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Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis.

Zlatic M, Li F, Strigini M, Grueber W, Bate M - PLoS Biol. (2009)

Bottom Line: The range of alternative targets is reduced by well organised patterns of growth, termination, and branching that deliver the terminals of appropriate pre- and postsynaptic partners to restricted volumes of the developing nervous system.We show that a combination of Plexin A (Plex A) and Plexin B (Plex B) receptors specifies the ventral projection of sensory neurons by responding to high concentrations of Semaphorin 1a (Sema 1a) and Semaphorin 2a (Sema 2a).Together our findings support the idea that axons are delivered to particular regions of the neuropile by their responses to systems of positional cues in each dimension.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom. zlaticm@janelia.hhmi.org

ABSTRACT
During the development of neural circuitry, neurons of different kinds establish specific synaptic connections by selecting appropriate targets from large numbers of alternatives. The range of alternative targets is reduced by well organised patterns of growth, termination, and branching that deliver the terminals of appropriate pre- and postsynaptic partners to restricted volumes of the developing nervous system. We use the axons of embryonic Drosophila sensory neurons as a model system in which to study the way in which growing neurons are guided to terminate in specific volumes of the developing nervous system. The mediolateral positions of sensory arbors are controlled by the response of Robo receptors to a Slit gradient. Here we make a genetic analysis of factors regulating position in the dorso-ventral axis. We find that dorso-ventral layers of neuropile contain different levels and combinations of Semaphorins. We demonstrate the existence of a central to dorsal and central to ventral gradient of Sema 2a, perpendicular to the Slit gradient. We show that a combination of Plexin A (Plex A) and Plexin B (Plex B) receptors specifies the ventral projection of sensory neurons by responding to high concentrations of Semaphorin 1a (Sema 1a) and Semaphorin 2a (Sema 2a). Together our findings support the idea that axons are delivered to particular regions of the neuropile by their responses to systems of positional cues in each dimension.

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Class IV md neurons terminate in a neuropile region with low levels of Sema 1a and Sema 2a.Immunofluorescence visualisation of Sema 2a (A) and Sema 1a (B and C)) (green) with respect to ppk-EGFP (red), in the CNS at 13 (A and B) or 21 (C)-h AEL. Images show projections of a confocal z series of transverse sections through A7. (A) Class IV axon terminals are in a region of low Sema 2a levels. (B and C) Class IV axons, grow to ventral-most neuropile, where Sema 1a levels are lowest. Class IV terminals are just beneath regions of higher Sema1a expression levels in layer 3 at both 13 (B) and 21 (C)-h AEL. Note that neither Sema 1a nor Sema 2a is expressed at high levels in most lateral regions of neuropile, thus providing a potential corridor for axons to grow from their entry points to more ventral neuropile regions. Dorsal up. Arrowheads show midline. Magenta lines, neuropile outlines. Scale bar: 5 µm.
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pbio-1000135-g004: Class IV md neurons terminate in a neuropile region with low levels of Sema 1a and Sema 2a.Immunofluorescence visualisation of Sema 2a (A) and Sema 1a (B and C)) (green) with respect to ppk-EGFP (red), in the CNS at 13 (A and B) or 21 (C)-h AEL. Images show projections of a confocal z series of transverse sections through A7. (A) Class IV axon terminals are in a region of low Sema 2a levels. (B and C) Class IV axons, grow to ventral-most neuropile, where Sema 1a levels are lowest. Class IV terminals are just beneath regions of higher Sema1a expression levels in layer 3 at both 13 (B) and 21 (C)-h AEL. Note that neither Sema 1a nor Sema 2a is expressed at high levels in most lateral regions of neuropile, thus providing a potential corridor for axons to grow from their entry points to more ventral neuropile regions. Dorsal up. Arrowheads show midline. Magenta lines, neuropile outlines. Scale bar: 5 µm.

Mentions: By examining the location of these ppkEGFP-expressing axons with respect to Sema expression we confirmed that at 13-h AEL these axons terminate in a region of low Sema 2a (Figure 4A) and just below regions of high Sema 1a expression levels (Figure 4B). At 21-h AEL the class IV terminals remain in a region with low Sema 1a expression (Figure 4C).


Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis.

Zlatic M, Li F, Strigini M, Grueber W, Bate M - PLoS Biol. (2009)

Class IV md neurons terminate in a neuropile region with low levels of Sema 1a and Sema 2a.Immunofluorescence visualisation of Sema 2a (A) and Sema 1a (B and C)) (green) with respect to ppk-EGFP (red), in the CNS at 13 (A and B) or 21 (C)-h AEL. Images show projections of a confocal z series of transverse sections through A7. (A) Class IV axon terminals are in a region of low Sema 2a levels. (B and C) Class IV axons, grow to ventral-most neuropile, where Sema 1a levels are lowest. Class IV terminals are just beneath regions of higher Sema1a expression levels in layer 3 at both 13 (B) and 21 (C)-h AEL. Note that neither Sema 1a nor Sema 2a is expressed at high levels in most lateral regions of neuropile, thus providing a potential corridor for axons to grow from their entry points to more ventral neuropile regions. Dorsal up. Arrowheads show midline. Magenta lines, neuropile outlines. Scale bar: 5 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2690435&req=5

pbio-1000135-g004: Class IV md neurons terminate in a neuropile region with low levels of Sema 1a and Sema 2a.Immunofluorescence visualisation of Sema 2a (A) and Sema 1a (B and C)) (green) with respect to ppk-EGFP (red), in the CNS at 13 (A and B) or 21 (C)-h AEL. Images show projections of a confocal z series of transverse sections through A7. (A) Class IV axon terminals are in a region of low Sema 2a levels. (B and C) Class IV axons, grow to ventral-most neuropile, where Sema 1a levels are lowest. Class IV terminals are just beneath regions of higher Sema1a expression levels in layer 3 at both 13 (B) and 21 (C)-h AEL. Note that neither Sema 1a nor Sema 2a is expressed at high levels in most lateral regions of neuropile, thus providing a potential corridor for axons to grow from their entry points to more ventral neuropile regions. Dorsal up. Arrowheads show midline. Magenta lines, neuropile outlines. Scale bar: 5 µm.
Mentions: By examining the location of these ppkEGFP-expressing axons with respect to Sema expression we confirmed that at 13-h AEL these axons terminate in a region of low Sema 2a (Figure 4A) and just below regions of high Sema 1a expression levels (Figure 4B). At 21-h AEL the class IV terminals remain in a region with low Sema 1a expression (Figure 4C).

Bottom Line: The range of alternative targets is reduced by well organised patterns of growth, termination, and branching that deliver the terminals of appropriate pre- and postsynaptic partners to restricted volumes of the developing nervous system.We show that a combination of Plexin A (Plex A) and Plexin B (Plex B) receptors specifies the ventral projection of sensory neurons by responding to high concentrations of Semaphorin 1a (Sema 1a) and Semaphorin 2a (Sema 2a).Together our findings support the idea that axons are delivered to particular regions of the neuropile by their responses to systems of positional cues in each dimension.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom. zlaticm@janelia.hhmi.org

ABSTRACT
During the development of neural circuitry, neurons of different kinds establish specific synaptic connections by selecting appropriate targets from large numbers of alternatives. The range of alternative targets is reduced by well organised patterns of growth, termination, and branching that deliver the terminals of appropriate pre- and postsynaptic partners to restricted volumes of the developing nervous system. We use the axons of embryonic Drosophila sensory neurons as a model system in which to study the way in which growing neurons are guided to terminate in specific volumes of the developing nervous system. The mediolateral positions of sensory arbors are controlled by the response of Robo receptors to a Slit gradient. Here we make a genetic analysis of factors regulating position in the dorso-ventral axis. We find that dorso-ventral layers of neuropile contain different levels and combinations of Semaphorins. We demonstrate the existence of a central to dorsal and central to ventral gradient of Sema 2a, perpendicular to the Slit gradient. We show that a combination of Plexin A (Plex A) and Plexin B (Plex B) receptors specifies the ventral projection of sensory neurons by responding to high concentrations of Semaphorin 1a (Sema 1a) and Semaphorin 2a (Sema 2a). Together our findings support the idea that axons are delivered to particular regions of the neuropile by their responses to systems of positional cues in each dimension.

Show MeSH