Distribution and functional significance of Leu-callatostatins in the blowfly Calliphora vomitoria

Abstract

The Leu-callatostatins are a series of four neuropeptides isolated from nervous tissues of the blowfly Calliphora vomitoria that show C-terminal sequence homology to the allatostatins of cockroaches. The allatostatins have an important role in the reproductive processes of insects as inhibitors of the synthesis and release of juvenile hormone from the corpus allatum. In this study, the distribution of the Leu-callatostatin-immunoreactive neurones and endocrine cells has been mapped in C. vomitoria and, in contrast to the cockroach allatostatins, it has been shown that there is no cytological basis to suggest that the dipteran peptides act as regulators of juvenile hormone. Although occurring in various neurones in the brain and thoracico-abdominal ganglion, there is no evidence of Leu-callatostatin-immunoreactive pathways linking the brain to the corpus allatum, or of immunoreactive terminals in this gland. Three different types of functions for the Leu-callatostatins are suggested by the occurrence of immunoreactive material in cells and by the pathways that have been identified. (1) A role in neurotransmission or neuromodulation appears evident from immunoreactive neurones in the medulla of the optic lobes, and from immunoreactive material in the central body and in descending interneurones in the suboesophageal ganglion that project to the neuropile of the thoracico-abdominal ganglion. (2) Leu-callatostatin neurones directly innervate muscles of the hindgut and the heart. Immunoreactive fibres from neurones of the abdominal ganglion pass by way of the median abdominal nerve to ramify extensively over several areas of the hindgut. Physiological experiments with synthetic peptides show that the Leu-callatostatins are potent inhibitors of peristaltic movements of the ileum. Leu-callatostatin 3 is active at 10(-16) to 10(-13) M. This form of regulatory control over gut motility appears to be highly specific since the patterns of contraction in other regions are unaffected by these peptides. (3) Evidence that the Leu-callatostatins act as neurohormones comes from the presence of varicosities in axons passing through the corpus cardiacum (but not the corpus allatum) and also from material in extraganglionic neurosecretory cells in the thorax. Fibres from these peripheral neurones are especially prominent over the large nerve bundles supplying the legs. There are also a considerable number of Leu-callatostatin-immunoreactive endocrine cells in a specific region of the midgut. The conclusion from this study is that although conservation of the structure of the allatostatin-type of peptides is evident through a long period of evolution it cannot be assumed that all of their functions have also been conserved.(ABSTRACT TRUNCATED AT 400 WORDS)

A Family of Neuropeptides That Inhibit Juvenile Hormone Biosynthesis in the Cricket, Gryllus bimaculatus

“…The immunocytochemical localization of Tyr-Xaa-Phe-Gly-Leu-NH 2 allatostatin-like peptides in the central nervous system as well as in midgut cells of many invertebrates (8,27) suggests that allatostatins are multifunctional neuropeptides, even though inhibition of JH biosynthesis by CA in vitro was the only bioassay utilized in their isolation. Sequence homology, as found between Lom-MIP and the family of allatostatic neuropeptides presented in this paper, may indicate a myomodulatory role of these peptides, as was also discussed for the Tyr-Xaa-Phe-Gly-Leu-NH 2 allatostatin family (28,29). …”

The neural and peptidergic control of gut contraction in Locusta migratoria: the effect of an FGLa/AST

“…FGLa/ASTs modulate each region of the gut, coordinating the functioning of each region. It would appear that a physiological function in the gut is a common role for FGLa/ASTs in insects (see Audsley and Weaver, 2009;Lange et al, 1995;Duve and Thorpe, 1994) (see also current study). The ancestral role for the FGLa/ASTs may be as brain/gut peptides, as a myoinhibitory role for visceral muscle contraction is so widespread for the FGLa/ASTs, and because the FGLa/ASTs do not function as true allatostatins in most species of insects (see Gäde, 2002).…”

“…This myoinhibitory property of FGLa/ASTs is well documented in a number of insect species. For example, FGLa/ASTs inhibit peristaltic contractions of the foregut in Calliphora vomitoria, S. gregaria and Leucophaea maderae (Duve and Thorpe, 1994;Zilberstein et al, 2004;Duve et al, 1995), proctolin-induced contractions of the midgut in Diploptera punctata (Fusé et al, 1999), and spontaneous and proctolin-induced contractions of the hindgut in D. punctata and S. gregaria (Lange et al, 1993;Lange et al, 1995;Veelaert et al, 1996). Other myoinhibitory effects of FGLa/ASTs include inhibition of spontaneous oviducal contractions in S. gregaria (Veelaert et al, 1996) and modulation of the cardiac rhythm in Blattella germanica (Vilaplana et al, 1999).…”

Expression of the allatostatin gene in endocrine cells of the cockroach midgut.

“…An inhibitory effect of allatostatins on hindgut contraction and a proctolin-antagonistic activity was also shown in D. punctata (25). Most recently, Duve and Thorpe (28) showed that Leu-callatostatins 1 and 3, peptides from the blowfly that share a homologous Tyr-Gly-Phe-GlyLeu-NH2 C terminus with ASAL, are potent inhibitors of peristalsis of the hindgut of C. vomitoria. Leu-callatostatins are not found in terminal arborizations within the corpus allatum (13,28), and they are devoid of allatostatic activity in the blowfly (13).…”