1932

Abstract

How the nervous system is wired has been a central question of neuroscience since the inception of the field, and many of the foundational discoveries and conceptual advances have been made through the study of invertebrate experimental organisms, including and . Although many guidance molecules and receptors have been identified, recent experiments have shed light on the many modes of action for these pathways. Here, we summarize the recent progress in determining how the physical and temporal constraints of the surrounding environment provide instructive regulations in nervous system wiring. We use Netrin and its receptors as an example to analyze the complexity of how they guide neurite outgrowth. In neurite repair, conserved injury detection and response-signaling pathways regulate gene expression and cytoskeletal dynamics. We also describe recent developments in the research on molecular mechanisms of neurite regeneration in worms and flies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-070918-050208
2019-07-08
2024-06-12
Loading full text...

Full text loading...

/deliver/fulltext/neuro/42/1/annurev-neuro-070918-050208.html?itemId=/content/journals/10.1146/annurev-neuro-070918-050208&mimeType=html&fmt=ahah

Literature Cited

  1. Adib EA, Smithson LJ, Collins CA 2018. An axonal stress response pathway: degenerative and regenerative signaling by DLK. Curr. Opin. Neurobiol. 53:110–19
    [Google Scholar]
  2. Adler CE, Fetter RD, Bargmann CI 2006. UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat. Neurosci. 9:511–18
    [Google Scholar]
  3. Akin O, Zipursky SL. 2016. Frazzled promotes growth cone attachment at the source of a Netrin gradient in the Drosophila visual system. eLife 5:e20762
    [Google Scholar]
  4. Alam T, Maruyama H, Li C, Pastuhov SI, Nix P et al. 2016. Axotomy-induced HIF-serotonin signalling axis promotes axon regeneration in C. elegans. Nat. . Commun 7:10388
    [Google Scholar]
  5. Avery MA, Rooney TM, Pandya JD, Wishart TM, Gillingwater TH et al. 2012. WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial Ca2+ buffering. Curr. Biol. 22:596–600
    [Google Scholar]
  6. Basu A, Dey S, Puri D, Saha ND, Sabharwal V et al. 2017. let-7 miRNA controls CED-7 homotypic adhesion and EFF-1-mediated axonal self-fusion to restore touch sensation following injury. PNAS 114:E10206–15
    [Google Scholar]
  7. Bounoutas A, Kratz J, Emtage L, Ma C, Nguyen KC, Chalfie M 2011. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. PNAS 108:3982–87
    [Google Scholar]
  8. Brankatschk M, Dickson BJ. 2006. Netrins guide Drosophila commissural axons at short range. Nat. Neurosci. 9:188–194
    [Google Scholar]
  9. Byrne AB, McWhirter RD, Sekine Y, Strittmatter SM, Miller DM, Hammarlund M 2016. Inhibiting poly(ADP-ribosylation) improves axon regeneration. eLife 5:e12734
    [Google Scholar]
  10. Byrne AB, Walradt T, Gardner KE, Hubbert A, Reinke V, Hammarlund M 2014. Insulin/IGF1 signaling inhibits age-dependent axon regeneration. Neuron 81:561–73
    [Google Scholar]
  11. Carrillo RA, Özkan E, Menon KP, Nagarkar-Jaiswal S, Lee P-T et al. 2015. Control of synaptic connectivity by a network of Drosophila IgSF cell surface proteins. Cell 163:1770–82
    [Google Scholar]
  12. Cartoni R, Norsworthy MW, Bei F, Wang C, Li S et al. 2016. The mammalian-specific protein Armcx1 regulates mitochondrial transport during axon regeneration. Neuron 92:1294–307
    [Google Scholar]
  13. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT et al. 1996. UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87:187–95
    [Google Scholar]
  14. Chédotal A, Richards LJ. 2010. Wiring the brain: the biology of neuronal guidance. Cold Spring Harb. Perspect. Biol. 2:a001917
    [Google Scholar]
  15. Chen C-H, Lee A, Liao C-P, Liu Y-W, Pan C-L 2014. RHGF-1/PDZ-RhoGEF and retrograde DLK-1 signaling drive neuronal remodeling on microtubule disassembly. PNAS 111:16568–73
    [Google Scholar]
  16. Chen L, Chuang M, Koorman T, Boxem M, Jin Y, Chisholm AD 2015. Axon injury triggers EFA-6 mediated destabilization of axonal microtubules via TACC and doublecortin like kinase. eLife 4:e08695
    [Google Scholar]
  17. Chen L, Nye DM, Stone MC, Weiner AT, Gheres KW et al. 2016. Mitochondria and caspases tune Nmnat-mediated stabilization to promote axon regeneration. PLOS Genet 12:e1006503
    [Google Scholar]
  18. Chen L, Stone MC, Tao J, Rolls MM 2012. Axon injury and stress trigger a microtubule-based neuroprotective pathway. PNAS 109:11842–47
    [Google Scholar]
  19. Chen L, Wang Z, Ghosh-Roy A, Hubert T, Yan D et al. 2011. Axon regeneration pathways identified by systematic genetic screening in C. elegans. . Neuron 71:1043–57
    [Google Scholar]
  20. Chisholm AD, Hutter H, Jin Y, Wadsworth WG 2016. The genetics of axon guidance and axon regeneration in Caenorhabditis elegans. . Genetics 204:849–82
    [Google Scholar]
  21. Collins CA, Wairkar YP, Johnson SL, DiAntonio A 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51:57–69
    [Google Scholar]
  22. DeVault L, Li T, Izabel S, Thompson-Peer KL, Jan LY, Jan YN 2018. Dendrite regeneration of adult Drosophila sensory neurons diminishes with aging and is inhibited by epidermal-derived matrix metalloproteinase 2. Genes Dev 32:402–14
    [Google Scholar]
  23. Dominici C, Moreno-Bravo JA, Puiggros SR, Rappeneau Q, Rama N et al. 2017. Floor-plate-derived netrin-1 is dispensable for commissural axon guidance. Nature 545:350–54
    [Google Scholar]
  24. Dong X, Liu OW, Howell AS, Shen K 2013. An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 155:296–307
    [Google Scholar]
  25. Dong X, Shen K, Bülow HE 2015. Intrinsic and extrinsic mechanisms of dendritic morphogenesis. Annu. Rev. Physiol. 77:271–300
    [Google Scholar]
  26. Edwards TJ, Hammarlund M. 2014. Syndecan promotes axon regeneration by stabilizing growth cone migration. Cell Rep 8:272–83
    [Google Scholar]
  27. Emoto K, He Y, Ye B, Grueber WB, Adler PN 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]
  28. Emoto K, Parrish JZ, Jan LY, Jan Y-N 2006. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443:210–13
    [Google Scholar]
  29. Gabel CV, Antoine F, Chuang C-F, Samuel ADT, Chang C 2008. Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. . Development 135:1129–36
    [Google Scholar]
  30. Geoffroy CG, Meves JM, Zheng B 2017. The age factor in axonal repair after spinal cord injury: a focus on neuron-intrinsic mechanisms. Neurosci. Lett. 652:41–49
    [Google Scholar]
  31. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD 2012. Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev. Cell 23:716–28
    [Google Scholar]
  32. Ghosh-Roy A, Wu Z, Goncharov A, Jin Y, Chisholm AD 2010. Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J. Neurosci. 30:3175–83
    [Google Scholar]
  33. Gotenstein JR, Swale RE, Fukuda T, Wu Z, Giurumescu CA et al. 2010. The C. elegans peroxidasin PXN-2 is essential for embryonic morphogenesis and inhibits adult axon regeneration. Development 137:3603–13
    [Google Scholar]
  34. Hagedorn EJ, Ziel JW, Morrissey MA, Linden LM, Wang Z et al. 2013. The netrin receptor DCC focuses invadopodia-driven basement membrane transmigration in vivo. J. Cell Biol. 201:903–13
    [Google Scholar]
  35. Hammarlund M, Jorgensen EM, Bastiani MJ 2007. Axons break in animals lacking β-spectrin. J. Cell Biol. 176:269–75
    [Google Scholar]
  36. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M 2009. Axon regeneration requires a conserved MAP kinase pathway. Science 323:802–6
    [Google Scholar]
  37. Han C, Wang D, Soba P, Zhu S, Lin X 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]
  38. Han SM, Baig HS, Hammarlund M 2016. Mitochondria localize to injured axons to support regeneration. Neuron 92:1308–23
    [Google Scholar]
  39. He H, Kise Y, Izadifar A, Urwyler O, Ayaz D et al. 2014. Cell-intrinsic requirement of Dscam1 isoform diversity for axon collateral formation. Science 344:1182–86
    [Google Scholar]
  40. Hedgecock EM, Culotti JG, Hall DH 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]
  41. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ et al. 2011. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331:928–31
    [Google Scholar]
  42. Hisamoto N, Nagamori Y, Shimizu T, Pastuhov SI, Matsumoto K 2016. The C. elegans discoidin domain receptor DDR-2 modulates the met-like RTK-JNK signaling pathway in axon regeneration. PLOS Genet 12:e1006475
    [Google Scholar]
  43. Hisamoto N, Tsuge A, Pastuhov SI, Shimizu T, Hanafusa H, Matsumoto K 2018. Phosphatidylserine exposure mediated by ABC transporter activates the integrin signaling pathway promoting axon regeneration. Nat. Commun. 9:3099
    [Google Scholar]
  44. Hobert O. 2016. Terminal selectors of neuronal identity. Curr. Top. Dev. Biol. 116:455–75
    [Google Scholar]
  45. Holland SM, Collura KM, Ketschek A, Noma K, Ferguson TA et al. 2016. Palmitoylation controls DLK localization, interactions and activity to ensure effective axonal injury signaling. PNAS 113:763–86
    [Google Scholar]
  46. Howard LJ, Brown HE, Wadsworth BC, Evans TA 2019. Midline axon guidance in the Drosophila embryonic central nervous system. Semin. Cell Dev. Biol. 85:13–25
    [Google Scholar]
  47. Hubert T, Wu Z, Chisholm AD, Jin Y 2014. S6 kinase inhibits intrinsic axon regeneration capacity via AMP kinase in Caenorhabditis elegans. J. . Neurosci 34:758–63
    [Google Scholar]
  48. Inberg S, Meledin A, Kravtsov V, Iosilevskii Y, Oren-Suissa M, Podbilewicz B 2019. Lessons from worm dendritic patterning. Annu. Rev. Neurosci. 42: 365–83
    [Google Scholar]
  49. Ishii N, Wadsworth WG, Stern BD, Culotti JG, Hedgecock EM 1992. UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. . Neuron 9:873–81
    [Google Scholar]
  50. Jiang N, Soba P, Parker E, Kim CC, Parrish JZ 2014. The microRNA bantam regulates a developmental transition in epithelial cells that restricts sensory dendrite growth. Development 141:2657–68
    [Google Scholar]
  51. Kaletsky R, Lakhina V, Arey R, Williams A, Landis J et al. 2016. The C. elegans adult neuronal IIS/FOXO transcriptome reveals adult phenotype regulators. Nature 529:92–96
    [Google Scholar]
  52. Kennedy TE, Serafini T, de la Torre JR, Tessier-Lavigne M 1994. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78:425–35
    [Google Scholar]
  53. Kennedy TE, Wang H, Marshall W, Tessier-Lavigne M 2006. Axon guidance by diffusible chemoattractants: a gradient of netrin protein in the developing spinal cord. J. Neurosci. 26:8866–74
    [Google Scholar]
  54. Kim I-J, Zhang Y, Meister M, Sanes JR 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]
  55. Kim ME, Shrestha BR, Blazeski R, Mason CA, Grueber WB 2012. Integrins establish dendrite-substrate relationships that promote dendritic self-avoidance and patterning in Drosophila sensory neurons. Neuron 73:79–91
    [Google Scholar]
  56. Koch M, Nicolas M, Zschaetzsch M, de Geest N, Claeys A et al. 2017. A Fat-Facets-Dscam1-JNK pathway enhances axonal growth in development and after injury. Front. Cell. Neurosci. 11:416
    [Google Scholar]
  57. Koike-Kumagai M, Yasunaga K, Morikawa R, Kanamori T, Emoto K 2009. The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway. EMBO J 28:3879–92
    [Google Scholar]
  58. Kulkarni G, Xu Z, Mohamed AM, Li H, Tang X et al. 2013. Experimental evidence for UNC-6 (netrin) axon guidance by stochastic fluctuations of intracellular UNC-40 (DCC) outgrowth activity. Biol. Open 2:1300–12
    [Google Scholar]
  59. Lah GJ, Li JSS, Millard SS 2014. Cell-specific alternative splicing of Drosophila Dscam2 is crucial for proper neuronal wiring. Neuron 83:1376–88
    [Google Scholar]
  60. Langen M, Agi E, Altschuler DJ, Wu LF, Altschuler SJ, Hiesinger PR 2015. The developmental rules of neural superposition in Drosophila. . Cell 162:120–33
    [Google Scholar]
  61. Lee JK, Geoffroy CG, Chan AF, Tolentino KE, Crawford MJ et al. 2010. Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 66:663–70
    [Google Scholar]
  62. Lee RC, Clandinin TR, Lee C-H, Chen P-L, Meinertzhagen IA, Zipursky SL 2003. The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat. Neurosci. 6:557–63
    [Google Scholar]
  63. Leung-Hagesteijn C, Spence AM, Stern BD, Zhou Y, Su MW et al. 1992. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. . Cell 71:289–99
    [Google Scholar]
  64. Li C, Hisamoto N, Nix P, Kanao S, Mizuno T et al. 2012. The growth factor SVH-1 regulates axon regeneration in C. elegans via the JNK MAPK cascade. Nat. Neurosci. 15:551–57
    [Google Scholar]
  65. Lilja J, Ivaska J. 2018. Integrin activity in neuronal connectivity. J. Cell Sci. 131:jcs212803
    [Google Scholar]
  66. Liu K, Lu Y, Lee JK, Samara R, Willenberg R et al. 2010. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 13:1075–81
    [Google Scholar]
  67. Liu OW, Shen K. 2012. The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat. Neurosci. 15:57–63
    [Google Scholar]
  68. Lu W, Fox P, Lakonishok M, Davidson MW, Gelfand VI 2013. Initial neurite outgrowth in Drosophila neurons is driven by kinesin-powered microtubule sliding. Curr. Biol. 23:1018–23
    [Google Scholar]
  69. Lu W, Lakonishok M, Gelfand VI 2015. Kinesin-1-powered microtubule sliding initiates axonal regeneration in Drosophila cultured neurons. Mol. Biol. Cell 26:1296–307
    [Google Scholar]
  70. Meinertzhagen IA. 1993. Sleeping neuroblasts. Curr. Biol. 3:904–6
    [Google Scholar]
  71. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305:232–63
    [Google Scholar]
  72. Meltzer S, Yadav S, Lee J, Soba P, Younger SH et al. 2016. Epidermis-derived semaphorin promotes dendrite self-avoidance by regulating dendrite-substrate adhesion in Drosophila sensory neurons. Neuron 89:741–55
    [Google Scholar]
  73. Neumann B, Coakley S, Giordano-Santini R, Linton C, Lee ES et al. 2015. EFF-1-mediated regenerative axonal fusion requires components of the apoptotic pathway. Nature 517:219–22
    [Google Scholar]
  74. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI 2002. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885–93
    [Google Scholar]
  75. Nix P, Hammarlund M, Hauth L, Lachnit M, Jorgensen EM, Bastiani M 2014. Axon regeneration genes identified by RNAi screening in C. elegans. J. Neurosci. 34:629–45
    [Google Scholar]
  76. Nix P, Hisamoto N, Matsumoto K, Bastiani M 2011. Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. PNAS 108:10738–43
    [Google Scholar]
  77. Omotade OF, Pollitt SL, Zheng JQ 2017. Actin-based growth cone motility and guidance. Mol. Cell. Neurosci. 84:4–10
    [Google Scholar]
  78. Oren-Suissa M, Gattegno T, Kravtsov V, Podbilewicz B 2017. Extrinsic repair of injured dendrites as a paradigm for regeneration by fusion in Caenorhabditis elegans. . Genetics 206:215–30
    [Google Scholar]
  79. Özel MN, Langen M, Hassan BA, Hiesinger PR 2015. Filopodial dynamics and growth cone stabilization in Drosophila visual circuit development. eLife 4:e10721
    [Google Scholar]
  80. Özkan E, Carrillo RA, Eastman CL, Weiszmann R, Waghray D et al. 2013. An extracellular interactome of immunoglobulin and LRR proteins reveals receptor-ligand networks. Cell 154:228–39
    [Google Scholar]
  81. Park KK, Liu K, Hu Y, Smith PD, Wang C et al. 2008. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322:963–66
    [Google Scholar]
  82. Pastuhov SI, Fujiki K, Nix P, Kanao S, Bastiani M et al. 2012. Endocannabinoid-Goα signalling inhibits axon regeneration in Caenorhabditis elegans by antagonizing Gqα-PKC-JNK signalling. Nat. Commun. 3:1136
    [Google Scholar]
  83. Pastuhov SI, Fujiki K, Tsuge A, Asai K, Ishikawa S et al. 2016. The core molecular machinery used for engulfment of apoptotic cells regulates the JNK pathway mediating axon regeneration in Caenorhabditis elegans. J. Neurosci. 36:9710–21
    [Google Scholar]
  84. Pichichero M, Beer B, Clody DE 1973. Effects of dibutyryl cyclic AMP on restoration of function of damaged sciatic nerve in rats. Science 182:724–25
    [Google Scholar]
  85. Pinan-Lucarre B, Gabel CV, Reina CP, Hulme SE, Shevkoplyas SS et al. 2012. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. . PLOS Biol 10:e1001331
    [Google Scholar]
  86. Prakash S, Caldwell JC, Eberl DF, Clandinin TR 2005. Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets. Nat. Neurosci. 8:443–50
    [Google Scholar]
  87. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN et al. 2002. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895–903
    [Google Scholar]
  88. Ramón y Cajal S. 1928. Degeneration and Regeneration of the Nervous System Oxford, UK: Clarendon
    [Google Scholar]
  89. Rapti G, Li C, Shan A, Lu Y, Shaham S 2017. Glia initiate brain assembly through noncanonical Chimaerin-Furin axon guidance in C. elegans. Nat. Neurosci. 20:1350–60
    [Google Scholar]
  90. Rooney TM, Freeman MR. 2014. Drosophila models of neuronal injury. ILAR J 54:291–95
    [Google Scholar]
  91. Salzberg Y, Díaz-Balzac CA, Ramirez-Suarez NJ, Attreed M, Tecle E et al. 2013. Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. . Cell 155:308–20
    [Google Scholar]
  92. Schwabe T, Borycz JA, Meinertzhagen IA, Clandinin TR 2014. Differential adhesion determines the organization of synaptic fascicles in the Drosophila visual system. Curr. Biol. 24:1304–13
    [Google Scholar]
  93. Schwabe T, Neuert H, Clandinin TR 2013. A network of cadherin-mediated interactions polarizes growth cones to determine targeting specificity. Cell 154:351–64
    [Google Scholar]
  94. Segawa K, Nagata S. 2015. An apoptotic ‘eat me’ signal: phosphatidylserine exposure. Trends Cell Biol 25:639–50
    [Google Scholar]
  95. Sengottuvel V, Leibinger M, Pfreimer M, Andreadaki A, Fischer D 2011. Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 31:2688–99
    [Google Scholar]
  96. Serafini T, Kennedy TE, Gaiko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M 1994. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409–24
    [Google Scholar]
  97. Shimizu T, Pastuhov SI, Hanafusa H, Matsumoto K, Hisamoto N 2018. The C. elegans BRCA2-ALP/Enigma complex regulates axon regeneration via a Rho GTPase-ROCK-MLC phosphorylation pathway. Cell Rep 24:1880–89
    [Google Scholar]
  98. Shin JE, Cho Y, Beirowski B, Milbrandt J, Cavalli V, DiAntonio A 2012. Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74:1015–22
    [Google Scholar]
  99. Singhal A, Shaham S. 2017. Infrared laser-induced gene expression for tracking development and function of single C. elegans embryonic neurons. Nat. Commun. 8:14100
    [Google Scholar]
  100. Soares L, Parisi M, Bonini NM 2015. Axon injury and regeneration in the adult Drosophila. Sci. Rep. 4:6199
    [Google Scholar]
  101. Song Y, Ori-McKenney KM, Zheng Y, Han C, Jan LY, Jan YN 2012. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. . Genes Dev 26:1612–25
    [Google Scholar]
  102. Song Y, Sretavan D, Salegio EA, Berg J, Huang X et al. 2015. Regulation of axon regeneration by the RNA repair and splicing pathway. Nat. Neurosci. 18:817–25
    [Google Scholar]
  103. Spencer T, Filbin MT. 2004. A role for cAMP in regeneration of the adult mammalian CNS. J. Anat. 204:49–55
    [Google Scholar]
  104. Stoeckli ET. 2018. Understanding axon guidance: Are we nearly there yet?. Development 145:dev151415
    [Google Scholar]
  105. Stone MC, Albertson RM, Chen L, Rolls MM 2014. Dendrite injury triggers DLK-independent regeneration. Cell Rep 6:247–53
    [Google Scholar]
  106. Stone MC, Nguyen MM, Tao J, Allender DL, Rolls MM 2010. Global up-regulation of microtubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol. Biol. Cell 21:767–77
    [Google Scholar]
  107. Sugimura K, Yamamoto M, Niwa R, Satoh D, Goto S 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]
  108. Sun F, Park KK, Belin S, Wang D, Lu T et al. 2011. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 480:372–75
    [Google Scholar]
  109. Sun KLW, Correia JP, Kennedy TE 2011. Netrins: versatile extracellular cues with diverse functions. Development 138:2153–69
    [Google Scholar]
  110. Tadros W, Xu S, Akin O, Yi CH, Shin GJ et al. 2016. Dscam proteins direct dendritic targeting through adhesion. Neuron 89:480–93
    [Google Scholar]
  111. Tan L, Zhang KX, Pecot MY, Nagarkar-Jaiswal S, Lee P-T et al. 2015. Ig superfamily ligand and receptor pairs expressed in synaptic partners in Drosophila. . Cell 163:1756–69
    [Google Scholar]
  112. Tedeschi A, Bradke F. 2013. The DLK signaling pathway—a double-edged sword in neural development and regeneration. EMBO Rep 14:605–14
    [Google Scholar]
  113. Teichmann HM, Shen K. 2011. UNC-6 and UNC-40 promote dendritic growth through PAR-4 in Caenorhabditis elegans neurons. Nat. Neurosci. 14:165–72
    [Google Scholar]
  114. Thompson-Peer KL, DeVault L, Li T, Jan LY, Jan YN 2016. In vivo dendrite regeneration after injury is different from dendrite development. Genes Dev 30:1776–89
    [Google Scholar]
  115. Timofeev K, Joly W, Hadjieconomou D, Salecker I 2012. Localized netrins act as positional cues to control layer-specific targeting of photoreceptor axons in Drosophila. . Neuron 75:80–93
    [Google Scholar]
  116. Valakh V, Frey E, Babetto E, Walker LJ, DiAntonio A 2015. Cytoskeletal disruption activates the DLK/JNK pathway, which promotes axonal regeneration and mimics a preconditioning injury. Neurobiol. Dis. 77:13–25
    [Google Scholar]
  117. Valakh V, Walker LJ, Skeath JB, DiAntonio A 2013. Loss of the spectraplakin short stop activates the DLK injury response pathway in Drosophila. J. Neurosci. 33:17863–73
    [Google Scholar]
  118. Varadarajan SG, Kong JH, Phan KD, Kao T-J, Panaitof SC et al. 2017. Netrin1 produced by neural progenitors, not floor plate cells, is required for axon guidance in the spinal cord. Neuron 94:790–99.e3
    [Google Scholar]
  119. Wang Z, Linden LM, Naegeli KM, Ziel JW, Chi Q et al. 2014. UNC-6 (netrin) stabilizes oscillatory clustering of the UNC-40 (DCC) receptor to orient polarity. J. Cell Biol. 206:619–33
    [Google Scholar]
  120. White JG, Southgate E, Thomson JN, Brenner S 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314:1–340
    [Google Scholar]
  121. Wu Z, Ghosh-Roy A, Yanik MF, Zhang JZ, Jin Y, Chisholm AD 2007. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. PNAS 104:15132–37
    [Google Scholar]
  122. Xiong X, Wang X, Ewanek R, Bhat P, Diantonio A, Collins CA 2010. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 191:211–23
    [Google Scholar]
  123. Xu Z, Li H, Wadsworth WG 2009. The roles of multiple UNC-40 (DCC) receptor-mediated signals in determining neuronal asymmetry induced by the UNC-6 (Netrin) ligand. Genetics 183:941–49
    [Google Scholar]
  124. Yan D, Jin Y. 2012. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76:534–48
    [Google Scholar]
  125. Yan D, Wu Z, Chisholm AD, Jin Y 2009. The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005–18
    [Google Scholar]
  126. Yanik MF, Cinar H, Cinar HN, Chisholm AD, Jin Y, Ben-Yakar A 2004. Functional regeneration after laser axotomy. Nature 432:822
    [Google Scholar]
  127. Yaniv SP, Schuldiner O. 2016. A fly's view of neuronal remodeling. Wiley Interdiscip. Rev. Dev. Biol. 5:618–35
    [Google Scholar]
  128. Yoshimura S, Murray JI, Lu Y, Waterston RH, Shaham S 2008. mls-2 and vab-3 control glia development, hlh-17/Olig expression and glia-dependent neurite extension in C. elegans. Development 135:2263–75
    [Google Scholar]
  129. Zhou B, Yu P, Lin M-Y, Sun T, Chen Y, Sheng Z-H 2016. Facilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits. J. Cell Biol. 214:103–19
    [Google Scholar]
  130. Zipursky LS, Grueber WB. 2013. The molecular basis of self-avoidance. Annu. Rev. Neurosci. 36:547–68
    [Google Scholar]
  131. Zou W, Dong X, Broederdorf TR, Shen A, Kramer DA et al. 2018. A dendritic guidance receptor complex brings together distinct actin regulators to drive efficient F-actin assembly and branching. Dev. Cell 45:362–75.e3
    [Google Scholar]
  132. Zou W, Shen A, Dong X, Tugizova M, Xiang YK, Shen K 2016. A multi-protein receptor-ligand complex underlies combinatorial dendrite guidance choices in C. elegans. . Elife 5:e18345
    [Google Scholar]
  133. Zou Y, Chiu H, Zinovyeva A, Ambros V, Chuang C-F, Chang C 2013. Developmental decline in neuronal regeneration by the progressive change of two intrinsic timers. Science 340:372–76
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-070918-050208
Loading
/content/journals/10.1146/annurev-neuro-070918-050208
Loading

Data & Media loading...

Supplementary Data

  • 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