Neurotrophin and Wnt signaling cooperatively regulate dendritic spine formation

Molecular and Cellular Neuroscience

Volumn 56, Issue , 2013, Pages 115-127

  Hiester, Brian G ^a   Galati, Domenico F ^a   Salinas, Patricia C ^b   Jones, Kevin R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

BDNF; Dendrite branching; Dendritic spine; Synapse; Wnt signaling

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIN; WNT PROTEIN; WNT2 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DENDRITIC SPINE; HYPOTHESIS; IMAGE ANALYSIS; INHIBITION KINETICS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

BDNF; DENDRITE BRANCHING; DENDRITIC SPINE; SYNAPSE; WNT SIGNALING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL GROWTH PROCESSES; CELLS, CULTURED; CEREBRAL CORTEX; DENDRITIC SPINES; MICE; WNT SIGNALING PATHWAY; WNT2 PROTEIN;

EID: 84878152890     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.04.006     Document Type: Article

References (115)

1. Adachi M., Barrot M., Autry A.E., Theobald D., Monteggia L.M. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 2008, 63:642-649.
2. Adasme T., Haeger P., Paula-Lima A.C., Espinoza I., Casas-Alarcon M.M., Carrasco M.A., Hidalgo C. Involvement of ryanodine receptors in neurotrophin-induced hippocampal synaptic plasticity and spatial memory formation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3029-3034.
3. Ahmad-Annuar A., Ciani L., Simeonidis I., Herreros J., Fredj N.B., Rosso S.B., Hall A., Brickley S., Salinas P.C. Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release. J. Cell Biol. 2006, 174:127-139.
4. Allen Developing Mouse Brain Atlas Allen Developing Mouse Brain Atlas [Internet] 2009, Allen Institute for Brain Science, Seattle (WA), (Available from: http://www.developingmouse.brain-map.org).
5. Alonso M., Medina J.H., Pozzo-Miller L. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn. Mem. 2004, 11:172-178.
6. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
7. Amaral M.D., Pozzo-Miller L. TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J. Neurosci. 2007, 27:5179-5189.
8. Ampuero E., Rubio F.J., Falcon R., Sandoval M., Diaz-Veliz G., Gonzalez R.E., Earle N., Dagnino-Subiabre A., Aboitiz F., Orrego F., Wyneken U. Chronic fluoxetine treatment induces structural plasticity and selective changes in glutamate receptor subunits in the rat cerebral cortex. Neuroscience 2010, 169:98-108.
9. Antar L.N., Li C., Zhang H., Carroll R.C., Bassell G.J. Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. Mol. Cell. Neurosci. 2006, 32:37-48.
10. Arellano J.I., Espinosa A., Fairen A., Yuste R., DeFelipe J. Non-synaptic dendritic spines in neocortex. Neuroscience 2007, 145:464-469.
11. Ataman B., Ashley J., Gorczyca M., Ramachandran P., Fouquet W., Sigrist S.J., Budnik V. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron 2008, 57:705-718.
12. Banasr M., Duman R.S. Keeping 'trk' of antidepressant actions. Neuron 2008, 59:349-351.
13. Baquet Z.C., Gorski J.A., Jones K.R. Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci. 2004, 24:4250-4258.
14. Bodmer D., Levine-Wilkinson S., Richmond A., Hirsh S., Kuruvilla R. Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons. J. Neurosci. 2009, 29:7569-7581.
15. Bracken B.K., Turrigiano G.G. Experience-dependent regulation of TrkB isoforms in rodent visual cortex. Dev. Neurobiol. 2009, 69:267-278.
16. Budnik V., Salinas P.C. Wnt signaling during synaptic development and plasticity. Curr. Opin. Neurobiol. 2011, 21:151-159.
17. Calella A.M., Nerlov C., Lopez R.G., Sciarretta C., von Bohlen und Halbach O., Bereshchenko O., Minichiello L. Neurotrophin/Trk receptor signaling mediates C/EBPalpha, -beta and NeuroD recruitment to immediate-early gene promoters in neuronal cells and requires C/EBPs to induce immediate-early gene transcription. Neural. Dev. 2007, 2:4.
18. Carmon K.S., Loose D.S. Development of a bioassay for detection of Wnt-binding affinities for individual frizzled receptors. Anal. Biochem. 2010, 401:288-294.
19. Castren E., Rantamaki T. The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev. Neurobiol. 2010, 70:289-297.
20. Cerpa W., Godoy J.A., Alfaro I., Farias G.G., Metcalfe M.J., Fuentealba R., Bonansco C., Inestrosa N.C. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J. Biol. Chem. 2008, 283:5918-5927.
21. Cerpa W., Gambrill A., Inestrosa N.C., Barria A. Regulation of NMDA-receptor synaptic transmission by Wnt signaling. J. Neurosci. 2011, 31:9466-9471.
22. Chakravarthy S., Saiepour M.H., Bence M., Perry S., Hartman R., Couey J.J., Mansvelder H.D., Levelt C.N. Postsynaptic TrkB signaling has distinct roles in spine maintenance in adult visual cortex and hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1071-1076.
23. Chapleau C.A., Larimore J.L., Theibert A., Pozzo-Miller L. Modulation of dendritic spine development and plasticity by BDNF and vesicular trafficking: fundamental roles in neurodevelopmental disorders associated with mental retardation and autism. J. Neurodev. Disord. 2009, 1:185-196.
24. Chen J., Park C.S., Tang S.J. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J. Biol. Chem. 2006, 281:11910-11916.
25. Chen B.Y., Wang X., Wang Z.Y., Wang Y.Z., Chen L.W., Luo Z.J. Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/beta-catenin signaling pathway. J. Neurosci. Res. 2013, 91:30-41.
26. Ciani L., Salinas P.C. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat. Rev. Neurosci. 2005, 6:351-362.
27. Ciani L., Boyle K.A., Dickins E., Sahores M., Anane D., Lopes D.M., Gibb A.J., Salinas P.C. Wnt7a signaling promotes dendritic spine growth and synaptic strength through Ca(2)(+)/Calmodulin-dependent protein kinase II. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10732-10737.
28. Cline H., Haas K. The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J. Physiol. 2008, 586:1509-1517.
29. Croce J.C., McClay D.R. Evolution of the Wnt pathways. Methods Mol. Biol. 2008, 469:3-18.
30. Cruz-Martin A., Crespo M., Portera-Cailliau C. Delayed stabilization of dendritic spines in fragile X mice. J. Neurosci. 2010, 30:7793-7803.
31. Davis E.K., Zou Y., Ghosh A. Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocampal synapse formation. Neural. Dev. 2008, 3:32.
32. Doyle J.P., Dougherty J.D., Heiman M., Schmidt E.F., Stevens T.R., Ma G., Bupp S., Shrestha P., Shah R.D., Doughty M.L., Gong S., Greengard P., Heintz N. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 2008, 135:749-762.
33. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59:1116-1127.
34. El-Husseini A.E., Schnell E., Chetkovich D.M., Nicoll R.A., Bredt D.S. PSD-95 involvement in maturation of excitatory synapses. Science 2000, 290:1364-1368.
35. English C.N., Vigers A.J., Jones K.R. Genetic evidence that brain-derived neurotrophic factor mediates competitive interactions between individual cortical neurons. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:19456-19461.
36. Farias G.G., Valles A.S., Colombres M., Godoy J.A., Toledo E.M., Lukas R.J., Barrantes F.J., Inestrosa N.C. Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J. Neurosci. 2007, 27:5313-5325.
37. Farias G.G., Alfaro I.E., Cerpa W., Grabowski C.P., Godoy J.A., Bonansco C., Inestrosa N.C. Wnt-5a/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons. J. Biol. Chem. 2009, 284:15857-15866.
38. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 1998, 18:8900-8911.
39. Freese J.L., Pino D., Pleasure S.J. Wnt signaling in development and disease. Neurobiol. Dis. 2010, 38:148-153.
40. Gaiddon C., Loeffler J.P., Larmet Y. Brain-derived neurotrophic factor stimulates AP-1 and cyclic AMP-responsive element dependent transcriptional activity in central nervous system neurons. J. Neurochem. 1996, 66:2279-2286.
41. Galli L.M., Barnes T., Cheng T., Acosta L., Anglade A., Willert K., Nusse R., Burrus L.W. Differential inhibition of Wnt-3a by Sfrp-1, Sfrp-2, and Sfrp-3. Dev. Dyn. 2006, 235:681-690.
42. Gao C., Chen Y.G. Dishevelled: the hub of Wnt signaling. Cell. Signal. 2010, 22:717-727.
43. Ghosh A., Carnahan J., Greenberg M.E. Requirement for BDNF in activity-dependent survival of cortical neurons. Science 1994, 263:1618-1623.
44. Gogolla N., Galimberti I., Deguchi Y., Caroni P. Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62:510-525.
45. Gorski J.A., Zeiler S.R., Tamowski S., Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J. Neurosci. 2003, 23:6856-6865.
46. Hajszan T., Dow A., Warner-Schmidt J.L., Szigeti-Buck K., Sallam N.L., Parducz A., Leranth C., Duman R.S. Remodeling of hippocampal spine synapses in the rat learned helplessness model of depression. Biol. Psychiatry 2009, 65:392-400.
47. Hale C.F., Dietz K.C., Varela J.A., Wood C.B., Zirlin B.C., Leverich L.S., Greene R.W., Cowan C.W. Essential role for vav Guanine nucleotide exchange factors in brain-derived neurotrophic factor-induced dendritic spine growth and synapse plasticity. J. Neurosci. 2011, 31:12426-12436.
48. Hallbook F. Evolution of the vertebrate neurotrophin and Trk receptor gene families. Curr. Opin. Neurobiol. 1999, 9:616-621.
49. Harris K.M., Kater S.B. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu. Rev. Neurosci. 1994, 17:341-371.
50. Horch H.W., Kruttgen A., Portbury S.D., Katz L.C. Destabilization of cortical dendrites and spines by BDNF. Neuron 1999, 23:353-364.
51. Hsieh J.C., Rattner A., Smallwood P.M., Nathans J. Biochemical characterization of Wnt-frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3546-3551.
52. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24:677-736.
53. Irwin S.A., Patel B., Idupulapati M., Harris J.B., Crisostomo R.A., Larsen B.P., Kooy F., Willems P.J., Cras P., Kozlowski P.B., Swain R.A., Weiler I.J., Greenough W.T. Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am. J. Med. Genet. 2001, 98:161-167.
54. Kaneko M., Xie Y., An J.J., Stryker M.P., Xu B. Dendritic BDNF synthesis is required for late-phase spine maturation and recovery of cortical responses following sensory deprivation. J. Neurosci. 2012, 32:4790-4802.
55. Knott G.W., Holtmaat A., Wilbrecht L., Welker E., Svoboda K. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat. Neurosci. 2006, 9:1117-1124.
56. Kuczewski N., Porcher C., Gaiarsa J.L. Activity-dependent dendritic secretion of brain-derived neurotrophic factor modulates synaptic plasticity. Eur. J. Neurosci. 2010, 32:1239-1244.
57. Lin Y.C., Koleske A.J. Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu. Rev. Neurosci. 2010, 33:349-378.
58. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
59. Lohmann C., Bonhoeffer T. A role for local calcium signaling in rapid synaptic partner selection by dendritic filopodia. Neuron 2008, 59:253-260.
60. Lohmann C., Myhr K.L., Wong R.O. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 2002, 418:177-181.
61. Lu C.S., Van Vactor D. Synapse specificity: Wnts keep motor axons on target. Curr. Biol. 2007, 17:R895-R898.
62. Luikart B.W., Nef S., Virmani T., Lush M.E., Liu Y., Kavalali E.T., Parada L.F. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J. Neurosci. 2005, 25:3774-3786.
63. Madara J.C., Levine E.S. Presynaptic and postsynaptic NMDA receptors mediate distinct effects of brain-derived neurotrophic factor on synaptic transmission. J. Neurophysiol. 2008, 100:3175-3184.
64. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 1999, 283:1923-1927.
65. Malinauskas T., Aricescu A.R., Lu W., Siebold C., Jones E.Y. Modular mechanism of Wnt signaling inhibition by Wnt inhibitory factor 1. Nat. Struct. Mol. Biol. 2011, 18:886-893.
66. Margolis S.S., Salogiannis J., Lipton D.M., Mandel-Brehm C., Wills Z.P., Mardinly A.R., Hu L., Greer P.L., Bikoff J.B., Ho H.Y., Soskis M.J., Sahin M., Greenberg M.E. EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation. Cell 2010, 143:442-455.
67. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
68. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
69. McAllister A.K., Katz L.C., Lo D.C. Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron 1997, 18:767-778.
70. Nimchinsky E.A., Oberlander A.M., Svoboda K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 2001, 21:5139-5146.
71. Norrholm S.D., Ouimet C.C. Altered dendritic spine density in animal models of depression and in response to antidepressant treatment. Synapse 2001, 42:151-163.
72. Okamoto H., Voleti B., Banasr M., Sarhan M., Duric V., Girgenti M.J., Dileone R.J., Newton S.S., Duman R.S. Wnt2 expression and signaling is increased by different classes of antidepressant treatments. Biol. Psychiatry 2010, 68:521-527.
73. Packard M., Mathew D., Budnik V. Wnts and TGF beta in synaptogenesis: old friends signalling at new places. Nat. Rev. Neurosci. 2003, 4:113-120.
74. Pan F., Aldridge G.M., Greenough W.T., Gan W.B. Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17768-17773.
75. Patapoutian A., Backus C., Kispert A., Reichardt L.F. Regulation of neurotrophin-3 expression by epithelial-mesenchymal interactions: the role of Wnt factors. Science 1999, 283:1180-1183.
76. Penzes P., Cahill M.E., Jones K.A., VanLeeuwen J.E., Woolfrey K.M. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 2011, 14:285-293.
77. Pozzo-Miller L. BDNF enhances dendritic Ca2+ signals evoked by coincident EPSPs and back-propagating action potentials in CA1 pyramidal neurons. Brain Res. 2006, 1104:45-54.
78. Purro S.A., Dickins E.M., Salinas P.C. The secreted Wnt antagonist Dickkopf-1 is required for amyloid beta-mediated synaptic loss. J. Neurosci. 2012, 32:3492-3498.
79. Rajan I., Witte S., Cline H.T. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J. Neurobiol. 1999, 38:357-368.
80. Rattner A., Hsieh J.C., Smallwood P.M., Gilbert D.J., Copeland N.G., Jenkins N.A., Nathans J. A family of secreted proteins contains homology to the cysteine-rich ligand-binding domain of frizzled receptors. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2859-2863.
81. Rauskolb S., Zagrebelsky M., Dreznjak A., Deogracias R., Matsumoto T., Wiese S., Erne B., Sendtner M., Schaeren-Wiemers N., Korte M., Barde Y.A. Global deprivation of brain-derived neurotrophic factor in the CNS reveals an area-specific requirement for dendritic growth. J. Neurosci. 2010, 30:1739-1749.
82. Rosso S.B., Sussman D., Wynshaw-Boris A., Salinas P.C. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 2005, 8:34-42.
83. Ryan T.J., Grant S.G. The origin and evolution of synapses. Nat. Rev. Neurosci. 2009, 10:701-712.
84. Sahores M., Gibb A., Salinas P.C. Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis. Development 2010, 137:2215-2225.
85. Salinas P.C. Signaling at the vertebrate synapse: new roles for embryonic morphogens?. J. Neurobiol. 2005, 64:435-445.
86. Salinas P.C., Zou Y. Wnt signaling in neural circuit assembly. Annu. Rev. Neurosci. 2008, 31:339-358.
87. Schmidt H.D., Banasr M., Duman R.S. Future antidepressant targets: neurotrophic factors and related signaling cascades. Drug discovery today. Ther. Strateg. 2008, 5:151-156.
88. Schoups A.A., Elliott R.C., Friedman W.J., Black I.B. NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Brain Res. Dev. Brain Res. 1995, 86:326-334.
89. Schratt G.M., Nigh E.A., Chen W.G., Hu L., Greenberg M.E. BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J. Neurosci. 2004, 24:7366-7377.
90. Semenov M.V., Tamai K., Brott B.K., Kuhl M., Sokol S., He X. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 2001, 11:951-961.
91. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 2002, 22:3251-3261.
92. Sholl D.A. Dendritic organization in the visual and motor cortices of the cat. J. Anat. 1953, 87:387-406.
93. Strand A.D., Baquet Z.C., Aragaki A.K., Holmans P., Yang L., Cleren C., Beal M.F., Jones L., Kooperberg C., Olson J.M., Jones K.R. Expression profiling of Huntington's disease models suggests that brain-derived neurotrophic factor depletion plays a major role in striatal degeneration. J. Neurosci. 2007, 27:11758-11768.
94. Tabatadze N., Tomas C., McGonigal R., Lin B., Schook A., Routtenberg A. WNT Transmembrane Signaling and Long-term Spatial Memory 2011, Hippocampus.
95. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G.C., Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 2008, 319:1683-1687.
96. Tyler W.J., Pozzo-Miller L. Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. J. Physiol. 2003, 553:497-509.
97. Varela-Nallar L., Grabowski C.P., Alfaro I.E., Alvarez A.R., Inestrosa N.C. Role of the Wnt receptor Frizzled-1 in presynaptic differentiation and function. Neural. Dev. 2009, 4:41.
98. Varela-Nallar L., Alfaro I.E., Serrano F.G., Parodi J., Inestrosa N.C. Wingless-type family member 5A (Wnt-5a) stimulates synaptic differentiation and function of glutamatergic synapses. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21164-21169.
99. Vaughn J.E., Barber R.P., Sims T.J. Dendritic development and preferential growth into synaptogenic fields: a quantitative study of Golgi-impregnated spinal motor neurons. Synapse 1988, 2:69-78.
100. Verpelli C., Piccoli G., Zanchi A., Gardoni F., Huang K., Brambilla D., Di Luca M., Battaglioli E., Sala C. Synaptic activity controls dendritic spine morphology by modulating eEF2-dependent BDNF synthesis. J. Neurosci. 2010, 30:5830-5842.
101. Vigers A.J., Amin D.S., Talley-Farnham T., Gorski J.A., Xu B., Jones K.R. Sustained expression of brain-derived neurotrophic factor is required for maintenance of dendritic spines and normal behavior. Neuroscience 2012, 212:1-18.
102. von Bohlen und Halbach O., Minichiello L., Unsicker K. TrkB but not trkC receptors are necessary for postnatal maintenance of hippocampal spines. Neurobiol. Aging 2008, 29:1247-1255.
103. Waterhouse E.G., Xu B. New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Mol. Cell. Neurosci. 2009, 42:81-89.
104. Wayman G.A., Impey S., Marks D., Saneyoshi T., Grant W.F., Derkach V., Soderling T.R. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 2006, 50:897-909.
105. Wirth M.J., Brun A., Grabert J., Patz S., Wahle P. Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5. Development 2003, 130:5827-5838.
106. Xu B., Zang K., Ruff N.L., Zhang Y.A., McConnell S.K., Stryker M.P., Reichardt L.F. Cortical degeneration in the absence of neurotrophin signaling: dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 2000, 26:233-245.
107. Yang Y., Wang X.B., Frerking M., Zhou Q. Spine expansion and stabilization associated with long-term potentiation. J. Neurosci. 2008, 28:5740-5751.
108. Yi H., Hu J., Qian J., Hackam A.S. Expression of brain-derived neurotrophic factor is regulated by the Wnt signaling pathway. Neuroreport 2012, 23:189-194.
109. Yoshii A., Constantine-Paton M. BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat. Neurosci. 2007, 10:702-711.
110. Yu H., Chen Z.Y. The role of BDNF in depression on the basis of its location in the neural circuitry. Acta Pharmacol. Sin. 2011, 32:3-11.
111. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 2001, 24:1071-1089.
112. Zhang A., Shen C.H., Ma S.Y., Ke Y., El Idrissi A. Altered expression of Autism-associated genes in the brain of Fragile X mouse model. Biochem. Biophys. Res. Commun. 2009, 379:920-923.
113. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.
114. Zito K., Scheuss V., Knott G., Hill T., Svoboda K. Rapid functional maturation of nascent dendritic spines. Neuron 2009, 61:247-258.
115. Ziv N.E., Smith S.J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 1996, 17:91-102.