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Chromatin Modulatory Proteins and Olfactory Receptor Signaling in the Refinement and Maintenance of Fruitless Expression in Olfactory Receptor Neurons.

Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC - PLoS Biol. (2016)

Bottom Line: This regulation requires the chromatin modulatory protein Alhambra (Alh).Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs.Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
During development, sensory neurons must choose identities that allow them to detect specific signals and connect with appropriate target neurons. Ultimately, these sensory neurons will successfully integrate into appropriate neural circuits to generate defined motor outputs, or behavior. This integration requires a developmental coordination between the identity of the neuron and the identity of the circuit. The mechanisms that underlie this coordination are currently unknown. Here, we describe two modes of regulation that coordinate the sensory identities of Drosophila melanogaster olfactory receptor neurons (ORNs) involved in sex-specific behaviors with the sex-specific behavioral circuit identity marker fruitless (fru). The first mode involves a developmental program that coordinately restricts to appropriate ORNs the expression of fru and two olfactory receptors (Or47b and Ir84a) involved in sex-specific behaviors. This regulation requires the chromatin modulatory protein Alhambra (Alh). The second mode relies on the signaling from the olfactory receptors through CamK and histone acetyl transferase p300/CBP to maintain ORN-specific fru expression. Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs. Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

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fru expression expands together with Or47b expression in alh mutants.(A/B) Antennae labeled with fruGAL4UAS-RedStinger (magenta), and Or47bCD8GFP (green) in wild type and alh mutant clones. Right panels represent higher magnification images. Arrows label Or47b/fru-positive nuclei in wild type images. In alh mutants, arrows point to sensilla with 2–3 Or47b ORNs that are also fru-positive. (C) Antennal lobes labeled with fruGal4 UAS-sytGFP (Z-stack, anterior sections of antennal lobe). (D) Antennal lobes labeled with fruGal4 UAS-CD8GFP (Z-stack, posterior sections of antennal lobe). Asterisks denote fru-labeled glomeruli thought to be innervated by neurons from the antennal sacculus.GENOTYPES:(A) wild type: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 fruGAL4/FRT82Gal80E2F(B) alh mutant: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 alh1353fruGAL4/FRT82Gal80E2F(C) wild type: eyFLP/+; UAS-syTGFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-syTGFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F(D) wild type: eyFLP/+; UAS-CD8GFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-CD8GFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F
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pbio.1002443.g003: fru expression expands together with Or47b expression in alh mutants.(A/B) Antennae labeled with fruGAL4UAS-RedStinger (magenta), and Or47bCD8GFP (green) in wild type and alh mutant clones. Right panels represent higher magnification images. Arrows label Or47b/fru-positive nuclei in wild type images. In alh mutants, arrows point to sensilla with 2–3 Or47b ORNs that are also fru-positive. (C) Antennal lobes labeled with fruGal4 UAS-sytGFP (Z-stack, anterior sections of antennal lobe). (D) Antennal lobes labeled with fruGal4 UAS-CD8GFP (Z-stack, posterior sections of antennal lobe). Asterisks denote fru-labeled glomeruli thought to be innervated by neurons from the antennal sacculus.GENOTYPES:(A) wild type: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 fruGAL4/FRT82Gal80E2F(B) alh mutant: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 alh1353fruGAL4/FRT82Gal80E2F(C) wild type: eyFLP/+; UAS-syTGFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-syTGFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F(D) wild type: eyFLP/+; UAS-CD8GFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-CD8GFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F

Mentions: We observed an expansion of fru expression in alh1353 mutant antennae (Fig 3). When we examined fru expression closely in alh1353 mutant ORNs, we found clusters of 2–3 fru-positive ORNs within the same sensillum, mimicking Or47b expression in the alh1353 mutants (Fig 3B). Indeed, colabeling for Or47b and fru revealed that both were coexpressed in alh mutant ORN clusters (Fig 3B). The expansion of fru expression to multiple at4 and ac4 ORNs observed in the antenna was confirmed when we examined fru-positive axon guidance in the antennal lobes of alh1353 mutants, which show a striking similarity to the expression patterns of Or47b and Ir84a in alh1353 mutants. (Fig 3C and 3D). Additional double-labeling experiments show that the innervation of the Va1d glomerulus by fru-positive axons in alh mutants is a result of the expansion of Or47b- and fru-positive axons to this location as previously found. The remaining nonclonal wild type Or88a ORNs in these mutants do not express fruitless (S4B Fig). These results suggest that fru expression accompanies Or47b and Ir84a expansion, and alh1353 disrupts a program that is normally required to corepress both Or47b/Ir84a and fru expression in inappropriate, yet developmentally related ORNs.


Chromatin Modulatory Proteins and Olfactory Receptor Signaling in the Refinement and Maintenance of Fruitless Expression in Olfactory Receptor Neurons.

Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC - PLoS Biol. (2016)

fru expression expands together with Or47b expression in alh mutants.(A/B) Antennae labeled with fruGAL4UAS-RedStinger (magenta), and Or47bCD8GFP (green) in wild type and alh mutant clones. Right panels represent higher magnification images. Arrows label Or47b/fru-positive nuclei in wild type images. In alh mutants, arrows point to sensilla with 2–3 Or47b ORNs that are also fru-positive. (C) Antennal lobes labeled with fruGal4 UAS-sytGFP (Z-stack, anterior sections of antennal lobe). (D) Antennal lobes labeled with fruGal4 UAS-CD8GFP (Z-stack, posterior sections of antennal lobe). Asterisks denote fru-labeled glomeruli thought to be innervated by neurons from the antennal sacculus.GENOTYPES:(A) wild type: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 fruGAL4/FRT82Gal80E2F(B) alh mutant: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 alh1353fruGAL4/FRT82Gal80E2F(C) wild type: eyFLP/+; UAS-syTGFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-syTGFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F(D) wild type: eyFLP/+; UAS-CD8GFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-CD8GFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F
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pbio.1002443.g003: fru expression expands together with Or47b expression in alh mutants.(A/B) Antennae labeled with fruGAL4UAS-RedStinger (magenta), and Or47bCD8GFP (green) in wild type and alh mutant clones. Right panels represent higher magnification images. Arrows label Or47b/fru-positive nuclei in wild type images. In alh mutants, arrows point to sensilla with 2–3 Or47b ORNs that are also fru-positive. (C) Antennal lobes labeled with fruGal4 UAS-sytGFP (Z-stack, anterior sections of antennal lobe). (D) Antennal lobes labeled with fruGal4 UAS-CD8GFP (Z-stack, posterior sections of antennal lobe). Asterisks denote fru-labeled glomeruli thought to be innervated by neurons from the antennal sacculus.GENOTYPES:(A) wild type: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 fruGAL4/FRT82Gal80E2F(B) alh mutant: eyFLP/+;Or47bCD8GFP/UAS-RedStinger; FRT82 alh1353fruGAL4/FRT82Gal80E2F(C) wild type: eyFLP/+; UAS-syTGFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-syTGFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F(D) wild type: eyFLP/+; UAS-CD8GFP/+; FRT82 fruGAL4/FRT82Gal80E2Falh mutant: eyFLP/+; UAS-CD8GFP/+; FRT82 alh1353fruGAL4/FRT82Gal80E2F
Mentions: We observed an expansion of fru expression in alh1353 mutant antennae (Fig 3). When we examined fru expression closely in alh1353 mutant ORNs, we found clusters of 2–3 fru-positive ORNs within the same sensillum, mimicking Or47b expression in the alh1353 mutants (Fig 3B). Indeed, colabeling for Or47b and fru revealed that both were coexpressed in alh mutant ORN clusters (Fig 3B). The expansion of fru expression to multiple at4 and ac4 ORNs observed in the antenna was confirmed when we examined fru-positive axon guidance in the antennal lobes of alh1353 mutants, which show a striking similarity to the expression patterns of Or47b and Ir84a in alh1353 mutants. (Fig 3C and 3D). Additional double-labeling experiments show that the innervation of the Va1d glomerulus by fru-positive axons in alh mutants is a result of the expansion of Or47b- and fru-positive axons to this location as previously found. The remaining nonclonal wild type Or88a ORNs in these mutants do not express fruitless (S4B Fig). These results suggest that fru expression accompanies Or47b and Ir84a expansion, and alh1353 disrupts a program that is normally required to corepress both Or47b/Ir84a and fru expression in inappropriate, yet developmentally related ORNs.

Bottom Line: This regulation requires the chromatin modulatory protein Alhambra (Alh).Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs.Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
During development, sensory neurons must choose identities that allow them to detect specific signals and connect with appropriate target neurons. Ultimately, these sensory neurons will successfully integrate into appropriate neural circuits to generate defined motor outputs, or behavior. This integration requires a developmental coordination between the identity of the neuron and the identity of the circuit. The mechanisms that underlie this coordination are currently unknown. Here, we describe two modes of regulation that coordinate the sensory identities of Drosophila melanogaster olfactory receptor neurons (ORNs) involved in sex-specific behaviors with the sex-specific behavioral circuit identity marker fruitless (fru). The first mode involves a developmental program that coordinately restricts to appropriate ORNs the expression of fru and two olfactory receptors (Or47b and Ir84a) involved in sex-specific behaviors. This regulation requires the chromatin modulatory protein Alhambra (Alh). The second mode relies on the signaling from the olfactory receptors through CamK and histone acetyl transferase p300/CBP to maintain ORN-specific fru expression. Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs. Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

Show MeSH