The complex, branched morphology of dendrites is a cardinal feature of neurons and has been used as a criterion for cell type identification since the beginning of neurobiology. Regulated dendritic outgrowth and branching during development form the basis of receptive fields for neurons and are essential for the wiring of the nervous system. The cellular and molecular mechanisms of dendritic morphogenesis have been an intensely studied area. In this review, we summarize the major experimental systems that have contributed to our understandings of dendritic development as well as the intrinsic and extrinsic mechanisms that instruct the neurons to form cell type–specific dendritic arbors.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Nicholls JG, Baylor DA. 1.  1968. Specific modalities and receptive fields of sensory neurons in CNS of the leech. J. Neurophysiol. 31:740–56 [Google Scholar]
  2. Kramer AP, Kuwada JY. 2.  1983. Formation of the receptive fields of leech mechanosensory neurons during embryonic development. J. Neurosci. 3:2474–86 [Google Scholar]
  3. Kramer AP, Stent GS. 3.  1985. Developmental arborization of sensory neurons in the leech Haementeria ghilianii. II. Experimentally induced variations in the branching pattern. J. Neurosci. 5:768–75 [Google Scholar]
  4. Grueber WB, Sagasti A. 4.  2010. Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harb. Perspect. Biol. 2:a001750 [Google Scholar]
  5. Smith CJ, Watson JD, VanHoven MK, Colon-Ramos DA, Miller DM 3rd. 5.  2012. Netrin (UNC-6) mediates dendritic self-avoidance. Nat. Neurosci. 15:731–37 [Google Scholar]
  6. Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. 6.  2012. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488:517–21 [Google Scholar]
  7. Montague PR, Friedlander MJ. 7.  1989. Expression of an intrinsic growth strategy by mammalian retinal neurons. PNAS 86:7223–27 [Google Scholar]
  8. Montague PR, Friedlander MJ. 8.  1991. Morphogenesis and territorial coverage by isolated mammalian retinal ganglion cells. J. Neurosci. 11:1440–57 [Google Scholar]
  9. Wässle H, Peichl L, Boycott BB. 9.  1981. Dendritic territories of cat retinal ganglion cells. Nature 292:344–45 [Google Scholar]
  10. Jan YN, Jan LY. 10.  2010. Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11:316–28 [Google Scholar]
  11. Grueber WB, Jan LY, Jan YN. 11.  2002. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129:2867–78 [Google Scholar]
  12. Tsubouchi A, Caldwell JC, Tracey WD. 12.  2012. Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr. Biol. 22:2124–34 [Google Scholar]
  13. Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F. 13.  et al. 2007. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17:2105–16 [Google Scholar]
  14. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN. 14.  2010. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921–26 [Google Scholar]
  15. Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y. 15.  et al. 2013. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:221–25 [Google Scholar]
  16. Grueber WB, Ye B, Yang CH, Younger S, Borden K. 16.  et al. 2007. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 134:55–64 [Google Scholar]
  17. Parrish JZ, Kim MD, Jan LY, Jan YN. 17.  2006. Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev. 20:820–35 [Google Scholar]
  18. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC. 18.  et al. 2007. Dendrite self-avoidance is controlled by Dscam. Cell 129:593–604 [Google Scholar]
  19. Parrish JZ, Xu P, Kim CC, Jan LY, Jan YN. 19.  2009. The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in Drosophila sensory neurons. Neuron 63:788–802 [Google Scholar]
  20. Sulston JE, Horvitz HR. 20.  1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56:110–56 [Google Scholar]
  21. Albeg A, Smith CJ, Chatzigeorgiou M, Feitelson DG, Hall DH. 21.  et al. 2011. C. elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell. Neurosci. 46:308–17 [Google Scholar]
  22. Hall DH, Treinin M. 22.  2011. How does morphology relate to function in sensory arbors. Trends Neurosci. 34:443–51 [Google Scholar]
  23. Smith CJ, Watson JD, Spencer WC, O'Brien T, Cha B. 23.  et al. 2010. Time-lapse imaging and cell-specific expression profiling reveal dynamic branching and molecular determinants of a multi-dendritic nociceptor in C. elegans. Dev. Biol. 345:18–33 [Google Scholar]
  24. Oren-Suissa M, Hall DH, Treinin M, Shemer G, Podbilewicz B. 23a.  2010. The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328:1285–88 [Google Scholar]
  25. Liu OW, Shen K. 24.  2012. The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat. Neurosci. 15:57–63 [Google Scholar]
  26. Salzberg Y, Diaz-Balzac CA, Ramirez-Suarez NJ, Attreed M, Tecle E. 25.  et al. 2013. Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155:308–20 [Google Scholar]
  27. Dong X, Liu OW, Howell AS, Shen K. 26.  2013. An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 155:296–307 [Google Scholar]
  28. Wu GY, Cline HT. 27.  1998. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–26 [Google Scholar]
  29. Cline HT. 28.  2001. Dendritic arbor development and synaptogenesis. Curr. Opin. Neurobiol. 11:118–26 [Google Scholar]
  30. Hua JY, Smith SJ. 29.  2004. Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 7:327–32 [Google Scholar]
  31. Shipp S. 30.  2007. Structure and function of the cerebral cortex. Curr. Biol. 17:R443–49 [Google Scholar]
  32. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. 31.  2008. The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 18:28–35 [Google Scholar]
  33. Polleux F, Morrow T, Ghosh A. 32.  2000. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:567–73 [Google Scholar]
  34. Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M. 33.  et al. 2002. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33:47–61 [Google Scholar]
  35. Sanes JR, Zipursky SL. 34.  2010. Design principles of insect and vertebrate visual systems. Neuron 66:15–36 [Google Scholar]
  36. Choi J-H, Law M-Y, Chien C-B, Link B, Wong R. 35.  2010. In vivo development of dendritic orientation in wild-type and mislocalized retinal ganglion cells. Neural Dev. 5:29 [Google Scholar]
  37. Walsh MK, Quigley HA. 36.  2008. In vivo time-lapse fluorescence imaging of individual retinal ganglion cells in mice. J. Neurosci. Methods 169:214–21 [Google Scholar]
  38. Mumm JS, Williams PR, Godinho L, Koerber A, Pittman AJ. 37.  et al. 2006. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52:609–21 [Google Scholar]
  39. Duan X, Krishnaswamy A, de la Huerta I, Sanes JR. 38.  2014. Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158:4793–807 [Google Scholar]
  40. Kim I-J, Zhang Y, Meister M, Sanes JR. 39.  2010. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J. Neurosci. 30:1452–62 [Google Scholar]
  41. Zipursky SL, Sanes JR. 40.  2010. Chemoaffinity revisited: Dscams, protocadherins, and neural circuit assembly. Cell 143:343–53 [Google Scholar]
  42. Koleske AJ. 41.  2013. Molecular mechanisms of dendrite stability. Nat. Rev. Neurosci. 14:536–50 [Google Scholar]
  43. Sweeney NT, Li W, Gao FB. 42.  2002. Genetic manipulation of single neurons in vivo reveals specific roles of Flamingo in neuronal morphogenesis. Dev. Biol. 247:76–88 [Google Scholar]
  44. Gao F-B, Brenman JE, Jan LY, Jan YN. 43.  1999. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13:2549–61 [Google Scholar]
  45. Moore AW, Jan LY, Jan YN. 44.  2002. hamlet, a binary genetic switch between single- and multiple-dendrite neuron morphology. Science 297:1355–58 [Google Scholar]
  46. Corty MM, Matthews BJ, Grueber WB. 45.  2009. Molecules and mechanisms of dendrite development in Drosophila. Development 136:1049–61 [Google Scholar]
  47. Sugimura K, Satoh D, Estes P, Crews S, Uemura T. 46.  2004. Development of morphological diversity of dendrites in Drosophila by the BTB–zinc finger protein abrupt. Neuron 43:809–22 [Google Scholar]
  48. Li W, Wang F, Menut L, Gao FB. 47.  2004. BTB/POZ–zinc finger protein abrupt suppresses dendritic branching in a neuronal subtype–specific and dosage-dependent manner. Neuron 43:823–34 [Google Scholar]
  49. Blochlinger K, Bodmer R, Jan LY, Jan YN. 48.  1990. Patterns of expression of Cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 4:1322–31 [Google Scholar]
  50. Grueber WB, Jan LY, Jan YN. 49.  2003. Different levels of the homeodomain protein Cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112:805–18 [Google Scholar]
  51. Crozatier M, Vincent A. 50.  2008. Control of multidendritic neuron differentiation in Drosophila: the role of Collier. Dev. Biol. 315:232–42 [Google Scholar]
  52. Hattori Y, Sugimura K, Uemura T. 51.  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 12:1011–22 [Google Scholar]
  53. Jinushi-Nakao S, Arvind R, Amikura R, Kinameri E, Liu AW, Moore AW. 52.  2007. Knot/Collier and Cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 56:963–78 [Google Scholar]
  54. Kim MD, Jan LY, Jan YN. 53.  2006. The bHLH-PAS protein Spineless is necessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes Dev. 20:2806–19 [Google Scholar]
  55. Li N, Zhao CT, Wang Y, Yuan XB. 54.  2010. The transcription factor Cux1 regulates dendritic morphology of cortical pyramidal neurons. PLOS ONE 5:e10596 [Google Scholar]
  56. Cubelos B, Sebastian-Serrano A, Beccari L, Calcagnotto ME, Cisneros E. 55.  et al. 2010. Cux1 and Cux2 regulate dendritic branching, spine morphology, and synapses of the upper layer neurons of the cortex. Neuron 66:523–35 [Google Scholar]
  57. Matsui A, Tran M, Yoshida AC, Kikuchi SS, Ogawa UM, Shimogori MT. 56.  2013. BTBD3 controls dendrite orientation toward active axons in mammalian neocortex. Science 342:1114–18 [Google Scholar]
  58. Way JC, Chalfie M. 57.  1989. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3:1823–33 [Google Scholar]
  59. Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O. 58.  2003. LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev. Biol. 263:81–102 [Google Scholar]
  60. Smith CJ, O'Brien T, Chatzigeorgiou M, Spencer WC, Feingold-Link E. 59.  et al. 2013. Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization. Neuron 79:266–80 [Google Scholar]
  61. Hattori Y, Usui T, Satoh D, Moriyama S, Shimono K. 60.  et al. 2013. Sensory-neuron subtype–specific transcriptional programs controlling dendrite morphogenesis: genome-wide analysis of Abrupt and Knot/Collier. Dev. Cell 27:530–44 [Google Scholar]
  62. Sharp DJ, Yu W, Ferhat L, Kuriyama R, Rueger DC, Baas PW. 61.  1997. Identification of a microtubule-associated motor protein essential for dendritic differentiation. J. Cell Biol. 138:833–43 [Google Scholar]
  63. Yu W, Cook C, Sauter C, Kuriyama R, Kaplan PL, Baas PW. 62.  2000. Depletion of a microtubule-associated motor protein induces the loss of dendritic identity. J. Neurosci. 20:5782–91 [Google Scholar]
  64. Zheng Y, Wildonger J, Ye B, Zhang Y, Kita A. 63.  et al. 2008. Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10:1172–80 [Google Scholar]
  65. Satoh D, Sato D, Tsuyama T, Saito M, Ohkura H. 64.  et al. 2008. Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol. 10:1164–71 [Google Scholar]
  66. Horton AC, Ehlers MD. 65.  2003. Dual modes of endoplasmic reticulum–to–Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23:6188–99 [Google Scholar]
  67. Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. 66.  2005. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48:757–71 [Google Scholar]
  68. Papoulas O, Hays TS, Sisson JC. 67.  2005. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat. Cell Biol. 7:612–18 [Google Scholar]
  69. Aguirre-Chen C, Bülow HE, Kaprielian Z. 68.  2011. C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites. Development 138:507–18 [Google Scholar]
  70. Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, Sheng M. 69.  2005. GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat. Neurosci. 8:906–15 [Google Scholar]
  71. Geiger JC, Lipka J, Segura I, Hoyer S, Schlager MA. 70.  et al. 2014. The GRIP1/14-3-3 pathway coordinates cargo trafficking and dendrite development. Dev. Cell 28:381–93 [Google Scholar]
  72. Ng J, Nardine T, Harms M, Tzu J, Goldstein A. 71.  et al. 2002. Rac GTPases control axon growth, guidance and branching. Nature 416:442–47 [Google Scholar]
  73. Li W, Gao FB. 72.  2003. Actin filament–stabilizing protein tropomyosin regulates the size of dendritic fields. J. Neurosci. 23:6171–75 [Google Scholar]
  74. Lee A, Li W, Xu K, Bogert BA, Su K, Gao FB. 73.  2003. Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130:5543–52 [Google Scholar]
  75. Scott EK, Reuter JE, Luo L. 74.  2003. Small GTPase Cdc42 is required for multiple aspects of dendritic morphogenesis. J. Neurosci. 23:3118–23 [Google Scholar]
  76. Lee T, Winter C, Marticke SS, Lee A, Luo L. 75.  2000. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25:307–16 [Google Scholar]
  77. Ruchhoeft ML, Ohnuma S, McNeill L, Holt CE, Harris WA. 76.  1999. The neuronal architecture of Xenopus retinal ganglion cells is sculpted by Rho-family GTPases in vivo. J. Neurosci. 19:8454–63 [Google Scholar]
  78. Li Z, Van Aelst L, Cline HT. 77.  2000. Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3:217–25 [Google Scholar]
  79. Wong WT, Faulkner-Jones BE, Sanes JR, Wong RO. 78.  2000. Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho. J. Neurosci. 20:5024–36 [Google Scholar]
  80. Nakayama AY, Harms MB, Luo L. 79.  2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20:5329–38 [Google Scholar]
  81. Rosário M, Schuster S, Juttner R, Parthasarathy S, Tarabykin V, Birchmeier W. 80.  2012. Neocortical dendritic complexity is controlled during development by NOMA-GAP-dependent inhibition of Cdc42 and activation of cofilin. Genes Dev. 26:1743–57 [Google Scholar]
  82. Tolias KF, Bikoff JB, Burette A, Paradis S, Harrar D. 81.  et al. 2005. The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45:525–38 [Google Scholar]
  83. Tolias KF, Bikoff JB, Kane CG, Tolias CS, Hu L, Greenberg ME. 82.  2007. The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor–dependent dendritic spine development. PNAS 104:7265–70 [Google Scholar]
  84. Hayashi K, Ohshima T, Hashimoto M, Mikoshiba K. 83.  2007. Pak1 regulates dendritic branching and spine formation. Dev. Neurobiol. 67:655–69 [Google Scholar]
  85. Gao FB, Brenman JE, Jan LY, Jan YN. 84.  1999. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13:2549–61 [Google Scholar]
  86. Conde C, Caceres A. 85.  2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10:319–32 [Google Scholar]
  87. Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH. 86.  1998. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395:194–98 [Google Scholar]
  88. Niethammer M, Smith DS, Ayala R, Peng J, Ko J. 87.  et al. 2000. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697–711 [Google Scholar]
  89. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J. 88.  et al. 2000. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28:681–96 [Google Scholar]
  90. Fleck MW, Hirotsune S, Gambello MJ, Phillips-Tansey E, Suares G. 89.  et al. 2000. Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J. Neurosci. 20:2439–50 [Google Scholar]
  91. Cahana A, Escamez T, Nowakowski RS, Hayes NL, Giacobini M. 90.  et al. 2001. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization. PNAS 98:6429–34 [Google Scholar]
  92. Strumpf D, Volk T. 91.  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. 143:1259–70 [Google Scholar]
  93. Gregory SL, Brown NH. 92.  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. 143:1271–82 [Google Scholar]
  94. Ori-McKenney KM, Jan LY, Jan YN. 93.  2012. Golgi outposts shape dendrite morphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76:921–30 [Google Scholar]
  95. Yau KW, van Beuningen SF, Cunha-Ferreira I, Cloin BM, van Battum EY. 94.  et al. 2014. Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82:1058–73 [Google Scholar]
  96. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN. 95.  2007. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717–29 [Google Scholar]
  97. Lord C, Ferro-Novick S, Miller EA. 96.  2013. The highly conserved COPII coat complex sorts cargo from the endoplasmic reticulum and targets it to the Golgi. Cold Spring Harb. Perspect. Biol. 5:a013367 [Google Scholar]
  98. Polleux F, Giger RJ, Ginty DD, Kolodkin AL, Ghosh A. 97.  1998. Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282:1904–6 [Google Scholar]
  99. Goodman CS, Kolodkin AL, Luo Y, Püschel AW, Raper JA. 98.  1999. Unified nomenclature for the semaphorins/collapsins. Cell 97:551–52 [Google Scholar]
  100. Raper JA. 99.  2000. Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10:88–94 [Google Scholar]
  101. Brose K, Bland KS, Wang KH, Arnott D, Henzel W. 100.  et al. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795–806 [Google Scholar]
  102. Kidd T, Bland KS, Goodman CS. 101.  1999. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96:785–94 [Google Scholar]
  103. Wang KH, Brose K, Arnott D, Kidd T, Goodman CS. 102.  et al. 1999. Biochemical purification of a mammalian Slit protein as a positive regulator of sensory axon elongation and branching. Cell 96:771–84 [Google Scholar]
  104. Whitford KL, Dijkhuizen P, Polleux F, Ghosh A. 103.  2002. Molecular control of cortical dendrite development. Annu. Rev. Neurosci. 25:127–49 [Google Scholar]
  105. Campbell DS, Stringham SA, Timm A, Xiao T, Law M-Y. 104.  et al. 2007. Slit1a inhibits retinal ganglion cell arborization and synaptogenesis via Robo2-dependent and -independent pathways. Neuron 55:231–45 [Google Scholar]
  106. Chao MV. 105.  2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4:299–309 [Google Scholar]
  107. McAllister AK, Lo DC, Katz LC. 106.  1995. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791–803 [Google Scholar]
  108. Snider W. 107.  1988. Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals. J. Neurosci. 8:2628–34 [Google Scholar]
  109. Causing CG, Gloster A, Aloyz R, Bamji SX, Chang E. 108.  et al. 1997. Synaptic innervation density is regulated by neuron-derived BDNF. Neuron 18:257–67 [Google Scholar]
  110. Dijkhuizen PA, Ghosh A. 109.  2005. BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J. Neurobiol. 62:278–88 [Google Scholar]
  111. Cheung ZH, Chin WH, Chen Y, Ng YP, Ip NY. 110.  2007. Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLOS Biol. 5:e63 [Google Scholar]
  112. Chen Y, Fu W-Y, Ip JPK, Ye T, Fu AKY. 111.  et al. 2012. Ankyrin repeat-rich membrane spanning protein (Kidins220) is required for neurotrophin and ephrin receptor–dependent dendrite development. J. Neurosci. 32:8263–69 [Google Scholar]
  113. Zweifel LS, Kuruvilla R, Ginty DD. 112.  2005. Functions and mechanisms of retrograde neurotrophin signalling. Nat. Rev. Neurosci. 6:615–25 [Google Scholar]
  114. Zhou B, Cai Q, Xie Y, Sheng Z-H. 113.  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 [Google Scholar]
  115. Šestan N, Artavanis-Tsakonas S, Rakic P. 114.  1999. Contact-dependent inhibition of cortical neurite growth mediated by Notch signaling. Science 286:741–46 [Google Scholar]
  116. Redmond L, Oh S-R, Hicks C, Weinmaster G, Ghosh A. 115.  2000. Nuclear Notch1 signaling and the regulation of dendritic development. Nat. Neurosci. 3:30–40 [Google Scholar]
  117. Ables JL, Breunig JJ, Eisch AJ, Rakic P. 116.  2011. Not(ch) just development: Notch signalling in the adult brain. Nat. Rev. Neurosci. 12:269–83 [Google Scholar]
  118. Louvi A, Artavanis-Tsakonas S. 117.  2006. Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7:93–102 [Google Scholar]
  119. Greenwald I. 118.  1998. LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12:1751–62 [Google Scholar]
  120. Artavanis-Tsakonas S, Rand MD, Lake RJ. 119.  1999. Notch signaling: cell fate control and signal integration in development. Science 284:770–76 [Google Scholar]
  121. Furrer M-P, Vasenkova I, Kamiyama D, Rosado Y, Chiba A. 120.  2007. Slit and Robo control the development of dendrites in Drosophila CNS. Development 134:3795–804 [Google Scholar]
  122. Dimitrova S, Reissaus A, Tavosanis G. 121.  2008. Slit and Robo regulate dendrite branching and elongation of space-filling neurons in Drosophila. Dev. Biol. 324:18–30 [Google Scholar]
  123. Tessier-Lavigne M, Goodman CS. 122.  1996. The molecular biology of axon guidance. Science 274:1123–33 [Google Scholar]
  124. Hedgecock EM, Culotti JG, Hall DH. 123.  1990. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61–85 [Google Scholar]
  125. Serafini T, Kennedy TE, Gaiko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. 124.  1994. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409–24 [Google Scholar]
  126. Furrer M-P, Kim S, Wolf B, Chiba A. 125.  2003. Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline. Nat. Neurosci. 6:223–30 [Google Scholar]
  127. Matthews BJ, Grueber WB. 126.  2011. Dscam1-mediated self-avoidance counters netrin-dependent targeting of dendrites in Drosophila. Curr. Biol. 21:1480–87 [Google Scholar]
  128. Teichmann HM, Shen K. 127.  2011. UNC-6 and UNC-40 promote dendritic growth through PAR-4 in Caenorhabditis elegans neurons. Nat. Neurosci. 14:165–72 [Google Scholar]
  129. Yasunaga K-I, Kanamori T, Morikawa R, Suzuki E, Emoto K. 128.  2010. Dendrite reshaping of adult Drosophila sensory neurons requires matrix metalloproteinase–mediated modification of the basement membranes. Dev. Cell 18:621–32 [Google Scholar]
  130. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L. 129.  et al. 2011. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615–27 [Google Scholar]
  131. Yamagata M, Sanes JR. 130.  2012. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J. Neurosci. 32:14402–14 [Google Scholar]
  132. Yamagata M, Sanes JR. 131.  2008. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465–69 [Google Scholar]
  133. Yamagata M, Sanes JR. 132.  2010. Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins. J. Neurosci. 30:3579–88 [Google Scholar]
  134. Matsuoka RL, Chivatakarn O, Badea TC, Samuels IS, Cahill H. 133.  et al. 2011. Class 5 transmembrane semaphorins control selective mammalian retinal lamination and function. Neuron 71:460–73 [Google Scholar]
  135. Matsuoka RL, Nguyen-Ba-Charvet KT, Parray A, Badea TC, Chedotal A, Kolodkin AL. 134.  2011. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 470:259–63 [Google Scholar]
  136. Sun LO, Jiang Z, Rivlin-Etzion M, Hand R, Brady CM. 135.  et al. 2013. On and off retinal circuit assembly by divergent molecular mechanisms. Science 342:6158 [Google Scholar]
  137. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L. 136.  2007. Graded expression of Semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128:399–410 [Google Scholar]
  138. Sweeney LB, Chou Y-H, Wu Z, Joo W, Komiyama T. 137.  et al. 2011. Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting. Neuron 72:734–47 [Google Scholar]
  139. Komiyama T, Luo L. 138.  2006. Development of wiring specificity in the olfactory system. Curr. Opin. Neurobiol. 16:67–73 [Google Scholar]
  140. Hong W, Zhu H, Potter CJ, Barsh G, Kurusu M. 139.  et al. 2009. Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nat. Neurosci. 12:1542–50 [Google Scholar]
  141. Hong W, Mosca TJ, Luo L. 140.  2012. Teneurins instruct synaptic partner matching in an olfactory map. Nature 484:201–7 [Google Scholar]
  142. Kim ME, Shrestha BR, Blazeski R, Mason CA, Grueber WB. 141.  2012. Integrins establish dendrite-substrate relationships that promote dendritic self-avoidance and patterning in Drosophila sensory neurons. Neuron 73:79–91 [Google Scholar]
  143. Han C, Wang D, Soba P, Zhu S, Lin X. 142.  et al. 2012. Integrins regulate repulsion-mediated dendritic patterning of Drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 73:64–78 [Google Scholar]
  144. Bülow HE, Hobert O. 143.  2006. The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22:375–407 [Google Scholar]
  145. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML. 144.  et al. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729–77 [Google Scholar]
  146. Coles CH, Shen Y, Tenney AP, Siebold C, Sutton GC. 145.  et al. 2011. Proteoglycan-specific molecular switch for RPTPσ clustering and neuronal extension. Science 332:484–88 [Google Scholar]
  147. Sagasti A, Guido MR, Raible DW, Schier AF. 146.  2005. Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr. Biol. 15:804–14 [Google Scholar]
  148. Wang F, Wolfson SN, Gharib A, Sagasti A. 147.  2012. LAR receptor tyrosine phosphatases and HSPGs guide peripheral sensory axons to the skin. Curr. Biol. 22:373–82 [Google Scholar]
  149. Hughes ME, Bortnick R, Tsubouchi A, Bäumer P, Kondo M. 148.  et al. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417–27 [Google Scholar]
  150. Soba P, Zhu S, Emoto K, Younger S, Yang S-J. 149.  et al. 2007. Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54:403–16 [Google Scholar]
  151. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J. 150.  et al. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–84 [Google Scholar]
  152. Miura SK, Martins A, Zhang KX, Graveley BR, Zipursky SL. 151.  2013. Probabilistic splicing of Dscam1 establishes identity at the level of single neurons. Cell 155:1166–77 [Google Scholar]
  153. Wojtowicz WM, Flanagan JJ, Millard SS, Zipursky SL, Clemens JC. 152.  2004. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118:619–33 [Google Scholar]
  154. Wojtowicz WM, Wu W, Andre I, Qian B, Baker D, Zipursky SL. 153.  2007. A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130:1134–45 [Google Scholar]
  155. Zipursky SL, Grueber WB. 154.  2013. The molecular basis of self-avoidance. Annu. Rev. Neurosci. 36:547–68 [Google Scholar]
  156. Gibson DA, Tymanskyj S, Yuan RC, Leung HC, Lefebvre JL. 155.  et al. 2014. Dendrite self-avoidance requires cell-autonomous Slit/Robo signaling in cerebellar Purkinje cells. Neuron 81:1040–56 [Google Scholar]
  157. Gao F-B, Kohwi M, Brenman JE, Jan LY, Jan YN. 156.  2000. Control of dendritic field formation in Drosophila: the roles of Flamingo and competition between homologous neurons. Neuron 28:91–101 [Google Scholar]
  158. Grueber WB, Ye B, Moore AW, Jan LY, Jan YN. 157.  2003. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 13:618–26 [Google Scholar]
  159. Sugimura K, Yamamoto M, Niwa R, Satoh D, Goto S. 158.  et al. 2003. Distinct developmental modes and lesion-induced reactions of dendrites of two classes of Drosophila sensory neurons. J. Neurosci. 23:3752–60 [Google Scholar]
  160. Emoto K, He Y, Ye B, Grueber WB, Adler PN. 159.  et al. 2004. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons. Cell 119:245–56 [Google Scholar]
  161. Emoto K, Parrish JZ, Jan LY, Jan Y-N. 160.  2006. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443:210–13 [Google Scholar]
  162. Wu GY, Zou DJ, Rajan I, Cline H. 161.  1999. Dendritic dynamics in vivo change during neuronal maturation. J. Neurosci. 19:4472–83 [Google Scholar]
  163. Dailey ME, Smith SJ. 162.  1996. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16:2983–94 [Google Scholar]
  164. Sin WC, Haas K, Ruthazer ES, Cline HT. 163.  2002. Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475–80 [Google Scholar]
  165. Rajan I, Cline HT. 164.  1998. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J. Neurosci. 18:7836–46 [Google Scholar]
  166. Ewald RC, Van Keuren–Jensen KR, Aizenman CD, Cline HT. 165.  2008. Roles of NR2A and NR2B in the development of dendritic arbor morphology in vivo. J. Neurosci. 28:850–61 [Google Scholar]
  167. Niell CM, Meyer MP, Smith SJ. 166.  2004. In vivo imaging of synapse formation on a growing dendritic arbor. Nat. Neurosci. 7:254–60 [Google Scholar]
  168. Aizawa H, Hu S-C, Bobb K, Balakrishnan K, Ince G. 167.  et al. 2004. Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science 303:197–202 [Google Scholar]
  169. Shieh PB, Hu S-C, Bobb K, Timmusk T, Ghosh A. 168.  1998. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20:727–40 [Google Scholar]
  170. Wu G-Y, Cline HT. 169.  1998. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–26 [Google Scholar]
  171. Cline H, Haas K. 170.  2008. The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J. Physiol. 586:1509–17 [Google Scholar]
  172. Haas K, Li J, Cline HT. 171.  2006. AMPA receptors regulate experience-dependent dendritic arbor growth in vivo. Proc. Natl. Acad. Sci. 103:12127–31 [Google Scholar]
  173. Shen W, Da Silva JS, He H, Cline HT. 172.  2009. Type A GABA-receptor–dependent synaptic transmission sculpts dendritic arbor structure in Xenopus tadpoles in vivo. J. Neurosci. 29:5032–43 [Google Scholar]
  174. Greenough WT, Chang F-LF. 173.  1988. Dendritic pattern formation involves both oriented regression and oriented growth in the barrels of mouse somatosensory cortex. Dev. Brain Res. 43:148–52 [Google Scholar]
  175. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y. 174.  et al. 2000. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406:726–31 [Google Scholar]
  176. Espinosa JS, Wheeler DG, Tsien RW, Luo L. 175.  2009. Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B. Neuron 62:205–17 [Google Scholar]
  177. Katz L, Gilbert C, Wiesel T. 176.  1989. Local circuits and ocular dominance columns in monkey striate cortex. J. Neurosci. 9:1389–99 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error