascual M., Soriano E. Upregulation of BDNF mRNA expression in the barrel cortex of adult mice after sensory stimulation. J. Neurosci. 16:1996;4411-4419.
50. Schaaf M.J., de Jong J., de Kloet E.R., Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res. 813:1998;112-120.
51. Schoups A.A., Elliott R.C., Friedman W.J., Black I.B. NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Brain Res. Dev. Brain Res. 86:1995;326-334.
52. Shieh P.B., Hu S.C., Bobb K., Timmusk T., Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron. 20:1998;727-740.
53. Tao X., Finkbeiner S., Arnold D.B., Shaywitz A.J., Greenberg M.E. CA2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron. 20:1998;709-726.
54. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M., Persson H. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron. 10:1993;475-489.
55. Timmusk T., Persson H., Metsis M. Analysis of transcriptional initiation and translatability of brain-derived neurotrophic factor mRNAs in the rat brain. Neurosci. Lett. 177:1994;27-31.
56. Zafra F., Hengerer B., Leibrock J., Thoenen H., Lindholm D. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9:1990;3545-3550.
57. Zimmer A., Zimmer A.M., Reynolds K. Tissue specific expression of the retinoic acid receptor-beta 2: Regulation by short open reading frames in the 5′-noncoding region. J. Cell Biol. 127:1994;1111-1119.