Neuronal activity alters BDNF-TrkB signaling kinetics and downstream functions

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2249-2260

  Guo, Wei ^a,b,c   Ji, Yuanyuan ^d   Wang, Shudan ^a,c   Sun, Yun ^a,e,f   Lu, Bai ^a,b  

^a Tsinghua University   (China)

^b Tsinghua University   (China)

^c TSINGHUA UNIVERSITY   (China)

^d GLAXOSMITHKLINE   (China)

^e NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^f PEKING UNIVERSITY   (China)

Author keywords

Neuronal activity; Neuronal surface receptor; Neurotrophin; Signal transduction; Signaling kinetics

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLUTAMIC ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL KINETICS; CELL SURFACE; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; IN VIVO STUDY; INTRACELLULAR SIGNALING; LONG TERM POTENTIATION; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; KINETICS; METABOLISM; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; KINETICS; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 84900824932     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.139964     Document Type: Article

References (53)

1. Almeida, R. D., Manadas, B. J., Melo, C. V., Gomes, J. R., Mendes, C. S., Grãos, M. M., Carvalho, R. F., Carvalho, A. P. and Duarte, C. B. (2005). Neuroprotection by BDNF against glutamate-induced apoptotic cell death is mediated by ERK and PI3-kinase pathways. Cell Death Differ. 12, 1329-1343.
2. Arancibia, S., Silhol, M., Moulière, F., Meffre, J., Höllinger, I., Maurice, T. and Tapia-Arancibia, L. (2008). Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol. Dis. 31, 316-326.
3. 2+ signaling. Neuron 21, 13-26.
4. Bito, H., Deisseroth, K. and Tsien, R. W. (1996). CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87, 1203-1214.
5. Boulanger, L. M. and Poo, M. M. (1999). Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation. Nat. Neurosci. 2, 346-351.
6. Buzsáki, G. (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340.
7. Cheung, Z. H., Chin, W. H., Chen, Y., Ng, Y. P. and Ip, N. Y. (2007). Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol. 5, e63.
8. Cotman, C. W. and Berchtold, N. C. (2002). Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25, 295-301.
9. Du, J., Feng, L., Yang, F. and Lu, B. (2000). Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons. J. Cell Biol. 150, 1423-1434.
10. 2+ influx. J. Cell Biol. 163, 385-395.
11. Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T. and Lu, B. (1996). Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709.
12. Finkbeiner, S., Tavazoie, S. F., Maloratsky, A., Jacobs, K. M., Harris, K. M. and Greenberg, M. E. (1997). CREB: a major mediator of neuronal neurotrophin responses. Neuron 19, 1031-1047.
13. Frank, L., Ventimiglia, R., Anderson, K., Lindsay, R. M. and Rudge, J. S. (1996). BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur. J. Neurosci. 8, 1220-1230.
14. Fritsch, B., Reis, J., Martinowich, K., Schambra, H. M., Ji, Y., Cohen, L. G. and Lu, B. (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66, 198-204.
15. Gärtner, A. and Staiger, V. (2002). Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns. Proc. Natl. Acad. Sci. USA 99, 6386-6391.
16. Ghosh, A., Carnahan, J. and Greenberg, M. E. (1994). Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618-1623.
17. Gottschalk, W., Pozzo-Miller, L. D., Figurov, A. and Lu, B. (1998). Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J. Neurosci. 18, 6830-6839.
18. Grubb, M. S. and Burrone, J. (2010). Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465, 1070-1074.
19. Haapasalo, A., Sipola, I., Larsson, K., Åkerman, K. E. O., Stoilov, P., Stamm, S., Wong, G. and Castrén, E. (2002). Regulation of TRKB surface expression by brain-derived neurotrophic factor and truncated TRKB isoforms. J. Biol. Chem. 277, 43160-43167.
20. Huang, E. J. and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
21. Ishida, A., Kameshita, I., Okuno, S., Kitani, T. and Fujisawa, H. (1995). A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun. 212, 806-812.
22. Jeneson, A. and Squire, L. R. (2012). Working memory, long-term memory, and medial temporal lobe function. Learn. Mem. 19, 15-25.
23. Ji, Y., Pang, P. T., Feng, L. and Lu, B. (2005). Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons. Nat. Neurosci. 8, 164-172.
24. Ji, Y., Lu, Y., Yang, F., Shen, W., Tang, T. T. T., Feng, L., Duan, S. and Lu, B. (2010). Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat. Neurosci. 13, 302-309.
25. Kaplan, D. R. and Stephens, R. M. (1994). Neurotrophin signal transduction by the Trk receptor. J. Neurobiol. 25, 1404-1417.
26. Kuczewski, N., Porcher, C., Ferrand, N., Fiorentino, H., Pellegrino, C., Kolarow, R., Lessmann, V., Medina, I. and Gaiarsa, J.-L. (2008). Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity. J. Neurosci. 28, 7013-7023.
27. Kuo, T. B. J., Li, J. Y., Chen, C. Y. and Yang, C. C. H. (2011). Changes in hippocampal h activity during initiation and maintenance of running in the rat. Neuroscience 194, 27-35.
28. Lewin, G. R. and Barde, Y. A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
29. Lisman, J., Schulman, H. and Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3, 175-190.
30. Lu, B. and Figurov, A. (1997). Role of neurotrophins in synapse development and plasticity. Rev. Neurosci. 8, 1-12.
31. Lu, Y., Christian, K. and Lu, B. (2008). BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol. Learn. Mem. 89, 312-323.
32. Lu, B., Nagappan, G., Guan, X., Nathan, P. J. and Wren, P. (2013). BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat. Rev. Neurosci. 14, 401-416.
33. Martinowich, K., Manji, H. and Lu, B. (2007). New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10, 1089-1093.
34. Mattson, M. P., Lovell, M. A., Furukawa, K. and Markesbery, W. R. (1995). 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, 1740-1751.
35. McAllister, A. K., Lo, D. C. and Katz, L. C. (1995). Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15, 791-803.
36. McAllister, A. K., Katz, L. C. and Lo, D. C. (1996). Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064.
37. McAllister, A. K., Katz, L. C. and Lo, D. C. (1999). Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci. 22, 295-318.
38. Meyer-Franke, A., Wilkinson, G. A., Kruttgen, A., Hu, M., Munro, E., Hanson, M. G., Jr, Reichardt, L. F. and Barres, B. A. (1998). Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21, 681-693.
39. Nagahara, A. H. and Tuszynski, M. H. (2011). Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 10, 209-219.
40. Nagappan, G., Zaitsev, E., Senatorov, V. V., Jr, Yang, J., Hempstead, B. L. and Lu, B. (2009). Control of extracellular cleavage of ProBDNF by high frequency neuronal activity. Proc. Natl. Acad. Sci. USA 106, 1267-1272.
41. Nitsche, M. A. and Paulus, W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527, 633-639.
42. Obrietan, K., Gao, X.-B. and Van Den Pol, A. N. (2002). Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism - a positive feedback circuit in developing neurons. J. Neurophysiol. 88, 1005-1015.
43. Oladehin, A. and Waters, R. S. (2001). Location and distribution of Fos protein expression in rat hippocampus following acute moderate aerobic exercise. Exp. Brain Res. 137, 26-35.
44. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., Celnik, P. A. and Krakauer, J. W. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. USA 106, 1590-1595.
45. Sala, C., Rudolph-Correia, S. and Sheng, M. (2000). Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element- binding protein (CREB) in hippocampal neurons. J. Neurosci. 20, 3529-3536.
46. Shimada, A., Mason, C. A. and Morrison, M. E. (1998). TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J. Neurosci. 18, 8559-8570.
47. Sommerfeld, M. T., Schweigreiter, R., Barde, Y.-A. and Hoppe, E. (2000). 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, 8982-8990.
48. Squinto, S. P., Stitt, T. N., Aldrich, T. H., Davis, S., Bianco, S. M., Radziejewski, C., Glass, D. J., Masiakowski, P., Furth, M. E., Valenzuela, D. M. et al. (1991). trkB encodes a functional receptor for brain-derived neurotrophic factor and neurotrophin-3 but not nerve growth factor. Cell 65, 885-893.
49. Tongiorgi, E., Righi, M. and Cattaneo, A. (1997). Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17, 9492-9505.
50. Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418.
51. Yanagita, S., Amemiya, S., Suzuki, S. and Kita, I. (2007). Effects of spontaneous and forced running on activation of hypothalamic corticotropin-releasing hormone neurons in rats. Life Sci. 80, 356-363.
52. Zhao, L., Sheng, A.-L., Huang, S.-H., Yin, Y.-X., Chen, B., Li, X.-Z., Zhang, Y. and Chen, Z.-Y. (2009). Mechanism underlying activity-dependent insertion of TrkB into the neuronal surface. J. Cell Sci. 122, 3123-3136.
53. Zuccato, C. and Cattaneo, E. (2009). Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5, 311-322.