Extrinsic repair of injured dendrites as a paradigm for regeneration by fusion in Caenorhabditis elegans

Genetics

Volumn 206, Issue 1, 2017, Pages 215-230

  Oren Suissa, Meital ^a   Gattegno, Tamar ^a   Kravtsov, Veronika ^a   Podbilewicz, Benjamin ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

AFF 1; Degeneration following dendrotomy; Dendrite auto fusion; EFF 1; Regeneration of dendritic trees

Indexed keywords

PROTEIN; AFF-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; EFF-1 PROTEIN, C ELEGANS; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; AXON; CAENORHABDITIS ELEGANS; CELL FUSION; CELL REGENERATION; CELL STRUCTURE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; DENDRITE; EXOSOME; MODEL; MOLECULAR BIOLOGY; NERVE CELL DEGENERATION; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOLOGY; REGENERATION; SENSORY NERVE CELL; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DENDRITES; MEMBRANE GLYCOPROTEINS; NEURONAL PLASTICITY; REGENERATION; SENSORY RECEPTOR CELLS;

EID: 85020720883     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.196386     Document Type: Article

References (108)

1. Aguirre-Chen, C., H. E. Bulow, and Z. Kaprielian, 2011 C. elegans bicd-1, homolog of the Drosophila dynein accessory factor Bicaudal D, regulates the branching of PVD sensory neuron dendrites. Development 138: 507-518.
2. Albeg, A., C. Smith, M. Chatzigeorgiou, D. G. Feitelson, D. H. Hall et al., 2011 C. elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell. Neurosci. 46: 308-317.
3. Avinoam, O., and B. Podbilewicz, 2011 Eukaryotic cell-cell fusion families. Curr. Top. Membr. 68: 209-234.
4. Avinoam,O., K. Fridman,C.Valansi, I. Abutbul, T. Zeev-Ben-Mordehai et al., 2011 Conserved eukaryotic fusogens can fuse viral envelopes to cells. Science 332: 589-592.
5. Bedi, S. S., and D. L. Glanzman, 2001 Axonal rejoining inhibits injury-induced long-term changes in Aplysia sensory neurons in vitro. J. Neurosci. 21: 9667-9677.
6. Beveridge, T. J., 1999 Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181: 4725-4733.
7. Bond, S. R., and C. C. Naus, 2012 RF-Cloning.org: an online tool for the design of restriction-free cloning projects. Nucleic Acids Res. 40: W209-W213.
8. Bourgeois, F., and A. Ben-Yakar, 2007 Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C. elegans. Opt. Express 15: 8521-8531.
9. Bradbury, E. J., L. D. Moon, R. J. Popat, V. R. King, G. S. Bennett et al., 2002 Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416: 636-640.
10. Bradke, F., J. W. Fawcett, and M. E. Spira, 2012 Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 13: 183-193.
11. Bratt, M. A., and W. R. Gallaher, 1969 Preliminary analysis of the requirements for fusion from within and fusion from without by Newcastle disease virus. Proc. Natl. Acad. Sci. USA 64: 536-543.
12. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
13. Cajal, S. R., 1899 Histología del Sistema Nervioso del Hombre y de Los Vertebrados. Ministerio de Sanidad y Consumo, Madrid.
14. Chatzigeorgiou, M., and W. R. Schafer, 2011 Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 70: 299-309.
15. Chatzigeorgiou, M., S. Yoo, J. D. Watson, W. H. Lee, W. C. Spencer et al., 2010 Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat. Neurosci. 13: 861-868.
16. Chiorazzi, M., L. Rui, Y. Yang, M. Ceribelli, N. Tishbi et al., 2013 Related F-box proteins control cell death in Caenorhabditis elegans and human lymphoma. Proc. Natl. Acad. Sci. USA 110: 3943-3948.
17. Chisholm, A. D., H. Hutter, Y. Jin, and W. G. Wadsworth, 2016 The genetics of axon guidance and axon regeneration in Caenorhabditis elegans. Genetics 204: 849-882.
18. Clavel, F., and P. Charneau, 1994 Fusion from without directed by human immunodeficiency virus particles. J. Virol. 68: 1179-1185.
19. Coleman, M. P., and M. R. Freeman, 2010 Wallerian degeneration, WldS, and Nmnat. Annu. Rev. Neurosci. 33: 245-267.
20. Devor, M., 1976 Neuroplasticity in the rearrangement of olfactory tract fibers after neonatal transection in hamsters. J. Comp. Neurol. 166: 49-72.
21. Dong, X., H. Chiu, Y. J. Park, W. Zou, Y. Zou et al., 2016 Precise regulation of the guidance receptor DMA-1 by KPC-1/Furin instructs dendritic branching decisions. eLife. 5: e11008.
22. Duelli, D., and Y. Lazebnik, 2007 Cell-to-cell fusion as a link between viruses and cancer. Nat. Rev. Cancer 7: 968-976.
23. Edwards, T. J., and M. Hammarlund, 2014 Syndecan promotes axon regeneration by stabilizing growth cone migration. Cell Rep. 8: 272-283.
24. Fernandez-Gonzalez, A., A. R. La Spada, J. Treadaway, J. C. Higdon, B. S. Harris et al., 2002 Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295: 1904-1906.
25. Fridman, K., 2012 Ultrastructure and function of AFF-1 and EFF-1 in membrane remodeling. M.Sc. Thesis, Technion - Israel Institute of Technology, Haifa, Israel.
26. Gabel, C. V., F. Antoine, C. F. Chuang, A. D. Samuel, and C. Chang, 2008 Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 135: 1129-1136.
27. Gattegno, T., A. Mittal, C. Valansi, K. C. Nguyen, D. H. Hall et al., 2007 Genetic control of fusion pore expansion in the epidermis of Caenorhabditis elegans. Mol. Biol. Cell 18: 1153-1166.
28. Ghosh-Roy, A., and A. D. Chisholm, 2010 Caenorhabditis elegans: a new model organism for studies of axon regeneration. Dev. Dyn. 239: 1460-1464.
29. Ghosh-Roy, A., Z. Wu, A. Goncharov, Y. Jin, and A. D. Chisholm, 2010 Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J. Neurosci. 30: 3175-3183.
30. Giordano-Santini, R., C. Linton, and M. A. Hilliard, 2016 Cell-cell fusion in the nervous system: alternative mechanisms of development, injury, and repair. Semin. Cell Dev. Biol. 60: 146-154.
31. Goodman, M. B., 2003 Sensation is painless. Trends Neurosci. 26: 643-645.
32. Halevi, S., J. McKay, M. Palfreyman, L. Yassin, M. Eshel et al., 2002 The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J. 21: 1012-1020.
33. Hall, D. H., and M. Treinin, 2011 How does morphology relate to function in sensory arbors? Trends Neurosci. 34: 443-451.
34. Hall, G. F., and M. J. Cohen, 1988 Dendritic amputation redistributes sprouting evoked by axotomy in lamprey central neurons. J. Neurosci. 8: 3598-3606.
35. Hammarlund, M., and Y. Jin, 2014 Axon regeneration in C. elegans. Curr. Opin. Neurobiol. 27: 199-207.
36. Hammarlund, M., P. Nix, L. Hauth, E. M. Jorgensen, and M. Bastiani, 2009 Axon regeneration requires a conserved MAP kinase pathway. Science 323: 802-806.
37. Hilliard, M. A., 2009 Axonal degeneration and regeneration: a mechanistic tug-of-war. J. Neurochem. 108: 23-32.
38. Hoy, R. R., G. D. Bittner, and D. Kennedy, 1967 Regeneration in crustacean motoneurons: evidence for axonal fusion. Science 156: 251-252.
39. Hyenne, V., A. Apaydin, D. Rodriguez, C. Spiegelhalter, S. Hoff-Yoessle et al., 2015 RAL-1 controls multivesicular body biogenesis and exosome secretion. J. Cell Biol. 211: 27-37.
40. Kirby, C., M. Kusch, and K. Kemphues, 1990 Mutations in the par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle. Dev. Biol. 142: 203-215.
41. Kosinski, M., K. McDonald, J. Schwartz, I. Yamamoto, and D. Greenstein, 2005 C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes. Development 132: 3357-3369.
42. Kravtsov, V., M. Oren-Suissa, and B. Podbilewicz, 2016 Cell fusion proteins can rejuvenate adult dendritic trees. bioRxiv. Available at: http://www.biorxiv.org/content/early/2016/07/07/062679.
43. Kwon, S. H., K. D. Liu, and K. E. Mostov, 2014 Intercellular transfer of GPRC5B via exosomes drives HGF-mediated outward growth. Curr. Biol. 24: 199-204.
44. Li, S., C. Yang, L. Zhang, X. Gao, X. Wang et al., 2016 Promoting axon regeneration in the adult CNS by modulation of the melanopsin/GPCR signaling. Proc. Natl. Acad. Sci. USA 113: 1937-1942.
45. Liang, X., X. Dong, D. G. Moerman, K. Shen, and X. Wang, 2015 Sarcomeres pattern proprioceptive sensory dendritic endings through UNC-52/Perlecan in C. elegans. Dev. Cell 33: 388-400.
46. Liegeois, S., A. Benedetto, J. M. Garnier, Y. Schwab, and M. Labouesse, 2006 The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173: 949-961.
47. Maniar, T. A., M. Kaplan, G. J. Wang, K. Shen, L. Wei et al., 2012 UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat. Neurosci. 15: 48-56.
48. Mapes, J., Y. Z. Chen, A. Kim, S. Mitani, B. H. Kang et al., 2012 CED-1, CED-7, and TTR-52 regulate surface phosphatidylserine expression on apoptotic and phagocytic cells. Curr. Biol. 22: 1267-1275.
49. Mar, F. M., A. Bonni, and M. M. Sousa, 2014 Cell intrinsic control of axon regeneration. EMBO Rep. 15: 254-263.
50. Martin, S. M., G. S. O’Brien, C. Portera-Cailliau, and A. Sagasti, 2010 Wallerian degeneration of zebrafish trigeminal axons in the skin is required for regeneration and developmental pruning. Development 137: 3985-3994.
51. McCarter, J., B. Bartlett, T. Dang, and T. Schedl, 1997 Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev. Biol. 181: 121-143.
52. McCarter, J., B. Bartlett, T. Dang, and T. Schedl, 1999 On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205: 111-128.
53. Mello, C., and A. Fire, 1995 DNA transformation, pp. 451-482 in Methods in Cell Biology. Caenorhabditis Elegans: Model Biological Analysis of an Organism, edited by H. F. Epstein, and D. C. Shakes. Academic Press, San Diego.
54. Miyado, K., K. Yoshida, K. Yamagata, K. Sakakibara, M. Okabe et al., 2008 The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc. Natl. Acad. Sci. USA 105: 12921-12926.
55. Mohler, W. A., G. Shemer, J. del Campo, C. Valansi, E. Opoku-Serebuoh et al., 2002 The type I membrane protein EFF-1 is essential for developmental cell fusion in C. elegans. Dev. Cell 2: 355-362.
56. Moritz, C. T., S. I. Perlmutter, and E. E. Fetz, 2008 Direct control of paralysed muscles by cortical neurons. Nature 456: 639-642.
57. Nawabi, H., K. Zukor, and Z. He, 2012 No simpler than mammals: axon and dendrite regeneration in Drosophila. Genes Dev. 26: 1509-1514.
58. Neumann, B., K. C. Nguyen, D. H. Hall, A. Ben-Yakar, and M. A. Hilliard, 2011 Axonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons. Dev. Dyn. 240: 1365-1372.
59. Neumann, B., S. Coakley, R. Giordano-Santini, C. Linton, E. S. Lee et al., 2015 EFF-1-mediated regenerative axonal fusion requires components of the apoptotic pathway. Nature 517: 219-222.
60. Nix, P., M. Hammarlund, L. Hauth, M. Lachnit, E. M. Jorgensen et al., 2014 Axon regeneration genes identified by RNAi screening in C. elegans. J. Neurosci. 34: 629-645.
61. Oren-Suissa, M., and B. Podbilewicz, 2010 Evolution of programmed cell fusion: common mechanisms and distinct functions. Dev. Dyn. 239: 1515-1528.
62. Oren-Suissa, M., D. Hall, M. Treinin, G. Shemer, and B. Podbilewicz, 2010 The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328: 1285-1288.
63. Paltsyn, A., S. Komissarova, I. Dubrovin, and A. Kubatiev, 2013 Increased cell fusion in cerebral cortex may contribute to poststroke regeneration. Stroke Res. Treat. 2013: 869327.
64. Park, K. K., K. Liu, Y. Hu, P. D. Smith, C. Wang et al., 2008 Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322: 963-966.
65. Petersen, L. K., and R. S. Stowers, 2011 A Gateway MultiSite recombination cloning toolkit. PLoS One 6: e24531.
66. Podbilewicz, B., 2014 Virus and cell fusion mechanisms. Annu. Rev. Cell Dev. Biol. 30: 111-139.
67. Podbilewicz, B., and L. V. Chernomordik, 2005 Cell fusion in development and disease, pp. 221-244 in Protein-Lipids Interactions, edited by L. K. Tamm. Wiley-VCH, New York.
68. Podbilewicz, B., E. Leikina, A. Sapir, C. Valansi, M. Suissa et al., 2006 The C. elegans developmental fusogen EFF-1 mediates homotypic fusion in heterologous cells and in vivo. Dev. Cell 11: 471-481.
69. Procko, C., Y. Lu, and S. Shaham, 2011 Glia delimit shape changes of sensory neuron receptive endings in C. elegans. Development 138: 1371-1381.
70. Pujadas, L., A. Gruart, C. Bosch, L. Delgado, C. M. Teixeira et al., 2010 Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J. Neurosci. 30: 4636-4649.
71. Rao, K., M. C. Stone, A. T. Weiner, K. W. Gheres, C. Zhou et al., 2016 Spastin, atlastin, and ER relocalization are involved in axon but not dendrite regeneration. Mol. Biol. Cell 27: 3245-3256.
72. Rasmussen, J. P., K. English, J. R. Tenlen, and J. R. Priess, 2008 Notch signaling and morphogenesis of single-cell tubes in the C. elegans digestive tract. Dev. Cell 14: 559-569.
73. Ruschel, J., F. Hellal, K. C. Flynn, S. Dupraz, D. A. Elliott et al., 2015 Systemic administration of epothilone B promotes axon regeneration after spinal cord injury. Science 348: 347-352.
74. Salzberg, Y., C. A. Diaz-Balzac, N. J. Ramirez-Suarez, M. Attreed, E. Tecle et al., 2013 Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155: 308-320.
75. Sapir, A., J. Choi, E. Leikina, O. Avinoam, C. Valansi et al., 2007 AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12: 683-698.
76. Sarov, M., S. Schneider, A. Pozniakovski, A. Roguev, S. Ernst et al., 2006 A recombineering pipeline for functional genomics applied to Caenorhabditis elegans. Nat. Methods 3: 839-844.
77. Shemer, G., M. Suissa, I. Kolotuev, K. C. Q. Nguyen, D. H. Hall et al., 2004 EFF-1 is sufficient to initiate and execute tissue-specific cell fusion in C. elegans. Curr. Biol. 14: 1587-1591.
78. Shinn-Thomas, J. H., and W. A. Mohler, 2011 New insights into the mechanisms and roles of cell-cell fusion. Int. Rev. Cell Mol. Biol. 289: 149-209.
79. Shinn-Thomas, J. H., J. J. Del Campo, J. Wang, and W. A. Mohler, 2016 The EFF-1A cytoplasmic domain influences hypodermal cell fusions in. elegans but is not dependent on 14-3-3 proteins. PLoS One 11: e0146874.
80. Smith, C. J., J. D. Watson, W. C. Spencer, T. O’Brien, B. Cha 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.
81. Smith, C. J., J. D. Watson, M. K. VanHoven, D. A. Colon-Ramos, and D. M. Miller, III, 2012 Netrin (UNC-6) mediates dendritic selfavoidance. Nat. Neurosci. 15: 731-737.
82. Smurova, K., and B. Podbilewicz, 2016a Endocytosis regulates membrane localization and function of the fusogen EFF-1. Small GTPases 28: 1-4.
83. Smurova, K., and B. Podbilewicz, 2016b RAB-5- and DYNAMIN-1-mediated endocytosis of EFF-1 fusogen controls cell-cell fusion. Cell Rep. 14: 1517-1527.
84. Song, Y., K. M. Ori-McKenney, Y. Zheng, C. Han, L. Y. Jan et al., 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.
85. Soulavie, F., and M. V. Sundaram, 2016 Auto-fusion and the shaping of neurons and tubes. Semin. Cell Dev. Biol. 60: 136-145.
86. Standler, N. A., and J. J. Bernstein, 1982 Degeneration and regeneration of motoneuron dendrites after ventral root crush: computer reconstruction of dendritic fields. Exp. Neurol. 75: 600-615.
87. Stone, C. E., D. H. Hall, and M. V. Sundaram, 2009 Lipocalin signaling controls unicellular tube development in the Caenorhabditis elegans excretory system. Dev. Biol. 329: 201-211.
88. Stone, M. C., M. M. Nguyen, J. Tao, D. L. Allender, and M. M. Rolls, 2010 Global up-regulation of microtubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol. Biol. Cell 21: 767-777.
89. Stone, M. C., R. M. Albertson, L. Chen, and M. M. Rolls, 2014 Dendrite injury triggers DLK-independent regeneration. Cell Rep. 6: 247-253.
90. Sulston, J., and J. Hodgkin, 1988 Methods, pp. 587-606 in The Nematode Caenorhabditis Elegans, edited by W. B. Wood. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
91. Tao, J., C. Feng, and M. M. Rolls, 2016 The microtubule-severing protein fidgetin acts after dendrite injury to promote their degeneration. J. Cell Sci. 129: 3274-3281.
92. Taylor, A. M., M. Blurton-Jones, S. W. Rhee, D. H. Cribbs, C. W. Cotman et al., 2005 A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2: 599-605.
93. Taylor, C. A., J. Yan, A. S. Howell, X. Dong, and K. Shen, 2015 RAB-10 regulates dendritic branching by balancing dendritic transport. PLoS Genet. 11: e1005695.
94. Tkach, M., and C. Thery, 2016 Communication by extracellular vesicles: where we are and where we need to go. Cell 164: 1226-1232.
95. Tsalik, E. L., T. Niacaris, A. S. Wenick, K. Pau, L. Avery et al., 2003 LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev. Biol. 263: 81-102.
96. Valansi, C., D. Moi, E. Leikina, E. Matveev, M. Grana et al., 2017 Arabidopsis HAP2/GCS1 is a gamete fusion protein homologous to somatic and viral fusogens. J. Cell Biol. 216: 571-581.
97. Wang, H., and E. R. Macagno, 1998 A detached branch stops being recognized as self by other branches of a neuron. J. Neurobiol. 35: 53-64.
98. Wang, J., M. Silva, L. A. Haas, N. S. Morsci, K. C. Nguyen et al., 2014 C. elegans ciliated sensory neurons release extracellular vesicles that function in animal communication. Curr. Biol. 24: 519-525.
99. Way, J. C., and M. Chalfie, 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: 1823-1833.
100. Wehman, A. M., C. Poggioli, P. Schweinsberg, B. D. Grant, and J. Nance, 2011 The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr. Biol. 21: 1951-1959.
101. White, J., K. Matlin, and A. Helenius, 1981 Cell fusion by semliki forest, influenza, and vesicular stomatitis viruses. J. Cell Biol. 89: 674-679.
102. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner, 1986 The structure of the nervous system of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314: 1-340.
103. Wu, Z., A. Ghosh-Roy, M. F. Yanik, J. Z. Zhang, Y. Jin et al., 2007 Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl. Acad. Sci. USA 104: 15132-15137.
104. Yan, D., Z. Wu, A. D. Chisholm, and Y. Jin, 2009 The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138: 1005-1018.
105. Yanik, M. F., H. Cinar, H. N. Cinar, A. D. Chisholm, Y. Jin et al., 2004 Neurosurgery: functional regeneration after laser axotomy. Nature 432: 822.
106. Yaniv, S. P., N. Issman-Zecharya, M. Oren-Suissa, B. Podbilewicz, and O. Schuldiner, 2012 Axon regrowth during development and regeneration following injury share molecular mechanisms. Curr. Biol. 22: 1774-1782.
107. Yassin, L., B. Gillo, T. Kahan, S. Halevi, M. Eshel et al., 2001 Characterization of the DEG-3/DES-2 receptor: a nicotinic acetylcholine receptor that mutates to cause neuronal degeneration. Mol. Cell. Neurosci. 17: 589-599.
108. Yip, Z. C., and M. G. Heiman, 2016 Duplication of a single neuron in C. elegans reveals a pathway for dendrite tiling by mutual repulsion. Cell Rep. 15: 2109-2117.