Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting

Neuron

Volumn 72, Issue 5, 2011, Pages 734-747

  Sweeney, Lora B ^a,c   Chou, Ya Hui ^a,d   Wu, Zhuhao ^a,b   Joo, William ^a   Komiyama, Takaki ^a,e   Potter, Christopher J ^a,b   Kolodkin, Alex L ^a,b   Garcia, K Christopher ^a   Luo, Liqun ^a  

^a STANFORD UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN SEMA 1A; PROTEIN SEMA 2A; PROTEIN SEMA 2B; SEMAPHORIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTENNA (ORGAN); ARTHROPOD LARVA; ARTICLE; ASSOCIATION; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITE; DROSOPHILA; NERVE CELL DEGENERATION; NERVE PROJECTION; NONHUMAN; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TARGETING;

ABLATION TECHNIQUES; AGE FACTORS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; DENDRITES; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MUTATION; NERVE DEGENERATION; NERVE TISSUE PROTEINS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PROTEIN BINDING; SEMAPHORINS;

EID: 83255194575     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.09.026     Document Type: Article

References (39)

1. Ayoob J.C., Terman J.R., Kolodkin A.L. Drosophila Plexin B is a Sema-2a receptor required for axon guidance. Development 2006, 133:2125-2135.
2. Berdnik D., Chihara T., Couto A., Luo L. Wiring stability of the adult Drosophila olfactory circuit after lesion. J. Neurosci. 2006, 26:3367-3376.
3. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
4. Cafferty P., Yu L., Long H., Rao Y. Semaphorin-1a functions as a guidance receptor in the Drosophila visual system. J. Neurosci. 2006, 26:3999-4003.
5. 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 1995, 82:371-381.
6. Drescher U., Kremoser C., Handwerker C., Loschinger J., Noda M., Bonhoeffer F. In vitro guidance of a retinal ganglion cell axons by RAGS, a 25kDa tectal protein related to ligands for Eph receptor tyrosine kinase. Cell 1995, 82:369-370.
7. Han D.D., Stein D., Stevens L.M. Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. Development 2000, 127:573-583.
8. Hong W., Zhu H., Potter C.J., Barsh G., Kurusu M., Zinn K., Luo L. Leucine-rich repeat transmembrane proteins instruct discrete dendrite targeting in an olfactory map. Nat. Neurosci. 2009, 12:1542-1550.
9. Imai T., Yamazaki T., Kobayakawa R., Kobayakawa K., Abe T., Suzuki M., Sakano H. Pre-target axon sorting establishes the neural map topography. Science 2009, 325:585-590.
10. Janssen B.J., Robinson R.A., Pérez-Brangulí F., Bell C.H., Mitchell K.J., Siebold C., Jones E.Y. Structural basis of semaphorin-plexin signalling. Nature 2010, 467:1118-1122.
11. Jefferis G.S., Marin E.C., Stocker R.F., Luo L. Target neuron prespecification in the olfactory map of Drosophila. Nature 2001, 414:204-208.
12. Jefferis G.S.X.E., Vyas R.M., Berdnik D., Ramaekers A., Stocker R.F., Tanaka N.K., Ito K., Luo L. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 2004, 131:117-130.
13. Kaneko-Goto T., Yoshihara S.-I., Miyazaki H., Yoshihara Y. BIG-2 mediates olfactory axon convergence to target glomeruli. Neuron 2008, 57:834-846.
14. Kolodkin A.L., Matthes D.J., Goodman C.S. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993, 75:1389-1399.
15. Komiyama T., Johnson W.A., Luo L., Jefferis G.S. From lineage to wiring specificity. POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 2003, 112:157-167.
16. 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 2007, 128:399-410.
17. Larsson M.C., Domingos A.I., Jones W.D., Chiappe M.E., Amrein H., Vosshall L.B. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004, 43:703-714.
18. Lee T., Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999, 22:451-461.
19. Liu H., Juo Z.S., Shim A.H., Focia P.J., Chen X., Garcia K.C., He X. Structural basis of semaphorin-plexin recognition and viral mimicry from Sema7A and A39R complexes with PlexinC1. Cell 2010, 142:749-761.
20. Luo L., O'Leary D.D. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 2005, 28:127-156.
21. Luo L., Flanagan J.G. Development of continuous and discrete neural maps. Neuron 2007, 56:284-300.
22. Marin E.C., Watts R.J., Tanaka N.K., Ito K., Luo L. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 2005, 132:725-737.
23. McGuire S.E., Le P.T., Osborn A.J., Matsumoto K., Davis R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003, 302:1765-1768.
24. Nogi T., Yasui N., Mihara E., Matsunaga Y., Noda M., Yamashita N., Toyofuku T., Uchiyama S., Goshima Y., Kumanogoh A., Takagi J. Structural basis for semaphorin signalling through the plexin receptor. Nature 2010, 467:1123-1127.
25. 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 2010, 141:536-548.
26. Sanes J.R., Lichtman J.W. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 1999, 22:389-442.
27. Serizawa S., Miyamichi K., Takeuchi H., Yamagishi Y., Suzuki M., Sakano H. A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 2006, 127:1057-1069.
28. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell 1992, 68:201-219.
29. Stocker R.F. Design of the larval chemosensory system. Adv. Exp. Med. Biol. 2008, 628:69-81.
30. Sweeney L.B., Couto A., Chou Y.-H., Berdnik D., Dickson B.J., Luo L., Komiyama T. Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 2007, 53:185-200.
31. Takeuchi H., Inokuchi K., Aoki M., Suto F., Tsuboi A., Matsuda I., Suzuki M., Aiba A., Serizawa S., Yoshihara Y., et al. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 2010, 141:1056-1067.
32. Terman J.R., Mao T., Pasterkamp R.J., Yu H.H., Kolodkin A.L. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 2002, 109:887-900.
33. Thibault S.T., Singer M.A., Miyazaki W.Y., Milash B., Dompe N.A., Singh C.M., Buchholz R., Demsky M., Fawcett R., Francis-Lang H.L., et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 2004, 36:283-287.
34. Tran T.S., Kolodkin A.L., Bharadwaj R. Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 2007, 23:263-292.
35. Winberg M.L., Mitchell K.J., Goodman C.S. Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 1998, 93:581-591.
36. Winberg M.L., Noordermeer J.N., Tamagnone L., Comoglio P.M., Spriggs M.K., Tessier-Lavigne M., Goodman C.S. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 1998, 95:903-916.
37. Wu Z., Sweeney L.B., Ayoob J.C., Chak K., Andreone B.J., Ohyama T., Kerr R., Luo L., Zlatic M., Kolodkin A.L. A combinatorial semaphorin code instructs the initial steps of sensory circuit assembly in the Drosophila CNS. Neuron 2011, 70:281-298.
38. Yu H.H., Araj H.H., Ralls S.A., Kolodkin A.L. The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 1998, 20:207-220.
39. Zhu S., Lin S., Kao C.F., Awasaki T., Chiang A.S., Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006, 127:409-422.