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Rescheduling Behavioral Subunits of a Fixed Action Pattern by Genetic Manipulation of Peptidergic Signaling.

Kim DH, Han MR, Lee G, Lee SS, Kim YJ, Adams ME - PLoS Genet. (2015)

Bottom Line: Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior.Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP.Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California, Riverside, Riverside, California, United States of America.

ABSTRACT
The ecdysis behavioral sequence in insects is a classic fixed action pattern (FAP) initiated by hormonal signaling. Ecdysis triggering hormones (ETHs) release the FAP through direct actions on the CNS. Here we present evidence implicating two groups of central ETH receptor (ETHR) neurons in scheduling the first two steps of the FAP: kinin (aka drosokinin, leucokinin) neurons regulate pre-ecdysis behavior and CAMB neurons (CCAP, AstCC, MIP, and Bursicon) initiate the switch to ecdysis behavior. Ablation of kinin neurons or altering levels of ETH receptor (ETHR) expression in these neurons modifies timing and intensity of pre-ecdysis behavior. Cell ablation or ETHR knockdown in CAMB neurons delays the switch to ecdysis, whereas overexpression of ETHR or expression of pertussis toxin in these neurons accelerates timing of the switch. Calcium dynamics in kinin neurons are temporally aligned with pre-ecdysis behavior, whereas activity of CAMB neurons coincides with the switch from pre-ecdysis to ecdysis behavior. Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior. Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP. Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

No MeSH data available.


Related in: MedlinePlus

Role of G-Protein-mediated signal transduction in timing of the switch to ecdysis behavior.(A) Inhibition of Gαo signaling using two different fly lines expressing the pertussis toxin gene (PTX(2), PTX(3) on 2nd and 3rd chromosomes, respectively). (B) Enhancement of Gαo signaling by overexpression of a constitutively active form (GαoQ205L). (C) Overexpression of Gαq signaling in CCAP and kinin neurons by expression of a wild type Gαq. Error-bars represent standard error of mean (S.E.M). Data was analyzed using Mann-Whitney test (** P < 0.001, *** P < 0.0001).
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pgen.1005513.g005: Role of G-Protein-mediated signal transduction in timing of the switch to ecdysis behavior.(A) Inhibition of Gαo signaling using two different fly lines expressing the pertussis toxin gene (PTX(2), PTX(3) on 2nd and 3rd chromosomes, respectively). (B) Enhancement of Gαo signaling by overexpression of a constitutively active form (GαoQ205L). (C) Overexpression of Gαq signaling in CCAP and kinin neurons by expression of a wild type Gαq. Error-bars represent standard error of mean (S.E.M). Data was analyzed using Mann-Whitney test (** P < 0.001, *** P < 0.0001).

Mentions: Our previous studies in Manduca showed that a balance between excitation and inhibition in segmental ganglia is important in the delay of ecdysis behavior initiation following ETH release[15]. We have shown here that ETH-induced calcium dynamics in CCAP and CAMB ensembles and ecdysis behavior also show a characteristic delay. We tested the possibility that inhibitory Go signaling in these neurons contributes to this delay through expression of pertussus toxin (PTX), a known inhibitor of Gαo[16,17]. Indeed, expression of PTX in the entire CCAP ensemble (CCAP>PTX) accelerates the switch to ecdysis; presumably, disinhibition through block of Go signaling shifts the balance in favor of excitation (Fig 5A). The ecdysis switch is similarly accelerated when PTX expression is confined to CAMB neurons (Pburs>PTX). Next, we asked whether overexpression of Gαo, delays the switch to ecdysis, likely by favoring inhibition over excitation in CAMB neurons. This in fact does occur (Fig 5B). Significantly, manipulation of Gαs or Gαi signaling pathways has no effect on scheduling of the ecdysis switch (S6 Fig). These findings provide solid evidence that Gαo signaling functions in determining timing of the ecdysis switch.


Rescheduling Behavioral Subunits of a Fixed Action Pattern by Genetic Manipulation of Peptidergic Signaling.

Kim DH, Han MR, Lee G, Lee SS, Kim YJ, Adams ME - PLoS Genet. (2015)

Role of G-Protein-mediated signal transduction in timing of the switch to ecdysis behavior.(A) Inhibition of Gαo signaling using two different fly lines expressing the pertussis toxin gene (PTX(2), PTX(3) on 2nd and 3rd chromosomes, respectively). (B) Enhancement of Gαo signaling by overexpression of a constitutively active form (GαoQ205L). (C) Overexpression of Gαq signaling in CCAP and kinin neurons by expression of a wild type Gαq. Error-bars represent standard error of mean (S.E.M). Data was analyzed using Mann-Whitney test (** P < 0.001, *** P < 0.0001).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581697&req=5

pgen.1005513.g005: Role of G-Protein-mediated signal transduction in timing of the switch to ecdysis behavior.(A) Inhibition of Gαo signaling using two different fly lines expressing the pertussis toxin gene (PTX(2), PTX(3) on 2nd and 3rd chromosomes, respectively). (B) Enhancement of Gαo signaling by overexpression of a constitutively active form (GαoQ205L). (C) Overexpression of Gαq signaling in CCAP and kinin neurons by expression of a wild type Gαq. Error-bars represent standard error of mean (S.E.M). Data was analyzed using Mann-Whitney test (** P < 0.001, *** P < 0.0001).
Mentions: Our previous studies in Manduca showed that a balance between excitation and inhibition in segmental ganglia is important in the delay of ecdysis behavior initiation following ETH release[15]. We have shown here that ETH-induced calcium dynamics in CCAP and CAMB ensembles and ecdysis behavior also show a characteristic delay. We tested the possibility that inhibitory Go signaling in these neurons contributes to this delay through expression of pertussus toxin (PTX), a known inhibitor of Gαo[16,17]. Indeed, expression of PTX in the entire CCAP ensemble (CCAP>PTX) accelerates the switch to ecdysis; presumably, disinhibition through block of Go signaling shifts the balance in favor of excitation (Fig 5A). The ecdysis switch is similarly accelerated when PTX expression is confined to CAMB neurons (Pburs>PTX). Next, we asked whether overexpression of Gαo, delays the switch to ecdysis, likely by favoring inhibition over excitation in CAMB neurons. This in fact does occur (Fig 5B). Significantly, manipulation of Gαs or Gαi signaling pathways has no effect on scheduling of the ecdysis switch (S6 Fig). These findings provide solid evidence that Gαo signaling functions in determining timing of the ecdysis switch.

Bottom Line: Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior.Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP.Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, University of California, Riverside, Riverside, California, United States of America.

ABSTRACT
The ecdysis behavioral sequence in insects is a classic fixed action pattern (FAP) initiated by hormonal signaling. Ecdysis triggering hormones (ETHs) release the FAP through direct actions on the CNS. Here we present evidence implicating two groups of central ETH receptor (ETHR) neurons in scheduling the first two steps of the FAP: kinin (aka drosokinin, leucokinin) neurons regulate pre-ecdysis behavior and CAMB neurons (CCAP, AstCC, MIP, and Bursicon) initiate the switch to ecdysis behavior. Ablation of kinin neurons or altering levels of ETH receptor (ETHR) expression in these neurons modifies timing and intensity of pre-ecdysis behavior. Cell ablation or ETHR knockdown in CAMB neurons delays the switch to ecdysis, whereas overexpression of ETHR or expression of pertussis toxin in these neurons accelerates timing of the switch. Calcium dynamics in kinin neurons are temporally aligned with pre-ecdysis behavior, whereas activity of CAMB neurons coincides with the switch from pre-ecdysis to ecdysis behavior. Activation of CCAP or CAMB neurons through temperature-sensitive TRPM8 gating is sufficient to trigger ecdysis behavior. Our findings demonstrate that kinin and CAMB neurons are direct targets of ETH and play critical roles in scheduling successive behavioral steps in the ecdysis FAP. Moreover, temporal organization of the FAP is likely a function of ETH receptor density in target neurons.

No MeSH data available.


Related in: MedlinePlus