Biochemical, Molecular, and Functional Characterization of PISCF-Allatostatin, a Regulator of Juvenile Hormone Biosynthesis in the Mosquito Aedes aegypti

Li, Yiping; Hernández‐Martínez, Salvador; Fernández, Facundo M.; Mayoral, Jaime G.; Topalis, Pantelis; Priestap, Horacio A.; Pérez, María-Eglée; Navare, Arti T.; Noriega, Fernando G.

doi:10.1074/jbc.m606341200

Cited by 54 publications

(53 citation statements)

References 28 publications

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“…The third family consists of a small number of nonamidated peptides with a C-terminal PISCF-OH sequence, first isolated from the moth M. sexta (Kramer et al, 1991). These peptides inhibit JH biosynthesis in Lepidoptera and Diptera (Li et al, 2006). Allatostatins are pleiotropic in function and in addition to their allatostatic activity (in vivo and in vitro) all peptides show myoinhibitory properties on visceral muscles in insects and other invertebrates (Hoffmann et al, 1999;Stay, 2000).…”

Section: Introductionmentioning

confidence: 96%

Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae)

Abdel-latief

Hoffmann

2010

Arch Insect Biochem Physiol

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The genome of Tribolium castaneum encodes two allatostatin [AS type B; W(X)(6)Wamide and AS type C; PISCF-OH] and one allatotropin (AT) precursor, but no AS type A (FGLamide) (Tribolium Genome Sequencing Consortium, 2008: Nature 452:949-955). Here we studied the activity (in vitro) of peptides derived from these precursors on the synthesis/release of juvenile hormone (JH) III. The corpora cardiaca-corpora allata (CC-CA) complexes of adult females of another tenebrionid beetle, the mealworm Tenebrio molitor, were used. Incubating the gland complexes in a medium containing Trica-AS B3 peptide, we showed that the peptide has allatostatic function in T. molitor. The activity of the type C AS depended on the age of the test animals and their intrinsic rate of JH III biosynthesis. The Trica-AS C peptide inhibited the JH release from CA of 3-day-old females with a high intrinsic rate of JH synthesis, but activated JH release from the CA of 7-day-old females with a lower intrinsic rate of JH production. The allatotropin peptide (Trica-AT) also activated the JH release from the CA of 7-day-old females in a dose-dependent and reversible manner. Unexpectedly, a type A AS derived from the precursor of the American cockroach Periplaneta americana (Peram-AS A2b) inhibited the JH release from the CA of younger and older females in the concentration range of 10(-8) to 10(-4) M, and the effects were fully reversible in the absence of peptide. These data suggest a complex role of allatoactive neuropeptides in the regulation of JH III biosynthesis in beetles.

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Section: Introductionmentioning

confidence: 96%

Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae)

Abdel-latief

Hoffmann

2010

Arch Insect Biochem Physiol

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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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Biochemical, Molecular, and Functional Characterization of PISCF-Allatostatin, a Regulator of Juvenile Hormone Biosynthesis in the Mosquito Aedes aegypti

Cited by 54 publications

References 28 publications

Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae)

Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae)

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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