Programmed cell death of identified peptidergic neurons involved in ecdysis behavior in the moth,Manduca sexta

Ewer, John; Wang, Chiou Miin; Klukas, Kathleen A.; Mesce, Karen A.; Truman, James W.; Fahrbach, Susan E.

doi:10.1002/(sici)1097-4695(19981105)37:2<265::aid-neu6>3.0.co;2-c

Cited by 37 publications

(13 citation statements)

References 49 publications

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“…Maximal levels were observed just before adult emergence, consistent with the known role of bursicon in posteclosion tanning and sclerotization of the cuticle, wing inflation, and epidermal cell death (22). Earlier studies in moth (Manduca sexta) (24), locust (Schistocerca gregaria) (25), and Drosophila (26) demonstrated that most CCAP-expressing neurons undergo apoptosis after adult ecdysis, consistent with our findings of low transcript levels for pburs and burs in mature adult D. melanogaster. This low level of pburs and burs expression was accompanied by a reduction in the levels of DLGR2 message.…”

Section: Discussionsupporting

confidence: 91%

Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2

Luo

Dewey

Sudo

et al. 2005

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

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244

275

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All arthropods periodically molt to replace their exoskeleton (cuticle). Immediately after shedding the old cuticle, the neurohormone bursicon causes the hardening and darkening of the new cuticle. Here we show that bursicon, to our knowledge the first heterodimeric cystine knot hormone found in insects, consists of two proteins encoded by the genes burs and pburs (partner of burs). The pburs͞burs heterodimer from Drosophila melanogaster binds with high affinity and specificity to activate the G proteincoupled receptor DLGR2, leading to the stimulation of cAMP signaling in vitro and tanning in neck-ligated blowflies. Native bursicon from Periplaneta americana is also a heterodimer. In D. melanogaster the levels of pburs, burs, and DLGR2 transcripts are increased before ecdysis, consistent with their role in postecdysial cuticle changes. Immunohistochemical analyses in diverse insect species revealed the colocalization of pburs-and burs-immunoreactivity in some of the neurosecretory neurons that also express crustacean cardioactive peptide. Forty-three years after its initial description, the elucidation of the molecular identity of bursicon and the verification of its receptor allow for studies of bursicon actions in regulating cuticle tanning, wing expansion, and as yet unknown functions. Because bursicon subunit genes are homologous to the vertebrate bone morphogenetic protein antagonists, our findings also facilitate investigation on the function of these proteins during vertebrate development.BMP antagonist ͉ heterodimeric polypeptide ligand ͉ LGR I nsects comprise Ͼ90% of all animal species and are of great economical and ecological importance. The evolutionary success of insects is due partially to their exoskeleton, which provides protection, mechanical support, and an effective barrier to desiccation and infections. During immature stages, continued growth requires that insects replace their exoskeleton. During this molting process, a new cuticle is synthesized and secreted by underlying epidermal cells and then is hardened after the remains of the old cuticle are shed at ecdysis. Molting and ecdysis are regulated by at least six different hormones (1). The steroid 20-hydroxyecdysone directs the synthesis of the new cuticle (2), and then a cascade of peptide hormones orchestrates the events surrounding ecdysis.According to current knowledge, the last uncharacterized hormone in this cascade, bursicon, is an Ϸ30-kDa neurohormone that is released after the completion of ecdysis (3, 4) and triggers the tanning (melanization and sclerotization) of the new cuticle as well as wing expansion (5). Bursicon of diverse insects, including blowf ly (Calliphora erythrocephala), cockroach (Periplaneta americana), cricket (Gryllus bimaculatus), locust (Locusta migratoria), and meal beetle (Tenebrio molitor) (4), initiates tanning in neck-ligated flies (6, 7), suggesting the conservation of this signaling system that is essential for insect survival.Recently, a subfamily of G protein-coupled receptors with a large ectodo...

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Section: Discussionsupporting

confidence: 91%

Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2

Luo

Dewey

Sudo

et al. 2005

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

Self Cite

244

275

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“…We have previously shown that in newly eclosed mosquitoes, CCAP is highly expressed in neurons 27 and IN704 of the ventral nerve cord, but that these neurons undergo apoptosis by 12h post-eclosion (Honegger et al, 2011). This is similar to what has been reported for Manduca sexta immatures (Ewer et al, 1998;Davis et al, 2001). In the present study we show that in newly eclosed mosquitoes, neurons 27 extend numerous peripheral projections that span the pleuron and innervate the alary and cardiac muscles, as is also seen in M. sexta and Baculum extradendatum Ejaz and Lange, 2008).…”

Section: Discussionsupporting

confidence: 82%

Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae

Estévez‐Lao

Boyce

Honegger

et al. 2013

Journal of Experimental Biology

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SUMMARYCrustacean cardioactive peptide (CCAP) is a highly conserved arthropod neurohormone that is involved in ecdysis, hormone release and the modulation of muscle contractions. Here, we determined the CCAP gene structure in the malaria mosquito Anopheles gambiae, assessed the developmental expression of CCAP and its receptor and determined the role that CCAP plays in regulating mosquito cardiac function. RACE sequencing revealed that the A. gambiae CCAP gene encodes a neuropeptide that shares 100% amino acid identity with all sequenced CCAP peptides, with the exception of Daphnia pulex. Quantitative RT-PCR showed that expression of CCAP and the CCAP receptor displays a bimodal distribution, with peak mRNA levels in second instar larvae and pupae. Injection of CCAP revealed that augmenting hemocoelic CCAP levels in adult mosquitoes increases the anterograde and retrograde heart contraction rates by up to 28%, and increases intracardiac hemolymph flow velocities by up to 33%. Partial CCAP knockdown by RNAi had the opposite effect, decreasing the mosquito heart rate by 6%. Quantitative RT-PCR experiments showed that CCAP mRNA is enriched in the head region, and immunohistochemical experiments in newly eclosed mosquitoes detected CCAP in abdominal neurons and projections, some of which innervated the heart, but failed to detect CCAP in the abdomens of older mosquitoes. Instead, in older mosquitoes CCAP was detected in the pars lateralis, the subesophageal ganglion and the corpora cardiaca. In conclusion, CCAP has a potent effect on mosquito circulatory physiology, and thus heart physiology in this dipteran insect is under partial neuronal control. Supplementary material available online at

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“…We have shown that the lateral pairs of 704 interneurons in the abdominal ganglia of larvae of M. sexta, and comparable neurons in B. mori, are MIP-immunoreactive, and this immunoreactivity is colocalized with that of CCAP. Ewer et al (1998) have demonstrated cell death of the 704 interneurons in fully mature M. sexta adults, and, as expected, we have found that in adults, these cells are not labeled by MIP-immunostaining.…”

Section: Role For Myoinhibitory Peptide In Insect Ecdysissupporting

confidence: 90%

Localization of myoinhibitory peptide immunoreactivity inManduca sextaandBombyx mori, with indications that the peptide has a role in molting and ecdysis

Davis

Blackburn²,

Golubeva³

et al. 2003

Journal of Experimental Biology

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For normal development of Manduca sexta larvae, the ecdysteroid titer must drop following its sudden rise at the start of the molting cycle; this sudden decline in titer may be due to myoinhibitory peptide I (MIP I), which has an inhibitory effect on the release of ecdysone by the prothoracic glands of Bombyx mori in vitro. Using an antiserum to MIP, we have demonstrated secretion of an MIP-like peptide by the epiproctodeal glands of Manduca sexta, which are located on each proctodeal nerve, just anterior to the rectum. These MIP-immunoreactive glands are also present in B. mori. In fourth-instar larvae of M. sexta, the epiproctodeal glands show a distinct cycle of synthesis and sudden release of MIP that coincides with the time of the rapid decline in ecdysteroid titer. The function of the epiproctodeal glands appears to be the timely release of MIP during the molting cycle, so as to inhibit the prothoracic glands and thus to facilitate the sudden decline in ecdysteroid titer. In addition, we have found that MIP immunoreactivity is co-localized with that of crustacean cardioactive peptide (CCAP) in the 704 interneurons; these peptides appear to be co-released at the time of ecdysis. It is known that CCAP can initiate the ecdysis motor program; our results suggest that MIP may also be involved in activating ecdysis behavior.

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Programmed cell death of identified peptidergic neurons involved in ecdysis behavior in the moth,Manduca sexta

Cited by 37 publications

References 49 publications

Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2

Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2

Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae

Localization of myoinhibitory peptide immunoreactivity inManduca sextaandBombyx mori, with indications that the peptide has a role in molting and ecdysis

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