Cell-intrinsic drivers of dendrite morphogenesis

Development (Cambridge)

Volumn 140, Issue 23, 2013, Pages 4657-4671

  Puram, Sidharth V ^a   Bonni, Azad ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell intrinsic driver; Dendrite development; Dendrite morphogenesis; Dendrite patterning; Transcription factor; Ubiquitin ligases

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE; MAMMALIAN TARGET OF RAPAMYCIN; MOLECULAR MOTOR; PHOSPHATIDYLINOSITOL 3 KINASE; RHO FACTOR; STEROID HORMONE; UBIQUITIN PROTEIN LIGASE;

ACTIN FILAMENT; BRAIN DEVELOPMENT; CELL CYCLE REGULATION; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; COGNITIVE DEFECT; DENDRITE; DROSOPHILA; ENDOPLASMIC RETICULUM; GENE TARGETING; MAMMAL; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RNA TRANSLATION;

CELL-INTRINSIC DRIVER; DENDRITE DEVELOPMENT; DENDRITE MORPHOGENESIS; DENDRITE PATTERNING; TRANSCRIPTION FACTOR; UBIQUITIN LIGASES;

ANIMALS; BRAIN; DENDRITES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; NERVOUS SYSTEM; NEUROGENESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84887862561     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.087676     Document Type: Review

References (202)

1. Aizawa, H., Hu, S. C., Bobb, K., Balakrishnan, K., Ince, G., Gurevich, I., Cowan, M. and Ghosh, A. (2004). Dendrite development regulated by CREST, a calciumregulated transcriptional activator. Science 303, 197-202.
2. Al-Bassam, S., Xu, M., Wandless, T. J. and Arnold, D. B. (2012). Differential trafficking of transport vesicles contributes to the localization of dendritic proteins. Cell Rep. 2, 89-100.
3. Amthor, F. R. and Oyster, C. W. (1995). Spatial organization of retinal information about the direction of image motion. Proc. Natl. Acad. Sci. USA 92, 4002-4005.
4. Armstrong, D. D. (1995). The neuropathology of Rett syndrome-overview 1994. Neuropediatrics 26, 100-104.
5. Arnold, D., Feng, L., Kim, J. and Heintz, N. (1994). A strategy for the analysis of gene expression during neural development. Proc. Natl. Acad. Sci. USA 91, 9970-9974.
6. Atkins, C. M., Nozaki, N., Shigeri, Y. and Soderling, T. R. (2004). Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J. Neurosci. 24, 5193-5201.
7. Baas, P. W. and Lin, S. (2011). Hooks and comets: The story of microtubule polarity orientation in the neuron. Dev. Neurobiol. 71, 403-418.
8. Baas, P. W., Deitch, J. S., Black, M. M. and Banker, G. A. (1988). Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA 85, 8335-8339.
9. Baas, P. W., Black, M. M. and Banker, G. A. (1989). Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J. Cell Biol. 109, 3085-3094.
10. Baas, P. W., Slaughter, T., Brown, A. and Black, M. M. (1991). Microtubule dynamics in axons and dendrites. J. Neurosci. Res. 30, 134-153.
11. Bagni, C. and Greenough, W. T. (2005). From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat. Rev. Neurosci. 6, 376-387.
12. Barnes, A. P. and Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381.
13. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. and Goodman, C. S. (2000). Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715.
14. Becker, L. E., Armstrong, D. L. and Chan, F. (1986). Dendritic atrophy in children with Down's syndrome. Ann. Neurol. 20, 520-526.
15. Bestman, J. E. and Cline, H. T. (2008). The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo. Proc. Natl. Acad. Sci. USA 105, 20494-20499.
16. Blochlinger, K., Bodmer, R., Jan, L. Y. and Jan, Y. N. (1990). Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 4, 1322-1331.
17. Bokoch, G. M. (2003). Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781.
18. Boulanger, A., Clouet-Redt, C., Farge, M., Flandre, A., Guignard, T., Fernando, C., Juge, F. and Dura, J. M. (2011). ftz-f1 and Hr39 opposing roles on EcR expression during Drosophila mushroom body neuron remodeling. Nat. Neurosci. 14, 37-44.
19. Branco, T. and Häusser, M. (2011). Synaptic integration gradients in single cortical pyramidal cell dendrites. Neuron 69, 885-892.
20. Branco, T., Clark, B. A. and Häusser, M. (2010). Dendritic discrimination of temporal input sequences in cortical neurons. Science 329, 1671-1675.
21. Brechbiel, J. L. and Gavis, E. R. (2008). Spatial regulation of nanos is required for its function in dendrite morphogenesis. Curr. Biol. 18, 745-750.
22. Buckley, P. T., Lee, M. T., Sul, J. Y., Miyashiro, K. Y., Bell, T. J., Fisher, S. A., Kim, J. and Eberwine, J. (2011). Cytoplasmic intron sequence-retaining transcripts can be dendritically targeted via ID element retrotransposons. Neuron 69, 877-884.
23. Cáceres, A., Ye, B. and Dotti, C. G. (2012). Neuronal polarity: demarcation, growth and commitment. Curr. Opin. Cell Biol. 24, 547-553.
24. Cahana, A., Escamez, T., Nowakowski, R. S., Hayes, N. L., Giacobini, M., von Holst, A., Shmueli, O., Sapir, T., McConnell, S. K., Wurst, W. et al. (2001). Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. Proc. Natl. Acad. Sci. USA 98, 6429-6434.
25. Causeret, F., Terao, M., Jacobs, T., Nishimura, Y. V., Yanagawa, Y., Obata, K., Hoshino, M. and Nikolic, M. (2009). The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb. Cortex 19, 861-875.
26. Chen, H. and Firestein, B. L. (2007). RhoA regulates dendrite branching in hippocampal neurons by decreasing cypin protein levels. J. Neurosci. 27, 8378-8386.
27. Chen, Y., Wang, P. Y. and Ghosh, A. (2005). Regulation of cortical dendrite development by Rap1 signaling. Mol. Cell. Neurosci. 28, 215-228.
28. Chhabra, E. S. and Higgs, H. N. (2007). The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9, 1110-1121.
29. Chihara, T., Luginbuhl, D. and Luo, L. (2007). Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat. Neurosci. 10, 828-837.
30. Christensen, R., de la Torre-Ubieta, L., Bonni, A. and Colón-Ramos, D. A. (2011). A conserved PTEN/FOXO pathway regulates neuronal morphology during C. elegans development. Development 138, 5257-5267.
31. Corty, M. M., Matthews, B. J. and Grueber, W. B. (2009). Molecules and mechanisms of dendrite development in Drosophila. Development 136, 1049-1061.
32. Craig, A. M. and Banker, G. (1994). Neuronal polarity. Annu. Rev. Neurosci. 17, 267-310.
33. Crozatier, M. and Vincent, A. (2008). Control of multidendritic neuron differentiation in Drosophila: the role of Collier. Dev. Biol. 315, 232-242.
34. Cubelos, B., Sebastián-Serrano, A., Beccari, L., Calcagnotto, M. E., Cisneros, E., Kim, S., Dopazo, A., Alvarez-Dolado, M., Redondo, J. M., Bovolenta, P. et al. (2010). Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 66, 523-535.
35. Cui-Wang, T., Hanus, C., Cui, T., Helton, T., Bourne, J., Watson, D., Harris, K. M. and Ehlers, M. D. (2012). Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 148, 309-321.
36. Dailey, M. E. and Smith, S. J. (1996). The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994.
37. de la Torre-Ubieta, L. and Bonni, A. (2011). Transcriptional regulation of neuronal polarity and morphogenesis in the mammalian brain. Neuron 72, 22-40.
38. de la Torre-Ubieta, L., Gaudillière, B., Yang, Y., Ikeuchi, Y., Yamada, T., DiBacco, S., Stegmüller, J., Schüller, U., Salih, D. A., Rowitch, D. et al. (2010). A FOXOPak1 transcriptional pathway controls neuronal polarity. Genes Dev. 24, 799-813.
39. Dierssen, M. and Ramakers, G. J. (2006). Dendritic pathology in mental retardation: from molecular genetics to neurobiology. Genes Brain Behav. 5 Suppl., 48-60.
40. Dijkhuizen, P. A. and Ghosh, A. (2005). Regulation of dendritic growth by calcium and neurotrophin signaling. Prog. Brain Res. 147, 15-27.
41. Emoto, K., Parrish, J. Z., Jan, L. Y. and Jan, Y. N. (2006). The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443, 210-213.
42. Flavell, S. W., Cowan, C. W., Kim, T. K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C. and Greenberg, M. E. (2006). Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012.
43. Fleck, M. W., Hirotsune, S., Gambello, M. J., Phillips-Tansey, E., Suares, G., Mervis, R. F., Wynshaw-Boris, A. and McBain, C. J. (2000). Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J. Neurosci. 20, 2439-2450.
44. Gan, W. B., Grutzendler, J., Wong, W. T., Wong, R. O. and Lichtman, J. W. (2000). Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 27, 219-225.
45. Gao, F. B., Brenman, J. E., Jan, L. Y. and Jan, Y. N. (1999). Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13, 2549-2561.
46. Gao, Z., Ure, K., Ables, J. L., Lagace, D. C., Nave, K. A., Goebbels, S., Eisch, A. J. and Hsieh, J. (2009). Neurod1 is essential for the survival and maturation of adultborn neurons. Nat. Neurosci. 12, 1090-1092.
47. Gaudillière, B., Konishi, Y., de la Iglesia, N., Yao, G. and Bonni, A. (2004). A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron 41, 229-241.
48. Gidon, A. and Segev, I. (2012). Principles governing the operation of synaptic inhibition in dendrites. Neuron 75, 330-341.
49. Goldberg, J. L. (2004). Intrinsic neuronal regulation of axon and dendrite growth. Curr. Opin. Neurobiol. 14, 551-557.
50. Goldberg, J. L., Klassen, M. P., Hua, Y. and Barres, B. A. (2002). Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296, 1860-1864.
51. Graveland, G. A., Williams, R. S. and DiFiglia, M. (1985). Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 227, 770-773.
52. Gregory, S. L. and Brown, N. H. (1998). Kakapo, a gene required for adhesion between and within cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J. Cell Biol. 143, 1271-1282.
53. Grueber, W. B. and Jan, Y. N. (2004). Dendritic development: lessons from Drosophila and related branches. Curr. Opin. Neurobiol. 14, 74-82.
54. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878.
55. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2003). Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112, 805-818.
56. Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chem. Biol. Interact. 141, 131-160.
57. Hámori, J. and Somogyi, J. (1983). Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J. Comp. Neurol. 220, 365-377.
58. Han, C., Wang, D., Soba, P., Zhu, S., Lin, X., Jan, L. Y. and Jan, Y. N. (2012). Integrins regulate repulsion-mediated dendritic patterning of drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 73, 64-78.
59. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. I., Guerrier, S., Boutt, E., Peters, E., Barnes, A. P., Parras, C. et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62.
60. Hanson, D., Murray, P. G., Sud, A., Temtamy, S. A., Aglan, M., Superti-Furga, A., Holder, S. E., Urquhart, J., Hilton, E., Manson, F. D. et al. (2009). The primordial growth disorder 3-M syndrome connects ubiquitination to the cytoskeletal adaptor OBSL1. Am. J. Hum. Genet. 84, 801-806.
61. Hattori, Y., Sugimura, K. and Uemura, T. (2007). Selective expression of Knot/Collier, a transcriptional regulator of the EBF/Olf-1 family, endows the Drosophila sensory system with neuronal class-specific elaborated dendritic patterns. Genes Cells 12, 1011-1022.
62. Häusser, M., Spruston, N. and Stuart, G. J. (2000). Diversity and dynamics of dendritic signaling. Science 290, 739-744.
63. Hayashi, K., Ohshima, T., Hashimoto, M. and Mikoshiba, K. (2007). Pak1 regulates dendritic branching and spine formation. Dev. Neurobiol. 67, 655-669.
64. Hirose, M., Ishizaki, T., Watanabe, N., Uehata, M., Kranenburg, O., Moolenaar, W. H., Matsumura, F., Maekawa, M., Bito, H. and Narumiya, S. (1998). Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636.
65. Holtmaat, A., Bonhoeffer, T., Chow, D. K., Chuckowree, J., De Paola, V., Hofer, S. B., Hübener, M., Keck, T., Knott, G., Lee, W. C. et al. (2009). Long-term, highresolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144.
66. Hoogenraad, C. C., Milstein, A. D., Ethell, I. M., Henkemeyer, M. and Sheng, M. (2005). GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci. 8, 906-915.
67. Horch, H. W., Krüttgen, A., Portbury, S. D. and Katz, L. C. (1999). Destabilization of cortical dendrites and spines by BDNF. Neuron 23, 353-364.
68. Horton, A. C. and Ehlers, M. D. (2003). Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23, 6188-6199.
69. Horton, A. C., Rácz, B., Monson, E. E., Lin, A. L., Weinberg, R. J. and Ehlers, M. D. (2005). Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757-771.
70. Huang, Z., Zang, K. and Reichardt, L. F. (2005). The origin recognition core complex regulates dendrite and spine development in postmitotic neurons. J. Cell Biol. 170, 527-535.
71. Huber, C., Dias-Santagata, D., Glaser, A., O'Sullivan, J., Brauner, R., Wu, K., Xu, X., Pearce, K., Wang, R., Uzielli, M. L. et al. (2005). Identification of mutations in CUL7 in 3-M syndrome. Nat. Genet. 37, 1119-1124.
72. Huckfeldt, R. M., Schubert, T., Morgan, J. L., Godinho, L., Di Cristo, G., Huang, Z. J. and Wong, R. O. (2009). Transient neurites of retinal horizontal cells exhibit columnar tiling via homotypic interactions. Nat. Neurosci. 12, 35-43.
73. Huynh, M. A., Stegmüller, J., Litterman, N. and Bonni, A. (2009). Regulation of Cdh1-APC function in axon growth by Cdh1 phosphorylation. J. Neurosci. 29, 4322-4327.
74. Huynh, M. A., Ikeuchi, Y., Netherton, S., de la Torre-Ubieta, L., Kanadia, R., Stegmüller, J., Cepko, C., Bonni, S. and Bonni, A. (2011). An isoform-specific SnoN1-FOXO1 repressor complex controls neuronal morphogenesis and positioning in the mammalian brain. Neuron 69, 930-944.
75. Irwin, S. A., Galvez, R. and Greenough, W. T. (2000). Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex 10, 1038-1044.
76. Jacobs, T., Causeret, F., Nishimura, Y. V., Terao, M., Norman, A., Hoshino, M. and Nikolić, M. (2007). Localized activation of p21-activated kinase controls neuronal polarity and morphology. J. Neurosci. 27, 8604-8615.
77. Jan, Y. N. and Jan, L. Y. (2003). The control of dendrite development. Neuron 40, 229-242.
78. Jan, Y. N. and Jan, L. Y. (2010). Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11, 316-328.
79. Jaworski, J., Spangler, S., Seeburg, D. P., Hoogenraad, C. C. and Sheng, M. (2005). Control of dendritic arborization by the phosphoinositide-3′-kinase-Aktmammalian target of rapamycin pathway. J. Neurosci. 25, 11300-11312.
80. Jinushi-Nakao, S., Arvind, R., Amikura, R., Kinameri, E., Liu, A. W. and Moore, A. W. (2007). Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 56, 963-978.
81. Jossin, Y. and Goffinet, A. M. (2007). Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol. Cell. Biol. 27, 7113-7124.
82. Karlsgodt, K. H., Sun, D., Jimenez, A. M., Lutkenhoff, E. S., Willhite, R., van Erp, T. G. and Cannon, T. D. (2008). Developmental disruptions in neural connectivity in the pathophysiology of schizophrenia. Dev. Psychopathol. 20, 1297-1327.
83. Kaufmann, W. E. and Moser, H. W. (2000). Dendritic anomalies in disorders associated with mental retardation. Cereb. Cortex 10, 981-991.
84. Kim, A. H. and Bonni, A. (2007). Thinking within the D box: initial identification of Cdh1-APC substrates in the nervous system. Mol. Cell. Neurosci. 34, 281-287.
85. Kim, S. and Chiba, A. (2004). Dendritic guidance. Trends Neurosci. 27, 194-202.
86. Kim, M. D., Jan, L. Y. and Jan, Y. N. (2006). The bHLH-PAS protein Spineless is necessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes Dev. 20, 2806-2819.
87. Kim, A. H., Puram, S. V., Bilimoria, P. M., Ikeuchi, Y., Keough, S., Wong, M., Rowitch, D. and Bonni, A. (2009). A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 136, 322-336.
88. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
89. Kirilly, D., Wong, J. J., Lim, E. K., Wang, Y., Zhang, H., Wang, C., Liao, Q., Wang, H., Liou, Y. C., Wang, H. et al. (2011). Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron 72, 86-100.
90. Koike-Kumagai, M., Yasunaga, K., Morikawa, R., Kanamori, T. and Emoto, K. (2009). The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway. EMBO J. 28, 3879-3892.
91. Komiyama, T. and Luo, L. (2007). Intrinsic control of precise dendritic targeting by an ensemble of transcription factors. Curr. Biol. 17, 278-285.
92. Komiyama, T., Johnson, W. A., Luo, L. and Jefferis, G. S. (2003). From lineage to wiring specificity. POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112, 157-167.
93. Konishi, Y., Stegmüller, J., Matsuda, T., Bonni, S. and Bonni, A. (2004). Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303, 1026-1030.
94. Konur, S. and Ghosh, A. (2005). Calcium signaling and the control of dendritic development. Neuron 46, 401-405.
95. Kramer, A. P. and Kuwada, J. Y. (1983). Formation of the receptive fields of leech mechanosensory neurons during embryonic development. J. Neurosci. 3, 2474-2486.
96. Kumamoto, N., Gu, Y., Wang, J., Janoschka, S., Takemaru, K., Levine, J. and Ge, S. (2012). A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat. Neurosci. 15, 399-405, S1.
97. Kumar, V., Zhang, M. X., Swank, M. W., Kunz, J. and Wu, G. Y. (2005). Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25, 11288-11299.
98. Landgraf, M., Jeffrey, V., Fujioka, M., Jaynes, J. B. and Bate, M. (2003). Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila. PLoS Biol. 1, E41.
99. Lanier, L. M. and Gertler, F. B. (2000). From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr. Opin. Neurobiol. 10, 80-87.
100. Lasorella, A., Stegmüller, J., Guardavaccaro, D., Liu, G., Carro, M. S., Rothschild, G., de la Torre-Ubieta, L., Pagano, M., Bonni, A. and Iavarone, A. (2006). Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442, 471-474.
101. Lavzin, M., Rapoport, S., Polsky, A., Garion, L. and Schiller, J. (2012). Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo. Nature 490, 397-401.
102. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
103. Lee, T., Winter, C., Marticke, S. S., Lee, A. and Luo, L. (2000). Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316.
104. Lee, A., Li, W., Xu, K., Bogert, B. A., Su, K. and Gao, F. B. (2003). Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130, 5543-5552.
105. Leemhuis, J., Boutillier, S., Barth, H., Feuerstein, T. J., Brock, C., Nürnberg, B., Aktories, K. and Meyer, D. K. (2004). Rho GTPases and phosphoinositide 3-kinase organize formation of branched dendrites. J. Biol. Chem. 279, 585-596.
106. Li, W. and Gao, F. B. (2003). Actin filament-stabilizing protein tropomyosin regulates the size of dendritic fields. J. Neurosci. 23, 6171-6175.
107. Li, Z., Van Aelst, L. and Cline, H. T. (2000). Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3, 217-225.
108. Li, W., Wang, F., Menut, L. and Gao, F. B. (2004). BTB/POZ-zinc finger protein abrupt suppresses dendritic branching in a neuronal subtype-specific and dosagedependent manner. Neuron 43, 823-834.
109. Li, J., Gu, X., Ma, Y., Calicchio, M. L., Kong, D., Teng, Y. D., Yu, L., Crain, A. M., Vartanian, T. K., Pasqualini, R. et al. (2010a). Nna1 mediates Purkinje cell dendritic development via lysyl oxidase propeptide and NF-κB signaling. Neuron 68, 45-60.
110. Li, N., Zhao, C. T., Wang, Y. and Yuan, X. B. (2010b). The transcription factor Cux1 regulates dendritic morphology of cortical pyramidal neurons. PLoS ONE 5, e10596.
111. Litterman, N., Ikeuchi, Y., Gallardo, G., O'Connell, B. C., Sowa, M. E., Gygi, S. P., Harper, J. W. and Bonni, A. (2011). An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates Golgi morphology and dendrite patterning. PLoS Biol. 9, e1001060.
112. Liu, Z., Steward, R. and Luo, L. (2000). Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat. Cell Biol. 2, 776-783.
113. Lo, D. C., McAllister, A. K. and Katz, L. C. (1994). Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron 13, 1263-1268.
114. Maksimova, N., Hara, K., Miyashia, A., Nikolaeva, I., Shiga, A., Nogovicina, A., Sukhomyasova, A., Argunov, V., Shvedova, A., Ikeuchi, T. et al. (2007). Clinical, molecular and histopathological features of short stature syndrome with novel CUL7 mutation in Yakuts: new population isolate in Asia. J. Med. Genet. 44, 772-778.
115. 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. et al. (2010). EphBmediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation. Cell 143, 442-455.
116. McAllister, A. K., Lo, D. C. and Katz, L. C. (1995). Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15, 791-803.
117. McAllister, A. K., Katz, L. C. and Lo, D. C. (1996). Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064.
118. Mertz, K., Koscheck, T. and Schilling, K. (2000). Brain-derived neurotrophic factor modulates dendritic morphology of cerebellar basket and stellate cells: an in vitro study. Neuroscience 97, 303-310.
119. Millard, S. S. and Zipursky, S. L. (2008). Dscam-mediated repulsion controls tiling and self-avoidance. Curr. Opin. Neurobiol. 18, 84-89.
120. Miller, F. D. and Kaplan, D. R. (2003). Signaling mechanisms underlying dendrite formation. Curr. Opin. Neurobiol. 13, 391-398.
121. Mohideen, F., Capili, A. D., Bilimoria, P. M., Yamada, T., Bonni, A. and Lima, C. D. (2009). A molecular basis for phosphorylation-dependent SUMO conjugation by the E2 UBC9. Nat. Struct. Mol. Biol. 16, 945-952.
122. Moore, A. W., Jan, L. Y. and Jan, Y. N. (2002). Hamlet, a binary genetic switch between single-and multiple-dendrite neuron morphology. Science 297, 1355-1358.
123. Nagel, J., Delandre, C., Zhang, Y., Förstner, F., Moore, A. W. and Tavosanis, G. (2012). Fascin controls neuronal class-specific dendrite arbor morphology. Development 139, 2999-3009.
124. Nakayama, A. Y., Harms, M. B. and Luo, L. (2000). Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20, 5329-5338.
125. Nedivi, E., Wu, G. Y. and Cline, H. T. (1998). Promotion of dendritic growth by CPG15, an activity-induced signaling molecule. Science 281, 1863-1866.
126. Newey, S. E., Velamoor, V., Govek, E. E. and Van Aelst, L. (2005). Rho GTPases, dendritic structure, and mental retardation. J. Neurobiol. 64, 58-74.
127. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B. J. and Luo, L. (2002). Rac GTPases control axon growth, guidance and branching. Nature 416, 442-447.
128. Niethammer, M., Smith, D. S., Ayala, R., Peng, J., Ko, J., Lee, M. S., Morabito, M. and Tsai, L. H. (2000). NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28, 697-711.
129. Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J. and Tsai, L. H. (1998). The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395, 194-198.
130. Oe, S. and Yoneda, Y. (2010). Cytoplasmic polyadenylation element-like sequences are involved in dendritic targeting of BDNF mRNA in hippocampal neurons. FEBS Lett. 584, 3424-3430.
131. Okazawa, M., Abe, H., Katsukawa, M., Iijima, K., Kiwada, T. and Nakanishi, S. (2009). Role of calcineurin signaling in membrane potential-regulated maturation of cerebellar granule cells. J. Neurosci. 29, 2938-2947.
132. Ori-McKenney, K. M., Jan, L. Y. and Jan, Y. N. (2012). Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76, 921-930.
133. Palay, S. and Chan-Palay, V. (1974). Cerebellar Cortex: Cytology and Organization. New York, NY: Springer-Verlag.
134. Pan, D. (2007). Hippo signaling in organ size control. Genes Dev. 21, 886-897.
135. Pardo, C. A. and Eberhart, C. G. (2007). The neurobiology of autism. Brain Pathol. 17, 434-447.
136. Parrish, J. Z., Kim, M. D., Jan, L. Y. and Jan, Y. N. (2006). Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev. 20, 820-835.
137. Parrish, J. Z., Emoto, K., Jan, L. Y. and Jan, Y. N. (2007a). Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites. Genes Dev. 21, 956-972.
138. Parrish, J. Z., Emoto, K., Kim, M. D. and Jan, Y. N. (2007b). Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399-423.
139. Parrish, J. Z., Xu, P., Kim, C. C., Jan, L. Y. and Jan, Y. N. (2009). The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in drosophila sensory neurons. Neuron 63, 788-802.
140. Peng, Y. R., He, S., Marie, H., Zeng, S. Y., Ma, J., Tan, Z. J., Lee, S. Y., Malenka, R. C. and Yu, X. (2009). Coordinated changes in dendritic arborization and synaptic strength during neural circuit development. Neuron 61, 71-84.
141. Perry, V. H. and Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683-685.
142. Peters, A., Palay, S. L. and Webster, H. D. (1991). The Fine Structure of the Nervous System: Neurons and Their Supporting Cells. New York, NY: Oxford University Press.
143. Pfenninger, K. H. (2009). Plasma membrane expansion: a neuron's Herculean task. Nat. Rev. Neurosci. 10, 251-261.
144. Prokop, A., Uhler, J., Roote, J. and Bate, M. (1998). The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motorneurons. J. Cell Biol. 143, 1283-1294.
145. Puram, S. V. and Bonni, A. (2011). Novel functions for the anaphase-promoting complex in neurobiology. Semin. Cell Dev. Biol. 22, 586-594.
146. Puram, S. V., Kim, A. H. and Bonni, A. (2010). An old dog learns new tricks: a novel function for Cdc20-APC in dendrite morphogenesis in neurons. Cell Cycle 9, 482-485.
147. Puram, S. V., Kim, A. H., Ikeuchi, Y., Wilson-Grady, J. T., Merdes, A., Gygi, S. P. and Bonni, A. (2011a). A CaMKIIβ signaling pathway at the centrosome regulates dendrite patterning in the brain. Nat. Neurosci. 14, 973-983.
148. Puram, S. V., Riccio, A., Koirala, S., Ikeuchi, Y., Kim, A. H., Corfas, G. and Bonni, A. (2011b). A TRPC5-regulated calcium signaling pathway controls dendrite patterning in the mammalian brain. Genes Dev. 25, 2659-2673.
149. Puram, S. V., Kim, A. H., Park, H. Y., Anckar, J. and Bonni, A. (2013). The ubiquitin receptor S5a/Rpn10 links centrosomal proteasomes with dendrite development in the mammalian brain. Cell Rep. 4, 19-30.
150. Quitsch, A., Berhörster, K., Liew, C. W., Richter, D. and Kreienkamp, H. J. (2005). Postsynaptic shank antagonizes dendrite branching induced by the leucine-rich repeat protein Densin-180. J. Neurosci. 25, 479-487.
151. Ramón y Cajal, S. (1995). Histology of the Nervous System of Man and Vertebrates. New York, NY: Oxford University Press.
152. Ramos, B., Gaudillière, B., Bonni, A. and Gill, G. (2007). Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proc. Natl. Acad. Sci. USA 104, 9882-9887.
153. Ramos, B., Valín, A., Sun, X. and Gill, G. (2009). Sp4-dependent repression of neurotrophin-3 limits dendritic branching. Mol. Cell. Neurosci. 42, 152-159.
154. Redmond, L., Kashani, A. H. and Ghosh, A. (2002). Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34, 999-1010.
155. Rosário, M., Schuster, S., Jüttner, R., Parthasarathy, S., Tarabykin, V. and Birchmeier, W. (2012). Neocortical dendritic complexity is controlled during development by NOMA-GAP-dependent inhibition of Cdc42 and activation of cofilin. Genes Dev. 26, 1743-1757.
156. Rosso, S. B., Sussman, D., Wynshaw-Boris, A. and Salinas, P. C. (2005). Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 8, 34-42.
157. Ruchhoeft, M. L., Ohnuma, S., McNeill, L., Holt, C. E. and Harris, W. A. (1999). The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo. J. Neurosci. 19, 8454-8463.
158. Sagasti, A., Guido, M. R., Raible, D. W. and Schier, A. F. (2005). Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr. Biol. 15, 804-814.
159. Sahin, M., Greer, P. L., Lin, M. Z., Poucher, H., Eberhart, J., Schmidt, S., Wright, T. M., Shamah, S. M., O'connell, S., Cowan, C. W. et al. (2005). Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 46, 191-204.
160. Saksena, S., Wahlman, J., Teis, D., Johnson, A. E. and Emr, S. D. (2009). Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97-109.
161. Sasaki, S., Shionoya, A., Ishida, M., Gambello, M. J., Yingling, J., Wynshaw-Boris, A. and Hirotsune, S. (2000). A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28, 681-696.
162. Satoh, D., Sato, D., Tsuyama, T., Saito, M., Ohkura, H., Rolls, M. M., Ishikawa, F. and Uemura, T. (2008). Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol. 10, 1164-1171.
163. Schwartz, P. M., Borghesani, P. R., Levy, R. L., Pomeroy, S. L. and Segal, R. A. (1997). Abnormal cerebellar development and foliation in BDNF-/-mice reveals a role for neurotrophins in CNS patterning. Neuron 19, 269-281.
164. Scott, E. K. and Luo, L. (2001). How do dendrites take their shape? Nat. Neurosci. 4, 359-365.
165. Scott, E. K., Reuter, J. E. and Luo, L. (2003). Small GTPase Cdc42 is required for multiple aspects of dendritic morphogenesis. J. Neurosci. 23, 3118-3123.
166. Selkoe, D. J., Bell, D. S., Podlisny, M. B., Price, D. L. and Cork, L. C. (1987). Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science 235, 873-877.
167. Shalizi, A., Gaudillière, B., Yuan, Z., Stegmüller, J., Shirogane, T., Ge, Q., Tan, Y., Schulman, B., Harper, J. W. and Bonni, A. (2006). A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 311, 1012-1017.
168. Shalizi, A., Bilimoria, P. M., Stegmüller, J., Gaudillière, B., Yang, Y., Shuai, K. and Bonni, A. (2007). PIASx is a MEF2 SUMO E3 ligase that promotes postsynaptic dendritic morphogenesis. J. Neurosci. 27, 10037-10046.
169. Shamah, S. M., Lin, M. Z., Goldberg, J. L., Estrach, S., Sahin, M., Hu, L., Bazalakova, M., Neve, R. L., Corfas, G., Debant, A. et al. (2001). EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233-244.
170. Sharp, D. J., Yu, W., Ferhat, L., Kuriyama, R., Rueger, D. C. and Baas, P. W. (1997). Identification of a microtubule-associated motor protein essential for dendritic differentiation. J. Cell Biol. 138, 833-843.
171. Smith, D. S., Niethammer, M., Ayala, R., Zhou, Y., Gambello, M. J., Wynshaw-Boris, A. and Tsai, L. H. (2000). Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat. Cell Biol. 2, 767-775.
172. Song, Y., Ori-McKenney, K. M., Zheng, Y., Han, C., Jan, L. Y. and Jan, Y. N. (2012). Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. Genes Dev. 26, 1612-1625.
173. Spletter, M. L., Liu, J., Liu, J., Su, H., Giniger, E., Komiyama, T., Quake, S. and Luo, L. (2007). Lola regulates Drosophila olfactory projection neuron identity and targeting specificity. Neural Dev. 2, 14.
174. Stegmüller, J. and Bonni, A. (2010). Destroy to create: E3 ubiquitin ligases in neurogenesis. F1000 Biol. Rep. 2, 38.
175. Stegmüller, J., Konishi, Y., Huynh, M. A., Yuan, Z., Dibacco, S. and Bonni, A. (2006). Cell-intrinsic regulation of axonal morphogenesis by the Cdh1-APC target SnoN. Neuron 50, 389-400.
176. Strumpf, D. and Volk, T. (1998). Kakapo, a novel cytoskeletal-associated protein is essential for the restricted localization of the neuregulin-like factor, vein, at the muscle-tendon junction site. J. Cell Biol. 143, 1259-1270.
177. Sugimura, K., Satoh, D., Estes, P., Crews, S. and Uemura, T. (2004). Development of morphological diversity of dendrites in Drosophila by the BTB-zinc finger protein abrupt. Neuron 43, 809-822.
178. Sweeney, N. T., Brenman, J. E., Jan, Y. N. and Gao, F. B. (2006). The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr. Biol. 16, 1006-1011.
179. Tahirovic, S. and Bradke, F. (2009). Neuronal polarity. Cold Spring Harb. Perspect. Biol. 1, a001644.
180. Takashima, S., Becker, L. E., Armstrong, D. L. and Chan, F. (1981). Abnormal neuronal development in the visual cortex of the human fetus and infant with down's syndrome. A quantitative and qualitative Golgi study. Brain Res. 225, 1-21.
181. Tea, J. S. and Luo, L. (2011). The chromatin remodeling factor Bap55 functions through the TIP60 complex to regulate olfactory projection neuron dendrite targeting. Neural Dev. 6, 5.
182. Tea, J. S., Chihara, T. and Luo, L. (2010). Histone deacetylase Rpd3 regulates olfactory projection neuron dendrite targeting via the transcription factor Prospero. J. Neurosci. 30, 9939-9946.
183. Teis, D., Saksena, S. and Emr, S. D. (2008). Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev. Cell 15, 578-589.
184. Tolias, K. F., Bikoff, J. B., Burette, A., Paradis, S., Harrar, D., Tavazoie, S., Weinberg, R. J. and Greenberg, M. E. (2005). The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45, 525-538.
185. Ultanir, S. K., Hertz, N. T., Li, G., Ge, W. P., Burlingame, A. L., Pleasure, S. J., Shokat, K. M., Jan, L. Y. and Jan, Y. N. (2012). Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 uncovers their roles in dendrite arborization and spine development. Neuron 73, 1127-1142.
186. Vessey, J. P., Macchi, P., Stein, J. M., Mikl, M., Hawker, K. N., Vogelsang, P., Wieczorek, K., Vendra, G., Riefler, J., Tübing, F. et al. (2008). A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis. Proc. Natl. Acad. Sci. USA 105, 16374-16379.
187. Wässle, H., Peichl, L. and Boycott, B. B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344-345.
188. Whitford, K. L., Dijkhuizen, P., Polleux, F. and Ghosh, A. (2002). Molecular control of cortical dendrite development. Annu. Rev. Neurosci. 25, 127-149.
189. Williams, D. W. and Truman, J. W. (2005). Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132, 3631-3642.
190. Wills, Z., Bateman, J., Korey, C. A., Comer, A. and Van Vactor, D. (1999). The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22, 301-312.
191. Wingate, R. J. and Thompson, I. D. (1994). Targeting and activity-related dendritic modification in mammalian retinal ganglion cells. J. Neurosci. 14, 6621-6637.
192. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D. and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91.
193. Wong, W. T., Faulkner-Jones, B. E., Sanes, J. R. and Wong, R. O. (2000). Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho. J. Neurosci. 20, 5024-5036.
194. Wu, J. I., Lessard, J., Olave, I. A., Qiu, Z., Ghosh, A., Graef, I. A. and Crabtree, G. R. (2007). Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56, 94-108.
195. Yamada, T., Yang, Y. and Bonni, A. (2013). Spatial organization of ubiquitin ligase pathways orchestrates neuronal connectivity. Trends Neurosci. 36, 218-226.
196. Yang, Y., Kim, A. H. and Bonni, A. (2010). The dynamic ubiquitin ligase duo: Cdh1-APC and Cdc20-APC regulate neuronal morphogenesis and connectivity. Curr. Opin. Neurobiol. 20, 92-99.
197. Yang, W. K., Peng, Y. H., Li, H., Lin, H. C., Lin, Y. C., Lai, T. T., Suo, H., Wang, C. H., Lin, W. H., Ou, C. Y. et al. (2011). Nak regulates localization of clathrin sites in higher-order dendrites to promote local dendrite growth. Neuron 72, 285-299.
198. Ye, B., Petritsch, C., Clark, I. E., Gavis, E. R., Jan, L. Y. and Jan, Y. N. (2004). Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr. Biol. 14, 314-321.
199. Ye, B., Zhang, Y., Song, W., Younger, S. H., Jan, L. Y. and Jan, Y. N. (2007). Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130, 717-729.
200. Yu, X. and Malenka, R. C. (2003). Beta-catenin is critical for dendritic morphogenesis. Nat. Neurosci. 6, 1169-1177.
201. Yu, W., Cook, C., Sauter, C., Kuriyama, R., Kaplan, P. L. and Baas, P. W. (2000). Depletion of a microtubule-associated motor protein induces the loss of dendritic identity. J. Neurosci. 20, 5782-5791.
202. Zheng, Y., Wildonger, J., Ye, B., Zhang, Y., Kita, A., Younger, S. H., Zimmerman, S., Jan, L. Y. and Jan, Y. N. (2008). Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10, 1172-1180.