Endocytic Pathways Downregulate the L1-type Cell Adhesion Molecule Neuroglian to Promote Dendrite Pruning in Drosophila

Developmental Cell

Volumn 30, Issue 4, 2014, Pages 463-478

  Zhang, Heng ^a   Wang, Yan ^a,b   Wong, Jack Jing Lin ^a,b   Lim, Kah Leong ^a,c,d   Liou, Yih Cherng ^a   Wang, Hongyan ^a,b,c   Yu, Fengwei ^a,b,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NERVE CELL ADHESION MOLECULE L1; NEUROGLIAN PROTEIN; RAB PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL MATURATION; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; CYTOPLASM; DENDRITE; DOWN REGULATION; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; EPISTASIS; GENE OVEREXPRESSION; GLIA; MULTIVESICULAR BODY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN METABOLISM; RNA INTERFERENCE; SENSORY NERVE CELL;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; DENDRITES; DOWN-REGULATION; DROSOPHILA; DROSOPHILA PROTEINS; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; EPISTASIS, GENETIC; RAB5 GTP-BINDING PROTEINS;

EID: 84907322903     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.06.014     Document Type: Article

References (67)

1. Awasaki T., Ito K. Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 2004, 14:668-677.
2. Bagri A., Cheng H.J., Yaron A., Pleasure S.J., Tessier-Lavigne M. Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 2003, 113:285-299.
3. Castellani V., Falk J., Rougon G. Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Mol. Cell. Neurosci. 2004, 26:89-100.
4. Ceresa B.P., Schmid S.L. Regulation of signal transduction by endocytosis. Curr. Opin. Cell Biol. 2000, 12:204-210.
5. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
6. Dittman J., Ryan T.A. Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 2009, 25:133-160.
7. Dong X., Liu O.W., Howell A.S., Shen K. An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 2013, 155:296-307.
8. Enneking E.M., Kudumala S.R., Moreno E., Stephan R., Boerner J., Godenschwege T.A., Pielage J. Transsynaptic coordination of synaptic growth, function, and stability by the L1-type CAM Neuroglian. PLoS Biol. 2013, 11:e1001537.
9. Entchev E.V., Schwabedissen A., González-Gaitán M. Gradient formation of the TGF-beta homolog Dpp. Cell 2000, 103:981-991.
10. Fournier A.E., Nakamura F., Kawamoto S., Goshima Y., Kalb R.G., Strittmatter S.M. Semaphorin3A enhances endocytosis at sites of receptor-F-actin colocalization during growth cone collapse. J.Cell Biol. 2000, 149:411-422.
11. Godenschwege T.A., Kristiansen L.V., Uthaman S.B., Hortsch M., Murphey R.K. A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr. Biol. 2006, 16:12-23.
12. Goossens T., Kang Y.Y., Wuytens G., Zimmermann P., Callaerts-Végh Z., Pollarolo G., Islam R., Hortsch M., Callaerts P. The Drosophila L1CAM homolog Neuroglian signals through distinct pathways to control different aspects of mushroom body axon development. Development 2011, 138:1595-1605.
13. Grueber W.B., Ye B., Moore A.W., Jan L.Y., Jan Y.N. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 2003, 13:618-626.
14. Han C., Jan L.Y., Jan Y.N. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc. Natl. Acad. Sci. USA 2011, 108:9673-9678.
15. Han C., Wang D., Soba P., Zhu S., Lin X., Jan L.Y., Jan Y.N. Integrins regulate repulsion-mediated dendritic patterning of Drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 2012, 73:64-78.
16. Herz H.M., Chen Z., Scherr H., Lackey M., Bolduc C., Bergmann A. vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 2006, 133:1871-1880.
17. Hortsch M. Structural and functional evolution of the L1 family: are four adhesion molecules better than one?. Mol. Cell. Neurosci. 2000, 15:1-10.
18. Hortsch M., Bieber A.J., Patel N.H., Goodman C.S. Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron 1990, 4:697-709.
19. Islam R., Wei S.Y., Chiu W.H., Hortsch M., Hsu J.C. Neuroglian activates Echinoid to antagonize the Drosophila EGF receptor signaling pathway. Development 2003, 130:2051-2059.
20. Jahn R., Lang T., Südhof T.C. Membrane fusion. Cell 2003, 112:519-533.
21. Kage E., Hayashi Y., Takeuchi H., Hirotsu T., Kunitomo H., Inoue T., Arai H., Iino Y., Kubo T. MBR-1, a novel helix-turn-helix transcription factor, is required for pruning excessive neurites in Caenorhabditis elegans. Curr. Biol. 2005, 15:1554-1559.
22. Kanamori T., Kanai M.I., Dairyo Y., Yasunaga K., Morikawa R.K., Emoto K. Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 2013, 340:1475-1478.
23. Keleman K., Rajagopalan S., Cleppien D., Teis D., Paiha K., Huber L.A., Technau G.M., Dickson B.J. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 2002, 110:415-427.
24. Kennedy M.J., Ehlers M.D. Organelles and trafficking machinery for postsynaptic plasticity. Annu. Rev. Neurosci. 2006, 29:325-362.
25. Kenwrick S., Watkins A., De Angelis E. Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum. Mol. Genet. 2000, 9:879-886.
26. Kim M.E., Shrestha B.R., Blazeski R., Mason C.A., Grueber W.B. Integrins establish dendrite-substrate relationships that promote dendritic self-avoidance and patterning in Drosophila sensory neurons. Neuron 2012, 73:79-91.
27. Kirilly D., Gu Y., Huang Y., Wu Z., Bashirullah A., Low B.C., Kolodkin A.L., Wang H., Yu F. A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat. Neurosci. 2009, 12:1497-1505.
28. Kirilly D., Wong J.J., Lim E.K., Wang Y., Zhang H., Wang C., Liao Q., Wang H., Liou Y.C., Wang H., Yu F. Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron 2011, 72:86-100.
29. Kuo C.T., Jan L.Y., Jan Y.N. Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc. Natl. Acad. Sci. USA 2005, 102:15230-15235.
30. Kuo C.T., Zhu S., Younger S., Jan L.Y., Jan Y.N. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 2006, 51:283-290.
31. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
32. Lee T., Marticke S., Sung C., Robinow S., Luo L. Cell-autonomous requirement of the USP/EcR-B ecdysone receptor for mushroom body neuronal remodeling in Drosophila. Neuron 2000, 28:807-818.
33. Lee H.H., Jan L.Y., Jan Y.N. Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc. Natl. Acad. Sci. USA 2009, 106:6363-6368.
34. Lloyd T.E., Atkinson R., Wu M.N., Zhou Y., Pennetta G., Bellen H.J. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 2002, 108:261-269.
35. Loncle N., Williams D.W. An interaction screen identifies headcase as a regulator of large-scale pruning. J.Neurosci. 2012, 32:17086-17096.
36. Lu H., Bilder D. Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 2005, 7:1232-1239.
37. Luo L., O'Leary D.D. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005, 28:127-156.
38. Maness P.F., Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 2007, 10:19-26.
39. Nixon R.A., Yang D.S., Lee J.H. Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 2008, 4:590-599.
40. O'Donnell M., Chance R.K., Bashaw G.J. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 2009, 32:383-412.
41. O'Leary D.D., Koester S.E. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 1993, 10:991-1006.
42. Raiborg C., Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458:445-452.
43. Riccomagno M.M., Hurtado A., Wang H., Macopson J.G., Griner E.M., Betz A., Brose N., Kazanietz M.G., Kolodkin A.L. The RacGAP β2-Chimaerin selectively mediates axonal pruning in the hippocampus. Cell 2012, 149:1594-1606.
44. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
45. Rusten T.E., Vaccari T., Lindmo K., Rodahl L.M., Nezis I.P., Sem-Jacobsen C., Wendler F., Vincent J.P., Brech A., Bilder D., Stenmark H. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 2007, 17:1817-1825.
46. Rusten T.E., Vaccari T., Stenmark H. Shaping development with ESCRTs. Nat. Cell Biol. 2012, 14:38-45.
47. Salzberg Y., Díaz-Balzac C.A., Ramirez-Suarez N.J., Attreed M., Tecle E., Desbois M., Kaprielian Z., Bülow H.E. Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 2013, 155:308-320.
48. Sann S., Wang Z., Brown H., Jin Y. Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol. 2009, 19:317-324.
49. Satoh D., Sato D., Tsuyama T., Saito M., Ohkura H., Rolls M.M., Ishikawa F., Uemura T. Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat. Cell Biol. 2008, 10:1164-1171.
50. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
51. Schubiger M., Wade A.A., Carney G.E., Truman J.W., Bender M. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 1998, 125:2053-2062.
52. Sweeney N.T., Brenman J.E., Jan Y.N., Gao F.B. The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr. Biol. 2006, 16:1006-1011.
53. Thompson B.J., Mathieu J., Sung H.H., Loeser E., Rørth P., Cohen S.M. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 2005, 9:711-720.
54. Truman J.W. Metamorphosis of the central nervous system of Drosophila. J.Neurobiol. 1990, 21:1072-1084.
55. Vaccari T., Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 2005, 9:687-698.
56. Vaccari T., Rusten T.E., Menut L., Nezis I.P., Brech A., Stenmark H., Bilder D. Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J.Cell Sci. 2009, 122:2413-2423.
57. Watts R.J., Hoopfer E.D., Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003, 38:871-885.
58. Watts R.J., Schuldiner O., Perrino J., Larsen C., Luo L. Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 2004, 14:678-684.
59. Williams D.W., Truman J.W. Cellular mechanisms of dendrite pruning in Drosophila: insights from invivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 2005, 132:3631-3642.
60. Williams D.W., Kondo S., Krzyzanowska A., Hiromi Y., Truman J.W. Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 2006, 9:1234-1236.
61. Williamson W.R., Yang T., Terman J.R., Hiesinger P.R. Guidance receptor degradation is required for neuronal connectivity in the Drosophila nervous system. PLoS Biol. 2010, 8:e1000553.
62. Wong J.J., Li S., Lim E.K., Wang Y., Wang C., Zhang H., Kirilly D., Wu C., Liou Y.C., Wang H., Yu F. A Cullin1-based SCF E3 ubiquitin ligase targets the InR/PI3K/TOR pathway to regulate neuronal pruning. PLoS Biol. 2013, 11:e1001657.
63. Wucherpfennig T., Wilsch-Bräuninger M., González-Gaitán M. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J.Cell Biol. 2003, 161:609-624.
64. Yamamoto M., Ueda R., Takahashi K., Saigo K., Uemura T. Control of axonal sprouting and dendrite branching by the Nrg-Ank complex at the neuron-glia interface. Curr. Biol. 2006, 16:1678-1683.
65. Yang W.K., Peng Y.H., Li H., Lin H.C., Lin Y.C., Lai T.T., Suo H., Wang C.H., Lin W.H., Ou C.Y., et al. Nak regulates localization of clathrin sites in higher-order dendrites to promote local dendrite growth. Neuron 2011, 72:285-299.
66. Yap C.C., Winckler B. Harnessing the power of the endosome to regulate neural development. Neuron 2012, 74:440-451.
67. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.