Meigo governs dendrite targeting specificity by modulating Ephrin level and N-glycosylation

Nature Neuroscience

Volumn 16, Issue 6, 2013, Pages 683-691

  Sekine, Sayaka U ^a   Haraguchi, Shuka ^a   Chao, Kinhong ^a   Kato, Tomoko ^a   Luo, Liqun ^b   Miura, Masayuki ^a,c   Chihara, Takahiro ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b STANFORD UNIVERSITY   (United States)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DENDRITE; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GENETIC SCREENING; GLYCOSYLATION; NERVE CELL; NERVE CELL DIFFERENTIATION; NEUROMODULATION; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION;

ANIMALS; CONSERVED SEQUENCE; DENDRITES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; EPHRINS; GENE KNOCKDOWN TECHNIQUES; GENE TARGETING; GLYCOSYLATION; OLFACTORY RECEPTOR NEURONS; PROTEIN UNFOLDING;

EID: 84878586424     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3389     Document Type: Article

References (54)

1. Mumm, J.S. et al. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron 52, 609-621 (2006)
2. Vrieseling, E. & Arber, S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127, 1439-1452 (2006)
3. Jefferis, G.S. & Hummel, T. Wiring specificity in the olfactory system. Semin. Cell Dev. Biol. 17, 50-65 (2006)
4. Spletter, M.L. et al. Lola regulates Drosophila olfactory projection neuron identity and targeting specificity. Neural Dev. 2, 14 (2007)
5. Komiyama, T., Johnson, W., Luo, L. & Jefferis, G. From lineage to wiring specificity. POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112, 157-167 (2003)
6. Jefferis, G.S. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131, 117-130 (2004)
7. Komiyama, T., Sweeney, L., Schuldiner, O., Garcia, K. & Luo, L. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128, 399-410 (2007)
8. Sweeney, L.B. et al. Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting. Neuron 72, 734-747 (2011)
9. Zhu, H. & Luo, L. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42, 63-75 (2004)
10. Hong, W. et al. Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nat. Neurosci. 12, 1542-1550 (2009)
11. Zhu, H. et al. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat. Neurosci. 9, 349-355 (2006)
12. Hong, W., Mosca, T. & Luo, L. Teneurins instruct synaptic partner matching in an olfactory map. Nature 484, 201-207 (2012)
13. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529 (2007)
14. Cudna, R.E. & Dickson, A.J. Endoplasmic reticulum signaling as a determinant of recombinant protein expression. Biotechnol. Bioeng. 81, 56-65 (2003)
15. Schröder, M. & Kaufman, R.J. ER stress and the unfolded protein response. Mutat. Res. 569, 29-63 (2005)
16. Ryoo, H.D., Domingos, P., Kang, M. & Steller, H. Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J. 26, 242-252 (2007)
17. Souid, S., Lepesant, J. & Yanicostas, C. The xbp-1 gene is essential for development in Drosophila. Dev. Genes Evol. 217, 159-167 (2007)
18. Haecker, A. et al. Wollknauel is required for embryo patterning and encodes the Drosophila ALG5 UDP-glucose:dolichyl-phosphate glucosyltransferase. Development 135, 1745-1749 (2008)
19. Dejima, K. et al. The ortholog of human solute carrier family 35 member B1 (UDP-galactose transporter-related protein 1) is involved in maintenance of ER homeostasis and essential for larval development in Caenorhabditis elegans. FASEB J. 23, 2215-2225 (2009)
20. Chihara, T., Luginbuhl, D. & Luo, L. Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat. Neurosci. 10, 828-837 (2007)
21. Tanaka, N.K., Awasaki, T., Shimada, T. & Ito, K. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457 (2004)
22. Newsome, T.P., Asling, B. & Dickson, B. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860 (2000)
23. Kobayashi, T., Sleeman, J., Coughtrie, M. & Burchell, B. Molecular and functional characterization of microsomal UDP-glucuronic acid uptake by members of the nucleotide sugar transporter (NST) family. Biochem. J. 400, 281-289 (2006)
24. Komiyama, T., Carlson, J. & Luo, L. Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat. Neurosci. 7, 819-825 (2004
25. Khanna, M.R., Stanley, B. & Thomas, G. Towards a membrane proteome in Drosophila: a method for the isolation of plasma membrane. BMC Genomics 11, 302 (2010)
26. Papoulas, O., Hays, T. & Sisson, J. The golgin Lava lamp mediates dynein-based Golgi movements during Drosophila cellularization. Nat. Cell Biol. 7, 612-618 (2005)
27. Ishida, N. & Kawakita, M. Molecular physiology and pathology of the nucleotide sugar transporter family (SLC35). Pflugers Arch. 447, 768-775 (2004)
28. Goto, S. et al. UDP-sugar transporter implicated in glycosylation and processing of Notch. Nat. Cell Biol. 3, 816-822 (2001)
29. Lüders, F. et al. Slalom encodes an adenosine 3′-phosphate 5′-phosphosulfate transporter essential for development in Drosophila. EMBO J. 22, 3635-3644 (2003)
30. Selva, E.M. et al. Dual role of the fringe connection gene in both heparan sulphate and fringe-dependent signaling events. Nat. Cell Biol. 3, 809-815 (2001)
31. Ishikawa, H.O. et al. Two pathways for importing GDP-fucose into the endoplasmic reticulum lumen function redundantly in the O-fucosylation of Notch in Drosophila. J. Biol. Chem. 285, 4122-4129 (2010)
32. Lin, Y.R., Reddy, B. & Irvine, K. Requirement for a core 1 galactosyltransferase in the Drosophila nervous system. Dev. Dyn. 237, 3703-3714 (2008)
33. Repnikova, E. et al. Sialyltransferase regulates nervous system function in Drosophila. J. Neurosci. 30, 6466-6476 (2010)
34. Lin, X. & Perrimon, N. Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signaling. Nature 400, 281-284 (1999)
35. Takei, Y., Ozawa, Y., Sato, M., Watanabe, A. & Tabata, T. Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development 131, 73-82 (2004)
36. Kamimura, K. et al. Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J. Cell Biol. 174, 773-778 (2006)
37. Léonard, R. et al. The Drosophila fused lobes gene encodes an N-acetylglucosaminidase involved in N-glycan processing. J. Biol. Chem. 281, 4867-4875 (2006)
38. Nakanishi, H. et al. Hut1 proteins identified in Saccharomyces cerevisiae and Schizosaccharomyces pombe are functional homologues involved in the protein-folding process at the endoplasmic reticulum. Yeast 18, 543-554 (2001)
39. Hollien, J. & Weissman, J.S. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107 (2006)
40. Murray, J.I. et al. Diverse and specific gene expression responses to stresses in cultured human cells. Mol. Biol. Cell 15, 2361-2374 (2004)
41. Iwawaki, T., Akai, R., Kohno, K. & Miura, M. A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat. Med. 10, 98-102 (2004)
42. Elefant, F. & Palter, K. Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol. Biol. Cell 10, 2101-2117 (1999)
43. Iwai, Y. et al. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19, 77-89 (1997)
44. Chen, C.H. et al. A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316, 597-600 (2007)
45. Lehrman, M.A. Stimulation of N-linked glycosylation and lipid-linked oligosaccharide synthesis by stress responses in metazoan cells. Crit. Rev. Biochem. Mol. Biol. 41, 51-75 (2006)
46. Toth, J. et al. Crystal structure of an ephrin ectodomain. Dev. Cell 1, 83-92 (2001)
47. Tien, A.C. et al. Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster. J. Cell Biol. 182, 1113-1125 (2008)
48. Reyes, F. et al. The nucleotide sugar transporters AtUTr1 and AtUTr3 are required for the incorporation of UDP-glucose into the endoplasmic reticulum, are essential for pollen development and are needed for embryo sac progress in Arabidopsis thaliana. Plant J. 61, 423-435 (2010)
49. Cutforth, T. et al. Axonal ephrin-As and odorant receptors: coordinate determination of the olfactory sensory map. Cell 114, 311-322 (2003)
50. Mosca, T.J., Hong, W., Dani, V., Favaloro, V. & Luo, L. Trans-synaptic Teneurin signaling in neuromuscular synapse organization and target choice. Nature 484, 237-241 (2012)
51. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999)
52. Wu, J.S. & Luo, L. A protocol for mosaic analysis with a repressible cell marker (MARCM) in Drosophila. Nat. Protoc. 1, 2583-2589 (2006)
53. Yamamoto-Hino, M. et al. Cisterna-specific localization of glycosylation-related proteins to the Golgi apparatus. Cell Struct. Funct. 37, 55-63 (2012)
54. Bossing, T. & Brand, A. Dephrin, a transmembrane ephrin with a unique structure, prevents interneuronal axons from exiting the Drosophila embryonic CNS. Development 129, 4205-4218 (2002)