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Abstract

The structural and functional properties of neurons have intrigued scientists since the pioneering work of Santiago Ramón y Cajal. Since then, emerging cutting-edge technologies, including light and electron microscopy, electrophysiology, biochemistry, optogenetics, and molecular biology, have dramatically increased our understanding of dendritic properties. This advancement was also facilitated by the establishment of different animal model organisms, from flies to mammals. Here we describe the emerging model system of a polymodal neuron named PVD, whose dendritic tree follows a stereotypical structure characterized by repeating candelabra-like structural units. In the past decade, progress has been made in understanding PVD's functions, morphogenesis, regeneration, and aging, yet many questions still remain.

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2019-07-08
2024-06-23
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Literature Cited

  1. Aguirre-Chen C, Bülow HE, Kaprielian Z 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]
  2. Albeg A, Smith CJ, Chatzigeorgiou M, Feitelson DG, Hall DH et al. 2011. C. elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell Neurosci. 46:308–17
    [Google Scholar]
  3. Arikkath J. 2012. Molecular mechanisms of dendrite morphogenesis. Front. Cell Neurosci. 6:61
    [Google Scholar]
  4. Bacon JP, Murphey RK. 1984. Receptive fields of cricket giant interneurones are related to their dendritic structure. J. Physiol. 352:601–23
    [Google Scholar]
  5. Bano D, Agostini M, Melino G, Nicotera P 2011. Ageing, neuronal connectivity and brain disorders: an unsolved ripple effect. Mol. Neurobiol. 43:124–30
    [Google Scholar]
  6. Bianco A, Dienstbier M, Salter HK, Gatto G, Bullock SL 2010. Bicaudal-D regulates fragile X mental retardation protein levels, motility, and function during neuronal morphogenesis. Curr. Biol. 20:1487–92
    [Google Scholar]
  7. Bullock SL, Ish-Horowicz D. 2001. Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature 414:611–16
    [Google Scholar]
  8. Bullock SL, Nicol A, Gross SP, Zicha D 2006. Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr. Biol. 16:1447–52
    [Google Scholar]
  9. Cameron S, Rao Y. 2010. Molecular mechanisms of tiling and self-avoidance in neural development. Mol. Brain 3:28
    [Google Scholar]
  10. 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]
  11. Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer WC et al. 2010. Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 13:861–68 Covers the thermosensory and mechanosensory modalities of the PVD, the role of TRP channels, and DEG/ENaCs.
    [Google Scholar]
  12. Chen B, Chou HT, Brautigam CA, Xing W, Yang S et al. 2017. Rac1 GTPase activates the WAVE regulatory complex through two distinct binding sites. eLife 6:e29795
    [Google Scholar]
  13. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z et al. 2010. Structure and control of the actin regulatory WAVE complex. Nature 468:533–38
    [Google Scholar]
  14. Cohen E, Chatzigeorgiou M, Husson SJ, Steuer-Costa W, Gottschalk A et al. 2014. Caenorhabditis elegans nicotinic acetylcholine receptors are required for nociception. Mol. Cell Neurosci. 59:85–96
    [Google Scholar]
  15. Corty MM, Matthews BJ, Grueber WB 2009. Molecules and mechanisms of dendrite development in Drosophila. . Development 136:1049–61
    [Google Scholar]
  16. Desai A, Mitchison TJ. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83–117
    [Google Scholar]
  17. Diaz-Balzac CA, Rahman M, Lazaro-Pena MI, Martin Hernandez LA, Salzberg Y et al. 2016. Muscle- and skin-derived cues jointly orchestrate patterning of somatosensory dendrites. Curr. Biol. 26:2397
    [Google Scholar]
  18. 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]
  19. Dong X, Shen K, Bulow HE 2015. Intrinsic and extrinsic mechanisms of dendritic morphogenesis. Annu. Rev. Physiol. 77:271–300
    [Google Scholar]
  20. E L, Zhou T, Koh S, Chuang M, Sharma R et al. 2018. An antimicrobial peptide and its neuronal receptor regulate dendrite degeneration in aging and infection. Neuron 97:125–38.e5
    [Google Scholar]
  21. Ebara S, Kumamoto K, Matsuura T, Mazurkiewicz JE, Rice FL 2002. Similarities and differences in the innervation of mystacial vibrissal follicle-sinus complexes in the rat and cat: a confocal microscopic study. J. Comp. Neurol. 449:103–19
    [Google Scholar]
  22. Emmons SW. 2014. The development of sexual dimorphism: studies of the Caenorhabditis elegans male. Wiley Interdiscip. Rev. Dev. Biol. 3:239–62
    [Google Scholar]
  23. Emmons SW. 2018. Neural circuits of sexual behavior in Caenorhabditis elegans. Annu. Rev. . Neurosci 41:349–69
    [Google Scholar]
  24. Fernandez-Gonzalez A, La Spada AR, Treadaway J, Higdon JC, Harris BS et al. 2002. Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene. Nna1. Science 295:1904–6
    [Google Scholar]
  25. Fiala JC, Spacek J, Harris KM 2002. Dendritic spine pathology: cause or consequence of neurological disorders. ? Brain Res. Rev. 39:29–54
    [Google Scholar]
  26. Ghose P, Rashid A, Insley P, Trivedi M, Shah P et al. 2018. EFF-1 fusogen promotes phagosome sealing during cell process clearance in Caenorhabditis elegans. Nat. Cell Biol 20:393–99
    [Google Scholar]
  27. Ghosh-Roy A, Chisholm AD. 2010. Caenorhabditis elegans: a new model organism for studies of axon regeneration. Dev. Dyn. 239:1460–64
    [Google Scholar]
  28. 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]
  29. Giordano-Santini R, Linton C, Hilliard MA 2016. Cell-cell fusion in the nervous system: alternative mechanisms of development, injury, and repair. Semin. Cell Dev. Biol. 60:146–54
    [Google Scholar]
  30. Goto J, Mikawa Y, Koganezawa M, Ito H, Yamamoto D 2011. Sexually dimorphic shaping of interneuron dendrites involves the hunchback transcription factor. J. Neurosci. 31:5454–59
    [Google Scholar]
  31. Grueber WB, Sagasti A. 2010. Self-avoidance and tiling: mechanisms of dendrite and axon spacing. Cold Spring Harb. Perspect. Biol. 2:a001750
    [Google Scholar]
  32. Hafidi A, Sanes DH, Hillman DE 1995. Regeneration of the auditory midbrain intercommissural projection in organotypic culture. J. Neurosci. 15:1298–307
    [Google Scholar]
  33. Halevi S, McKay J, Palfreyman M, Yassin L, Eshel M et al. 2002. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J 21:1012–20
    [Google Scholar]
  34. Hall DH, Treinin M. 2011. How does morphology relate to function in sensory arbors. ? Trends Neurosci 34:443–51
    [Google Scholar]
  35. Hart MP, Hobert O. 2018. Neurexin controls plasticity of a mature, sexually dimorphic neuron. Nature 553:165–70 Discusses the DVB neuron as an example of morphological sexual dimorphism, which is also activity dependent.
    [Google Scholar]
  36. Hattori D, Millard SS, Wojtowicz WM, Zipursky SL 2008. Dscam-mediated cell recognition regulates neural circuit formation. Annu. Rev. Cell Dev. Biol. 24:597–620
    [Google Scholar]
  37. Hausser M, Mel B. 2003. Dendrites: bug or feature?. Curr. Opin. Neurobiol. 13:372–83
    [Google Scholar]
  38. Hilliard MA. 2009. Axonal degeneration and regeneration: a mechanistic tug-of-war. J. Neurochem. 108:23–32
    [Google Scholar]
  39. Hughes ME, Bortnick R, Tsubouchi A, Baumer P, Kondo M et al. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417–27
    [Google Scholar]
  40. Husson SJ, Costa WS, Wabnig S, Stirman JN, Watson JD et al. 2012. Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr. Biol. 22:743–52 RNAi screen of genes influencing PVD-mediated behavior, employing optogenetic specific activation of the PVD.
    [Google Scholar]
  41. Inberg S, Podbilewicz B. 2018. Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins. bioRxiv 436758. https://doi.org/10.1101/436758
    [Crossref]
  42. Jaarsma D, van den Berg R, Wulf PS, van Erp S, Keijzer N et al. 2014. A role for Bicaudal-D2 in radial cerebellar granule cell migration. Nat. Commun. 5:3411
    [Google Scholar]
  43. Jan YN, Jan LY. 2010. Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11:316–28
    [Google Scholar]
  44. Kenyon C. 2010. The genetics of ageing. Nature 464:504–12
    [Google Scholar]
  45. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R 1993. A C. elegans mutant that lives twice as long as wild type. Nature 366:461–64
    [Google Scholar]
  46. Kim MD, Jan LY, Jan YN 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]
  47. Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H et al. 2007. Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat. Neurosci. 10:568–77
    [Google Scholar]
  48. Kolb B, Whishaw IQ. 1998. Brain plasticity and behavior. Annu. Rev. Psychol. 49:43–64
    [Google Scholar]
  49. Kravtsov V. 2015. Branching and aging of mechanosensory neurons in C. elegans. MSc Thesis, Technion-Isr. Inst. Technol., Haifa, Isr .
    [Google Scholar]
  50. Kravtsov V, Oren-Suissa M, Podbilewicz B 2017. The fusogen AFF-1 can rejuvenate the regenerative potential of adult dendritic trees by self-fusion. Development 144:2364–74 PVD responses in aging, regenerative potential, and connection to the insulin/IGF-1 receptor (DAF-2) pathway.
    [Google Scholar]
  51. Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y et al. 2008. ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J. Biol. Chem. 283:32944–56
    [Google Scholar]
  52. Kueh HY, Mitchison TJ. 2009. Structural plasticity in actin and tubulin polymer dynamics. Science 325:960–63
    [Google Scholar]
  53. Kuner R, Flor H. 2017. Structural plasticity and reorganisation in chronic pain. Nat. Rev. Neurosci. 18:20–30
    [Google Scholar]
  54. Le Bars D, Gozariu M, Cadden SW 2001. Animal models of nociception. Pharmacol. Rev. 53:597–652
    [Google Scholar]
  55. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Ackerman SL, Tessier-Lavigne M 1997. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386:833–38
    [Google Scholar]
  56. Li W, Feng Z, Sternberg PW, Xu XS 2006. A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684–87
    [Google Scholar]
  57. Liang X, Dong X, Moerman DG, Shen K, Wang X 2015. Sarcomeres pattern proprioceptive sensory dendritic endings through UNC-52/Perlecan in C. elegans. Dev. Cell 33:388–400
    [Google Scholar]
  58. Liao CP, Li H, Lee HH, Chien CT, Pan CL 2018. Cell-autonomous regulation of dendrite self-avoidance by the Wnt secretory factor MIG-14/Wntless. Neuron 98:320–34.e6
    [Google Scholar]
  59. 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]
  60. Liu X, Wang X, Shen K 2016. Receptor tyrosine phosphatase CLR-1 acts in skin cells to promote sensory dendrite outgrowth. Dev. Biol. 413:60–69
    [Google Scholar]
  61. Lom B, Cohen-Cory S. 1999. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arborization in vivo. J. Neurosci. 19:9928–38
    [Google Scholar]
  62. Long H, Ou Y, Rao Y, van Meyel DJ 2009. Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila. . Development 136:3475–84
    [Google Scholar]
  63. Mainen ZF, Sejnowski TJ. 1996. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–66
    [Google Scholar]
  64. Maniar TA, Kaplan M, Wang GJ, Shen K, Wei L et al. 2011. UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat. Neurosci. 15:48–56
    [Google Scholar]
  65. Matsubara D, Horiuchi SY, Shimono K, Usui T, Uemura T 2011. The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. Genes Dev 25:1982–96
    [Google Scholar]
  66. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC et al. 2007. Dendrite self-avoidance is controlled by Dscam. Cell 129:593–604
    [Google Scholar]
  67. McAllister AK. 2000. Cellular and molecular mechanisms of dendrite growth. Cereb. Cortex 10:963–73
    [Google Scholar]
  68. 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]
  69. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M et al. 1996. Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17:203–15
    [Google Scholar]
  70. Moench KM, Wellman CL. 2017. Differential dendritic remodeling in prelimbic cortex of male and female rats during recovery from chronic stress. Neuroscience 357:145–59
    [Google Scholar]
  71. Mohler WA, Shemer G, del Campo JJ, Valansi C, Opoku-Serebuoh E et al. 2002. The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev. Cell 2:355–62
    [Google Scholar]
  72. Morsch M, Radford R, Lee A, Don EK, Badrock AP et al. 2015. In vivo characterization of microglial engulfment of dying neurons in the zebrafish spinal cord. Front. Cell Neurosci. 9:321
    [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. Oates EC, Rossor AM, Hafezparast M, Gonzalez M, Speziani F et al. 2013. Mutations in BICD2 cause dominant congenital spinal muscular atrophy and hereditary spastic paraplegia. Am. J. Hum. Genet. 92:965–73
    [Google Scholar]
  75. Oren-Suissa M, Bayer EA, Hobert O 2016. Sex-specific pruning of neuronal synapses in Caenorhabditis elegans. . Nature 533:206–11
    [Google Scholar]
  76. 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]
  77. Oren-Suissa M, Hall DH, Treinin M, Shemer G, Podbilewicz B 2010. The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328:1285–88 Characterization of the PVD structure, development, and direct, cell-autonomous view of EFF-1-mediated maintenance of the PVD by dynamic dendrite pruning and self-fusion.
    [Google Scholar]
  78. Pan CL, Peng CY, Chen CH, McIntire S 2011. Genetic analysis of age-dependent defects of the Caenorhabditis elegans touch receptor neurons. PNAS 108:9274–79
    [Google Scholar]
  79. Parrish JZ, Emoto K, Kim MD, Jan YN 2007. Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30:399–423
    [Google Scholar]
  80. Parrish JZ, Kim MD, Jan LY, Jan YN 2006. Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev 20:820–35
    [Google Scholar]
  81. Pfister A, Johnson A, Ellers O, Horch HW 2013. Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus. Front. Physiol 3:367
    [Google Scholar]
  82. Podbilewicz B, Leikina E, Sapir A, Valansi C, Suissa M et al. 2006. The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo. Dev. Cell 11:471–81
    [Google Scholar]
  83. Portera-Cailliau C, Pan DT, Yuste R 2003. Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J. Neurosci. 23:7129–42
    [Google Scholar]
  84. Redila V, Christie B. 2006. Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 137:1299–307
    [Google Scholar]
  85. Roebroek AJ, Umans L, Pauli IG, Robertson EJ, van Leuven F et al. 1998. Failure of ventral closure and axial rotation in embryos lacking the proprotein convertase Furin. Development 125:4863–76
    [Google Scholar]
  86. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8:519–29
    [Google Scholar]
  87. Salzberg Y, Coleman AJ, Celestrin K, Cohen-Berkman M, Biederer T et al. 2017. Reduced insulin/insulin-like growth factor receptor signaling mitigates defective dendrite morphogenesis in mutants of the ER stress sensor IRE-1. PLOS Genet 13:e1006579
    [Google Scholar]
  88. Salzberg Y, Diaz-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 Describes the tri-partite PVD guidance complex of MNR-1, DMA-1, and SAX-7.
    [Google Scholar]
  89. Salzberg Y, Ramirez-Suarez NJ, Bulow HE 2014. The proprotein convertase KPC-1/furin controls branching and self-avoidance of sensory dendrites in Caenorhabditis elegans. . PLOS Genet 10:e1004657
    [Google Scholar]
  90. Sapir A, Choi J, Leikina E, Avinoam O, Valansi C et al. 2007. AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12:683–98
    [Google Scholar]
  91. Schroeder NE, Androwski RJ, Rashid A, Lee H, Lee J, Barr MM 2013. Dauer-specific dendrite arborization in C. elegans is regulated by KPC-1/Furin. Curr. Biol. 23:1527–35
    [Google Scholar]
  92. Serafini T, Kennedy TE, Galko 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]
  93. Shewan D, Berry M, Cohen J 1995. Extensive regeneration in vitro by early embryonic neurons on immature and adult CNS tissue. J. Neurosci. 15:2057–62
    [Google Scholar]
  94. Smith CJ, Watson JD, Spencer WC, O'Brien T, Cha B 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 Discusses PVD development and dynamics, PVD-specific expression profile, and the FLP neuron.
    [Google Scholar]
  95. Smith CJ, Watson JD, VanHoven MK, Colon-Ramos DA, Miller DM 3rd 2012. Netrin (UNC-6) mediates dendritic self-avoidance. Nat. Neurosci. 15:731–37 Proposes a mechanism by which UNC-6/netrin mediates dendritic self-avoidance by interactions with its receptors.
    [Google Scholar]
  96. Snider WD. 1988. Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals. J. Neurosci. 8:2628–34
    [Google Scholar]
  97. Soba P, Zhu S, Emoto K, Younger S, Yang SJ et al. 2007. Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54:403–16
    [Google Scholar]
  98. Stephens GJ, de Mesquita MB, Ryu WS, Bialek W 2011. Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans. . PNAS 108:7286–89
    [Google Scholar]
  99. Stoll G, Jander S, Myers RR 2002. Degeneration and regeneration of the peripheral nervous system: from Augustus Waller's observations to neuroinflammation. J. Peripher. Nerv. Syst. 7:13–27
    [Google Scholar]
  100. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol 56:110–56
    [Google Scholar]
  101. Swan A, Nguyen T, Suter B 1999. Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nat. Cell Biol. 1:444–49
    [Google Scholar]
  102. Swierczek NA, Giles AC, Rankin CH, Kerr RA 2011. High-throughput behavioral analysis in C. elegans. Nat. Methods 8:592–98
    [Google Scholar]
  103. Tank EM, Rodgers KE, Kenyon C 2011. Spontaneous age-related neurite branching in Caenorhabditis elegans. J. Neurosci 31:9279–88
    [Google Scholar]
  104. Taylor CA, Yan J, Howell AS, Dong X, Shen K 2015. RAB-10 regulates dendritic branching by balancing dendritic transport. PLOS Genet 11:e1005695 Discusses PVD microtubule directionality and the roles of protein transport and RAB-10 in the localization of DMA-1.
    [Google Scholar]
  105. Tonomura S, Ebara S, Bagdasarian K, Uta D, Ahissar E et al. 2015. Structure-function correlations of rat trigeminal primary neurons: emphasis on club-like endings, a vibrissal mechanoreceptor. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 91:560–76
    [Google Scholar]
  106. Toth ML, Melentijevic I, Shah L, Bhatia A, Lu K et al. 2012. Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J. Neurosci. 32:8778–90
    [Google Scholar]
  107. Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O 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]
  108. Urbanska M, Blazejczyk M, Jaworski J 2008. Molecular basis of dendritic arborization. Acta Neurobiol. Exp. 68:264–88
    [Google Scholar]
  109. Verdu E, Ceballos D, Vilches JJ, Navarro X 2000. Influence of aging on peripheral nerve function and regeneration. J. Peripher. Nerv. Syst. 5:191–208
    [Google Scholar]
  110. Vetter P, Roth A, Häusser M 2001. Propagation of action potentials in dendrites depends on dendritic morphology. J. Neurophysiol. 85:926–37
    [Google Scholar]
  111. Von Stetina SE, Treinin M, Miller D 2006. The motor circuit. Int. Rev. Neurobiol. 69:125–67
    [Google Scholar]
  112. Wadsworth WG, Bhatt H, Hedgecock EM 1996. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16:35–46
    [Google Scholar]
  113. Warren MS, Bradley WD, Gourley SL, Lin YC, Simpson MA et al. 2012. Integrin β1 signals through Arg to regulate postnatal dendritic arborization, synapse density, and behavior. J. Neurosci. 32:2824–34
    [Google Scholar]
  114. Way JC, Chalfie M. 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]
  115. Wei X, Howell AS, Dong X, Taylor CA, Cooper RC et al. 2015. The unfolded protein response is required for dendrite morphogenesis. eLife 4:e06963
    [Google Scholar]
  116. 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]
  117. Wu G-Y, Cline HT. 1998. Stabilization of dendritic arbor structure in vivo by CaMKII. Science 279:222–26
    [Google Scholar]
  118. Yamada M, Hayashi H, Yuuki M, Matsushima N, Yuan B, Takagi N 2018. Furin inhibitor protects against neuronal cell death induced by activated NMDA receptors. Sci. Rep. 8:5212
    [Google Scholar]
  119. Yang G, Masland RH. 1994. Receptive fields and dendritic structure of directionally selective retinal ganglion cells. J. Neurosci. 14:5267–80
    [Google Scholar]
  120. Yankner BA, Lu T, Loerch P 2008. The aging brain. Annu. Rev. Pathol. 3:41–66
    [Google Scholar]
  121. Yassin L, Gillo B, Kahan T, Halevi S, Eshel M, Treinin M 2001. Characterization of the deg-3/des-2 receptor: a nicotinic acetylcholine receptor that mutates to cause neuronal degeneration. Mol. Cell Neurosci. 17:589–99
    [Google Scholar]
  122. Yassin L, Samson AO, Halevi S, Eshel M, Treinin M 2002. Mutations in the extracellular domain and in the membrane-spanning domains interfere with nicotinic acetylcholine receptor maturation. Biochemistry 41:12329–35
    [Google Scholar]
  123. Yip ZC, Heiman MG. 2016. Duplication of a single neuron in C. elegans reveals a pathway for dendrite tiling by mutual repulsion. Cell Rep 15:2109–17
    [Google Scholar]
  124. Yu X, Malenka RC. 2003. β-catenin is critical for dendritic morphogenesis. Nat. Neurosci. 6:1169–77
    [Google Scholar]
  125. Zhu T, Liang X, Wang XM, Shen K 2017. Dynein and EFF-1 control dendrite morphology by regulating the localization pattern of SAX-7 in epidermal cells. J. Cell Sci. 130:4063–71
    [Google Scholar]
  126. 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 Links the quad-partite component DMA-1 with HPO-30 to downstream cytoskeleton-related signaling pathways affecting morphogenesis.
    [Google Scholar]
  127. 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]
  128. Zou W, Yadav S, DeVault L, Nung Jan Y, Sherwood DR 2015. RAB-10-dependent membrane transport is required for dendrite arborization. PLOS Genet 11:e1005484
    [Google Scholar]
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