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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 in adult Or47b ORNs requires Or47b function.(A) Heterozygous Or47b mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous Or47b mutant antennae (3–5 d old). (C) Overexpression of UAS-Or47b under the control of fruGal4 in Or47b mutants (14 d old). (D) Overexpression of UAS-Or88a under the control of fruGal4 in Or47b mutants (14 d old).GENOTYPES:A–A”: Or47b-CD2 Or47b2/+;fruGAL4UAS-40XCD8GFP/+B–B”: Or47b-CD2 Or47b2/or47b2;fruGAL4UAS-40XCD8GFP/+C: Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or47bD: Or47b-CD2 Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or88a
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pbio.1002443.g005: fru expression in adult Or47b ORNs requires Or47b function.(A) Heterozygous Or47b mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous Or47b mutant antennae (3–5 d old). (C) Overexpression of UAS-Or47b under the control of fruGal4 in Or47b mutants (14 d old). (D) Overexpression of UAS-Or88a under the control of fruGal4 in Or47b mutants (14 d old).GENOTYPES:A–A”: Or47b-CD2 Or47b2/+;fruGAL4UAS-40XCD8GFP/+B–B”: Or47b-CD2 Or47b2/or47b2;fruGAL4UAS-40XCD8GFP/+C: Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or47bD: Or47b-CD2 Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or88a

Mentions: To test this hypothesis, we first asked whether Fru regulates Or47b expression in Or47b ORNs. However, we found that Or47b expression is unaffected in fru mutants, suggesting that Fru does not regulate Or47b expression (S7 Fig). We then examined fru expression in the absence of Or47b function. Surprisingly, we observed that fru expression in Or47b ORNs is abolished in Or47b mutants, (Fig 5B). This finding was confirmed by qRT-PCR (S8 Fig). This phenotype could be rescued by the expression of a UAS-Or47b transgene driven with fruGAL4 (Fig 5C). The expression of UAS-Or88a, a closely related receptor that detects similar ligands to Or47b [17] was partially able to rescue fru expression. This indicates a requirement for the function of ORs activated by the same ligand in fru regulation (Fig 5D and 5D’ and S11 Fig). Expression of Or67d, the third fru-expressing Or gene, which detects cVA, was not able to rescue fru expression in Or47b ORNs (S9D Fig).


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 in adult Or47b ORNs requires Or47b function.(A) Heterozygous Or47b mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous Or47b mutant antennae (3–5 d old). (C) Overexpression of UAS-Or47b under the control of fruGal4 in Or47b mutants (14 d old). (D) Overexpression of UAS-Or88a under the control of fruGal4 in Or47b mutants (14 d old).GENOTYPES:A–A”: Or47b-CD2 Or47b2/+;fruGAL4UAS-40XCD8GFP/+B–B”: Or47b-CD2 Or47b2/or47b2;fruGAL4UAS-40XCD8GFP/+C: Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or47bD: Or47b-CD2 Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or88a
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4836687&req=5

pbio.1002443.g005: fru expression in adult Or47b ORNs requires Or47b function.(A) Heterozygous Or47b mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous Or47b mutant antennae (3–5 d old). (C) Overexpression of UAS-Or47b under the control of fruGal4 in Or47b mutants (14 d old). (D) Overexpression of UAS-Or88a under the control of fruGal4 in Or47b mutants (14 d old).GENOTYPES:A–A”: Or47b-CD2 Or47b2/+;fruGAL4UAS-40XCD8GFP/+B–B”: Or47b-CD2 Or47b2/or47b2;fruGAL4UAS-40XCD8GFP/+C: Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or47bD: Or47b-CD2 Or47b2/Or47b2;fruGAL4UAS-40XCD8GFP/UAS-Or88a
Mentions: To test this hypothesis, we first asked whether Fru regulates Or47b expression in Or47b ORNs. However, we found that Or47b expression is unaffected in fru mutants, suggesting that Fru does not regulate Or47b expression (S7 Fig). We then examined fru expression in the absence of Or47b function. Surprisingly, we observed that fru expression in Or47b ORNs is abolished in Or47b mutants, (Fig 5B). This finding was confirmed by qRT-PCR (S8 Fig). This phenotype could be rescued by the expression of a UAS-Or47b transgene driven with fruGAL4 (Fig 5C). The expression of UAS-Or88a, a closely related receptor that detects similar ligands to Or47b [17] was partially able to rescue fru expression. This indicates a requirement for the function of ORs activated by the same ligand in fru regulation (Fig 5D and 5D’ and S11 Fig). Expression of Or67d, the third fru-expressing Or gene, which detects cVA, was not able to rescue fru expression in Or47b ORNs (S9D Fig).

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