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

Abstract

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...

Peptidomics of Neuropeptidergic Tissues of the Tsetse FlyGlossina morsitans morsitans

“…The PM contained two of the predicted neuropeptides. The presence of AstA peptides in the CNS and midgut has previously been reported in other dipterans including D. melanogaster [33,[35][36][37], the cabbage root fly Delia radicum larvae, the midge Chironomus riparius, and mosquitoes Aedes aegypti and Anopheles albimanus [36,[38][39][40][41].…”

Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior

“…Chironomus riparius, Locusta migratoria and Lacanobia oleracea [700][701][702][703][704][705][706][707]. It is also possible that some of the peptides regulate activity in gut epithelial cells that produce digestive enzymes [28,208,708,709] or cells involved in nutrient or ion absorption [700,701,710].…”

FLUID AND ION SECRETION BY MALPIGHIAN TUBULES OF LARVAL CHIRONOMIDS, Chironomus riparius: EFFECTS OF REARING SALINITY, TRANSPORT INHIBITORS, AND SEROTONIN

“…The neuroendocrinology of chironomids is an understudied area; however, a single study showed serotonin‐like immunoreactivity in the nervous system and gastrointestinal tract of a larval chironomid, Chironomus tentans (Johansson et al., ). This same study found immunoreactivity to several peptidergic factors and a second study mapped allatostatin‐like immunoreactivity in larval C. riparius (Robertson et al., ). Nothing is known about the potential regulation of chironomid Malpighian tubule activity by these or any other neuroendocrine factors.…”

“…Larval C. riparius physiologically respond to salinity by decreasing the activities of the ionomotive enzymes V‐type H + ‐ATPase and Na + /K + ‐ATPase in the rectal portion of the hindgut that reduces ion reabsorption from the rectal fluid (Jonusaite et al., ). This effect is mimicked by exogenous application of allatostatin, a peptidergic neuroendocrine factor, to the rectum, which is innervated by nerves containing an allatostatin‐like factor (Robertson et al., ). The results would suggest that more ions are left in the rectal fluid for excretion that would help deal with the increased ion load in the salinated conditions.…”