Multiple Interactions Control Synaptic Layer Specificity in the Drosophila Visual System

Neuron

Volumn 77, Issue 2, 2013, Pages 299-310

  Pecot, Matthew Y ^a   Tadros, Wael ^a   Nern, Aljoscha ^b   Bader, Maya ^a   Chen, Yi ^a   Zipursky, S Lawrence ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NERVE CELL ADHESION MOLECULE; PLEXIN; PLEXIN A; SEMAPHORIN; SEMAPHORIN 1A; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; GROWTH CONE; MEDULLA OBLONGATA; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA INTERFERENCE; SYNAPSE; VISUAL SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL COMMUNICATION; DROSOPHILA; DROSOPHILA PROTEINS; GROWTH CONES; MEDULLA OBLONGATA; PROTEIN INTERACTION MAPPING; SYNAPSES; VISUAL PATHWAYS;

EID: 84872718788     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.11.007     Document Type: Article

References (37)

1. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
2. 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.
3. Clandinin T.R., Lee C.H., Herman T., Lee R.C., Yang A.Y., Ovasapyan S., Zipursky S.L. Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 2001, 32:237-248.
4. 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.
5. Godenschwege T.A., Hu H., Shan-Crofts X., Goodman C.S., Murphey R.K. Bi-directional signaling by Semaphorin 1a during central synapse formation in Drosophila. Nat. Neurosci. 2002, 5:1294-1301.
6. Honjo M., Tanihara H., Suzuki S., Tanaka T., Honda Y., Takeichi M. Differential expression of cadherin adhesion receptors in neural retina of the postnatal mouse. Invest. Ophthalmol. Vis. Sci. 2000, 41:546-551.
7. Iwai Y., Usui T., Hirano S., Steward R., Takeichi M., Uemura T. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 1997, 19:77-89.
8. Fischbach K.F., Dittrich A.P.M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 1989, 258:441-475.
9. 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.
10. Kurusu M., Cording A., Taniguchi M., Menon K., Suzuki E., Zinn K. A screen of cell-surface molecules identifies leucine-rich repeat proteins as key mediators of synaptic target selection. Neuron 2008, 59:972-985.
11. Lai S.L., Lee T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 2006, 9:703-709.
12. Lee T., Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 2001, 24:251-254.
13. Lee C.H., Herman T., Clandinin T.R., Lee R., Zipursky S.L. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 2001, 30:437-450.
14. Matsuoka R.L., Nguyen-Ba-Charvet K.T., Parray A., Badea T.C., Chédotal A., Kolodkin A.L. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature 2011, 470:259-263.
15. Maurel-Zaffran C., Suzuki T., Gahmon G., Treisman J.E., Dickson B.J. Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 2001, 32:225-235.
16. Millard S.S., Flanagan J.J., Pappu K.S., Wu W., Zipursky S.L. Dscam2 mediates axonal tiling in the Drosophila visual system. Nature 2007, 447:720-724.
17. Nern A., Zhu Y., Zipursky S.L. Local N-cadherin interactions mediate distinct steps in the targeting of lamina neurons. Neuron 2008, 58:34-41.
18. Newsome T.P., Asling B., Dickson B.J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 2000, 127:851-860.
19. Pfeiffer B.D., Ngo T.T., Hibbard K.L., Murphy C., Jenett A., Truman J.W., Rubin G.M. Refinement of tools for targeted gene expression in Drosophila. Genetics 2010, 186:735-755.
20. Prakash S., Caldwell J.C., Eberl D.F., Clandinin T.R. Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets. Nat. Neurosci. 2005, 8:443-450.
21. Sanes J.R., Zipursky S.L. Design principles of insect and vertebrate visual systems. Neuron 2010, 66:15-36.
22. 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 2006, 49:205-213.
23. Struhl G., Basler K. Organizing activity of wingless protein in Drosophila. Cell 1993, 72:527-540.
24. 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.
25. Tang W., Ehrlich I., Wolff S.B., Michalski A.M., Wölfl S., Hasan M.T., Lüthi A., Sprengel R. Faithful expression of multiple proteins via 2A-peptide self-processing: a versatile and reliable method for manipulating brain circuits. J. Neurosci. 2009, 29:8621-8629.
26. Timofeev K., Joly W., Hadjieconomou D., Salecker I. Localized netrins act as positional cues to control layer-specific targeting of photoreceptor axons in Drosophila. Neuron 2012, 75:80-93.
27. Ting C.Y., Yonekura S., Chung P., Hsu S.N., Robertson H.M., Chiba A., Lee C.H. Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. Development 2005, 132:953-963.
28. Tomaselli K.J., Neugebauer K.M., Bixby J.L., Lilien J., Reichardt L.F. N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1988, 1:33-43.
29. Toyofuku T., Zhang H., Kumanogoh A., Takegahara N., Yabuki M., Harada K., Hori M., Kikutani H. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. Nat. Cell Biol. 2004, 6:1204-1211.
30. Venken K.J., Carlson J.W., Schulze K.L., Pan H., He Y., Spokony R., Wan K.H., Koriabine M., de Jong P.J., White K.P., et al. Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat. Methods 2009, 6:431-434.
31. Venken K.J., Schulze K.L., Haelterman N.A., Pan H., He Y., Evans-Holm M., Carlson J.W., Levis R.W., Spradling A.C., Hoskins R.A., Bellen H.J. MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes. Nat. Methods 2011, 8:737-743.
32. 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.
33. 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.
34. 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.
35. Yu L., Zhou Y., Cheng S., Rao Y. Plexin a-semaphorin-1a reverse signaling regulates photoreceptor axon guidance in Drosophila. J. Neurosci. 2010, 30:12151-12156.
36. Zipursky S.L., Venkatesh T.R., Teplow D.B., Benzer S. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 1984, 36:15-26.
37. Zlatic M., Li F., Strigini M., Grueber W., Bate M. Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis. PLoS Biol. 2009, 7:e1000135.