Neurotrophin signalling: Novel insights into mechanisms and pathophysiology

Clinical Science

Volumn 131, Issue 1, 2017, Pages 13-23

  Mitre, Mariela ^a   Mariga, Abigail ^a   Chao, Moses V ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activity dependent expression; Deep brain stimulation; Neuroprotection; Neurotrophin; Signalling; Synaptic plasticity

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; TROPOMYOSIN; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANXIETY DISORDER; BRAIN DEPTH STIMULATION; CLINICAL OUTCOME; DEGENERATIVE DISEASE; DEPRESSION; ELECTROCONVULSIVE THERAPY; HUMAN; HUNTINGTON CHOREA; MEDICAL DECISION MAKING; NERVE CELL PLASTICITY; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; GENETICS; METABOLISM;

ANIMALS; BRAIN; HUMANS; NERVE GROWTH FACTORS; NEURODEGENERATIVE DISEASES; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 85014053606     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160044     Document Type: Review

References (124)

1. Levi-Montalcini, R. (1964) Growth control of nerve cells by a protein factor and its antiserum. Science 143, 105-110.
2. Levi-Montalcini, R. and Booker, B. (1960) Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein. Proc. Natl. Acad. Sci. U.S.A. 46, 384-391.
3. Levi-Montalcini, R. and Angeletti, P.U. (1963) Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro. Dev. Biol. 6, 653-659.
4. Davies, A.M., Bandtlow, C., Heumann, R., Korsching, S., Rohrer, H. and Thoenen, H. (1987) Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. Nature 326, 353-358.
5. Sutter, A., Riopelle, R.J., Harris-Warrick, R.M. and Shooter, E.M. (1979) Nerve growth factor receptors. Characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J. Biol. Chem. 254, 5972-5982.
6. Dumas, M., Schwab, M.E. and Thoenen, H. (1979) Retrograde axonal transport of specific macromolecules as a tool for characterizing nerve terminal membranes. J. Neurobiol. 10, 179-197.
7. Thoenen, H. (1995) Neurotrophins and neuronal plasticity. Science 270, 593-598.
8. Ginty, D.D. and Segal, R.A. (2002) Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 12, 268-274.
9. Park, H. and Poo, M.M. (2013) Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14, 7-23.
10. Cohen-Cory, S. and Fraser, S.E. (1995) Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196.
11. Korte, M., Carroll, P., Wolf, E., Brem, G., Thoenen, H. and Bonhoeffer, T. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. U.S.A. 92, 8856-8860.
12. Pozzo-Miller, L.D., Gottschalk, W., Zhang, L., McDermott, K., Du, J., Gopalakrishnan, R. et al. (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J. Neurosci. 19, 4972-4983.
13. Jeanneteau, F., Deinhardt, K., Miyoshi, G., Bennett, A.M. and Chao, M.V. (2010) The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nat. Neurosci. 13, 1373-1379.
14. Chao, M.V. and Hempstead, B.L. (1995) p75 and Trk: a two-receptor system. Trends Neurosci. 18, 321-326.
15. Hempstead, B.L., Martin-Zanca, D., Kaplan, D.R., Parada, L.F. and Chao, M.V. (1991) High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-683.
16. Squinto, S.P., Stitt, T.N., Aldrich, T.H., Davis, S., Bianco, S.M., Radziejewski, C. 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.
17. Benedetti, M., Levi, A. and Chao, M.V. (1993) Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc. Natl. Acad. Sci. U.S.A. 90, 7859-7863.
18. Bibel, M., Hoppe, E. and Barde, Y.A. (1999) Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J. 18, 616-622.
19. Esposito, D., Patel, P., Stephens, R.M., Perez, P., Chao, M.V., Kaplan, D.R. et al. (2001) The cytoplasmic and transmembrane domains of the p75 and Trk A receptors regulate high affinity binding to nerve growth factor. J. Biol. Chem. 276, 32687-32695.
20. Yano, H., Torkin, R., Martin, L.A., Chao, M.V. and Teng, K.K. (2009) Proneurotrophin-3 is a neuronal apoptotic ligand: evidence for retrograde-directed cell killing. J. Neurosci. 29, 14790-14802.
21. Deinhardt, K., Kim, T., Spellman, D.S., Mains, R.E., Eipper, B.A., Neubert, T.A. et al. (2011) Neuronal growth cone retraction relies on proneurotrophin receptor signaling through Rac. Sci. Signal. 4, ra82.
22. Teng, H.K., Teng, K.K., Lee, R., Wright, S., Tevar, S., Almeida, R.D. et al. (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J. Neurosci. 25, 5455-5463.
23. Nykjaer, A., Lee, R., Teng, K.K., Jansen, P., Madsen, P., Nielsen, M.S. et al. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-848.
24. Lee, R., Kermani, P., Teng, K.K. and Hempstead, B.L. (2001) Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948.
25. Ventriglia, M., Bocchio Chiavetto, L., Benussi, L., Binetti, G., Zanetti, O., Riva, M.A. et al. (2002) Association between the BDNF 196 A/G polymorphism and sporadic Alzheimer's disease. Mol. Psychiatry. 7, 136-7.
26. Sklar, P., Gabriel, S.B., McInnis, M.G., Bennett, P., Lim, Y., Tsan, G. et al. (2002) Family-based association study of 76 candidate genes in bipolar disorder: BDNF is a potential risk locus. Brain-derived neutrophic factor. Mol. Psychiatry 7, 579-93.
27. Neves-Pereira, M., Mundo, E., Muglia, P., King, N., Macciardi, F. and Kennedy, J.L. (2002) The brain-derived neurotrophic factor gene confers susceptibility to bipolar disorder: evidence from a family-based association study. Am. J. Hum. Genet. 71, 651-655.
28. Shimizu, E., Hashimoto, K. and Iyo, M. (2004) Ethnic difference of the BDNF 196G/A (val66met) polymorphism frequencies: the possibility to explain ethnic mental traits. Am. J. Med. Genet. B Neuropsychiatr. Genet. 126B, 122-123.
29. Egan, M.F., Kojima, M., Callicott, J.H., Goldberg, T.E., Kolachana, B.S., Bertolino, A. et al. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112, 257-269.
30. Chen, Z.Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C. J., Herrera, D. G., Toth, M., Yang, C., McEwen, B. S., Hempstead, B. L. and Lee, F.S. (2006) Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143.
31. Anastasia, A., Deinhardt, K., Chao, M.V., Will, N.E., Irmady, K., Lee, F.S. et al. (2013) Val66Met polymorphism of BDNF alters prodomain structure to induce neuronal growth cone retraction. Nat. Commun. 4, 2490.
32. Pucilowska, J., Vithayathil, J., Tavares, E.J., Kelly, C., Karlo, J.C. and Landreth, G.E. (2015) The 16p11.2 deletion mouse model of autism exhibits altered cortical progenitor proliferation and brain cytoarchitecture linked to the ERK MAPK pathway. J. Neurosci. 35, 3190-3200.
33. Xia, Y., Wang, C.Z., Liu, J., Anastasio, N.C. and Johnson, K.M. (2010) Brain-derived neurotrophic factor prevents phencyclidine-induced apoptosis in developing brain by parallel activation of both the ERK and PI-3K/Akt pathways. Neuropharmacology 58, 330-336.
34. Gu, B., Huang, Y.Z., He, X.P., Joshi, R.B., Jang, W. and McNamara, J.O. (2015) A peptide uncoupling BDNF receptor TrkB from phospholipase Cgamma1 prevents epilepsy induced by status Epilepticus. Neuron 88, 484-491.
35. Lee, F.S. and Chao, M.V. (2001) Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc. Natl. Acad. Sci. U.S.A. 98, 3555-3560.
36. Lee, F.S., Rajagopal, R., Kim, A.H., Chang, P.C. and Chao, M.V. (2002) Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J. Biol. Chem. 277, 9096-9102.
37. Takei, N., Torres, E., Yuhara, A., Jongsma, H., Otto, C., Korhonen, L. et al. (2000) Pituitary adenylate cyclase-activating polypeptide promotes the survival of basal forebrain cholinergic neurons in vitro and in vivo: comparison with effects of nerve growth factor. Eur. J. Neurosci. 12, 2273-2280.
38. Puehringer, D., Orel, N., Luningschror, P., Subramanian, N., Herrmann, T., Chao, M.V. et al. (2013) EGF transactivation of Trk receptors regulates the migration of newborn cortical neurons. Nat. Neurosci. 16, 407-415.
39. Jeanneteau, F., Garabedian, M.J. and Chao, M.V. (2008) Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect. Proc. Natl. Acad. Sci. U.S.A. 105, 4862-4867.
40. Iwakura, Y., Nawa, H., Sora, I. and Chao, M.V. (2008) Dopamine D1 receptor-induced signaling through TrkB receptors in striatal neurons. J. Biol. Chem. 283, 15799-15806.
41. Huang, Y.Z., Pan, E., Xiong, Z.Q. and McNamara, J.O. (2008) Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fiber-CA3 pyramid synapse. Neuron 57, 546-558.
42. Jeanneteau, F.D., Lambert, W.M., Ismaili, N., Bath, K.G., Lee, F.S., Garabedian, M.J. et al. (2012) BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus. Proc. Natl. Acad. Sci. U.S.A. 109, 1305-1310.
43. Lambert, W.M., Xu, C.F., Neubert, T.A., Chao, M.V., Garabedian, M.J. and Jeanneteau, F.D. (2013) Brain-derived neurotrophic factor signaling rewrites the glucocorticoid transcriptome via glucocorticoid receptor phosphorylation. Mol. Cell. Biol. 33, 3700-3714.
44. Arango-Lievano, M., Lambert, W.M., Bath, K.G., Garabedian, M.J., Chao, M.V. and Jeanneteau, F. (2015) Neurotrophic-priming of glucocorticoid receptor signaling is essential for neuronal plasticity to stress and antidepressant treatment. Proc. Natl. Acad. Sci. U.S.A. 112, 15737-15742.
45. Gartner, A., Polnau, D.G., Staiger, V., Sciarretta, C., Minichiello, L., Thoenen, H. et al. (2006) Hippocampal long-term potentiation is supported by presynaptic and postsynaptic tyrosine receptor kinase B-mediated phospholipase Cgamma signaling. J. Neurosci. 26, 3496-3504.
46. Lu, Y., Ji, Y., Ganesan, S., Schloesser, R., Martinowich, K., Sun, M. et al. (2011) TrkB as a potential synaptic and behavioral tag. J. Neurosci. 31, 11762-11771.
47. Slack, S.E., Pezet, S., McMahon, S.B., Thompson, S.W. and Malcangio, M. (2004) Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord. Eur. J. Neurosci. 20, 1769-1778.
48. Cao, C., Rioult-Pedotti, M.S., Migani, P., Yu, C.J., Tiwari, R., Parang, K. et al. (2013) Impairment of TrkB-PSD-95 signaling in Angelman syndrome. PLoS Biol. 11, e1001478.
49. Suzuki, K., Sato, M., Morishima, Y. and Nakanishi, S. (2005) Neuronal depolarization controls brain-derived neurotrophic factor-induced upregulation of NR2C NMDA receptor via calcineurin signaling. J. Neurosci. 25, 9535-9543.
50. Elmariah, S.B., Crumling, M.A., Parsons, T.D. and Balice-Gordon, R.J. (2004) Postsynaptic TrkB-mediated signaling modulates excitatory and inhibitory neurotransmitter receptor clustering at hippocampal synapses. J. Neurosci. 24, 2380-2393.
51. Mariga, A., Glaser, J., Mathias, L., Xu, D., Xiao, M., Worley, P. et al. (2015) Definition of a bidirectional activity-dependent pathway involving BDNF and Narp. Cell Rep. 13, 1-10.
52. Pang, P.T., Teng, H.K., Zaitsev, E., Woo, N.T., Sakata, K., Zhen, S. et al. (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491.
53. Lussier, M.P., Sanz-Clemente, A. and Roche, K.W. (2015) Dynamic regulation of N-methyl-D-aspartate (NMDA) and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by posttranslational modifications. J. Biol. Chem. 290, 28596-28603.
54. Lin, S.Y., Wu, K., Levine, E.S., Mount, H.T., Suen, P.C. and Black, I.B. (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20-27.
55. Suen, P.C., Wu, K., Levine, E.S., Mount, H.T., Xu, J.L., Lin, S.Y. et al. (1997) 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, 8191-8195.
56. Hawrylycz, M.J., Lein, E.S., Guillozet-Bongaarts, A.L., Shen, E.H., Ng, L., Miller, J.A. et al. (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489, 391-399.
57. Thoenen, H. and Sendtner, M. (2002) Neurotrophins: from enthusiastic expectations through sobering experiences to rational therapeutic approaches. Nat. Neurosci. 5 (Suppl.), 1046-1050.
58. Williams, L.R., Varon, S., Peterson, G.M., Wictorin, K., Fischer, W., Bjorklund, A. et al. (1986) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl. Acad. Sci. U.S.A. 83, 9231-9235.
59. Durany, N., Michel, T., Kurt, J., Cruz-Sanchez, F.F., Cervas-Navarro, J. and Riederer, P. (2000) Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer's disease brains. Int. J. Dev. Neurosci. 18, 807-13.
60. Hock, C., Heese, K., Hulette, C., Rosenberg, C. and Otten, U. (2000) Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch. Neurol. 57, 846-851.
61. Phillips, H.S., Hains, J.M., Armanini, M., Laramee, G.R., Johnson, S.A. and Winslow, J.W. (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695-702.
62. Murer, M.G., Yan, Q. and Raisman-Vozari, R. (2001) Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 63, 71-124.
63. Narisawa-Saito, M., Wakabayashi, K., Tsuji, S., Takahashi, H. and Nawa, H. (1996) Regional specificity of alterations in NGF, BDNF and NT-3 levels in Alzheimer's disease. Neuroreport 7, 2925-2928.
64. Murer, M.G., Boissiere, F., Yan, Q., Hunot, S., Villares, J., Faucheux, B. et al. (1999) An immunohistochemical study of the distribution of brain-derived neurotrophic factor in the adult human brain, with particular reference to Alzheimer's disease. Neuroscience 88, 1015-1032.
65. Benedetti, E., D'Angelo, B., Cristiano, L., Di Giacomo, E., Fanelli, F., Moreno, S. et al. (2014) Involvement of peroxisome proliferator-activated receptor beta/delta (PPAR beta/delta) in BDNF signaling during aging and in Alzheimer disease: possible role of 4-hydroxynonenal (4-HNE). Cell Cycle 13, 1335-1344.
66. Nagahara, A.H., Merrill, D.A., Coppola, G., Tsukada, S., Schroeder, B.E., Shaked, G.M. et al. (2009) Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat. Med. 15, 331-337.
67. Blurton-Jones, M., Kitazawa, M., Martinez-Coria, H., Castello, N.A., Muller, F.J., Loring, J.F. et al. (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 106, 13594-13599.
68. Mariga, A., Zavadil, J., Ginsberg, S.D. and Chao, M.V. (2015) Withdrawal of BDNF from hippocampal cultures leads to changes in genes involved in synaptic function. Dev. Neurobiol. 75, 173-192.
69. Berchtold, N.C., Coleman, P.D., Cribbs, D.H., Rogers, J., Gillen, D.L. and Cotman, C.W. (2013) Synaptic genes are extensively downregulated across multiple brain regions in normal human aging and Alzheimer's disease. Neurobiol. Aging 34, 1653-1661.
70. Ginsberg, S.D., Alldred, M.J. and Che, S. (2012) Gene expression levels assessed by CA1 pyramidal neuron and regional hippocampal dissections in Alzheimer's disease. Neurobiol. Dis. 45, 99-107.
71. Duffy, A.M., Schaner, M.J., Wu, S.H., Staniszewski, A., Kumar, A., Arevalo, J.C. et al. (2011) A selective role for ARMS/Kidins220 scaffold protein in spatial memory and trophic support of entorhinal and frontal cortical neurons. Exp. Neurol. 229, 409-420.
72. Goldberg, N.R., Caesar, J., Park, A., Sedgh, S., Finogenov, G., Masliah, E. et al. (2015) Neural stem cells rescue cognitive and motor dysfunction in a transgenic model of dementia with lewy bodies through a BDNF-dependent mechanism. Stem Cell Reports 5, 791-804.
73. Parain, K., Murer, M.G., Yan, Q., Faucheux, B., Agid, Y., Hirsch, E. et al. (1999) Reduced expression of BDNF protein in Parkinson's disease substantia nigra. Neuroreport 10, 557-561.
74. Fenner, M.E., Achim, C.L. and Fenner, B.M. (2014) Expression of full-length and truncated trkB in human striatum and substantia nigra neurons: implications for Parkinson's disease. J. Mol. Histol. 45, 349-361.
75. Jha, S.K., Jha, N.K., Kar, R., Ambasta, R.K. and Kumar, P. (2015) p38 MAPK and PI3K/AKT signalling cascades in Parkinson's disease. Int. J. Mol. Cell. Med. 4, 67-86.
76. Mogi, M., Togari, A., Kondo, T., Mizuno, Y., Komure, O., Kuno, S. et al. (1999) Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 270, 45-48.
77. Kohno, R., Sawada, H., Kawamoto, Y., Uemura, K., Shibasaki, H. and Shimohama, S. (2004) BDNF is induced by wild-type alpha-synuclein but not by the two mutants, A30P or A53T, in glioma cell line. Biochem. Biophys. Res. Commun. 318, 113-118.
78. Zuccato, C. and Cattaneo, E. (2009) Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5, 311-322.
79. Porritt, M.J., Batchelor, P.E. and Howells, D.W. (2005) Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Exp. Neurol. 192, 226-234.
80. Baquet, Z.C., Gorski, J.A. and Jones, K.R. (2004) Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci. 24, 4250-4258.
81. Fumagalli, F., Racagni, G., Colombo, E. and Riva, M.A. (2003) BDNF gene expression is reduced in the frontal cortex of dopamine transporter knockout mice. Mol. Psychiatry 8, 898-899.
82. Nguyen, K.Q., Rymar, V.V. and Sadikot, A.F. (2016) Impaired TrkB signaling underlies reduced BDNF-mediated trophic support of striatal neurons in the R6/2 mouse model of Huntington's disease. Front. Cell. Neurosci. 10, 37.
83. Altar, C.A., Cai, N., Bliven, T., Juhasz, M., Conner, J.M., Acheson, A.L. et al. (1997) Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389, 856-860.
84. Gauthier, L.R., Charrin, B.C., Borrell-Pages, M., Dompierre, J.P., Rangone, H., Cordelieres, F.P. et al. (2004) Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118, 127-138.
85. Zuccato, C., Ciammola, A., Rigamonti, D., Leavitt, B.R., Goffredo, D., Conti, L. et al. (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293, 493-498.
86. Zuccato, C. and Cattaneo, E. (2007) Role of brain-derived neurotrophic factor in Huntington's disease. Prog. Neurobiol. 81, 294-330.
87. Zuccato, C., Marullo, M., Conforti, P., MacDonald, M.E., Tartari, M. and Cattaneo, E. (2008) Systematic assessment of BDNF and its receptor levels in human cortices affected by Huntington's disease. Brain Pathol 18, 225-238.
88. Strand, A.D., Baquet, Z.C., Aragaki, A.K., Holmans, P., Yang, L., Cleren, C. et al. (2007) Expression profiling of Huntington's disease models suggests that brain-derived neurotrophic factor depletion plays a major role in striatal degeneration. J. Neurosci. 27, 11758-11768.
89. Jeon, J., Kim, W., Jang, J., Isacson, O. and Seo, H. (2016) Gene therapy by proteasome activator, PA28gamma, improves motor coordination and proteasome function in Huntington's disease YAC128 mice. Neuroscience 324, 20-28.
90. Mitsumoto, H., Ikeda, K., Klinkosz, B., Cedarbaum, J.M., Wong, V. and Lindsay, R.M. (1994) Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265, 1107-1110.
91. Korkmaz, O.T., Aytan, N., Carreras, I., Choi, J.K., Kowall, N.W., Jenkins, B.G. et al. (2014) 7, 8-Dihydroxyflavone improves motor performance and enhances lower motor neuronal survival in a mouse model of amyotrophic lateral sclerosis. Neurosci. Lett. 566, 286-291.
92. Todd, D., Gowers, I., Dowler, S.J., Wall, M.D., McAllister, G., Fischer, D.F. et al. (2014) A monoclonal antibody TrkB receptor agonist as a potential therapeutic for Huntington's disease. PLoS One 9, e87923.
93. Fulgenzi, G., Tomassoni-Ardori, F., Babini, L., Becker, J., Barrick, C., Puverel, S. et al. (2015) BDNF modulates heart contraction force and long-term homeostasis through truncated TrkB.T1 receptor activation. J. Cell Biol. 210, 1003-1012.
94. Yanpallewar, S.U., Barrick, C.A., Buckley, H., Becker, J. and Tessarollo, L. (2012) Deletion of the BDNF truncated receptor TrkB.T1 delays disease onset in a mouse model of amyotrophic lateral sclerosis. PLoS One 7, e39946.
95. The BDNF Study Group (Phase III) (1999) A controlled trial of recombinant methionyl human BDNF in ALS. Neurology 52, 1427-1433.
96. Siuciak, J.A., Lewis, D.R., Wiegand, S.J. and Lindsay, R.M. (1997) Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol. Biochem. Behav. 56, 131-137.
97. Shirayama, Y., Chen, A.C., Nakagawa, S., Russell, D.S. and Duman, R.S. (2002) Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22, 3251-3261.
98. Russo-Neustadt, A., Beard, R.C. and Cotman, C.W. (1999) Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology 21, 679-682.
99. Lepack, A.E., Fuchikami, M., Dwyer, J.M., Banasr, M. and Duman, R.S. (2015) BDNF release is required for the behavioral actions of ketamine. Int. J. Neuropsychopharmacol. 18, pyu033.
100. Bjorkholm, C. and Monteggia, L.M. (2016) BDNF-a key transducer of antidepressant effects. Neuropharmacology 102, 72-79.
101. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F. et al. (2011) NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475, 91-95.
102. Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., MacDonald, E. et al. (2003) Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J. Neurosci. 23, 349-357.
103. Hashimoto, T., Bergen, S.E., Nguyen, Q.L., Xu, B., Monteggia, L.M., Pierri, J.N. et al. (2005) Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J. Neurosci. 25, 372-383.
104. Issa, G., Wilson, C., Terry, Jr, A.V. and Pillai, A. (2010) An inverse relationship between cortisol and BDNF levels in schizophrenia: data from human postmortem and animal studies. Neurobiol. Dis. 39, 327-333.
105. Ray, M.T., Shannon Weickert, C. and Webster, M.J. (2014) Decreased BDNF and TrkB mRNA expression in multiple cortical areas of patients with schizophrenia and mood disorders. Transl. Psychiatry 4, e389.
106. Thompson Ray, M., Weickert, C.S., Wyatt, E. and Webster, M.J. (2011) Decreased BDNF, trkB-TK+ and GAD67 mRNA expression in the hippocampus of individuals with schizophrenia and mood disorders. J. Psychiatry Neurosci. 36, 195-203.
107. Weickert, C.S., Hyde, T.M., Lipska, B.K., Herman, M.M., Weinberger, D.R. and Kleinman, J.E. (2003) Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8, 592-610.
108. Wong, J., Hyde, T.M., Cassano, H.L., Deep-Soboslay, A., Kleinman, J.E. and Weickert, C.S. (2010) Promoter specific alterations of brain-derived neurotrophic factor mRNA in schizophrenia. Neuroscience 169, 1071-1084.
109. Weickert, C.S., Ligons, D.L., Romanczyk, T., Ungaro, G., Hyde, T.M., Herman, M.M. et al. (2005) Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 10, 637-650.
110. Lin, Z., Su, Y., Zhang, C., Xing, M., Ding, W., Liao, L. et al. (2013) The interaction of BDNF and NTRK2 gene increases the susceptibility of paranoid schizophrenia. PLoS One 8, e74264.
111. Kranz, T.M., Goetz, R.R., Walsh-Messinger, J., Goetz, D., Antonius, D., Dolgalev, I. et al. (2015) Rare variants in the neurotrophin signaling pathway implicated in schizophrenia risk. Schizophr. Res. 168, 421-428.
112. Arevalo, J.C., Wu, S.H., Takahashi, T., Zhang, H., Yu, T., Yano, H. et al. (2010) The ARMS/Kidins220 scaffold protein modulates synaptic transmission. Mol. Cell Neurosci. 45, 92-100.
113. Arevalo, J.C., Yano, H., Teng, K.K. and Chao, M.V. (2004) A unique pathway for sustained neurotrophin signaling through an ankyrin-rich membrane-spanning protein. EMBO J. 23, 2358-2368.
114. Holtzheimer, P.E., Kelley, M.E., Gross, R.E., Filkowski, M.M., Garlow, S.J., Barrocas, A. et al. (2012) Subcallosal cingulate deep brain stimulation for treatment-resistant unipolar and bipolar depression. Arch. Gen. Psychiatry 69, 150-158.
115. Moldovan, A.S., Groiss, S.J., Elben, S., Sudmeyer, M., Schnitzler, A. and Wojtecki, L. (2015) The treatment of Parkinson's disease with deep brain stimulation: current issues. Neural Regen. Res. 10, 1018-1022.
116. Aksay, S.S., Hausner, L., Frolich, L. and Sartorius, A. (2014) Severe agitation in severe early-onset Alzheimer's disease resolves with ECT. Neuropsychiatr. Dis. Treat. 10, 2147-2151.
117. Hao, S., Tang, B., Wu, Z., Ure, K., Sun, Y., Tao, H. et al. (2015) Forniceal deep brain stimulation rescues hippocampal memory in Rett syndrome mice. Nature 526, 430-434.
118. Sleiman, S.F., Henry, J., Al-Haddad, R., El Hayek, L., Abou Haidar, E., Stringer, T. et al. (2016) Exercise promotes the expression of brain derived neurotrophic factor (BDNF) through the action of the ketone body beta-hydroxybutyrate. eLife 5, e15092.
119. Zetterstrom, T.S., Pei, Q. and Grahame-Smith, D.G. (1998) Repeated electroconvulsive shock extends the duration of enhanced gene expression for BDNF in rat brain compared with a single administration. Brain Res. Mol. Brain Res. 57, 106-110.
120. Intlekofer, K.A. and Cotman, C.W. (2013) Exercise counteracts declining hippocampal function in aging and Alzheimer's disease. Neurobiol. Dis. 57, 47-55.
121. Zheng, K., An, J.J., Yang, F., Xu, W., Xu, Z.Q., Wu, J. et al. (2011) TrkB signaling in parvalbumin-positive interneurons is critical for gamma-band network synchronization in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 108, 17201-17206.
122. Weinstein, G., Beiser, A.S., Choi, S.H., Preis, S.R., Chen, T.C., Vorgas, D. et al. (2014) Serum brain-derived neurotrophic factor and the risk for dementia: the Framingham Heart Study. JAMA Neurol 71, 55-61.
123. Erickson, K.I., Prakash, R.S., Voss, M.W., Chaddock, L., Heo, S., McLaren, M. et al. (2010) Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. J. Neurosci. 30, 5368-5375.
124. Pinyon, J.L., Tadros, S.F., Froud, K.E., Young Acy, Tompson, I.T., Crawford, E.N. et al. (2014) Close-field electroporation gene delivery using the cochlear implant electrode array enhances the bionic ear. Sci. Transl. Med. 6, 233ra54.