The activity of the rectal gland of the North Pacific spiny dogfish Squalus suckleyi is glucose dependent and stimulated by glucagon-like peptide-1

Abstract

Elasmobranchs possess a specialised organ, the rectal gland, which is responsible for excreting sodium chloride via the posterior intestine. Previous work has indicated that the gland may be activated by a number of hormones, some of which are likely related to the salt or volume loads associated with feeding. Furthermore, evidence exists for the gland being glucose dependent which is atypical for an elasmobranch tissue. In this study, the presence of sodium-glucose co-transporters (SGLTs) in the rectal gland and their regulation by feeding were investigated. In addition, the hypothesis of glucose dependence was examined through the use of glucose transporter (GLUT and SGLT) inhibitors, phlorizin, Indinavir, and STF-31 and their effect on secretion by the rectal gland. Finally, the effects on rectal gland activity of insulin, glucagon, and glucagon-like peptide-1, hormones typically involved in glucoregulation, were examined. The results showed that sglt1 mRNA is present in the gland, and there was a significant reduction in sglt1 transcript abundance 24 h post-feeding. An almost complete suppression of chloride secretion was observed when glucose uptake was inhibited, confirming the organ's glucose dependence. Finally, perfusion with dogfish GLP-1 (10 nmol L), but not dogfish glucagon, was shown to markedly stimulate the activity of the gland, increasing chloride secretion rates above baseline by approximately 16-fold (p < 0.001). As GLP-1 is released from the intestine upon feeding, we propose that this may be the primary signal for activation of the rectal gland post-feeding.

Cortisol and Dexamethasone Mediate Glucocorticoid Actions in the Lesser Spotted Catshark (Scyliorhinus canicula)

“…In this sense, maximum secretion rates occurred at physiological basal levels of glucose in the incubation medium (2.3 mM glucose), while they decreased drastically in the absence of external glucose, and to a lesser extent when glucose incubation medium concentration doubled (4.6 mM glucose). Further studies are mandatory to unravel this question, including analysis of transmembrane glucose transporters [ 34 , 81 ], the feasible action of non-canonical corticosteroid mechanisms [ 35 , 37 ] that may be associated to membrane processes, or the presence of glucosensors involved in GC actions.…”

“…Glucose metabolism also results of major importance after short-term situations as described in vertebrates, including sharks, to provide energy to demanding tissues [ 32 , 33 , 34 ]. Acute responses of cortisol include rapid glycolytic actions mediated by GR in teleost fish that affect liver and muscle [ 35 , 36 ].…”

The Rectal Gland of the Shark: The Road to Understanding the Mechanism and Regulation of Transepithelial Chloride Transport

“…Yet, another peptide, glucagon like peptide 1, stimulated the secretion of chloride by the rectal gland of the Pacific spiny dogfish ( Squalus suckleyi ). 46 …”

“…The fuel supporting the secretion of chloride by the rectal gland is glucose. 46 , 78 Glucose is taken up into rectal gland cells by sodium glucose linked transporter 1. It is stored inside the cells as glycogen that can be seen as storage granules in electron micrographs of the gland and has been measured in homogenates of the gland.…”

Diagnostic agreement between three point-of-care glucose and β-hydroxybutyrate meters and reference laboratory methods in stingrays

“…Glucose is potentially of less metabolic importance in elasmobranchs, although differences between tissues, species, and metabolic states exist ( 3–5 , 7 , 8 ). Plasma glucose concentrations are often low relative to teleosts and terrestrial vertebrates and appear relatively unchanged after feeding or during long-term fasting ( 3 ).…”