Limits...
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.

Show MeSH
Or and Ir function is required to regulate fru expression in the adult olfactory system.(A) Heterozygous orco mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous orco mutant antennae (3–5 d old). (C) Overexpression of UAS-orco under the control of fruGal4 in orco mutants (14 d old). (D) Homozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (E) Homozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (F) Heterozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (G) Heterozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (H) Quantification and statistical analysis of fru-positive ORN cell bodies observed in adult antennae of the indicated genotypes. n = 5–27. For all graphs, asterisks indicate significant (p < .005) differences from or47b heterozygotes. Error bars represent SEM. A one-way ANOVA was performed and followed with Tukey’s HSD—see Materials and Methods. All count data may be found in the Supporting Information as S1 Data.GENOTYPES:A–A”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /+B–B”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /orco1C: +/ UAS-orco; orco1fruGAL4UAS-40XCD8GFP /orco1D: Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501E: Ir8a1/Y; fruGAL4UAS-40XCD8GFPF: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / +G: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4836687&req=5

pbio.1002443.g006: Or and Ir function is required to regulate fru expression in the adult olfactory system.(A) Heterozygous orco mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous orco mutant antennae (3–5 d old). (C) Overexpression of UAS-orco under the control of fruGal4 in orco mutants (14 d old). (D) Homozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (E) Homozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (F) Heterozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (G) Heterozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (H) Quantification and statistical analysis of fru-positive ORN cell bodies observed in adult antennae of the indicated genotypes. n = 5–27. For all graphs, asterisks indicate significant (p < .005) differences from or47b heterozygotes. Error bars represent SEM. A one-way ANOVA was performed and followed with Tukey’s HSD—see Materials and Methods. All count data may be found in the Supporting Information as S1 Data.GENOTYPES:A–A”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /+B–B”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /orco1C: +/ UAS-orco; orco1fruGAL4UAS-40XCD8GFP /orco1D: Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501E: Ir8a1/Y; fruGAL4UAS-40XCD8GFPF: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / +G: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501

Mentions: We also abolished Or47b function using mutants for the general Or coreceptor orco [28]. A loss of fru expression, similar to that seen in Or47b mutants, was observed in orco mutants (Figs 6A, 6B and 6H, 8E and S11 Fig) and was confirmed by qRT-PCR (S8 Fig). This phenotype could be rescued by expression of a UAS-orco transgene (Figs 6C and 6H, 8E and S11 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)

Or and Ir function is required to regulate fru expression in the adult olfactory system.(A) Heterozygous orco mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous orco mutant antennae (3–5 d old). (C) Overexpression of UAS-orco under the control of fruGal4 in orco mutants (14 d old). (D) Homozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (E) Homozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (F) Heterozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (G) Heterozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (H) Quantification and statistical analysis of fru-positive ORN cell bodies observed in adult antennae of the indicated genotypes. n = 5–27. For all graphs, asterisks indicate significant (p < .005) differences from or47b heterozygotes. Error bars represent SEM. A one-way ANOVA was performed and followed with Tukey’s HSD—see Materials and Methods. All count data may be found in the Supporting Information as S1 Data.GENOTYPES:A–A”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /+B–B”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /orco1C: +/ UAS-orco; orco1fruGAL4UAS-40XCD8GFP /orco1D: Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501E: Ir8a1/Y; fruGAL4UAS-40XCD8GFPF: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / +G: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4836687&req=5

pbio.1002443.g006: Or and Ir function is required to regulate fru expression in the adult olfactory system.(A) Heterozygous orco mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP(A) and OR47b-CD2(A’). (A”) shows the merge of two images. (B) Homozygous orco mutant antennae (3–5 d old). (C) Overexpression of UAS-orco under the control of fruGal4 in orco mutants (14 d old). (D) Homozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (E) Homozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP. (F) Heterozygous Ir84a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (G) Heterozygous Ir8a mutant antennae (3–5 d old) expressing fruGal4 40XUASCD8GFP and orco-Gal80. (H) Quantification and statistical analysis of fru-positive ORN cell bodies observed in adult antennae of the indicated genotypes. n = 5–27. For all graphs, asterisks indicate significant (p < .005) differences from or47b heterozygotes. Error bars represent SEM. A one-way ANOVA was performed and followed with Tukey’s HSD—see Materials and Methods. All count data may be found in the Supporting Information as S1 Data.GENOTYPES:A–A”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /+B–B”: Or47b-CD2 /+;orco1fruGAL4UAS-40XCD8GFP /orco1C: +/ UAS-orco; orco1fruGAL4UAS-40XCD8GFP /orco1D: Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501E: Ir8a1/Y; fruGAL4UAS-40XCD8GFPF: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / +G: orco-GAL80/+; Ir84aMI00501fruGAL4UAS-40XCD8GFP / Ir84aMI00501
Mentions: We also abolished Or47b function using mutants for the general Or coreceptor orco [28]. A loss of fru expression, similar to that seen in Or47b mutants, was observed in orco mutants (Figs 6A, 6B and 6H, 8E and S11 Fig) and was confirmed by qRT-PCR (S8 Fig). This phenotype could be rescued by expression of a UAS-orco transgene (Figs 6C and 6H, 8E and S11 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