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Orthodenticle Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Drosophila Retina.

Mencarelli C, Pichaud F - PLoS Genet. (2015)

Bottom Line: Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo).In addition, we find that otd regulates synaptic-layer targeting of R8.Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

View Article: PubMed Central - PubMed

Affiliation: MRC Laboratory for Molecular Cell Biology, University College London, London, United Kingdom.

ABSTRACT
Parallel processing of neuronal inputs relies on assembling neural circuits into distinct synaptic-columns and layers. This is orchestrated by matching recognition molecules between afferent growth cones and target areas. Controlling the expression of these molecules during development is crucial but not well understood. The developing Drosophila visual system is a powerful genetic model for addressing this question. In this model system, the achromatic R1-6 photoreceptors project their axons in the lamina while the R7 and R8 photoreceptors, which are involved in colour detection, project their axons to two distinct synaptic-layers in the medulla. Here we show that the conserved homeodomain transcription factor Orthodenticle (Otd), which in the eye is a main regulator of rhodopsin expression, is also required for R1-6 photoreceptor synaptic-column specific innervation of the lamina. Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo). In addition, we find that otd regulates synaptic-layer targeting of R8. We demonstrate that during this process, otd and the R8-specific transcription factor senseless/Gfi1 (sens) function as independent transcriptional inputs that are required for the expression of fmi, gogo and the adhesion molecule capricious (caps), which govern R8 synaptic-layer targeting. Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

No MeSH data available.


Related in: MedlinePlus

Transcriptional inputs required for proper photoreceptor targeting in the Drosophila visual system.Summary of the transcription factors that regulate column- and layer-specific targeting of the R1-6 and R7 and R8 photoreceptors. Predicted indirect regulation is shown with a double arrowhead (Sens binds directly on the caps promoter). Although all of the currently known transcriptional regulators (i.e., seq, sens and otd) are presented, for clarity, only those CAMs and adhesion molecules most relevant to our findings are shown here.
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pgen.1005303.g007: Transcriptional inputs required for proper photoreceptor targeting in the Drosophila visual system.Summary of the transcription factors that regulate column- and layer-specific targeting of the R1-6 and R7 and R8 photoreceptors. Predicted indirect regulation is shown with a double arrowhead (Sens binds directly on the caps promoter). Although all of the currently known transcriptional regulators (i.e., seq, sens and otd) are presented, for clarity, only those CAMs and adhesion molecules most relevant to our findings are shown here.

Mentions: Little is known about the transcriptional regulation that controls the establishment of genetically hardwired patterns of synaptic connections during development. The factors and molecular pathways that govern the establishment of the typical pattern of R1-6 connectivity in the lamina have yet to be fully characterized. During neural superposition in the main part of the retina, each lamina column is innervated by axons coming from at least six neighbouring facets (i.e., one axon per facet is contributed to one synaptic-column) (Fig 1B). Although the CAMs and recognition molecules NCad, Fmi, Gogo and LAR have been shown to regulate this process, very little is known about the upstream transcriptional regulatory gene networks that control the expression of these molecules. Here we identify otd as a transcription factor required for synaptic-column targeting of R1-6 in the fly visual system (Fig 7). We show that in the developing retina, this phenotype correlates with a significant downregulation of fmi and gogo, and that re-introducing these genes in otd mutant R1-6 can ameliorate the lamina column innervation defects observed in otduvi mutant retinae. This indicates that otd function is required in R1-6 to promote the expression of optimal levels of these key factors to control lamina synaptic-column targeting. Our finding that the expression of NCad or LAR are not affected by the loss of otd suggests that additional independent transcriptional inputs are likely to operate in R1-6 during synaptic-column innervation.


Orthodenticle Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Drosophila Retina.

Mencarelli C, Pichaud F - PLoS Genet. (2015)

Transcriptional inputs required for proper photoreceptor targeting in the Drosophila visual system.Summary of the transcription factors that regulate column- and layer-specific targeting of the R1-6 and R7 and R8 photoreceptors. Predicted indirect regulation is shown with a double arrowhead (Sens binds directly on the caps promoter). Although all of the currently known transcriptional regulators (i.e., seq, sens and otd) are presented, for clarity, only those CAMs and adhesion molecules most relevant to our findings are shown here.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482733&req=5

pgen.1005303.g007: Transcriptional inputs required for proper photoreceptor targeting in the Drosophila visual system.Summary of the transcription factors that regulate column- and layer-specific targeting of the R1-6 and R7 and R8 photoreceptors. Predicted indirect regulation is shown with a double arrowhead (Sens binds directly on the caps promoter). Although all of the currently known transcriptional regulators (i.e., seq, sens and otd) are presented, for clarity, only those CAMs and adhesion molecules most relevant to our findings are shown here.
Mentions: Little is known about the transcriptional regulation that controls the establishment of genetically hardwired patterns of synaptic connections during development. The factors and molecular pathways that govern the establishment of the typical pattern of R1-6 connectivity in the lamina have yet to be fully characterized. During neural superposition in the main part of the retina, each lamina column is innervated by axons coming from at least six neighbouring facets (i.e., one axon per facet is contributed to one synaptic-column) (Fig 1B). Although the CAMs and recognition molecules NCad, Fmi, Gogo and LAR have been shown to regulate this process, very little is known about the upstream transcriptional regulatory gene networks that control the expression of these molecules. Here we identify otd as a transcription factor required for synaptic-column targeting of R1-6 in the fly visual system (Fig 7). We show that in the developing retina, this phenotype correlates with a significant downregulation of fmi and gogo, and that re-introducing these genes in otd mutant R1-6 can ameliorate the lamina column innervation defects observed in otduvi mutant retinae. This indicates that otd function is required in R1-6 to promote the expression of optimal levels of these key factors to control lamina synaptic-column targeting. Our finding that the expression of NCad or LAR are not affected by the loss of otd suggests that additional independent transcriptional inputs are likely to operate in R1-6 during synaptic-column innervation.

Bottom Line: Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo).In addition, we find that otd regulates synaptic-layer targeting of R8.Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

View Article: PubMed Central - PubMed

Affiliation: MRC Laboratory for Molecular Cell Biology, University College London, London, United Kingdom.

ABSTRACT
Parallel processing of neuronal inputs relies on assembling neural circuits into distinct synaptic-columns and layers. This is orchestrated by matching recognition molecules between afferent growth cones and target areas. Controlling the expression of these molecules during development is crucial but not well understood. The developing Drosophila visual system is a powerful genetic model for addressing this question. In this model system, the achromatic R1-6 photoreceptors project their axons in the lamina while the R7 and R8 photoreceptors, which are involved in colour detection, project their axons to two distinct synaptic-layers in the medulla. Here we show that the conserved homeodomain transcription factor Orthodenticle (Otd), which in the eye is a main regulator of rhodopsin expression, is also required for R1-6 photoreceptor synaptic-column specific innervation of the lamina. Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo). In addition, we find that otd regulates synaptic-layer targeting of R8. We demonstrate that during this process, otd and the R8-specific transcription factor senseless/Gfi1 (sens) function as independent transcriptional inputs that are required for the expression of fmi, gogo and the adhesion molecule capricious (caps), which govern R8 synaptic-layer targeting. Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

No MeSH data available.


Related in: MedlinePlus