Molecular Cloning, Genomic Organization, and Expression of a C-Type (Manduca sexta-Type) Allatostatin Preprohormone from Drosophila melanogaster

Williamson, Michael; Lenz, Camilla; Winther, Åsa M.E.; Nässel, Dick R.; Grimmelikhuijzen, Cornelis J.P.

doi:10.1006/bbrc.2001.4565

Cited by 89 publications

(47 citation statements)

References 26 publications

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“…Analyzed by Edman degradation, this peptide revealed the sequence XVRYRQXYFNPIX. Table IA shows that this sequence aligns with part of a hormone precursor sequence derived from the Drosophila genome data base and referred to as Drostatin precursor (11). The resulting decapentapeptide is reminiscent to allatostatin C isolated from the tobacco hornworm, M. sexta (12), except that in Manduca the first amino acid residue is a pyroglutamate, and in position 4 the tyrosine is replaced by phenylalanine (Table IB).…”

Section: Functional Annotation Of Drostar1 and -2mentioning

confidence: 94%

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Functional Annotation of Two Orphan G-protein-coupled Receptors, Drostar1 and -2, from Drosophila melanogaster and Their Ligands by Reverse Pharmacology

Kreienkamp

Larusson

Witte

et al. 2002

Journal of Biological Chemistry

121

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By combining a Drosophila genome data base search and reverse transcriptase-PCR-based cDNA isolation, two G-protein-coupled receptors were cloned, which are the closest known invertebrate homologs of the mammalian opioid/somatostatin receptors. However, when functionally expressed in Xenopus oocytes by injection of Drosophila orphan receptor RNAs together with a coexpressed potassium channel, neither receptor was activated by known mammalian agonists. By applying a reverse pharmacological approach, the physiological ligands were isolated from peptide extracts from adult flies and larvae. Edman sequencing and mass spectrometry of the purified ligands revealed two decapentapeptides, which differ only by an N-terminal pyroglutamate/ glutamine. The peptides align to a hormone precursor sequence of the Drosophila genome data base and are almost identical to allatostatin C from Manduca sexta. Both receptors were activated by the synthetic peptides irrespective of the N-terminal modification. Sitedirected mutagenesis of a residue in transmembrane region 3 and the loop between transmembrane regions 6 and 7 affect ligand binding, as previously described for somatostatin receptors. The two receptor genes each containing three exons and transcribed in opposite directions are separated by 80 kb with no other genes predicted between. Localization of receptor transcripts identifies a role of the new transmitter system in visual information processing as well as endocrine regulation.Insect development and behavior are largely controlled by hormones and neurotransmitters often identified using a diverse array of bioassays. Besides the biogenic amines and the steroid-like hormones, insect hormones have been frequently classified as neuropeptides, which are widely distributed throughout the invertebrate kingdom (1, 2). Despite the large number of neuropeptides, the number of known cognate receptors in insects is still rather limited, with only a few examples in Drosophila that have been cloned based on homology with mammalian G-protein-coupled receptors (GPCRs) 1 (i.e. neuropeptide Y-like and tachykinin-like receptors) (3, 4). With the completion of the Drosophila genome project, a more thorough analysis of neuropeptide/receptor relations in insects is now possible. Whereas this genome data base allows the identification of peptide hormones previously isolated from other insect species as part of larger precursors (5), Drosophila GPCR-like sequences have been predicted mostly based on structural analogy of the transmembrane regions to mammalian neuropeptide receptor groups (6).Structural evidence for the existence of ligands identical or similar to their mammalian neuropeptide counterparts are lacking when searching the Drosophila genome data base. This may indicate that in insects these receptors are activated by an entirely different set of ligands. This view is supported by data reported here on the identification of two novel GPCRs from Drosophila melanogaster, termed Drostar1 and -2, which are structurally related to the mam...

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Section: Functional Annotation Of Drostar1 and -2mentioning

confidence: 94%

“…4B) obtained by Edman degradation with the Drosophila precursor Drostatin (DAP C 102-121 ) sequence (11). Identical amino acid residues are inverted.…”

Section: Table Imentioning

confidence: 99%

Functional Annotation of Two Orphan G-protein-coupled Receptors, Drostar1 and -2, from Drosophila melanogaster and Their Ligands by Reverse Pharmacology

Kreienkamp

Larusson

Witte

et al. 2002

Journal of Biological Chemistry

121

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“…The C-type allatostatins with an N-terminal pGlu residue and a free C terminus have been discovered in the moth Manduca sexta, the fly Drosophila melanogaster and the mosquito Aedes aegypti (Kramer et al, 1991;Williamson et al, 2001;Li et al, 2006). The B-type allatostatins all have a common Trp-(X6)-Trp-amide C terminus and were first discovered in the cricket (Wang et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…In adult insect females, juvenile hormones can also regulate reproductive activities such as the maturation of oocytes. Synthesis of juvenile hormones is inhibited by allatostatins (ASTs), members of a large and diverse family of peptides that are structurally characterized into three distinct groups (Gäde and Goldsworthy, 2003).The C-type allatostatins with an N-terminal pGlu residue and a free C terminus have been discovered in the moth Manduca sexta, the fly Drosophila melanogaster and the mosquito Aedes aegypti (Kramer et al, 1991;Williamson et al, 2001;Li et al, 2006). The B-type allatostatins all have a common Trp-(X6)-Trp-amide C terminus and were first discovered in the cricket (Wang et al, 2004).…”

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confidence: 99%

Allatostatin A-like immunoreactivity in the nervous system and gut of the larval midge, Chironomus riparius (Meigen): Modulation of hindgut motility, rectal K+ transport and implications for exposure to salinity

Robertson

Chasiotis

Galperin

et al. 2014

Journal of Experimental Biology

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Evidence for the presence of allatostatin (AST) A-like neuropeptides in the larval midge Chironomus riparius is reported. Immunohistochemical studies on the nervous system and gut revealed the presence of AST A-like immunoreactive (AST-IR) cells and processes. The nerve cord contained AST-IR processes that originated from cells in the brain and travelled the length of nerve cord to the terminal ganglion. Within each ganglion, these processes gave rise to varicosities, suggesting that they formed synapses with neurons in the ganglia. Endocrine cells containing AST-IR were present in three regions of the midgut: near the attachment of the Malpighian tubules, between the anterior and posterior midgut, and in the vicinity of the gastric caecae. The terminal ganglion also contained four AST-IR cells that gave rise to axons that projected onto the hindgut and posterior midgut. Application of a cockroach AST to the semi-isolated hindgut of larval C. riparius led to dosedependent inhibition of muscle contractions with an EC 50 of 10 nmol l −1 and a decrease in rectal K + reabsorption resulting from reduced rectal Na + /K + -ATPase and vacuolar type H + -ATPase activities. The results suggest the presence of endogenous AST-like neuropeptides in larval C. riparius, where these factors play a role in the function of the gut. Furthermore, regulation of ion reabsorption by ASTs at the rectum could serve as an ideal mechanism of ion regulation in the face of abrupt and acute elevated salt levels. KEY WORDS: Na INTRODUCTIONJuvenile hormones are synthesized by the corpora allata and control the juvenile characteristics of insects during growth and development. In adult insect females, juvenile hormones can also regulate reproductive activities such as the maturation of oocytes. Synthesis of juvenile hormones is inhibited by allatostatins (ASTs), members of a large and diverse family of peptides that are structurally characterized into three distinct groups (Gäde and Goldsworthy, 2003).The C-type allatostatins with an N-terminal pGlu residue and a free C terminus have been discovered in the moth Manduca sexta, the fly Drosophila melanogaster and the mosquito Aedes aegypti (Kramer et al., 1991;Williamson et al., 2001;Li et al., 2006). The B-type allatostatins all have a common Trp-(X6)-Trp-amide C terminus and were first discovered in the cricket (Wang et al., 2004). The A-type allatostatins (ASTs) were the first to be discovered in the cockroach and share a Phe-Gly-Leu-amide C terminus (Donly et al., 1993;Siju et al., 2014). RESEARCH ARTICLEDepartmentAll allatostatins inhibit juvenile hormone synthesis in at least one group or species of insect; however, many do not in other insects, and instead have known inhibitory activity on contractile properties of muscle (Gäde and Goldsworthy, 2003). In particular, the ASTs have been shown to inhibit contractions of visceral muscle including the foregut and hindgut (Lange et al., 1993;Sarkar et al., 2003;Predel et al., 2001;Matthews et al., 2008), and have been localized to end...

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“…In contrast to the A-and B-ASTs, only a single C-type isoform has been identified in any given insect, and only a single C-AST is encoded by the known prepro-C-ASTs (e.g. Williamson et al, 2001b;Li et al, 2006;Sheng et al, 2007). No information is currently available on the presence or function of CASTs in decapod crustaceans, though a putative C-type-related peptide, SYWKQCAFNAVSCFamide, originally described from the honeybee Apis mellifera (Hummon et al, 2006), has recently been predicted via transcriptomics from the cladoceran crustacean Daphnia pulex (Gard et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Identification of SYWKQCAFNAVSCFamide: a broadly conserved crustacean C-type allatostatin-like peptide with both neuromodulatory and cardioactive properties

Dickinson

Wiwatpanit

Gabranski

et al. 2009

Journal of Experimental Biology

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SUMMARYThe allatostatins comprise three structurally distinct peptide families that regulate juvenile hormone production by the insect corpora allata. A-type family members contain the C-terminal motif -YXFGLamide and have been found in species from numerous arthropod taxa. Members of the B-type family exhibit a -WX 6 Wamide C-terminus and, like the A-type peptides, appear to be broadly conserved within the Arthropoda. By contrast, members of the C-type family, typified by the unblocked C-terminus -PISCF, a pyroglutamine blocked N-terminus, and a disulfide bridge between two internal Cys residues, have only been found in holometabolous insects, i.e. lepidopterans and dipterans. Here, using transcriptomics, we have identified SYWKQCAFNAVSCFamide (disulfide bridging predicted between the two Cys residues), a known honeybee and water flea C-typelike peptide, from the American lobster Homarus americanus (infraorder Astacidea). Using matrix assisted laser desorption/ionization Fourier transform mass spectrometry (MALDI-FTMS), a mass corresponding to that of SYWKQCAFNAVSCFamide was detected in the H. americanus brain, supporting the existence of this peptide and its theorized structure. Furthermore, SYWKQCAFNAVSCFamide was detected by MALDI-FTMS in neural tissues from five additional astacideans as well as 19 members of four other decapod infraorders (i.e. Achelata, Anomura, Brachyura and Thalassinidea), suggesting that it is a broadly conserved decapod peptide. In H. americanus, SYWKQCAFNAVSCFamide is capable of modulating the output of both the pyloric circuit of the stomatogastric nervous system and the heart. This is the first demonstration of bioactivity for this peptide in any species.

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Molecular Cloning, Genomic Organization, and Expression of a C-Type (Manduca sexta-Type) Allatostatin Preprohormone from Drosophila melanogaster

Cited by 89 publications

References 26 publications

Functional Annotation of Two Orphan G-protein-coupled Receptors, Drostar1 and -2, from Drosophila melanogaster and Their Ligands by Reverse Pharmacology

Functional Annotation of Two Orphan G-protein-coupled Receptors, Drostar1 and -2, from Drosophila melanogaster and Their Ligands by Reverse Pharmacology

Allatostatin A-like immunoreactivity in the nervous system and gut of the larval midge, Chironomus riparius (Meigen): Modulation of hindgut motility, rectal K+ transport and implications for exposure to salinity

Identification of SYWKQCAFNAVSCFamide: a broadly conserved crustacean C-type allatostatin-like peptide with both neuromodulatory and cardioactive properties

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