Differential effects of protein synthesis inhibition on the activity- dependent expression of BDNF transcripts: Evidence for immediate-early gene responses from specific promoters

Journal of Neuroscience

Volumn 16, Issue 23, 1996, Pages 7428-7436

  Lauterborn, Julie C ^a,b   Rivera, Santiago ^a,e   Stinis, Curtiss T ^a   Hayes, Valerie Y ^c   Isackson, Paul J ^c,d   Gall, Christine M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

^e Université Paris Descartes   (France)

Author keywords

brain derived neurotrophic factor; cycloheximide; gene regulation; hippocampus; immediate early gene; nerve growth factor

Indexed keywords

ANISOMYCIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLOHEXIMIDE; KAINIC ACID; MESSENGER RNA; NERVE GROWTH FACTOR;

AFTERDISCHARGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXON; GENE EXPRESSION; HIPPOCAMPUS; IMMEDIATE EARLY GENE; MALE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS INHIBITION; RAT;

EID: 0029860885     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-23-07428.1996     Document Type: Article

References (58)

1. Bengzon J, Soderstrom S, Kokaia Z, Kokaia M, Ernfors P, Persson H, Ebendal T, Lindvall O (1992) Widespread increase of nerve growth factor protein in the rat forebrain after kindling-induced seizures. Brain Res 587:338-342.
2. Bengzon J, Kokaia Z, Ernfors P, Kokaia M, Leanza G, Nilsson OG, Persson H, Lindvall O (1993) Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling. Neuroscience 53:433-446.
3. Bennett EL, Orme A, Hebert M (1972) Cerebral protein synthesis inhibition and amnesia produced by scopolamine, cycloheximide, streptovitacin A, anisomycin, and emetine in rat. Fed Proc 31:838.
4. Bishop JF, Mueller GP, Mouradian MM (1994) Alternate 5′ exons in the rat brain-derived neurotrophic factor gene: differential patterns of expression across brain regions. Mol Brain Res 26:225-232.
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
6. Castrén E, Pitkänen M, Sirviö J, Parsadanian A, Lindholm D, Thoenen H, Riekkinen PJ (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. NeuroReport 4:895-898.
7. Cowie A, Ivanco TL, Fahnestock M (1994) Mouse NGF promoter upstream sequences do not affect gene expression in mouse fibroblasts. Mol Brain Res 27:58-62.
8. Curran T, Gordon MB, Rubino KL, Sambucetti LC (1987) Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modification in vitro. Oncogene 2:79-84.
9. D'Mello S, Heinrich G (1990) Induction of nerve growth factor gene expression by 12-O-tetradecanoyl phorbol 13-acetate. J Neurochem 55:718-721.
10. D'Mello S, Heinrich G (1991) Nerve growth factor gene expression: involvement of a downstream AP-1 element in basal and modulated transcription. Mol Cell Neurosci 2:157-167.
11. Dragunow M, Beilharz E, Mason B, Lawlor P, Abraham W, Gluckman P (1993) Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci Lett 160:232-236.
12. Edwards DR, Mahadevan LC (1992) Protein synthesis inhibitors differentially superinduce c-fos and c-jun by three distinct mechanisms: lack of evidence for labile repressors. EMBO J 11:2415-2424.
13. Ernfors P, Wetmore C, Olson L, Persson L (1990) Identification of cells in the rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5:511-526.
14. Ernfors P, Bengzon J, Kokaia A, Persson H, Lindvall O (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7:165-176.
15. Falkenberg T, Metsis M, Timmusk T, Lindefors N (1993) Entorhinal cortex regulation of multiple brain-derived neurotrophic factor promoters in the rat hippocampus. Neuroscience 57:891-896.
16. Flood JF, Rosenzweig MR, Bennett EL, Orme AE (1973) The influence of duration of protein synthesis inhibition on memory. Physiol Behav 10:555-562.
17. Gall C (1993) Seizure-induced changes in neurotrophin expression: implications for epilepsy. Exp Neurol 124:150-166.
18. Gall C, Lauterborn J (1992) The dentate gyrus: a model system for studies of neurotrophin regulation. In: The dentate gyrus and its role in seizures. Epilepsy Research Supplement (Ribak CE, Gall CM, Mody I, eds), pp 171-185. Amsterdam: Elsevier.
19. Gall CM, Berschauer R, Isackson PJ (1994) Basic fibroblast growth factor mRNA is increased in forebrain neurons and glia following recurrent limbic seizures. Mol Brain Res 21:190-205.
20. Gall C, Lauterborn J, Guthrie K (1995) In situ hybridization as a sensitive measure of activity dependent neuronal gene expression. In: Autoradiography and correlative imaging (Strumpf WE, Solomon HF, eds), pp 379-399. San Diego: Academic.
21. Ghosh A, Carnahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1616-1623.
22. Hayes VY, Murray KD, Isackson PJ (1995) Differential regulation of BDNF transcripts through a calcium/calmodulin-dependent protein kinase pathway. Soc Neurosci Abstr 21:1046.
23. Hengerer B, Lindholm D, Heumann R, Ruther U, Wagner EF, Thoenen H (1990) Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc Natl Acad Sci USA 87:3899-3903.
24. Hughes P, Beilharz E, Gluckman P, Dragunow M (1993) Brain-derived neurotrophic factor is induced as an immediate early gene following N-methyl-D-aspartate receptor activation. Neuroscience 57:319-328.
25. Humpel C, Wetmore C, Olson L (1993) Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience 53:909-918.
26. Hyman C, Juhasz M, Jackson C, Wright P, Ip NY, Lindsay RM (1994) Overlapping and distinct actions of the neurotrophins BDNF, NT-3, and NT-4/5 on cultured dopaminergic and GABAergic neurons of ventral mesencephalon. J Neurosci 14:335-347.
27. Ip NY, Li Y, Yancopoulos GD, Lindsay RM (1993) Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4 but not NGF. J Neurosci 13:3394-3405.
28. Isackson PJ, Murray K, Huntsman M, Gall CM (1991) BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6:937-948.
29. Kokaia Z, Metsis M, Kokaia M, Bengzon J, Elmér E, Smith M-L, Timmusk T, Siesjö BK, Persson H, Lindvall O (1994a) Brain insults in rats induce increased expression of the BDNF gene through differential use of multiple promoters. Eur J Neurosci 6:587-596.
30. Kokaia Z, Othberg A, Kokaia M, Lindvall O (1994b) BDNF makes cultured dentate granule cells more resistant to hypoglycaemic damage. NeuroReport 5:1241-1224.
31. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL (1993) Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359-367.
32. Lauterborn JC, Tran TM, Isackson P, Gall CM (1993) NGF mRNA is expressed by GABAergic neurons in rat hippocampus. NeuroReport 5:273-276.
33. Lauterborn JC, Isackson PJ, Gall CM (1994) Cellular localization of NGF and NT-3 mRNAs in postnatal rat forebrain. Mol Cell Neurosci 5:46-62.
34. Leibrock J, Lottespeich AH, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde Y (1989) Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341:149-152.
35. Leingärtner A, Lindholm D (1994) Two promoters direct transcription of the mouse NT-3 gene. Eur J Neurosci 6:1149-1159.
36. Lindefors N, Ernfors P, Falkenberg T, Persson H (1992) Septal cholinergic afferents regulate expression of brain-derived neurotrophic factor and β-nerve growth factor mRNA in rat hippocampus. Exp Brain Res 88:78-90.
37. Lindvall O, Kokaia Z, Bengzon J, Elmér E, Kokaia M (1994) Neurotrophins and brain insults. Trends Neurosci 17:490-496.
38. Metsis M, Timmusk T, Arenas E, Persson H (1993) Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc Natl Acad Sci USA 90:8802-8806.
39. Mocchetti I, De Bernadi M, Szekely A, Alho H, Brooker G, Costa E (1989) Regulation of nerve growth factor biosynthesis by β-adrenergic receptor activation in astrocytoma cells: a potential role of c-Fos protein. Proc Natl Acad Sci USA 86:3891-3895.
40. Motulsky H (1995) Intuitive biostatistics. New York: Oxford UP.
41. Nakao N, Kokaia Z, Odin P, Lindvall O (1995) Protective effects of BDNF and NT-3 but not PDNF against hypoglycemic injury to cultured striatal neurons. Exp Neurol 131:1-10.
42. Nakayama M, Gahara Y, Kitamura T, Ohara O (1994) Distinctive four promoters collectively direct expression of brain-derived neurotrophic factor gene. Mol Brain Res 21:206-218.
43. Nawa H, Carnahan J, Gall C (1995) BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur J Neurosci 7:1527-1535.
44. Omae E, Katsumata T, Sakuma M, Furukawa Y, Furukawa S (1994) Prolonged alkylcatechol-induced expression of c-jun proto-oncogene followed by elevation of NGF mRNA in cultured astroglial cells. J Neurosci Res 39:290-297.
45. Patterson SL, Grover LM, Schwartzkroin PA, Bothwell M (1992) Neurotrophin expression in rat hippocampal slices - a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 messenger RNAs. Neuron 9:1081-1088.
46. Qian Z, Gilbert ME, Colicos MA, Kandel ER, Kuhl D (1993) Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361:453-457.
47. Rivera S, Gold S, Gall CM (1994) Interleukin-1β increases basic fibroblast growth factor mRNA expression in adult rat brain and organotypic hippocampal cultures. Mol Brain Res 27:12-26.
48. Sassone-Corsi P, Sisson JC, Verma IM (1988) Transcriptional autoregulation of the proto-oncogene fos. Nature 334:314-319.
49. Selby MJ, Edwards R, Sharp F, Rutter WJ (1987) Mouse nerve growth factor gene: structure and expression. Mol Cell Biol 7:3057-3064,
50. Spina MB, Squinto SP, Miller J, Lindsay RM, Hyman C (1992) Brain-derived neurotrophic factor protects dopamine neurons against 6-hydroxydopamine and N-methyl-4-phenylpyridinium ion toxicity: involvement of the glutathione system. J Neurochem 59:99-106.
51. Squinto SP, Stitt TN, Aldrich TH, Davis S, Bianco SM, Masiakowski P, Furth ME, Valenzuela DM, DiStefano PS, Yancopoulos GD (1991) trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65:885-893.
52. Stoppini S, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
53. Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M, Persson H (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10:475-489.
54. Vigé X, Costa E, Wise BC (1991) Mechanism of nerve growth factor mRNA regulation by interleukin-1 and basic fibroblast growth factor in primary cultures of rat astrocytes. Mol Pharmacol 40:186-192.
55. Whittemore SR, Friedman PL, Larhammar D, Persson H, Gonzales-Carvajal M, Holets VR (1988) Rat β-nerve growth factor sequence and site of synthesis in the adult hippocampus. J Neurosci Res 20:403-410.
56. Wion D, Grogan DM, Houlgatte R, Brachet P (1990) Phorbol 12-myristate 13-acetate (PMA) increases the expression of nerve growth factor (NGF) gene in mouse L-929 fibroblasts. FEBS Lett 262:42-44.
57. Zafra F, Castrén E, Thoenen H, Lindholm D (1991) Interplay between glutamate and gamma-amino butyric 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.
58. Zafra F, Lindholm D, Castrén E, Hartikka J, Thoenen H (1992) Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J Neurosci 12:4793-4799.