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Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions

Nature Neuroscience volume 7, pages 819–825 (2004)Cite this article

Abstract

From insects to mammals, olfactory receptor neurons (ORNs) expressing a common olfactory receptor target their axons to specific glomeruli with high precision. Here we show in Drosophila that the POU transcription factor Acj6 controls the axon targeting specificity of a subset of ORN classes, as defined by the olfactory receptors that they express. Of these classes, some require Acj6 cell-autonomously, whereas others require Acj6 cell-nonautonomously. Mosaic analyses show that cooperative targeting occurs between axon terminals of the same ORN classes and that there are hierarchical interactions among different ORN classes. We propose that the precision of ORN axon targeting derives from both intrinsic transcriptional control and extensive axon-axon interactions.

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Figure 1: Acj6 is expressed in developing ORNs.
Figure 2: Some OR-Gal4 drivers are not expressed in acj6 mutant ORNs.
Figure 3: Some ORN classes do not require Acj6 for axon targeting.
Figure 4: Some ORN classes require Acj6 cell-autonomously for axon targeting.
Figure 5: Some ORN classes require Acj6 cell-nonautonomously for axon targeting.
Figure 6: Quantitative analysis of mistargeting defects in eyFlp MARCM.

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Acknowledgements

We thank L. Vosshall, K. Scott, C. Warr, A. Goldman, C. Miller, D. Lessing, A. Ray and R. Ignell for the OR-Gal4 drivers; E. Buchner for antibodies; and T. Clandinin, K. Shen and members of the Luo laboratory for comments on the manuscript. This work was supported by grants from the US National Institutes of Health (to L.L. and J.R.C.).

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Authors and Affiliations

  1. Department of Biological Sciences & Neurosciences Program, Stanford University, Stanford, 94305, California, USA

    Takaki Komiyama & Liqun Luo

  2. Department of Molecular, Cellular & Developmental Biology, Yale University, New Haven, 06520, Connecticut, USA

    John R Carlson

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Correspondence to Liqun Luo.

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Supplementary information

Supplementary Fig. 1

Drifter is not expressed in most developing ORNs. (a, b, c) Drifter is not expressed in the developing 3rd antennal segment (outlined in a3-c3) at 18 (a), 24 (b) and 50 (c) hour APF. (d, e) At both 50 (d) and 72 (e) hour APF, Drifter is expressed in the developing maxillary palp (outlined in d3 and e3), but mostly in Elav-negative cells. (JPG 155 kb)

Supplementary Fig. 2

Normal targeting of ipsi- and contralateral targeting of Or47b and 88a axons in acj6 heterozygous control and hemizygous mutant. The right antenna was excised and brains were dissected 10 days later. (JPG 119 kb)

Supplementary Fig. 3

Mistargeting studied using a presynaptic marker n-syb-GFP. Targeting defects of acj6 hemizygous mutants revealed by n-syb-GFP are similar to those observed using a membrane marker mCD8-GFP (Figs. 4&5). (JPG 79 kb)

Supplementary Fig. 4

ORN axons of the same class do not show extensive fasciculation prior to glomerular targeting. Arrows indicate non-fasciculated axons. (JPG 176 kb)

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Komiyama, T., Carlson, J. & Luo, L. Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat Neurosci 7, 819–825 (2004). https://doi.org/10.1038/nn1284

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