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Nerve Growth Factor Activates Brain-derived Neurotrophic Factor Promoter IV via Extracellular Signal-regulated Protein Kinase 1/2 in PC12 Cells  

Park, So Yun (School of Biological Sciences, Seoul National University)
Lee, Ji Yun (Department of Anatomy, School of Medicine, Kyungpook National University)
Choi, Jun Young (Department of Anatomy, School of Medicine, Kyungpook National University)
Park, Mae Ja (Department of Anatomy, School of Medicine, Kyungpook National University)
Kim, Dong Sun (Department of Anatomy, School of Medicine, Kyungpook National University)
Publication Information
Molecules and Cells / v.21, no.2, 2006 , pp. 237-243 More about this Journal
Abstract
Brain-derived neurotrophic factor (BDNF) is a neuromodulator of nociceptive responses in the dorsal root ganglia (DRG) and spinal cord. BDNF synthesis increases in response to nerve growth factor (NGF) in trkA-expressing small and medium-sized DRG neurons after inflammation. Previously we demonstrated differential activation of multiple BDNF promoters in the DRG following peripheral nerve injury and inflammation. Using reporter constructs containing individual promoter regions, we investigated the effect of NGF on the multiple BDNF promoters, and the signaling pathway by which NGF activates these promoters in PC12 cells. Although all the promoters were activated 2.4-7.1-fold by NGF treatment, promoter IV gave the greatest induction. The p38 mitogen-activated protein kinase (MAPK) inhibitor, SB203580, phosphatidylinositol 3-kinase (PI-3K) inhibitor, LY294003, protein kinase A (PKA) inhibitor, H89, and protein kinase C (PKC) inhibitor, chelerythrine, had no effect on activation of promoter IV by NGF. However, activation was completely abolished by the MAPK kinase (MEK) inhibitors, U0126 and PD98059. In addition, these inhibitors blocked NGF-induced phosphorylation of extracellular signal-regulated protein kinase (ERK) 1/2. Taken together, these results suggest that the ERK1/2 pathway activates BDNF promoter IV in response to NGF independently of NGF-activated signaling pathways involving PKA and PKC.
Keywords
BDNF; DRG; ERK1/2; Inflammatory Pain; Multiple Promoters; NGF; PC12 Cells;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
Times Cited By Web Of Science : 9  (Related Records In Web of Science)
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1 Aley, K. O. and Levine, J. D. (1999) Role of protein kinase A in the maintenance of inflammatory pain. J. Neurosci. 19, 2181-2186   DOI
2 Aley, K. O., Martin, A., McMahon, T., Mok, J., Levine, J. D., et al. (2001) Nociceptor sensitization by extracellular signalregulated kinases. J. Neurosci. 21, 6933-6939   DOI
3 Doya, H., Ohtori, S., Fujitani, M., Saito, T., Hata, K., et al. (2005) c-Jun N-terminal kinase activation in dorsal root ganglion contributes to pain hypersensitivity. Biochem. Biophys. Res. Commun. 335, 132-138   DOI   ScienceOn
4 Landry, J. R., Mager, D. L., and Wilhelm, B. T. (2003) Complex controls: the role of alternative promoters in mammalian genomes. Trends Genet. 19, 640-648   DOI   ScienceOn
5 Liu, Y. Z., Chirivia, J. C., and Latchman, D. S. (1998) Nerve growth factor up-regulates the transcriptional activity of CBP through activation of the p42/p44(MAPK) cascade. J. Biol. Chem. 273, 32400-32407   DOI   ScienceOn
6 Michael, G. J., Averill, S., Shortland, P. J., Yan, Q., and Priestley, J. V. (1999) Axotomy results in major changes in BDNF expression by dorsal root ganglion cells: BDNF expression in large trkB and trkC cells, in pericellular baskets, and in projection to deep dorsal horn and dorsal column nuclei. Eur. J. Neurosci. 11, 3539-3551   DOI   ScienceOn
7 Nakayama, M., Gahara, Y., Kitamura, T., and Ohara, D. (1994) Distinctive four promoters collectively direct expression of brain-derived neurotrophic factor gene. Brain Res. Mol. Brain Res. 21, 206-218   DOI
8 Obata, K., Yamanaka, H., Dai, Y., Mizushima, T., Fukuoka, T., et al. (2004a) Activation of extracellular signal-regulated protein kinase in the dorsal root ganglion following inflammation near the nerve cell body. Neuroscience 126, 1011-1021   DOI   ScienceOn
9 Shieh, P. B., Hu, S. C., Bobb, K., Timmusk, T., and Ghosh, A. (1998) Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20, 727-740   DOI   ScienceOn
10 Thoenen, H. (1995) Neurotrophins and neuronal plasticity. Science 270, 593-598   DOI
11 Ferreira, J., Triches, K. M., Medeiros, R., and Calixto, J. B. (2005) Mechanisms involved in the nociception produced by peripheral protein kinase C activation in mice. Pain 117, 171-181   DOI
12 Kim, D. S., Lee, S. J., and Cho, H. J. (2001) Differential usage of multiple brain-derived neurotrophic factor promoter in rat dorsal root ganglia following peripheral nerve injuries and inflammation. Brain Res. Mol. Brain Res. 92, 167-171   DOI
13 Michael, G. J., Averill, S., Nitkunan, A., Rattray, M., Bennett, D. L., et al. (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and their centrl terminations within the spinal cord. J. Neurosci. 17, 8476-8490   DOI
14 Watson, A. and Latchman, D. S. (1995) The cyclic AMP response element in the calcitonin/calcitonin gene-related peptide gene promoter is necessary but not sufficient for its activation by nerve growth factor. J. Biol. Chem. 270, 9655-9660   DOI   ScienceOn
15 Averill, S., Delcroix, J. D., Michael, G. J., Tomlinson, D. R., Fernyhough, P., et al. (2001) Nerve growth factor modulates the activation status and fast axonal transport of erk 1/2 in adult nociceptive neurons. Mol. Cell Neurosci. 18, 183-196   DOI   ScienceOn
16 Metsis, M., Timmusk, T., Arenas, E., and 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
17 Delcroix, J. D., Valletta, J. S., Wu, C., Hunt, S. J., Kowal, A. S., et al. (2003) NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron 39, 69-84   DOI   ScienceOn
18 Obata, K. and Noguchi, K. (2004) MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci. 74, 2643-2653   DOI   ScienceOn
19 Brons, R., Klesse, L. J., Shah, K., Parada, L. F., Winter, J. (2003) Activation of Ras is necessary and sufficient for upregulation of vanilloid receptor type 1 in sensory neurons by neurotrophic factors. Mol. Cell Neurosci. 22, 118-132   DOI   ScienceOn
20 Ji, R. R. (2004) Mitogen-activated protein kinases as a potential targets for pain killers. Curr. Opin. Investig. Drugs 5, 71- 75
21 Liu, Y. Z., Thomas, N. S. B., and Latchman, D. S. (1999) CBP associates with the p42/p44 MAPK enzymes and is phosphorylated following NGF treatment. Neuroreport 10, 1239-1243   DOI   ScienceOn
22 Cho, H. J., Kim, J. K., Park, H. C., Kim, J. K., Kim, D. S., et al. (1998) Changes in brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia, spinal cord, and gracile nuclei following cut or crush injuries. Exp. Neurol. 154, 224-230   DOI   ScienceOn
23 Ji, R. R., Baba, H., Brenner, G. J., and Woolf, C. J. (1999) Nociceptive- specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat. Neurosci. 2, 1114-1119   DOI   ScienceOn
24 Sweatt, J. D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 76, 1-10   DOI   ScienceOn
25 Dai, Y., Iwata, K., Fukuoka, T., Kondo, E., Tokunaga, A., et al. (2002) Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvemnet in peripheral sensitization. J. Neurosci. 22, 7737-7745   DOI
26 Kokaia, Z., Metsis, M., Kokaia, M., Bengzon, J., Elmer, E., et al. (1994) Brain insults in rats induce increased expression of the BDNF gene through differential use of multiple promoters. Eur. J. Neurosci. 6, 587-596   DOI   ScienceOn
27 Obata, K., Yamanaka, H., Dai, Y., Tachibana, T., Fukuoka, T., et al. (2004b) Differential activation of extracellular signalregulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J. Neurosci. 23, 4117-4126
28 Woolf, C. J. and Costigan, M. (1999) Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc. Natl. Acad. Sci. USA 96, 7723-7730
29 Thomson, S. W., Bennett, D. L. H., Kerr, B. J., Bradbury, E. J., and McMahon, S. B. (1999) Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc. Natl. Acad. Sci. USA 96, 7714-7718
30 Kim, S. Y., Bae, J. C., Kim, J. Y., Lee, H. L., Lee, M., et al. (2002) Activation of p38 Map kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. Neuroreport 13, 2483-2486   DOI   ScienceOn
31 Timmusk, T., Palm, K., Medis, M., Reintam, T., Paalme, V., et al. (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10, 475-489   DOI   ScienceOn
32 Ji, R. R., Befort, K., Brenner, G. J., and Woolf, C. J. (2002a) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J. Neurosci. 22, 478-485   DOI
33 Apfel, S. C., Wright, D. E., Wiideman, A. M., Dormia, C., Snider, W. D., et al. (1996) Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nerve system. Mol. Cell Neurosci. 7, 134-142   DOI   ScienceOn
34 Dina, O. A., McCarter, G. C., de Coupade, C., and Levine, J. D. (2003) Role of sensory neuron cytoskleton in second messenger signaling for inflammatory pain. Neuron 39, 613-624   DOI   ScienceOn
35 Khasar, S. G., Lin, Y. H., Martin, A., Dadgar, J., McMahon, T., et al. (1999) A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24, 253-260   DOI   ScienceOn
36 Oliff, H. S., Berchtold, N. C., Isackson, P., and Cotman, C. W. (1998) Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus. Brain Res. Mol. Brain Res. 61, 147-153   DOI
37 Slagsvold, H. H., Ostvold, A. C., Fallgren, A. B., and Paulsen, R. E. (2002) Nuclear recptor and apoptosis initiator NGFI-B is a substrate for kinase ERK2. Biochem. Biophys. Res. Commun. 291, 1146-1150   DOI   ScienceOn
38 Millan, M. J. (1999) The introduction of pain: an integrative review. Prog. Neurobiol. 57, 1-164   DOI   ScienceOn
39 Schaeffer, H. J. and Weber, M. J. (1999) Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 19, 2435-2444   DOI
40 Pezet, S., Malcangio, M., and McMahon, S. B. (2002) BDNF: a neuromodulator in nociceptive pathways. Brain Res. Rev. 40, 240-249   DOI
41 Bishop, J. F., Mueller, G. P., and Mouradian, M. M. (1994) Alternative 5′ exons in the rat brain-derived neurotrophic factor gene: differential patterns of expression across brain regions. Brain Res. Mol. Brain Res. 26, 225-232   DOI
42 Tabuchi, A., Nakaoka, R., Amano, K., Yukimine, M., Andoh, T., et al. (2000) Differential activation of brain-derived neurotrophic factor gene promoters I and III by $Ca^{2+}^ signals evoked via L-type voltage-dependent and N-methyl-Daspartate receptor $Ca^{2+}^ channels. J. Biol. Chem. 275, 17269- 17275   DOI   ScienceOn
43 Takeuchi, Y., Miyamoto, E., and Fukunaga, K. (2003) Analysis on the promoter region of exon IV brain-derived neurotrophic factor in NG108-15 cells. J. Neurochem. 83, 67-79
44 Ji, R. R., Samad, T. A., Jin, S. X., Schmoll, R., and Woolf, C. J. (2002b) p38 MAPK activation in primary sensory neurons after inflammation increase TRPV1 levels and maintains heat hyperalgesia. Neuron 36, 57-68   DOI   ScienceOn
45 Freeland, K., Liu, Y. Z., and Latchman, D. S. (2000) Distinct signalling pathways mediate the cAMP response element (CRE)-dependent activation of the calcitonin gene-related peptide gene promoter by cAMP and nerve growth factor. Biochem. J. 345, 233-238   DOI   ScienceOn
46 Nanda, S. and Mack, K. J. (1998) Multiple promoters direct stimulus and temporal specific expression of brain-derived neurotrophic actor in the somatosensory cortex. Brain Res. Mol. Brain Res. 62, 216-219   DOI
47 Tabuchi, A., Sakaya, H., Kisukeda, T., Fukuchi, M., and Tsuda, M. (2002) Involvement of an upstream stimulatory factor as well as cAMP-responsive element-binding protein in the activation of brain-derived neurotrophic factor gene promoter I. J. Biol. Chem. 277, 35920-31   DOI   ScienceOn
48 Xing, J., Ginty, D. D., and Greenberg, M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963   DOI
49 Zha, X. M., Bishop, J. F., Hansen, M. R., Victoria, L., Abbas, P. J., et al. (2001) BDNF synthesis in spiral ganglion neurons in constitutive and CREB-dependent. Hear. Res. 156, 53-68   DOI