Control of the release of digestive enzymes in the caeca of the cricket Gryllus bimaculatus

Abstract

In Gryllus bimaculatus, more digestive enzymes (amylase, trypsin, aminopeptidase) are secreted in the caecum of fed crickets than in unfed crickets, but the enzymes are released continuously at a basal rate in unfed animals. The rate of synthesis of the enzymes appears to parallel their rate of release. Digestive enzymes are released in response to a specific ratio of nutrients, although a high nutrient component in the food does not necessarily induce a high digestive enzyme release for that component. Rinsed flat‐sheet preparations of the caecum are incubated with specific nutrients (carbohydrates and proteins) and various concentrations of a neuropeptide (type‐A allatostatin), which affects generally the basal rates of secretion. Both maltose and glucose increase the release of amylase in vitro, but starch produces an inhibition of amylase release at lower concentrations. Bovine serum albumin (BSA), peptone and a mixture of amino acids have almost no effect on the release of aminopeptidase or carboxypeptidase, and only low concentrations of peptone increase trypsin release. High concentrations of both BSA and peptone strongly inhibit trypsin activity, perhaps by excess substrate binding to the trypsin active site. The allatostatin Grybi‐AST 5 elevates the release of amylase in vitro, but not of trypsin or aminopeptidase, in 2‐day‐old fed females. In the caeca from 1‐day‐old unfed crickets, both amylase and the trypsin release are stimulated in the presence of AST 5. The paracrine AST 5 is probably released from the gut endocrine cells and binds to the enzyme‐producing caecal cells.

Peptidergic control of food intake and digestion in insects1This review is part of a virtual symposium on recent advances in understanding a variety of complex regulatory processes in insect physiology and endocrinology, including development, metabolism, cold hardiness, food intake and digestion, and diuresis, through the use of omics technologies in the postgenomic era.

“…In addition, FGLa/AST also influences the carbohydrase levels in the cockroach midgut. Taken together, this suggests that FGLa/ASTs not only affect gut contractility but also regulate enzyme secretion (Fusé et al 1999;Woodring et al 2009). …”

“…FGLa/AST immunoreactivity was also observed in all ganglia of the CNS and within the open-type endocrine cells in midguts of L. migratoria (Robertson and Lange 2010) and the Pacific beetle cockroach (Diploptera punctata (Eschscholtz, 1822)) (Reichwald et al 1994). In addition, some regulatory peptides show stimulatory or inhibitory effects on enzyme activity levels in the gut, indicating that the control of enzyme release in response to food is likely (at least partially) mediated through these neuropeptides (Harshini et al 2002(Harshini et al , 2003Woodring et al 2009;Lwalaba et al 2010). The following sections provide an overview of neuropeptides associated with the SNS and (or) endocrine cells in the midgut and thus potentially involved in control of feeding and digestion mechanisms in insects.…”

“…Nonetheless, feeding stimulates amylase and trypsin release in G. bimaculatus. AST-A5 also stimulates amylase and trypsin activity in G. bimaculatus, indicating that the release of these enzymes possibly involves the release of FGLa/AST as a response to food intake (Woodring et al 2009). In contrast to this, in larvae of the lepidopteran fall armyworm (Spodoptera frugiperda (J.E.…”

“…Some neuropeptides present in the stomatogastric nervous system (SNS) have indeed also been localized in the midgut endocrine cells, suggesting a more prominent role in the regulation of digestive processes as well. In addition, some regulatory neuropeptides show stimulating or inhibitory effects on enzyme activity levels in the gut of insects, indicating that the control of enzyme release in response to food is likely to be (at least in part) under neuropeptidergic control (Harshini et al 2002(Harshini et al , 2003Woodring et al 2009;Lwalaba et al 2010). Understanding the endocrine control of digestion and feeding mechanisms is important in understanding the physiology of nutrition.…”

“…The physiology of the insect digestive system is largely coordinated by neurohormones, as well as by multiple regulatory peptides produced by endocrine cells located in the gut epithelium and (or) by neurons innervating different parts of the gut (reviewed by Audsley and Weaver 2009;Woodring et al 2009;Lwalaba et al 2010). Many of these regulatory peptides in insects have vertebrate homologues; however, much less is known about their specific functions or modes of action in invertebrates.…”