Autocrine BDNF-TrkB signalling within a single dendritic spine

Nature

Volumn 538, Issue 7623, 2016, Pages 99-103

  Harward, Stephen C ^a   Hedrick, Nathan G ^a,f   Hall, Charles E ^a   Parra Bueno, Paula ^b   Milner, Teresa A ^c,d   Pan, Enhui ^a   Laviv, Tal ^b   Hempstead, Barbara L ^c,e   Yasuda, Ryohei ^a,b   McNamara, James O ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^c FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CRE RECOMBINASE; PHOSPHOLIPASE C GAMMA1; PROTEIN SH2; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NTRK2 PROTEIN, MOUSE; PHLUORIN; PROTEIN TYROSINE KINASE;

BRAIN; CELLS AND CELL COMPONENTS; GENETIC ANALYSIS; LEARNING; NERVOUS SYSTEM; PLASTICITY; RODENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITIC SPINE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FEMALE; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CYTOLOGY; ENZYME ACTIVATION; HELA CELL LINE; HIPPOCAMPUS; METABOLISM; MULTIPHOTON MICROSCOPY; POSTSYNAPTIC DENSITY; RAT; SECRETION (PROCESS); TISSUE CULTURE TECHNIQUE; ULTRASTRUCTURE;

ANIMALIA; MURINAE;

ANIMALS; AUTOCRINE COMMUNICATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; DENDRITIC SPINES; ENZYME ACTIVATION; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HELA CELLS; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; POST-SYNAPTIC DENSITY; PROTEIN-TYROSINE KINASES; PYRAMIDAL CELLS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES;

EID: 84990203083     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19766     Document Type: Article

References (41)

1. Lohof, A. M., Ip, N. Y. & Poo, M. M. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353 (1993).
2. Kang, H., Welcher, A. A., Shelton, D. & Schuman, E. M. Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19, 653-664 (1997).
3. Minichiello, L. et al. Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24, 401-414 (1999).
4. Figurov, A., Pozzo-Miller, L. D., Olafsson, P., Wang, T. & Lu, B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381, 706-709 (1996).
5. Korte, M. et al. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl Acad. Sci. USA 92, 8856-8860 (1995).
6. Kovalchuk, Y., Hanse, E., Kafitz, K. W. & Konnerth, A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729-1734 (2002).
7. Tanaka, J. et al. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319, 1683-1687 (2008).
8. Lai, K.-O. O. et al. TrkB phosphorylation by Cdk5 is required for activitydependent structural plasticity and spatial memory. Nat. Neurosci. 15, 1506-1515 (2012).
9. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C. & Kasai, H. Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766 (2004).
10. Okamoto, K., Nagai, T., Miyawaki, A. & Hayashi, Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7, 1104-1112 (2004).
11. Kim, I. H. et al. Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J. Neurosci. 33, 6081-6092 (2013).
12. Kim, I. H., Wang, H., Soderling, S. H. & Yasuda, R. Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall. eLife 3, e02839 (2014).
13. Yasuda, R. Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy. Curr. Opin. Neurobiol. 16, 551-561 (2006).
14. Harvey, C. D., Yasuda, R., Zhong, H. & Svoboda, K. The spread of Ras activity triggered by activation of a single dendritic spine. Science 321, 136-140 (2008).
15. Lee, S.-J. R. J., Escobedo-Lozoya, Y., Szatmari, E. M. & Yasuda, R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458, 299-304 (2009).
16. Murakoshi, H., Wang, H. & Yasuda, R. Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472, 100-104 (2011).
17. Miesenböck, G., De Angelis, D. A. & Rothman, J. E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195 (1998).
18. Matsuda, N. et al. Differential activity-dependent secretion of brain-derived neurotrophic factor from axon and dendrite. J. Neurosci. 29, 14185-14198 (2009).
19. Dean, C. et al. Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat. Neurosci. 12, 767-776 (2009).
20. Hedrick, N. G. et al. Rho GTPase complementation underlies BDNF-dependent homo-and heterosynaptic plasticity. Nature http://dx. doi. org/10. 1038/ nature19784 (2016).
21. Middlemas, D. S., Meisenhelder, J. & Hunter, T. Identification of TrkB autophosphorylation sites and evidence that phospholipase C-?1 is a substrate of the TrkB receptor. J. Biol. Chem. 269, 5458-5466 (1994).
22. Vest, R. S., Davies, K. D., O'Leary, H., Port, J. D. & Bayer, K. U. Dual mechanism of a natural CaMKII inhibitor. Mol. Biol. Cell 18, 5024-5033 (2007).
23. Lu, W. et al. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254-268 (2009).
24. Huang, Y. Z., Pan, E., Xiong, Z.-Q. Q. & McNamara, J. O. Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fiber-CA3 pyramid synapse. Neuron 57, 546-558 (2008).
25. Dieni, S. et al. BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons. J. Cell Biol. 196, 775-788 (2012).
26. Yang, J. et al. Neuronal release of proBDNF. Nat. Neurosci. 12, 113-115 (2009).
27. Lou, H. et al. Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase E. Neuron 45, 245-255 (2005).
28. Chen, X. et al. A chemical-genetic approach to studying neurotrophin signaling. Neuron 46, 13-21 (2005).
29. He, X.-P. et al. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43, 31-42 (2004).
30. Luikart, B. W. et al. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J Neurosci. 25, 3774-3786 (2005).
31. Huang, Y. Z. & McNamara, J. O. Mutual regulation of Src family kinases and the neurotrophin receptor TrkB. J. Biol. Chem. 285, 8207-8217 (2010).
32. Zacharias, D. A., Violin, J. D., Newton, A. C. & Tsien, R. Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913-916 (2002).
33. Patterson, M. A., Szatmari, E. M. & Yasuda, R. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc. Natl Acad. Sci. USA 107, 15951-15956 (2010).
34. He, X.-P. P. et al. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 43, 31-42 (2004).
35. Xiong, Z. Q. & McNamara, J. O. Fleeting activation of ionotropic glutamate receptors sensitizes cortical neurons to complement attack. Neuron 36, 363-374 (2002).
36. Stoppini, L., Buchs, P. A. & Muller, D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182 (1991).
37. Murakoshi, H., Lee, S.-J. J. & Yasuda, R. Highly sensitive and quantitative FRET-FLIM imaging in single dendritic spines using improved non-radiative YFP. Brain Cell Biol. 36, 31-42 (2008).
38. Pologruto, T. A., Sabatini, B. L. & Svoboda, K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2, 13 (2003).
39. Pan, E. et al. Vesicular zinc promotes presynaptic and inhibits postsynaptic long-term potentiation of mossy fiber-CA3 synapse. Neuron 71, 1116-1126 (2011).
40. Milner, T. A., Waters, E. M., Robinson, D. C. & Pierce, J. P. in Neurodegeneration, Methods and Procedures (eds Manfredi, G. & Kawamata, H.) 23-59 (Spring, 2011).
41. Peters, A., Palay, S. L. & Webster, H. D. The Fine Structure of the Nervous System 3rd edn (Oxford Univ. Press, 1991).