Neurobiological actions by three distinct subtypes of brain-derived neurotrophic factor: Multi-ligand model of growth factor signaling

Pharmacological Research

Volumn 105, Issue , 2016, Pages 93-98

  Mizui, Toshiyuki ^a,c   Ishikawa, Yasuyuki ^b,c   Kumanogoh, Haruko ^a,c   Kojima, Masami ^a,c  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b MAEBASHI INSTITUTE OF TECHNOLOGY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

BDNF; Hippocampus; Long term depression; Polymorphism; Pro peptide

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; METHIONINE; NEUROTROPHIN; NEUROTROPHIN 3 RECEPTOR; NEUROTROPHIN RECEPTOR; VALINE; BRAIN-DERIVED NEUROTROPHIC FACTOR PRECURSOR; PROTEIN PRECURSOR;

HUMAN; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROBIOLOGY; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; ANIMAL; GENETIC POLYMORPHISM; GENETICS; LONG TERM DEPRESSION; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; HUMANS; LONG-TERM SYNAPTIC DEPRESSION; NEURONAL PLASTICITY; POLYMORPHISM, GENETIC; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84961329812     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.12.019     Document Type: Review

References (75)

1. M. Bibel, and Y.A. Barde Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system Genes Dev. 14 23 2000 2919 2937
2. H. Park, and M.M. Poo Neurotrophin regulation of neural circuit development and function Nat. Rev. Neurosci. 14 1 2013 7 23
3. R. Levi-Montalcini, and V. Hamburger A diffusible agent of mouse sarcoma, producing hyperplasia of sympathetic-ganglia and hyperneurotization of viscera in the chick embryo J. Exp. Zool. 123 2 1953 233 287
4. S. Cohen, and R. Levi-Montalcini A nerve growth-stimulating factor isolated from snake venom Proc. Natl. Acad. Sci. U. S. A. 42 9 1956 571 574
5. S. Cohen Purification of a nerve-growth promoting protein from the mouse salivary gland and its neuro-cytotoxic antiserum Proc. Natl. Acad. Sci. U. S. A. 46 3 1960 302 311
6. V. Bocchini, and P.U. Angeletti The nerve growth factor: purification as a 30,000-molecular-weight protein Proc. Natl. Acad. Sci. U. S. A. 64 2 1969 787 794
7. Y.A. Barde, D. Edgar, and H. Thoenen Purification of a new neurotrophic factor from mammalian brain EMBO J. 1 5 1982 549 553
8. J. Leibrock, F. Lottspeich, A. Hohn, M. Hofer, B. Hengerer, P. Masiakowski, H. Thoenen, and Y.A. Barde Molecular cloning and expression of brain-derived neurotrophic factor Nature 341 6238 1989 149 152
9. P.C. Maisonpierre, L. Belluscio, S. Squinto, N.Y. Ip, M.E. Furth, R.M. Lindsay, and G.D. Yancopoulos Neurotrophin-3: a neurotrophic factor related to NGF and BDNF Science 247 1990 1446 1451 (4949 Pt 1)
10. N.Y. Ip, C.F. Ibanez, S.H. Nye, J. McClain, P.F. Jones, D.R. Gies, L. Belluscio, M.M. Le Beau, R. Espinosa 3rd, S.P. Squinto, and et al. Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity Proc. Natl. Acad. Sci. U. S. A. 89 7 1992 3060 3064
11. V. Lessmann, K. Gottmann, and M. Malcangio Neurotrophin secretion: current facts and future prospects Prog. Neurobiol. 69 5 2003 341 374
12. N.G. Seidah, S. Benjannet, S. Pareek, M. Chretien, and R.A. Murphy Cellular processing of the neurotrophin precursors of NT3 and BDNF by the mammalian proprotein convertases FEBS Lett. 379 3 1996 247 250
13. R. Lee, P. Kermani, K.K. Teng, and B.L. Hempstead Regulation of cell survival by secreted proneurotrophins Science 294 5548 2001 1945 1948
14. P.T. Pang, H.K. Teng, E. Zaitsev, N.T. Woo, K. Sakata, S. Zhen, K.K. Teng, W.H. Yung, B.L. Hempstead, and B. Lu Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity Science 306 5695 2004 487 491
15. B. Lu, P.T. Pang, and N.H. Woo The yin and yang of neurotrophin action Nat. Rev. Neurosci. 6 8 2005 603 614
16. S.J. Mowla, S. Pareek, H.F. Farhadi, K. Petrecca, J.P. Fawcett, N.G. Seidah, S.J. Morris, W.S. Sossin, and R.A. Murphy Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons J. Neurosci. 19 6 1999 2069 2080
17. V. Lessmann, and T. Brigadski Mechanisms, locations, and kinetics of synaptic BDNF secretion: an update Neurosci. Res. 65 1 2009 11 22
18. M.V. Chao Neurotrophins and their receptors: a convergence point for many signalling pathways Nat. Rev. Neurosci. 4 4 2003 299 309
19. E. Liepinsh, L.L. Ilag, G. Otting, and C.F. Ibanez NMR structure of the death domain of the p75 neurotrophin receptor EMBO J. 16 16 1997 4999 5005
20. X.L. He, and K.C. Garcia Structure of nerve growth factor complexed with the shared neurotrophin receptor p75 Science 304 5672 2004 870 875
21. B.L. Hempstead Deciphering proneurotrophin actions Handb. Exp. Pharmacol. 220 2014 17 32
22. L.F. Reichardt Neurotrophin-regulated signalling pathways Philos. Trans. R. Soc. Lond. B: Biol. Sci. 361 1473 2006 1545 1564
23. B.L. Hempstead The many faces of p75NTR Curr. Opin. Neurobiol. 12 3 2002 260 267
24. K.K. Teng, S. Felice, T. Kim, and B.L. Hempstead Understanding proneurotrophin actions: recent advances and challenges Dev. Neurobiol. 70 5 2010 350 359
25. C.F. Ibanez, and A. Simi p75 Neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity Trends Neurosci. 35 7 2012 431 440
26. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 6407 1993 31 39
27. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 1 2004 5 21
28. U. Frey, M. Krug, K.G. Reymann, and H. Matthies Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA 1 region in vitro Brain Res. 452 1-2 1988 57 65
29. Y.Y. Huang, and E.R. Kandel Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization Learn. Mem. 1 1 1994 74 82
30. S.L. Patterson, L.M. Grover, P.A. Schwartzkroin, and M. Bothwell Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs Neuron 9 6 1992 1081 1088
31. E. Castren, M. Pitkanen, J. Sirvio, A. Parsadanian, D. Lindholm, H. Thoenen, and P.J. Riekkinen The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus Neuroreport 4 7 1993 895 898
32. F. Zafra, B. Hengerer, J. Leibrock, H. Thoenen, and D. Lindholm Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors EMBO J. 9 11 1990 3545 3550
33. P.J. Isackson, M.M. Huntsman, K.D. Murray, and C.M. Gall BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF Neuron 6 6 1991 937 948
34. L.J. Goodman, J. Valverde, F. Lim, M.D. Geschwind, H.J. Federoff, A.I. Geller, and F. Hefti Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons Mol. Cell. Neurosci. 7 3 1996 222 238
35. M. Canossa, O. Griesbeck, B. Berninger, G. Campana, R. Kolbeck, and H. Thoenen Neurotrophin release by neurotrophins: implications for activity-dependent neuronal plasticity Proc. Natl. Acad. Sci. U. S. A. 94 24 1997 13279 13286
36. V. Lessmann, K. Gottmann, and R. Heumann BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones NeuroReport 6 1 1994 21 25
37. E.S. Levine, C.F. Dreyfus, I.B. Black, and M.R. Plummer Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors Proc. Natl. Acad. Sci. U. S. A. 92 17 1995 8074 8077
38. A. Figurov, L.D. Pozzo-Miller, P. Olafsson, T. Wang, and B. Lu Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus Nature 381 6584 1996 706 709
39. H. Kang, A.A. Welcher, D. Shelton, and E.M. Schuman Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation Neuron 19 3 1997 653 664
40. P. Ernfors, K.F. Lee, and R. Jaenisch Mice lacking brain-derived neurotrophic factor develop with sensory deficits Nature 368 6467 1994 147 150
41. K.R. Jones, I. Farinas, C. Backus, and L.F. Reichardt Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development Cell 76 6 1994 989 999
42. S.L. Patterson, T. Abel, T.A. Deuel, K.C. Martin, J.C. Rose, and E.R. Kandel Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice Neuron 16 6 1996 1137 1145
43. M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, and T. Bonhoeffer Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor Proc. Natl. Acad. Sci. U. S. A. 92 19 1995 8856 8860
44. M. Korte, O. Griesbeck, C. Gravel, P. Carroll, V. Staiger, H. Thoenen, and T. Bonhoeffer Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice Proc. Natl. Acad. Sci. U. S. A. 93 22 1996 12547 12552
45. F. Yang, X. He, L. Feng, K. Mizuno, X.W. Liu, J. Russell, W.C. Xiong, and B. Lu PI-3 kinase and IP3 are both necessary and sufficient to mediate NT3-induced synaptic potentiation Nat. Neurosci. 4 1 2001 19 28
46. B. Xu, W. Gottschalk, A. Chow, R.I. Wilson, E. Schnell, K. Zang, D. Wang, R.A. Nicoll, B. Lu, and L.F. Reichardt The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB J. Neurosci. 20 18 2000 6888 6897
47. L. Minichiello, A.M. Calella, D.L. Medina, T. Bonhoeffer, R. Klein, and M. Korte Mechanism of TrkB-mediated hippocampal long-term potentiation Neuron 36 1 2002 121 137
48. P.C. Suen, K. Wu, E.S. Levine, H.T. Mount, J.L. Xu, S.Y. Lin, and I.B. Black Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-d-aspartate receptor subunit 1 Proc. Natl. Acad. Sci. U. S. A. 94 15 1997 8191 8195
49. S.Y. Lin, K. Wu, E.S. Levine, H.T. Mount, P.C. Suen, and I.B. Black BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities Brain Res. Mol. Brain Res. 55 1 1998 20 27
50. M. Narisawa-Saito, Y. Iwakura, M. Kawamura, K. Araki, S. Kozaki, N. Takei, and H. Nawa Brain-derived neurotrophic factor regulates surface expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethylmaleimide-sensitive factor/GluR2 interaction in developing neocortical neurons J. Biol. Chem. 277 43 2002 40901 40910
51. M.M. Holm, J.L. Nieto-Gonzalez, I. Vardya, C.B. Vaegter, A. Nykjaer, and K. Jensen Mature BDNF, but not proBDNF, reduces excitability of fast-spiking interneurons in mouse dentate gyrus J. Neurosci. 29 40 2009 12412 12418
52. V. Chevaleyre, and P.E. Castillo Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability Neuron 38 3 2003 461 472
53. N.H. Woo, H.K. Teng, C.J. Siao, C. Chiaruttini, P.T. Pang, T.A. Milner, B.L. Hempstead, and B. Lu Activation of p75NTR by proBDNF facilitates hippocampal long-term depression Nat. Neurosci. 8 8 2005 1069 1077
54. H.K. Teng, K.K. Teng, R. Lee, S. Wright, S. Tevar, R.D. Almeida, P. Kermani, R. Torkin, Z.Y. Chen, F.S. Lee, R.T. Kraemer, A. Nykjaer, and B.L. Hempstead ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin J. Neurosci. 25 22 2005 5455 5463
55. K. Deinhardt, T. Kim, D.S. Spellman, R.E. Mains, B.A. Eipper, T.A. Neubert, M.V. Chao, and B.L. Hempstead Neuronal growth cone retraction relies on proneurotrophin receptor signaling through Rac Sci. Signal. 4 202 2011 ra82
56. H. Koshimizu, K. Kiyosue, T. Hara, S. Hazama, S. Suzuki, K. Uegaki, G. Nagappan, E. Zaitsev, T. Hirokawa, Y. Tatsu, A. Ogura, B. Lu, and M. Kojima Multiple functions of precursor BDNF to CNS neurons: negative regulation of neurite growth, spine formation and cell survival Mol. Brain 2 2009 27
57. M.F. Egan, M. Kojima, J.H. Callicott, T.E. Goldberg, B.S. Kolachana, A. Bertolino, E. Zaitsev, B. Gold, D. Goldman, M. Dean, B. Lu, and D.R. Weinberger The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function Cell 112 2 2003 257 269
58. K.G. Bath, and F.S. Lee Variant BDNF (Val66Met) impact on brain structure and function Cogn. Affect Behav. Neurosci. 6 1 2006 79 85
59. R. Kolbeck, S. Jungbluth, and Y.A. Barde Characterisation of neurotrophin dimers and monomers Eur. J. Biochem. 225 3 1994 995 1003
60. M. Silhol, S. Arancibia, T. Maurice, and L. Tapia-Arancibia Spatial memory training modifies the expression of brain-derived neurotrophic factor tyrosine kinase receptors in young and aged rats Neuroscience 146 3 2007 962 973
61. E. Tongiorgi, M. Righi, and A. Cattaneo Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons J. Neurosci. 17 24 1997 9492 9505
62. M. Simonato, G. Bregola, M. Armellin, P. Del Piccolo, D. Rodi, S. Zucchini, and E. Tongiorgi Dendritic targeting of mRNAs for plasticity genes in experimental models of temporal lobe epilepsy Epilepsia 43 Suppl. 5 2002 153 158
63. E. Tongiorgi, M. Armellin, P.G. Giulianini, G. Bregola, S. Zucchini, B. Paradiso, O. Steward, A. Cattaneo, and M. Simonato Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis J. Neurosci. 24 30 2004 6842 6852
64. C. Chiaruttini, M. Sonego, G. Baj, M. Simonato, and E. Tongiorgi BDNF mRNA splice variants display activity-dependent targeting to distinct hippocampal laminae Mol. Cell. Neurosci. 37 1 2008 11 19
65. M.E. Greenberg, B. Xu, B. Lu, and B.L. Hempstead New insights in the biology of BDNF synthesis and release: implications in CNS function J. Neurosci. 29 41 2009 12764 12767
66. G. Nagappan, E. Zaitsev, V.V. Senatorov Jr., J. Yang, B.L. Hempstead, and B. Lu Control of extracellular cleavage of ProBDNF by high frequency neuronal activity Proc. Natl. Acad. Sci. U. S. A. 106 4 2009 1267 1272
67. J. Yang, C.J. Siao, G. Nagappan, T. Marinic, D. Jing, K. McGrath, Z.Y. Chen, W. Mark, L. Tessarollo, F.S. Lee, B. Lu, and B.L. Hempstead Neuronal release of proBDNF Nat. Neurosci. 12 2 2009 113 115
68. J. Yang, L.C. Harte-Hargrove, C.J. Siao, T. Marinic, R. Clarke, Q. Ma, D. Jing, J.J. Lafrancois, K.G. Bath, W. Mark, D. Ballon, F.S. Lee, H.E. Scharfman, and B.L. Hempstead proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus Cell Rep. 7 3 2014 796 806
69. T. Mizui, Y. Ishikawa, H. Kumanogoh, M. Lume, T. Matsumoto, T. Hara, S. Yamawaki, M. Takahashi, S. Shiosaka, C. Itami, K. Uegaki, M. Saarma, and M. Kojima BDNF pro-peptide actions facilitate hippocampal LTD and are altered by the common BDNF polymorphism Val66Met Proc. Natl. Acad. Sci. U. S. A. 112 23 2015 E3067 E3074
70. I. Ninan, K.G. Bath, K. Dagar, R. Perez-Castro, M.R. Plummer, F.S. Lee, and M.V. Chao The BDNF Val66Met polymorphism impairs NMDA receptor-dependent synaptic plasticity in the hippocampus J. Neurosci. 30 26 2010 8866 8870
71. A. Anastasia, K. Deinhardt, M.V. Chao, N.E. Will, K. Irmady, F.S. Lee, B.L. Hempstead, and C. Bracken Val66Met polymorphism of BDNF alters prodomain structure to induce neuronal growth cone retraction Nat. Commun. 4 2013 2490
72. K. Sugase, H.J. Dyson, and P.E. Wright Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 447 7147 2007 1021 1025
73. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 2 1999 321 331
74. W. Guo, Y. Ji, S. Wang, Y. Sun, and B. Lu Neuronal activity alters BDNF-TrkB signaling kinetics and downstream functions J. Cell Sci. 127 Pt 10 2014 2249 2260
75. S. Dieni, T. Matsumoto, M. Dekkers, S. Rauskolb, M.S. Ionescu, R. Deogracias, E.D. Gundelfinger, M. Kojima, S. Nestel, M. Frotscher, and Y.A. Barde BDNF and its pro-peptide are stored in presynaptic dense core vesicles in brain neurons J. Cell Biol. 196 6 2012 775 788