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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-positive OR expression in ac4 sensilla expands to developmentally related fru-negative ORNs in alh mutants.A) Adult antennae and brains labeled with Ir84aGal4 UAS-CD8GFP (green) in wild type and alh mutant clones. Magenta staining in brains is against N-cadherin, a neuropil marker. B) Total Ir84a-positive cells. Asterisks indicate significant (p < .05) differences from wild type. Error bars represent SEM. ANOVAs were performed and followed with Tukey’s HSD—see Materials and Methods. Wild type flies were significantly different from all alh conditions (p < .0001). n = 24–50. All count data may be found in the Supporting Information as S1 Data. C) Model: In alh mutants, the Ir84a odorant receptor identity is expanded to other coeloconic ORNs as observed through glomerular innervation. Ir84a expression is expanded to ir75a and ir76a ORNs. D) Adult antennae and brains labeled with Or67dGal4 UAS-CD8GFP (green) in wild type and alh mutant clones in Drosophila. Magenta staining in brains is against N-cadherin, a neuropil marker. E) Total Or67d-positive cells. An ANOVA for this data was not significant. n = 20–30. All count data may be found in the Supporting Information as S1 Data. F) Model: In alh mutants, the expression and axonal targeting patterns of or67d-positive ORNs are unchanged.GENOTYPES:A) eyflp; Ir84aGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alhj8c8/FRT82Gal80E2FD) eyflp; Or67dGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Or67dGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F
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pbio.1002443.g002: fru-positive OR expression in ac4 sensilla expands to developmentally related fru-negative ORNs in alh mutants.A) Adult antennae and brains labeled with Ir84aGal4 UAS-CD8GFP (green) in wild type and alh mutant clones. Magenta staining in brains is against N-cadherin, a neuropil marker. B) Total Ir84a-positive cells. Asterisks indicate significant (p < .05) differences from wild type. Error bars represent SEM. ANOVAs were performed and followed with Tukey’s HSD—see Materials and Methods. Wild type flies were significantly different from all alh conditions (p < .0001). n = 24–50. All count data may be found in the Supporting Information as S1 Data. C) Model: In alh mutants, the Ir84a odorant receptor identity is expanded to other coeloconic ORNs as observed through glomerular innervation. Ir84a expression is expanded to ir75a and ir76a ORNs. D) Adult antennae and brains labeled with Or67dGal4 UAS-CD8GFP (green) in wild type and alh mutant clones in Drosophila. Magenta staining in brains is against N-cadherin, a neuropil marker. E) Total Or67d-positive cells. An ANOVA for this data was not significant. n = 20–30. All count data may be found in the Supporting Information as S1 Data. F) Model: In alh mutants, the expression and axonal targeting patterns of or67d-positive ORNs are unchanged.GENOTYPES:A) eyflp; Ir84aGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alhj8c8/FRT82Gal80E2FD) eyflp; Or67dGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Or67dGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F

Mentions: The majority of the other ORN classes representing approximately ten different sensilla, including Or67d ORNs in at1 sensilla (Fig 2D–2F) examined, were not affected by similar sensory conversions (S2 Fig). In contrast, we detected a similar identity conversion in the sensilla housing Ir84a ORNs (Fig 2A–2C). We detected a general decrease in the total number of ac4 sensilla based on cell counts in alh1353 mutants (Fig 2B). This possibly is due to an earlier function of Alh on precursor patterning based on its expression in a ring of cells on the antennal disc known to give rise to some of the coeloconic and trichoid sensilla fates [31] (S6 Fig), which in alh mutants lead to decreased cell survival. Despite the effects on the total number of sensilla, within the formed sensilla, multiple Ir84a-positive ORNs were observed (Fig 2A–2C).


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-positive OR expression in ac4 sensilla expands to developmentally related fru-negative ORNs in alh mutants.A) Adult antennae and brains labeled with Ir84aGal4 UAS-CD8GFP (green) in wild type and alh mutant clones. Magenta staining in brains is against N-cadherin, a neuropil marker. B) Total Ir84a-positive cells. Asterisks indicate significant (p < .05) differences from wild type. Error bars represent SEM. ANOVAs were performed and followed with Tukey’s HSD—see Materials and Methods. Wild type flies were significantly different from all alh conditions (p < .0001). n = 24–50. All count data may be found in the Supporting Information as S1 Data. C) Model: In alh mutants, the Ir84a odorant receptor identity is expanded to other coeloconic ORNs as observed through glomerular innervation. Ir84a expression is expanded to ir75a and ir76a ORNs. D) Adult antennae and brains labeled with Or67dGal4 UAS-CD8GFP (green) in wild type and alh mutant clones in Drosophila. Magenta staining in brains is against N-cadherin, a neuropil marker. E) Total Or67d-positive cells. An ANOVA for this data was not significant. n = 20–30. All count data may be found in the Supporting Information as S1 Data. F) Model: In alh mutants, the expression and axonal targeting patterns of or67d-positive ORNs are unchanged.GENOTYPES:A) eyflp; Ir84aGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alhj8c8/FRT82Gal80E2FD) eyflp; Or67dGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Or67dGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F
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pbio.1002443.g002: fru-positive OR expression in ac4 sensilla expands to developmentally related fru-negative ORNs in alh mutants.A) Adult antennae and brains labeled with Ir84aGal4 UAS-CD8GFP (green) in wild type and alh mutant clones. Magenta staining in brains is against N-cadherin, a neuropil marker. B) Total Ir84a-positive cells. Asterisks indicate significant (p < .05) differences from wild type. Error bars represent SEM. ANOVAs were performed and followed with Tukey’s HSD—see Materials and Methods. Wild type flies were significantly different from all alh conditions (p < .0001). n = 24–50. All count data may be found in the Supporting Information as S1 Data. C) Model: In alh mutants, the Ir84a odorant receptor identity is expanded to other coeloconic ORNs as observed through glomerular innervation. Ir84a expression is expanded to ir75a and ir76a ORNs. D) Adult antennae and brains labeled with Or67dGal4 UAS-CD8GFP (green) in wild type and alh mutant clones in Drosophila. Magenta staining in brains is against N-cadherin, a neuropil marker. E) Total Or67d-positive cells. An ANOVA for this data was not significant. n = 20–30. All count data may be found in the Supporting Information as S1 Data. F) Model: In alh mutants, the expression and axonal targeting patterns of or67d-positive ORNs are unchanged.GENOTYPES:A) eyflp; Ir84aGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F,eyflp; Ir84aGal4/UAS-CD8GFP; FRT82alhj8c8/FRT82Gal80E2FD) eyflp; Or67dGal4/UAS-CD8GFP; FRT82/FRT82Gal80E2F,eyflp; Or67dGal4/UAS-CD8GFP; FRT82alh1353/FRT82Gal80E2F
Mentions: The majority of the other ORN classes representing approximately ten different sensilla, including Or67d ORNs in at1 sensilla (Fig 2D–2F) examined, were not affected by similar sensory conversions (S2 Fig). In contrast, we detected a similar identity conversion in the sensilla housing Ir84a ORNs (Fig 2A–2C). We detected a general decrease in the total number of ac4 sensilla based on cell counts in alh1353 mutants (Fig 2B). This possibly is due to an earlier function of Alh on precursor patterning based on its expression in a ring of cells on the antennal disc known to give rise to some of the coeloconic and trichoid sensilla fates [31] (S6 Fig), which in alh mutants lead to decreased cell survival. Despite the effects on the total number of sensilla, within the formed sensilla, multiple Ir84a-positive ORNs were observed (Fig 2A–2C).

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
Related in: MedlinePlus