Cellular and molecular mechanisms regulating neuronal growth by brain-derived neurotrophic factor

Cytoskeleton

Volumn 73, Issue 10, 2016, Pages 612-628

  Gonzalez, Andres ^a   Moya Alvarado, Guillermo ^a   Gonzalez Billaut, Christian ^b   Bronfman, Francisca C ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b Universidad de Chile and Geroscience Center for Brain Health and Metabolism   (Chile)

Author keywords

BDNF; cytoskeleton dynamics; dendritic growth; membrane trafficking; signaling

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; NEUROTROPHIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P75; RAB PROTEIN; MEMBRANE PROTEIN; NERVE GROWTH FACTOR RECEPTOR; NERVE PROTEIN; NGFR PROTEIN, HUMAN; TROPOMYOSIN-RELATED KINASE-B, HUMAN;

CELL MEMBRANE; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CYTOLOGY; CYTOSKELETON; DENDRITE; ENZYME ACTIVITY; GROWTH REGULATION; HUMAN; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; GENETIC TRANSCRIPTION; METABOLISM; NERVE CELL; PATHOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL MEMBRANE; CYTOSKELETON; HUMANS; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BIOSYNTHESIS; RECEPTOR, TRKB; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84976869242     PISSN: 19493584     EISSN: 19493592     Source Type: Journal    
DOI: 10.1002/cm.21312     Document Type: Review

References (185)

1. Akum BF, Chen M, Gunderson SI, Riefler GM, Scerri-Hansen MM, Firestein BL. 2004. Cypin regulates dendrite patterning in hippocampal neurons by promoting microtubule assembly. Nat Neurosci 7:145–152.
2. Alsina B, Vu T, Cohen-Cory S. 2001. Visualizing synapse formation in arborizing optic axons in vivo: Dynamics and modulation by BDNF. Nat Neurosci 4:1093–1101.
3. Anastasia A, Deinhardt K, Chao MV, Will NE, Irmady K, Lee FS, Hempstead BL, Bracken C. 2013. Val66Met polymorphism of BDNF alters prodomain structure to induce neuronal growth cone retraction. Nat Commun 4:2490.
4. Arevalo JC, Pereira DB, Yano H, Teng KK, Chao MV. 2006. Identification of a switch in neurotrophin signaling by selective tyrosine phosphorylation. J Biol Chem 281:1001–1007.
5. Armstrong DD, Dunn K, Antalffy B. 1998. Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol 57:1013–1017.
6. Ascano M, Richmond A, Borden P, Kuruvilla R. 2009. Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J Neurosci 29:11674–11685.
7. Ascano M, Bodmer D, Kuruvilla R. 2012. Endocytic trafficking of neurotrophins in neural development. Trend Cell Biol 22:266–273.
8. Assaker G, Ramel D, Wculek SK, Gonzalez-Gaitan M, Emery G. 2010. Spatial restriction of receptor tyrosine kinase activity through a polarized endocytic cycle controls border cell migration. Proc Natl Acad Sci U S A 107:22558–22563.
9. Baquet ZC, Gorski JA, Jones KR. 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.
10. Briz V, Zhu G, Wang Y, Liu Y, Avetisyan M, Bi X, Baudry M. 2015. Activity-dependent rapid local RhoA synthesis is required for hippocampal synaptic plasticity. J Neurosci 35:2269–2282.
11. Brock JH, Rosenzweig ES, Blesch A, Moseanko R, Havton LA, Edgerton VR, Tuszynski MH. 2010. Local and remote growth factor effects after primate spinal cord injury. J Neurosci 30:9728–9737.
12. Bronfman FC, Tcherpakov M, Jovin TM, Fainzilber M. 2003. Ligand-induced internalization of the p75 neurotrophin receptor: A slow route to the signaling endosome. J Neurosci 23:3209–3220.
13. Bronfman FC, Escudero CA, Weis J, Kruttgen A. 2007. Endosomal transport of neurotrophins: Roles in signaling and neurodegenerative diseases. Dev Neurobiol 67:1183–1203.
14. Bronfman FC, Lazo OM, Flores C, Escudero CA. 2014. Spatiotemporal intracellular dynamics of neurotrophin and its receptors. Implications for neurotrophin signaling and neuronal function. Handb Exp Pharmacol 220:33–65.
15. Bruns MB, Miller MW. 2007. Neurotrophin ligand-receptor systems in somatosensory cortex of adult rat are affected by repeated episodes of ethanol. Exp Neurol 204:680–692.
16. Cabelli RJ, Hohn A, Shatz CJ. 1995. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267:1662–1666.
17. Cabelli RJ, Shelton DL, Segal RA, Shatz CJ. 1997. Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19:63–76.
18. Cabeza C, Figueroa A, Lazo OM, Galleguillos C, Pissani C, Klein A, Gonzalez-Billault C, Inestrosa NC, Alvarez AR, Zanlungo S, Bronfman FC. 2012. Cholinergic abnormalities, endosomal alterations and up-regulation of nerve growth factor signaling in Niemann-Pick type C disease. Mol Neurodegener 7:11.
19. Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shan H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B. 2008. Nedd4 controls animal growth by regulating IGF-1 signaling. Sci Signal 1:ra5.
20. Carim-Todd L, Bath KG, Fulgenzi G, Yanpallewar S, Jing D, Barrick CA, Becker J, Buckley H, Dorsey SG, Lee FS, Tessarollo L. 2009. Endogenous truncated TrkB.T1 receptor regulates neuronal complexity and TrkB kinase receptor function in vivo. J Neurosci 29:678–685.
21. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M. 2003. JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4:521–533.
22. Chen Q, Zhou Z, Zhang L, Wang Y, Zhang YW, Zhong M, Xu SC, Chen CH, Li L, Yu ZP. 2012a. Tau protein is involved in morphological plasticity in hippocampal neurons in response to BDNF. Neurochem Int 60:233–242.
23. Chen Y, Fu WY, Ip JP, Ye T, Fu AK, Chao MV, Ip NY. 2012b. Ankyrin repeat-rich membrane spanning protein (kidins220) is required for neurotrophin and ephrin receptor-dependent dendrite development. J Neurosci 32:8263–8269.
24. Chen PI, Schauer K, Kong C, Harding AR, Goud B, Stahl PD. 2014. Rab5 isoforms orchestrate a “division of labor” in the endocytic network; Rab5C modulates Rac-mediated cell motility. PloS One 9:e90384.
25. Cheng PL, Song AH, Wong YH, Wang S, Zhang X, Poo MM. 2011. Self-amplifying autocrine actions of BDNF in axon development. Proc Natl Acad Sci U S A 108:18430–18435.
26. Cheung ZH, Chin WH, Chen Y, Ng YP, Ip NY. 2007. Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol 5:e63.
27. Cohen MS, C, Bas Orth HJ Kim NL. Jeon SR, Jaffrey 2011. Neurotrophin-mediated dendrite-to-nucleus signaling revealed by microfluidic compartmentalization of dendrites. Proc Natl Acad Sci U S A 108:11246–11251.
28. Cohen-Cory S, Fraser SE. 1995. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378:192–196.
29. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70:271–288.
30. Cosker KE, Segal RA. 2014. Neuronal signaling through endocytosis. Cold Spring Harbor Perspect Biol 6:
31. Curmi PA, Gavet O, Charbaut E, Ozon S, Lachkar-Colmerauer S, Manceau V, Siavoshian S, Maucuer A, Sobel A. 1999. Stathmin and its phosphoprotein family: General properties, biochemical and functional interaction with tubulin. Cell Struct Funct 24:345–357.
32. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N. 2012. microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat Neurosci 15:697–699.
33. Danzer SC, Crooks KR, Lo DC, McNamara JO. 2002. Increased expression of brain-derived neurotrophic factor induces formation of basal dendrites and axonal branching in dentate granule cells in hippocampal explant cultures. J Neurosci 22:9754–9763.
34. Dean C, Liu H, Staudt T, Stahlberg MA, Vingill S, Buckers J, Kamin D, Engelhardt J, Jackson MB, Hell SW, Chapman ER. 2012. Distinct subsets of Syt-IV/BDNF vesicles are sorted to axons versus dendrites and recruited to synapses by activity. J Neurosci 32:5398–5413.
35. Deinhardt K, Chao MV. 2014a. Shaping neurons: Long and short range effects of mature and proBDNF signalling upon neuronal structure. Neuropharmacology 76 Pt C:603–609.
36. Deinhardt K, Chao MV. 2014b. Trk receptors. Handb Exp Pharmacol 220:103–119.
37. Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G. 2006. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 52:293–305.
38. Deinhardt K, Kim T, Spellman DS, Mains RE, Eipper BA, Neubert TA, Chao MV, Hempstead BL. 2011. Neuronal growth cone retraction relies on proneurotrophin receptor signaling through Rac. Sci Signal 4:ra82.
39. Delcroix JD, Valletta JS, Wu C, Hunt SJ, Kowal AS, Mobley WC. 2003. NGF signaling in sensory neurons: Evidence that early endosomes carry NGF retrograde signals. Neuron 39:69–84.
40. Dickstein DL, Brautigam H, Stockton SD, Jr.,Schmeidler J, Hof PR. 2010. Changes in dendritic complexity and spine morphology in transgenic mice expressing human wild-type tau. Brain Struct Funct 214:161–179.
41. Dijkhuizen PA, Ghosh A. 2005. BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J Neurobiol 62:278–288.
42. Dong Q, Ji YS, Cai C, Chen ZY. 2012. LIM kinase 1 (LIMK1) interacts with tropomyosin-related kinase B (TrkB) and mediates brain-derived neurotrophic factor (BDNF)-induced axonal elongation. J Biol Chem 287:41720–41731.
43. Drinjakovic J, Jung H, Campbell DS, Strochlic L, Dwivedy A, Holt CE. 2010. E3 ligase Nedd4 promotes axon branching by downregulating PTEN. Neuron 65:341–357.
44. Du JL, Poo MM. 2004. Rapid BDNF-induced retrograde synaptic modification in a developing retinotectal system. Nature 429:878–883.
45. Edelmann E, Lessmann V, Brigadski T. 2014. Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity. Neuropharmacology 76 Pt C:610–627.
46. Eiland L, McEwen BS. 2012. Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus 22:82–91.
47. Emery G, Ramel D. 2013. Cell coordination of collective migration by Rab11 and Moesin. Commun Integr Biol 6:e24587.
48. Escudero CA, Lazo OM, Galleguillos C, Parraguez JI, Lopez-Verrilli MA, Cabeza C, Leon L, Saeed U, Retamal C, Gonzalez A, Marzolo MP, Carter BD, Court FA, Bronfman FC. 2014. The p75 neurotrophin receptor evades the endolysosomal route in neuronal cells, favouring multivesicular bodies specialised for exosomal release. J Cell Sci 127:1966–1979.
49. Etienne-Manneville S, Hall A. 2002. Rho GTPases in cell biology. Nature 420:629–635.
50. Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME. 1997. CREB: A major mediator of neuronal neurotrophin responses. Neuron 19:1031–1047.
51. Finsterwald C, Martin JL. 2011. Cellular mechanisms underlying the regulation of dendritic development by hepatocyte growth factor. Eur J Neurosci 34:1053–1061.
52. Finsterwald C, H Fiumelli JR. Cardinaux JL, Martin 2010. Regulation of dendritic development by BDNF requires activation of CRTC1 by glutamate. J Biol Chem 285:28587–28595.
53. Flavell SW, Greenberg ME. 2008. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Ann Rev Neurosci 31:563–590.
54. Flinn RJ, Yan Y, Goswami S, Parker PJ, Backer JM. 2010. The late endosome is essential for mTORC1 signaling. Mol Biol Cell 21:833–841.
55. Fu X, Yang Y, Xu C, Niu Y, Chen T, Zhou Q, Liu JJ. 2011. Retrolinkin cooperates with endophilin A1 to mediate BDNF-TrkB early endocytic trafficking and signaling from early endosomes. Mol Biol Cell 22:3684–3698.
56. Fukata Y, Itoh TJ, Kimura T, Menager C, Nishimura T, Shiromizu T, Watanabe H, Inagaki N, Iwamatsu A, Hotani H, Kaibuchi K. 2002. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol 4:583–591.
57. Gallo G. 2015. Localized regulation of the axon shaft during the emergence of collateral branches. Neural Regen Res 10:1206–1208.
58. Gao FB. 2007. Molecular and cellular mechanisms of dendritic morphogenesis. Curr Opin Neurobiol 17:525–532.
59. Gauthier LR, Charrin BC, Borrell-Pages M, Dompierre JP, Rangone H, Cordelieres FP, De Mey J, MacDonald ME, Lessmann V, Humbert S, Saudou F. 2004. Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules. Cell 118:127–138.
60. Geetha T, Jiang J, Wooten MW. 2005. Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol Cell 20:301–312.
61. Gehler S, Gallo G, Veien E, Letourneau PC. 2004. p75 neurotrophin receptor signaling regulates growth cone filopodial dynamics through modulating RhoA activity. J Neurosci 24:4363–4372.
62. Gibney J, Zheng JQ. 2003. Cytoskeletal dynamics underlying collateral membrane protrusions induced by neurotrophins in cultured Xenopus embryonic neurons. J Neurobiol 54:393–405.
63. Glebova NO, Ginty DD. 2005. Growth and survival signals controlling sympathetic nervous system development. Annu Rev Neurosci 28:191–222.
64. Gomes RA, Hampton C, El-Sabeawy F, Sabo SL, McAllister AK. 2006. The dynamic distribution of TrkB receptors before, during, and after synapse formation between cortical neurons. J Neurosci 26:11487–11500.
65. Gonzalez-Billault C, Avila J, Caceres A. 2001. Evidence for the role of MAP1B in axon formation. Mol Biol Cell 12:2087–2098.
66. Gonzalez-Billault C, Munoz-Llancao P, Henriquez DR, Wojnacki J, Conde C, Caceres A. 2012. The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton (Hoboken) 69:464–485.
67. Gorski JA, SR Zeiler S. Tamowski KR, Jones 2003. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J Neurosci 23:6856–6865.
68. Granseth B, Fukushima Y, Sugo N, Lagnado L, Yamamoto N. 2013. Regulation of thalamocortical axon branching by BDNF and synaptic vesicle cycling. Front Neural Circuit 7:202.
69. Guillemard V, Ivanisevic L, Garcia AG, Scholten V, Lazo OM, Bronfman FC, Saragovi HU. 2010. An agonistic mAb directed to the TrkC receptor juxtamembrane region defines a trophic hot spot and interactions with p75 coreceptors. Dev Neurobiol 70:150–164.
70. Guo SL, Tan GH, Li S, Cheng XW, Zhou Y, Jia YF, Xiong H, Tao J, Xiong ZQ. 2012. Serum inducible kinase is a positive regulator of cortical dendrite development and is required for BDNF-promoted dendritic arborization. Cell Res 22:387–398.
71. Hannila SS, Filbin MT. 2008. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321–332.
72. Harrington AW, Ginty DD. 2013. Long-distance retrograde neurotrophic factor signalling in neurons. Nat Rev Neurosci 14:177–187.
73. Heerssen HM, Pazyra MF, Segal RA. 2004. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 7:596–604.
74. Hempstead BL. 2014. Deciphering proneurotrophin actions. Handb Exp Pharmacol 220:17–32.
75. Higuchi H, Yamashita T, Yoshikawa H, Tohyama M. 2003. PKA phosphorylates the p75 receptor and regulates its localization to lipid rafts. EMBO J 22:1790–1800.
76. Higuero AM, Sanchez-Ruiloba L, Doglio LE, Portillo F, Abad-Rodriguez J, Dotti CG, Iglesias T. 2010. Kidins220/ARMS modulates the activity of microtubule-regulating proteins and controls neuronal polarity and development. J Biol Chem 285:1343–1357.
77. Hisata S, Sakisaka T, Baba T, Yamada T, Aoki K, Matsuda M, Takai Y. 2007. Rap1-PDZ-GEF1 interacts with a neurotrophin receptor at late endosomes, leading to sustained activation of Rap1 and ERK and neurite outgrowth. J Cell Biol 178:843–860.
78. Horch HW, Katz LC. 2002. BDNF release from single cells elicits local dendritic growth in nearby neurons. Nat Neurosci 5:1177–1184.
79. Horgan CP, SR, Hanscom RS Jolly CE. Futter MW, McCaffrey 2010. Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J Cell Sci 123:181–191.
80. Horton AC, Ehlers MD. 2004. Secretory trafficking in neuronal dendrites. Nat Cell Biol 6:585–591.
81. Hsu WL, Chung HW, Wu CY, Wu HI, Lee YT, Chen EC, Fang W, Chang YC. 2015. Glutamate stimulates local protein synthesis in the axons of rat cortical neurons by activating alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors and metabotropic glutamate receptors. J Biol Chem 290:20748–20760.
82. Huang EJ, Reichardt LF. 2001. Neurotrophins: Roles in neuronal development and function. Ann Rev Neurosci 24:677–736.
83. Huang EJ, Reichardt LF. 2003. Trk receptors: Roles in neuronal signal transduction. Ann Rev Biochem 72:609–642.
84. Huang JK, Dorey K, Ishibashi S, Amaya E. 2007. BDNF promotes target innervation of Xenopus mandibular trigeminal axons in vivo. BMC Dev Biol 7:59.
85. Huang SH, Zhao L, Sun ZP, Li XZ, Geng Z, Zhang KD, Chao MV, Chen ZY. 2009. Essential role of Hrs in endocytic recycling of full-length TrkB receptor but not its isoform TrkB.T1. J Biol Chem 284:15126–15136.
86. Huang SH, Wang J, Sui WH, Chen B, Zhang XY, Yan J, Geng Z, Chen ZY. 2013. BDNF-dependent recycling facilitates TrkB translocation to postsynaptic density during LTP via a Rab11-dependent pathway. J Neurosci 33:9214–9230.
87. Huttner WB, Schmidt A. 2000. Lipids, lipid modification and lipid-protein interaction in membrane budding and fission–insights from the roles of endophilin A1 and synaptophysin in synaptic vesicle endocytosis. Curr Opin Neurobiol 10:543–551.
88. Ip JP, Fu AK, Ip NY. 2014. CRMP2: Functional roles in neural development and therapeutic potential in neurological diseases. Neuroscientist 20:589–598.
89. Jan YN, Jan LY. 2010. Branching out: Mechanisms of dendritic arborization. Nat Rev Neurosci 11:316–328.
90. Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M. 2005. Control of dendritic arborization by the phosphoinositide-3'-kinase-Akt-mammalian target of rapamycin pathway. J Neurosci 25:11300–11312.
91. Jeanneteau F, Deinhardt K, Miyoshi G, Bennett AM, Chao MV. 2010. The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nat Neurosci 13:1373–1379.
92. Ji Y, Lu Y, Yang F, Shen W, Tang TT, Feng L, Duan S, Lu B. 2010. Acute and gradual increases in BDNF concentration elicit distinct signaling and functions in neurons. Nat Neurosci 13:302–309.
93. Jones KR, Farinas I, Backus C, Reichardt LF. 1994. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989–999.
94. Kalil K, Dent EW. 2014. Branch management: Mechanisms of axon branching in the developing vertebrate CNS. Nat Rev Neurosci 15:7–18.
95. Kaplan DR, Miller FD. 2000. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381–391.
96. Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, Nakajima K, Nabeshima Y, Hoshino M. 2010. Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67:588–602.
97. Ketschek A, Jones S, Spillane M, Korobova F, Svitkina T, Gallo G. 2015. Nerve growth factor promotes reorganization of the axonal microtubule array at sites of axon collateral branching. Dev Neurobiol 75:1441–1461.
98. Klein R, Parada LF, Coulier F, Barbacid M. 1989. trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J 8:3701–3709.
99. Klein R, Conway D, Parada LF, Barbacid M. 1990. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61:647–656.
100. Koles K, Nunnari J, Korkut C, Barria R, Brewer C, Li Y, Leszyk J, Zhang B, Budnik V. 2012. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 287:16820–16834.
101. Kraemer BR, Yoon SO, Carter BD. 2014. The biological functions and signaling mechanisms of the p75 neurotrophin receptor. Handb Exp Pharmacol 220:121–164.
102. Kulkarni VA, Firestein BL. 2012. The dendritic tree and brain disorders. Mol Cell Neurosci 50:10–20.
103. Kumar V, Zhang MX, Swank MW, Kunz J, Wu GY. 2005. Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25:11288–11299.
104. Kwon M, JR, Fernandez GF Zegarek SB. Lo BL, Firestein 2011. BDNF-promoted increases in proximal dendrites occur via CREB-dependent transcriptional regulation of cypin. J Neurosci 31:9735–9745.
105. La Torre A, del Mar Masdeu M, Cotrufo T, Moubarak RS, del Rio JA, Comella JX, Soriano E, Urena JM. 2013. A role for the tyrosine kinase ACK1 in neurotrophin signaling and neuronal extension and branching. Cell Death Dis 4:e602.
106. Lazo OM, Gonzalez A, Ascano M, Kuruvilla R, Couve A, Bronfman FC. 2013. BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J Neurosci 33:6112–6122.
107. Levi-Montalcini R. 1987. The nerve growth factor 35 years later. Science 237:1154–1162.
108. Liot G, Zala D, Pla P, Mottet G, Piel M, Saudou F. 2013. Mutant Huntingtin alters retrograde transport of TrkB receptors in striatal dendrites. J Neurosci 33:6298–6309.
109. Lipton JO, Sahin M. 2014. The neurology of mTOR. Neuron 84:275–291.
110. Liu JJ, Ding J, Wu C, Bhagavatula P, Cui B, Chu S, Mobley WC, Yang Y. 2007. Retrolinkin, a membrane protein, plays an important role in retrograde axonal transport. Proc Natl Acad Sci U S A 104:2223–2228.
111. Lom B, Cogen J, Sanchez AL, Vu T, Cohen-Cory S. 2002. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arborization of retinal ganglion cells in vivo. J Neurosci 22:7639–7649.
112. Lonze BE, Ginty DD. 2002. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–623.
113. Luikart BW, Zhang W, Wayman GA, Kwon CH, Westbrook GL, Parada LF. 2008. Neurotrophin-dependent dendritic filopodial motility: A convergence on PI3K signaling. J Neurosci 28:7006–7012.
114. Lush ME, Ma L, Parada LF. 2005. TrkB signaling regulates the developmental maturation of the somatosensory cortex. Int J Dev Neurosci 23:523–536.
115. Marler KJ, Suetterlin P, Dopplapudi A, Rubikaite A, Adnan J, Maiorano NA, Lowe AS, Thompson ID, Pathania M, Bordey A, Fulga T, Van Vactor DL, Hindges R, Drescher U. 2014. BDNF promotes axon branching of retinal ganglion cells via miRNA-132 and p250GAP. J Neurosci 34:969–979.
116. Marshak S, Nikolakopoulou AM, Dirks R, Martens GJ, Cohen-Cory S. 2007. Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J Neurosci 27:2444–2456.
117. Mason JM, Morrison DJ, Basson MA, Licht JD. 2006. Sprouty proteins: Multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trend Cell Biol 16:45–54.
118. Masuda M, Takeda S, Sone M, Ohki T, Mori H, Kamioka Y, Mochizuki N. 2006. Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J 25:2889–2897.
119. McCaffrey G, Welker J, Scott J, der Salm L, Grimes ML. 2009. High-resolution fractionation of signaling endosomes containing different receptors. Traffic 10:938–950.
120. Minichiello L. 2009. TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10:850–860.
121. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, Korte M. 2002. Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36:121–137.
122. Mitchell DJ, Blasier KR, Jeffery ED, Ross MW, Pullikuth AK, Suo D, Park J, Smiley WR, Lo KW, Shabanowitz J, Deppmann CD, Trinidad JC, Hunt DF, Catling AD, Pfister KK. 2012. Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J Neurosci 32:15495–15510.
123. Miyamoto Y, Yamauchi J, Tanoue A, Wu C, Mobley WC. 2006. TrkB binds and tyrosine-phosphorylates Tiam1, leading to activation of Rac1 and induction of changes in cellular morphology. Proc Natl Academy of Sciences of the United States of America 103:10444–10449.
124. Mochizuki N, Yamashita S, Kurokawa K, Ohba Y, Nagai T, Miyawaki A, Matsuda M. 2001. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411:1065–1068.
125. Mori Y, Matsui T, Furutani Y, Yoshihara Y, Fukuda M. 2012. Small GTPase Rab17 regulates dendritic morphogenesis and postsynaptic development of hippocampal neurons. J Biol Chem 287:8963–8973.
126. Mori Y, Matsui T, Fukuda M. 2013. Rabex-5 protein regulates dendritic localization of small GTPase Rab17 and neurite morphogenesis in hippocampal neurons. J Biol Chem 288:9835–9847.
127. Mufson EJ, Kroin JS, Sendera TJ, Sobreviela T. 1999. Distribution and retrograde transport of trophic factors in the central nervous system: Functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol 57:451–484.
128. Munoz-Llancao P, Henriquez DR, Wilson C, Bodaleo F, Boddeke EW, Lezoualc'h F, Schmidt M, Gonzalez-Billault C. 2015. Exchange protein directly activated by cAMP (EPAC) regulates neuronal polarization through Rap1B. J Neurosci 35:11315–11329.
129. Murakoshi H, Wang H, Yasuda R. 2011. Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472:100–104.
130. Myers JP, Robles E, Ducharme-Smith A, Gomez TM. 2012. Focal adhesion kinase modulates Cdc42 activity downstream of positive and negative axon guidance cues. J Cell Sci 125:2918–2929.
131. Namekata K, Harada C, Guo X, Kimura A, Kittaka D, Watanabe H, Harada T. 2012. Dock3 stimulates axonal outgrowth via GSK-3beta-mediated microtubule assembly. J Neurosci 32:264–274.
132. Ohira K, Homma KJ, Hirai H, Nakamura S, Hayashi M. 2006. TrkB-T1 regulates the RhoA signaling and cytoskeleton in glioma cells. Biochem Biophys Res Commun 343:867–74.
133. Ouyang Q, Lizarraga SB, Schmidt M, Yang U, Gong J, Ellisor D, Kauer JA, Morrow EM. 2013. Christianson syndrome protein NHE6 modulates TrkB endosomal signaling required for neuronal circuit development. Neuron 80:97–112.
134. Panagiotaki N, Dajas-Bailador F, Amaya E, Papalopulu N, Dorey K. 2010. Characterisation of a new regulator of BDNF signalling, Sprouty3, involved in axonal morphogenesis in vivo. Development 137:4005–4015.
135. Park H, Poo MM. 2013. Neurotrophin regulation of neural circuit development and function. Nat Rev Neurosci 14:7–23.
136. Philippidou P, Valdez G, Akmentin W, Bowers WJ, Federoff HJ, Halegoua S. 2011. Trk retrograde signaling requires persistent, Pincher-directed endosomes. Proc Natl Acad Sci U S A 108:852–857.
137. Rauskolb S, Zagrebelsky M, Dreznjak A, Deogracias R, Matsumoto T, Wiese S, Erne B, Sendtner M, Schaeren-Wiemers N, Korte M, Barde YA. 2010. Global deprivation of brain-derived neurotrophic factor in the CNS reveals an area-specific requirement for dendritic growth. J Neurosci 30:1739–1749.
138. Roland JT, DM, Bryant A, Datta A Itzen KE. Mostov JR, Goldenring 2011. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci U S A 108:2789–2794.
139. Roze E, Saudou F, Caboche J. 2008. Pathophysiology of Huntington's disease: From huntingtin functions to potential treatments. Curr Opin Neurol 21:497–503.
140. Ruiz CR, Shi J, Meffert MK. 2014. Transcript specificity in BDNF-regulated protein synthesis. Neuropharmacology 76 Pt C:657–663.
141. Saito A, Miyajima K, Akatsuka J, Kondo H, Mashiko T, Kiuchi T, Ohashi K, Mizuno K. 2013. CaMKIIbeta-mediated LIM-kinase activation plays a crucial role in BDNF-induced neuritogenesis. Genes Cells 18:533–543.
142. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496–1501.
143. Sarmiere PD. JR, Bamburg 2004. Regulation of the neuronal actin cytoskeleton by ADF/cofilin. J Neurobiol 58:103–117.
144. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H, Rolls MM, Ishikawa F, Uemura T. 2008. Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 10:1164–1171.
145. Schmieg N, Menendez G, Schiavo G, Terenzio M. 2014. Signalling endosomes in axonal transport: Travel updates on the molecular highway. Semin Cell Dev Biol 27:32–43.
146. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME. 2004. 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 24:7366–7377.
147. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME. 2006. A brain-specific microRNA regulates dendritic spine development. Nature 439:283–289.
148. Schwartz PM, Borghesani PR, Levy RL, Pomeroy SL, Segal RA. 1997. Abnormal cerebellar development and foliation in BDNF−/− mice reveals a role for neurotrophins in CNS patterning. Neuron 19:269–281.
149. Shi SH, Jan LY, Jan YN. 2003. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63–75.
150. Shimojo M, J, Courchet S, Pieraut N, Torabi-Rander R Sando 3rd F., Polleux A, Maximov 2015. SNAREs Controlling Vesicular Release of BDNF and Development of Callosal Axons. Cell Rep 11:1054–1066.
151. Song M, Giza J, Proenca CC, Jing D, Elliott M, Dincheva I, Shmelkov SV, Kim J, Schreiner R, Huang SH, Castren E, Prekeris R, Hempstead BL, Chao MV, Dictenberg JB, Rafii S, Chen ZY, Rodriguez-Boulan E, Lee FS. 2015. Slitrk5 mediates BDNF-dependent TrkB receptor trafficking and signaling. Dev Cell 33:690–702.
152. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525.
153. Sun Y, Lim Y, Li F, Liu S, Lu JJ, Haberberger R, Zhong JH, Zhou XF. 2012. ProBDNF collapses neurite outgrowth of primary neurons by activating RhoA. PloS One 7:e35883.
154. Suzuki S, Numakawa T, Shimazu K, Koshimizu H, Hara T, Hatanaka H, Mei L, Lu B, Kojima M. 2004. BDNF-induced recruitment of TrkB receptor into neuronal lipid rafts: Roles in synaptic modulation. J Cell Biol 167:1205–1215.
155. Takano T, Tomomura M, Yoshioka N, Tsutsumi K, Terasawa Y, Saito T, Kawano H, Kamiguchi H, Fukuda M, Hisanaga S. 2012. LMTK1/AATYK1 is a novel regulator of axonal outgrowth that acts via Rab11 in a Cdk5-dependent manner. J Neurosci 32:6587–6599.
156. Takei N, Inamura N, Kawamura M, Namba H, Hara K, Yonezawa K, Nawa H. 2004. Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24:9760–9769.
157. Takemoto-Kimura S, Ageta-Ishihara N, Nonaka M, Adachi-Morishima A, Mano T, Okamura M, Fujii H, Fuse T, Hoshino M, Suzuki S, Kojima M, Mishina M, Okuno H, Bito H. 2007. Regulation of dendritogenesis via a lipid-raft-associated Ca2+/calmodulin-dependent protein kinase CLICK-III/CaMKIgamma. Neuron 54:755–770.
158. Troca-Marin JA, Alves-Sampaio A, Tejedor FJ, Montesinos ML. 2010. Local translation of dendritic RhoA revealed by an improved synaptoneurosome preparation. Mol Cell Neurosci 43:308–314.
159. Van Aelst L, Cline HT. 2004. Rho GTPases and activity-dependent dendrite development. Curr Opin Neurobiol 14:297–304.
160. Villarroel-Campos D, Gonzalez-Billault C. 2014. The MAP1B case: An old MAP that is new again. Dev Neurobiol 74:953–971.
161. Villarroel-Campos D, Gastaldi L, Conde C, Caceres A, Gonzalez-Billault C. 2014. Rab-mediated trafficking role in neurite formation. J Neurochem 129:240–248.
162. Wong ST, JR, Henley KC, Kanning KH Huang M. Bothwell MM, Poo 2002. A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 5:1302–1308.
163. Wood GE, Young LT, Reagan LP, Chen B, McEwen BS. 2004. Stress-induced structural remodeling in hippocampus: Prevention by lithium treatment. Proc Nat Acad Sci U S A 101:3973–3978.
164. Wu C, Lai CF, Mobley WC. 2001. Nerve growth factor activates persistent Rap1 signaling in endosomes. J Neurosci 21:5406–5416.
165. Wu SH, Arevalo JC, Sarti F, Tessarollo L, Gan WB, Chao MV. 2009. Ankyrin Repeat-rich Membrane Spanning/Kidins220 protein regulates dendritic branching and spine stability in vivo. Dev Neurobiol 69:547–557.
166. Xing J, Kornhauser JM, Xia Z, Thiele EA, Greenberg ME. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol Cell Biol 18:1946–1955.
167. Xu B, Zang K, Ruff NL, Zhang YA, McConnell SK, Stryker MP, Reichardt LF. 2000. Cortical degeneration in the absence of neurotrophin signaling: Dendritic retraction and neuronal loss after removal of the receptor TrkB. Neuron 26:233–245.
168. Yacoubian TA, Lo DC. 2000. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 3:342–349.
169. Yamashita T, Tohyama M. 2003. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat Neurosci 6:461–467.
170. Yamashita T, Tucker KL, Barde YA. 1999. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 24:585–593.
171. Yamashita T, Higuchi H, Tohyama M. 2002. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho. J Cell Biol 157:565–570.
172. Yamashita N, Ohshima T, Nakamura F, Kolattukudy P, Honnorat J, Mikoshiba K, Goshima Y. 2012. Phosphorylation of CRMP2 (collapsin response mediator protein 2) is involved in proper dendritic field organization. J Neurosci 32:1360–1365.
173. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC. 1997. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol 378:135–157.
174. Yang J, Harte-Hargrove LC, Siao CJ, Marinic T, Clarke R, Ma Q, Jing D, Lafrancois JJ, Bath KG, Mark W, Ballon D, Lee FS, Scharfman HE, Hempstead BL. 2014. proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus. Cell Rep 7:796–806.
175. Yano H, Lee FS, Kong H, Chuang J, Arevalo J, Perez P, Sung C, Chao MV. 2001. Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J Neurosci 21:RC125.
176. Ye H, Kuruvilla R, Zweifel LS, Ginty DD. 2003. Evidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron 39:57–68.
177. York RD, Yao H, Dillon T, Ellig CL, Eckert SP, McCleskey EW, Stork PJ. 1998. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622–626.
178. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. 2005. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137–149.
179. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, Duan S. 2003. Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5:38–45.
180. Zagrebelsky M, Holz A, Dechant G, Barde YA, Bonhoeffer T, Korte M. 2005. The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons. J Neurosci 25:9989–9999.
181. Zhang Y, Moheban DB, Conway BR, Bhattacharyya A, Segal RA. 2000. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J Neurosci 20:5671–5678.
182. Zheng J, Shen WH, Lu TJ, Zhou Y, Chen Q, Wang Z, Xiang T, Zhu YC, Zhang C, Duan S, Xiong ZQ. 2008. Clathrin-dependent endocytosis is required for TrkB-dependent Akt-mediated neuronal protection and dendritic growth. J Biol Chem 283:13280–13288.
183. Zhou B, Cai Q, Xie Y, Sheng ZH. 2012. Snapin recruits dynein to BDNF-TrkB signaling endosomes for retrograde axonal transport and is essential for dendrite growth of cortical neurons. Cell Rep 2:42–51.
184. Zou W, Yadav S, DeVault L, Nung Jan Y, Sherwood DR. 2015. RAB-10-dependent membrane transport is required for dendrite arborization. PLoS Genet 11:e1005484.
185. Zuccaro E, Bergami M, Vignoli B, Bony G, Pierchala BA, Santi S, Cancedda L, Canossa M. 2014. Polarized expression of p75(NTR) specifies axons during development and adult neurogenesis. Cell Rep 7:138–152.