Teneurins instruct synaptic partner matching in an olfactory map

Nature

Volumn 484, Issue 7393, 2012, Pages 201-207

  Hong, Weizhe ^a   Mosca, Timothy J ^a   Luo, Liqun ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; MEMBRANE PROTEIN; PROTEIN TEN A; PROTEIN TEN M; TENEURIN; UNCLASSIFIED DRUG;

EVOLUTIONARY BIOLOGY; FLY; GENE EXPRESSION; NERVOUS SYSTEM; OLFACTORY CUE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DENDRITE; DROSOPHILA; GENETIC CONSERVATION; NERVE FIBER; NONHUMAN; OLFACTORY NERVE; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SYNAPTIC MEMBRANE;

ANIMALS; AXONS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SMELL; SYNAPSES; TENASCIN;

EID: 84859576773     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10926     Document Type: Article

References (64)

1. Sperry, R. W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl Acad. Sci. USA 50, 703-710 (1963).
2. Dickson, B. J. Molecular mechanisms ofaxon guidance. Science 298, 1959-1964 (2002).
3. Zipursky, S. L. & Sanes, J. R. Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143, 343-353 (2010).
4. Luo, L. & Flanagan, J. G. Development of continuous and discrete neural maps. Neuron 56, 284-300 (2007).
5. Komiyama, T. & Luo, L. Development of wiring specificity in the olfactory system. Curr. Opin. Neurobiol. 16, 67-73 (2006).
6. Brochtrup, A. & Hummel, T. Olfactory map formation in the Drosophila brain: genetic specificity and neuronal variability. Curr. Opin. Neurobiol. 21, 85-92 (2011).
7. Jefferis, G. S. X. E. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131, 117-130 (2003).
8. Komiyama, T., Sweeney, L. B., Schuldiner, O., Garcia, K. C. & Luo, L. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128, 399-410 (2007).
9. Hong, W. et al. Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nature Neurosci. 12, 1542-1550 (2009).
10. Hummel, T. et al. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221-231 (2004).
11. Hummel, T. & Zipursky, S. L. Afferent induction of olfactory glomeruli requires N-cadherin. Neuron 42, 77-88 (2004).
12. Sweeney, L. B. et al. Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 53, 185-200 (2007).
13. Lattemann, M. et al. Semaphorin-1a controls receptor neuron-specific axonal convergence in the primary olfactory center of Drosophila. Neuron 53, 169-184 (2007).
14. Chou, Y.-H., Zheng, X., Beachy, P. A. & Luo, L. Patterning axon targeting of olfactory receptor neurons by coupled Hedgehog signaling at two distinct steps. Cell 142, 954-966 (2010).
15. Zhu, H. et al. Dendritic patterningby Dscam and synaptic partner matching in the Drosophila antennal lobe. Nature Neurosci. 9, 349-355 (2006).
16. Kurusu, M. et al. A screen of cell-surface molecules identifies leucine-rich repeat proteins as key mediators of synaptic target selection. Neuron 59, 972-985 (2008).
17. Tucker, R. P. & Chiquet-Ehrismann, R. Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev. Biol. 290, 237-245 (2006).
18. Tucker, R. P., Kenzelmann, D., Trzebiatowska, A. & Chiquet-Ehrismann, R. Teneurins: transmembrane proteins with fundamental rolesindevelopment. Int. J. Biochem. Cell Biol. 39, 292-297 (2007).
19. Young, T. R. & Leamey, C. A. Teneurins: important regulatorsof neural circuitry. Int. J. Biochem. Cell Biol. 41, 990-993 (2009).
20. a, a Drosophila gene related to tenascin, shows selective transcript localization. Mech. Dev. 40, 165-176 (1993).
21. Baumgartner, S., Martin, D., Hagios, C. & Chiquet-Ehrismann, R. Tenm, aDrosophila gene related to tenascin, is a new pair-rule gene. EMBO J. 13, 3728-3740 (1994)
22. Psychiatric GWAS Consortium Bipolar Disorder Working Group. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nature Genet. 43, 977-983 (2011).
23. Levine, A. et al. odd Oz: a novel Drosophila pair rule gene. Cell 77, 587-598 (1994).
24. Zheng, L. et al. Drosophila Ten-m and Filamin affect motor neuron growth cone guidance. PLoS ONE 6, e22956 (2011).
25. Liebl, F. L. W. et al. Genome-wide P-element screen for Drosophila synaptogenesis mutants. J. Neurobiol. 66, 332-347 (2006).
26. Mosca, T. J., Hong, W., Dani, V. S., Favaloro, V. & Luo, L. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature http://dx.doi.org/10.1038/nature10923 (this issue).
27. Li, H., Bishop, K. M. & O'Leary, D. D. M. Potential target genesof EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning. Mol. Cell. Neurosci. 33, 136-149 (2006).
28. Rubin, B. P., Tucker, R. P., Brown-Luedi, M., Martin, D. & Chiquet-Ehrismann, R. Teneurin 2 is expressed by the neurons of the thalamofugal visual system in situ and promotes homophilic cell-cell adhesion in vitro. Development 129, 4697-4705 (2002).
29. Oohashi, T. et al. Mouse Ten-m/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues. J. Cell Biol. 145, 563-577 (1999).
30. Potter, C. J., Tasic, B., Russler, E. V., Liang, L. & Luo, L. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141, 536-548 (2010).
31. Jefferis, G. S., Marin, E. C., Stocker, R. F. & Luo, L. Target neuron prespecification in the olfactory map of Drosophila. Nature 414, 204-208 (2001).
32. Endo, K., Aoki, T., Yoda, Y., Kimura, K.-I. & Hama, C. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nature Neurosci. 10, 153-160 (2007).
33. Drescher, U. et al. Invitro guidance of retinal ganglion cell axons byRAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82, 359-370 (1995).
34. Cheng, H. J., Nakamoto, M., Bergemann, A. D. & Flanagan, J. G. Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82, 371-381 (1995).
35. Feldheim, D. A. et al. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirementinmultipleaspectsofretinocollicular mapping. Neuron 25, 563-574 (2000).
36. Yamagata, M. & Sanes, J. R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451, 465-469 (2008).
37. Shinza-Kameda, M., Takasu, E., Sakurai, K., Hayashi, S. & Nose, A. Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, Capricious. Neuron 49, 205-213 (2006).
38. Shishido, E., Takeichi, M. & Nose, A. Drosophila synapse formation: regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 280, 2118-2121 (1998).
39. de Wit, J., Hong, W., Luo, L. & Ghosh, A. Role of leucine-rich repeat proteins in the development and function of neural circuits. Annu. Rev. Cell Dev. Biol. 27, 697-729 (2011).
40. Shen, K., Fetter, R. D. & Bargmann, C. I. Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116, 869-881 (2004).
41. McLaughlin, T., Torborg, C. L., Feller, M. B. & O'Leary, D. D. M. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40, 1147-1160 (2003).
42. Pfeiffenberger, C., Yamada, J. & Feldheim, D. A. Ephrin-As and patterned retinal activity acttogether inthe developmentoftopographic mapsinthe primary visual system. J. Neurosci. 26, 12873-12884 (2006).
43. Imai, T. et al. Pre-target axon sorting establishes the neural map topography. Science 325, 585-590 (2009).
44. Serizawa, S. et al. A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127, 1057-1069 (2006).
45. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547 (2005).
46. van der Goes van Naters, W. & Carlson, J. R. Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606-612 (2007).
47. Leamey, C. A. et al. Ten-m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol. 5, e241 (2007).
48. Zhu, H. & Luo, L. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42, 63-75 (2004).
49. Kurtovic, A., Widmer, A. & Dickson, B. J. Asingle class ofolfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542-546 (2007).
50. Newsome, T. P., Asling, B. & Dickson, B. J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860 (2000).
51. Bohm, R. A. et al. A genetic mosaic approach for neural circuit mapping in Drosophila. Proc. Natl Acad. Sci. USA 107, 16378-16383 (2010).
52. Toba, G. et al. The gene search system. A method for efficient detection and rapid molecular identification of genes in Drosophila melanogaster. Genetics 151, 725-737 (1999).
53. Dietzl, G. et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156 (2007).
54. Hayashi, S. et al. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34, 58-61 (2002).
55. Fascetti, N. & Baumgartner, S. Expression of Drosophila Ten-a, a dimeric receptor during embryonic development. Mech. Dev. 114, 197-200 (2002).
56. Kinel-Tahan, Y., Weiss, H., Dgany, O., Levine, A. & Wides, R. Drosophila odz gene is requiredfor multiplecelltypesinthecompoundretina. Dev. Dyn. 236, 2541-2554 (2007).
57. Tea, J. S., Chihara, T. & Luo, L. Histone deacetylase Rpd3 regulates olfactory projection neuron dendrite targeting via the transcription factor Prospero. J. Neurosci. 30, 9939-9946 (2010).
58. Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E. & Perrimon, N. Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nature Genet. 40, 476 (2008).
59. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. & Basler, K. An optimized transgenesis system for Drosophila using germ-line-specific wC31 integrases. Proc. Natl Acad. Sci. USA 104, 3312-3317 (2007).
60. Venken, K. J. T. et al. Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nature Methods 6, 431-434 (2009).
61. Venken, K. J. T., He, Y., Hoskins, R. A. & Bellen, H. J. P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751 (2006).
62. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999).
63. Wu, J. S. & Luo, L. A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nature Protocols 1, 2110-2115 (2006).
64. Rakovitsky, N. et al. Drosophila Ten-a is a maternal pair-rule and patterning gene. Mech. Dev. 124, 911-924 (2007).