An endogenous elevation of cGMP increases the excitability of identified insect neurosecretory cells

Gammie, Stephen C.; Truman, James W.

doi:10.1007/s003590050052

Cited by 36 publications

(25 citation statements)

References 30 publications

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“…It is thought that the VM neurons release EH centrally to elevate cGMP in CCAP neurons of the ventral nerve cord, including the IN704s. Elevation of cGMP is associated with increased excitability and prolonged spike duration of CCAP neurons (24). Expression of ETHR-A in VM neurons provides further support for a positive feedback signaling pathway between VM neurons and Inka cells described in refs.…”

Section: Vm Neurons (Eh)supporting

confidence: 60%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

168

158

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At the end of each developmental stage, insects perform the ecdysis sequence, an innate behavior necessary for shedding the old cuticle. Ecdysis triggering hormones (ETHs) initiate these behaviors through direct actions on the CNS. Here, we identify the ETH receptor (ETHR) gene in the moth Manduca sexta, which encodes two subtypes of GPCR (ETHR-A and ETHR-B). Expression of ETHRs in the CNS coincides precisely with acquisition of CNS sensitivity to ETHs and behavioral competence. ETHR-A occurs in diverse networks of neurons, producing both excitatory and inhibitory neuropeptides, which appear to be downstream signals for behavior regulation. These peptides include allatostatins, crustacean cardioactive peptide (CCAP), calcitonin-like diuretic hormone, CRF-like diuretic hormones (DHs) 41 and 30, eclosion hormone, kinins, myoinhibitory peptides (MIPs), neuropeptide F, and short neuropeptide F. In particular, cells L 3,4 in abdominal ganglia coexpress kinins, DH41, and DH30, which together elicit the fictive preecdysis rhythm. Neurons IN704 in abdominal ganglia coexpress CCAP and MIPs, whose joint actions initiate the ecdysis motor program. ETHR-A also is expressed in brain ventromedial cells, whose release of EH increases excitability in CCAP͞MIP neurons. These findings provide insights into how innate, centrally patterned behaviors can be orchestrated via recruitment of peptide cotransmitter neurons.ecdysis sequence ͉ ecdysis triggering hormone ͉ G protein-coupled receptors ͉ neuropeptide ͉ steroid I nnate behaviors are highly stereotypic and fully functional in the absence of prior experience. Examples include nurturing, nest building, courtship, and escape behaviors as well as certain developmental behaviors such as the ecdysis sequence, necessary for the shedding of old cuticle at the end of each developmental stage in insects. Because the ecdysis sequence is hormonally controlled, it provides unique opportunities to define mechanisms by which chemical messengers assemble and regulate the performance of behaviors (for review, see ref. 1).The ecdysis sequence is initiated through direct actions of bloodborne pre-ecdysis triggering hormone (PETH) and ecdysis triggering hormone (ETH) on the CNS (2, 3). These peptides are released from endocrine Inka cells, which are present throughout the Insecta (4-6). In larval Manduca sexta, the sequence consists of three behavioral phases (3). In the first phase, PETH activates preecdysis I behavior; subsequently, ETH activates preecdysis II and ecdysis behaviors. These behaviors can be elicited by ETH from the isolated CNS in vitro and, hence, are centrally patterned (3, 7).The ecdysis behavioral sequence is repeatedly acquired and lost throughout the life history of insects (3,8). The signaling pathways triggered by PETH and ETH are assembled at the end of each developmental stage through steroid-induced gene expression, which is critical for synthesis of PETH and ETH in Inka cells and sensitivity of the CNS to these peptides. Once ecdysis is performed, CNS sensitivity to ET...

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Section: Vm Neurons (Eh)supporting

confidence: 60%

Central peptidergic ensembles associated with organization of an innate behavior

Kim

Žitňan

Cho³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

168

158

View full text Add to dashboard Cite

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“…6B shows that the coordination of the response between serial homologs was relatively low. These spikes are likely to correspond to large overshooting calcium action potentials, such as those recorded at ecdysis from homologous neurons in Manduca sexta (Gammie and Truman, 1997b).…”

Section: Response Of Ccap Network To Eth In the Absence Of Ehmentioning

confidence: 99%

Genetic analysis of Eclosion hormone action during Drosophila larval ecdysis

et al. 2015

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Insect growth is punctuated by molts, during which the animal produces a new exoskeleton. The molt culminates in ecdysis, an ordered sequence of behaviors that causes the old cuticle to be shed. This sequence is activated by Ecdysis triggering hormone (ETH), which acts on the CNS to activate neurons that produce neuropeptides implicated in ecdysis, including Eclosion hormone (EH), Crustacean cardioactive peptide (CCAP) and Bursicon. Despite more than 40 years of research on ecdysis, our understanding of the precise roles of these neurohormones remains rudimentary. Of particular interest is EH; although it is known to upregulate ETH release, other roles for EH have remained elusive. We isolated an Eh null mutant in Drosophila and used it to investigate the role of EH in larval ecdysis. We found that null mutant animals invariably died at around the time of ecdysis, revealing an essential role in its control. Further analyses showed that these animals failed to express the preparatory behavior of pre-ecdysis while directly expressing the motor program of ecdysis. Although ETH release could not be detected, the lack of pre-ecdysis could not be rescued by injections of ETH, suggesting that EH is required within the CNS for ETH to trigger the normal ecdysial sequence. Using a genetically encoded calcium probe, we showed that EH configured the response of the CNS to ETH. These findings show that EH plays an essential role in the Drosophila CNS in the control of ecdysis, in addition to its known role in the periphery of triggering ETH release.

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“…In the abdominal CNS of the Manduca for example, 2 pairs of CCAPimmunoreactive neurons up-regulate the second messenger cGMP at larval ecdysis, whereas only one pair does so at pupal and adult ecdysis (Ewer and Truman, 1997). Since this cGMP response likely increases the excitability of the CCAP neurons [it is known to do so for the thoracic set (Gammie and Truman, 1997a)], this change in the pattern of cGMP expression could change the relative participation of the different CCAP neurons at each ecdysis. It is not known if this sort of mechanism applies to Drosophila, since no cGMP response is detected in CCAP neurons at any ecdysis in this species (Ewer and Truman, 1996;Baker et al, 1999).…”

Section: Bases For the Changing Roles For Ccap During Postembryonic Dmentioning

confidence: 99%

Targeted ablation of CCAP neuropeptide-containing neurons ofDrosophilacauses specific defects in execution and circadian timing of ecdysis behavior

et al. 2003

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Insect growth and metamorphosis is punctuated by molts, during which a new cuticle is produced. Every molt culminates in ecdysis, the shedding of the remains of the old cuticle. Both the timing of ecdysis relative to the molt and the actual execution of this vital insect behavior are under peptidergic neuronal control. Based on studies in the moth, Manduca sexta, it has been postulated that the neuropeptide Crustacean cardioactive peptide (CCAP)plays a key role in the initiation of the ecdysis motor program. We have used Drosophila bearing targeted ablations of CCAP neurons (CCAP KO animals) to investigate the role of CCAP in the execution and circadian regulation of ecdysis. CCAP KO animals showed specific defects at ecdysis, yet the severity and nature of the defects varied at different developmental stages. The majority of CCAP KO animals died at the pupal stage from the failure of pupal ecdysis, whereas larval ecdysis and adult eclosion behaviors showed only subtle defects. Interestingly, the most severe failure seen at eclosion appeared to be in a function required for abdominal inflation, which could be cardioactive in nature. Although CCAP KO populations exhibited circadian eclosion rhythms, the daily distribution of eclosion events (i.e.,gating) was abnormal. Effects on the execution of ecdysis and its circadian regulation indicate that CCAP is a key regulator of the behavior. Nevertheless, an unexpected finding of this work is that the primary functions of CCAP as well as its importance in the control of ecdysis behaviors may change during the postembryonic development of Drosophila.

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An endogenous elevation of cGMP increases the excitability of identified insect neurosecretory cells

Cited by 36 publications

References 30 publications

Central peptidergic ensembles associated with organization of an innate behavior

Central peptidergic ensembles associated with organization of an innate behavior

Genetic analysis of Eclosion hormone action during Drosophila larval ecdysis

Targeted ablation of CCAP neuropeptide-containing neurons ofDrosophilacauses specific defects in execution and circadian timing of ecdysis behavior

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