Abstract
In the olfactory system of Drosophila melanogaster, axons of olfactory receptor neurons (ORNs) and dendrites of second-order projection neurons typically target 1 of ∼50 glomeruli. Dscam, an immunoglobulin superfamily protein, acts in ORNs to regulate axon targeting. Here we show that Dscam acts in projection neurons and local interneurons to control the elaboration of dendritic fields. The removal of Dscam selectively from projection neurons or local interneurons led to clumped dendrites and marked reduction in their dendritic field size. Overexpression of Dscam in projection neurons caused dendrites to be more diffuse during development and shifted their relative position in adulthood. Notably, the positional shift of projection neuron dendrites caused a corresponding shift of its partner ORN axons, thus maintaining the connection specificity. This observation provides evidence for a pre- and postsynaptic matching mechanism independent of precise glomerular positioning.
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References
Hildebrand, J.G. & Shepherd, G.M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595–631 (1997).
Vosshall, L.B., Amrein, H., Morozov, P.S., Rzhetsky, A. & Axel, R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725–736 (1999).
Clyne, P.J. et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327–338 (1999).
Gao, Q. & Chess, A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60, 31–39 (1999).
Goldman, A.L., Van der Goes van Naters, W., Lessing, D., Warr, C.G. & Carlson, J.R. Coexpression of two functional odor receptors in one neuron. Neuron 45, 661–666 (2005).
Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical and functional organization of the Drosophila olfactory system. Curr Biol (2005).
Fishilevich, E. & Vosshall, L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553 (2005).
Vosshall, L.B., Wong, A.M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147–159 (2000).
Gao, Q., Yuan, B. & Chess, A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3, 780–785 (2000).
Marin, E.C., Jefferis, G.S.X.E., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109, 243–255 (2002).
Wong, A.M., Wang, J.W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229–241 (2002).
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).
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 112, 157–167 (2003).
Marin, E.C., Watts, R.J., Tanaka, N.K., Ito, K. & Luo, L. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132, 725–737 (2005).
Jefferis, G.S. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131, 117–130 (2004).
Zhu, H. & Luo, L. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42, 63–75 (2004).
Komiyama, T., Carlson, J.R. & Luo, L. Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat. Neurosci. 7, 819–825 (2004).
Dobritsa, A.A., van der Goes van Naters, W., Warr, C.G., Steinbrecht, R.A. & Carlson, J.R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827–841 (2003).
Wang, J.W., Wong, A.M., Flores, J., Vosshall, L.B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282 (2003).
Mombaerts, P. et al. Visualizing an olfactory sensory map. Cell 87, 675–686 (1996).
Wang, F., Nemes, A., Mendelsohn, M. & Axel, R. Odorant receptors govern the formation of a precise topographic map. Cell 93, 47–60 (1998).
Feinstein, P., Bozza, T., Rodriguez, I., Vassalli, A. & Mombaerts, P. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117, 833–846 (2004).
Schmucker, D. et al. Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671–684 (2000).
Hummel, T. et al. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221–231 (2003).
Wang, J., Zugates, C.T., Liang, I.H., Lee, C.H. & Lee, T. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33, 559–571 (2002).
Wang, J. et al. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43, 663–672 (2004).
Zhan, X.L. et al. Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron 43, 673–686 (2004).
Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461 (1999).
Stocker, R.F., Heimbeck, G., Gendre, N. & de Belle, J.S. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32, 443–456 (1997).
Wojtowicz, W.M., Flanagan, J.J., Millard, S.S., Zipursky, S.L. & Clemens, J.C. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118, 619–633 (2004).
Feinstein, P. & Mombaerts, P. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117, 817–831 (2004).
Neves, G., Zucker, J., Daly, M. & Chess, A. Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat. Genet. 36, 240–246 (2004).
Jan, Y.N. & Jan, L.Y. The control of dendrite development. Neuron 40, 229–242 (2003).
Sperry, R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50, 703–710 (1963).
Acknowledgements
We thank E. Buchner for antibodies; and T. Komiyama, C. Potter, B. Tasic, T. Clandinin and K. Shen for comments on the manuscript. H.Z. is a recipient of an individual Kirschstein National Research Service Award (NRSA) postdoctoral fellowship. L.L. and S.L.Z. are investigators of the Howard Hughes Medical Institute. This work was supported by the US National Institutes of Health (grants R01-DC005982 to L.L. and R01-DC006485 to S.L.Z.).
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Supplementary information
Supplementary Fig. 1
Dscam is expressed in PN dendrites prior to ORN axon arrival. (PDF 4238 kb)
Supplementary Fig. 2
Dscam is requried in PNs for axon branching and terminal arborization. (PDF 2922 kb)
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Zhu, H., Hummel, T., Clemens, J. et al. Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat Neurosci 9, 349–355 (2006). https://doi.org/10.1038/nn1652
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DOI: https://doi.org/10.1038/nn1652
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