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−1), 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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson WG (2016) Endocrine systems in elasmobranchs. In: Shadwick, Farrell, Brauner (eds) Physiology of elasmobranch fishes: internal processes, vol 34B. Elsevier Academic Press, Oxford, pp 458–530
Anderson WG, Conlon JM, Hazon N (1995) Characterization of the endogenous intestinal peptide that stimulates the rectal gland of Scyliorhinus canicula. Am J Physiol 268:R1359–R1364
Brandt RB, Siegel SA, Waters MG, Bloch MH (1980) Spectrophotometric assay for d-(−)-lactate in plasma. Anal Biochem 102:39–46
Brubaker PL, Anini Y (2003) Direct and indirect mechanisms regulating secretion of glucagon-like peptide-1 and glucagon-like peptide-2. Can J Physiol Pharmacol 81:1005–1012
Burger JW (1962) Further studies on the function of the rectal gland in the spiny dogfish. Physiol Zool 35(3):205–217
Burger JW (1965) Roles of the rectal gland and the kidneys in salt and water excretion in the spiny dogfish. Physiol Zool 38(3):191–196
Burger JW, Hess WN (1960) Function of the rectal gland in the spiny dogfish. Science 131(3401):670–671
Conlon JM, Hazon N, Thim L (1994) Primary structures of peptides derived from proglucagon isolated from the pancreas of the elasmobranch fish, Scyliorhinus canicula. Peptides 15:163–167
Deck CA, McKay SJ, Fiedler TJ, LeMoine CMR, Kajimura M, Nawata CM, Wood CM, Walsh PJ (2013) Transcriptome responses in the rectal gland of fed and starved spiny dogfish shark (Squalus acanthias) determined by suppression subtractive hybridization. Comp Biochem Physiol D 8:334–343
Deck CA, LeMoine CMR, Walsh PJ (2016) Phylogenetic analysis and tissue distribution of elasmobranch glucose transporters and their response to feeding. Biol Open 5:256–261
Ebert DA, White WT, Goldman KJ, Compagno LJV, Daly-Engel TS, Ward RD (2010) Resurrection and redescription of Squalus suckleyi (Girard, 1854) from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae). Zootaxa 2612:22–40
Epstein FH, Stoff JS, Silva P (1983) Mechanism and control of hyperosmotic NaCl-rich secretion by the rectal gland of Squalus acanthias. J Exp Biol 106:25–41
Forrest JN (1996) Cellular and molecular biology of chloride secretion in the shark rectal gland: regulation by adenosine receptors. Kidney Int 49:1557–1562
Heckmann L-H, Sorensen PB, Krogh PH, Sorensen JG (2011) NORMA-gene: a simple and robust method for qPCR normalization based on target gene data. BMC Bioinform 12:250–256
Huang S, Czech MP (2007) The GLUT4 glucose transporter. Cell Metab 5:237–252
Kelley CA, Decker SE, Silva P, Forrest JN (2014) Gastric inhibitory peptide, serotonin, and glucagon are unexpected chloride secretagogues in the rectal gland of the skate (Leucoraja erinacea). Am J Physiol Regul Integr Comp Physiol 306:R674–R680
Matey V, Wood CM, Dowd WW, Kultz D, Walsh PJ (2009) Morphology of the rectal gland of the spiny dogfish (Squalus acanthias) shark in response to feeding. Can J Zool 87:440–452
Mueckler M, Thorens B (2013) The SLC2 (GLUT) family of membrane transporters. Mol Aspects Med 34:121–138
Shuttleworth TJ, Thompson JL (1980) Oxygen consumption in the rectal gland of the dogfish Scyliorhinus canicula and the effects of cyclic AMP. J Comp Physiol 136:39–43
Silva P, Stoff J, Field M, Fine L, Forrest JN, Epstein FH (1977) Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport. Am J Physiol Renal Physiol 233:F298–F306
Silva P, Stoff JS, Solomon RJ, Rosa R, Stevens A, Epstein J (1980) Oxygen cost of chloride transport in perfused rectal gland of Squalus acanthias. J Membr Biol 53:215–221
Silva P, Solomon RJ, Epstein FH (1996) The rectal gland of Squalus acanthias: a model for the transport of chloride. Kidney Int 49:1552–1556
Stoff JS, Silva P, Field M, Forrest J, Stevens A, Epstein FH (1977) Cyclic AMP regulation of active chloride transport in the rectal gland of marine elasmobranchs. J Exp Zool 199:443–448
Stoff JS, Rosa R, Hallac R, Silva P, Epstein FH (1979) Hormonal regulation of active chloride transport in the dogfish rectal gland. Am J Physiol Renal Physiol 237:F138–F144
Walsh PJ, Kajimura M, Mommsen TP, Wood CM (2006) Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland. J Exp Biol 209:2929–2938
Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2005) Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthias). J Exp Biol 208:2693–2705
Wood CM, Munger RS, Thompson J, Shuttleworth TJ (2007) Control of rectal gland secretion by blood acid-base status in the intact dogfish shark (Squalus acanthias). Resp Physiol Neurobiol 156:220–228
Wright EM, Turk E (2004) The sodium/glucose cotransport family SLC5. Eur J Physiol 447:510–518
Zall DM, Fisher D, Garner MQ (1956) Photometric determination of chlorides in water. Anal Chem 28(11):1665–1668
Acknowledgements
Many thanks to Dr. Eric Clelland, the research coordinator for the Bamfield Marine Sciences Centre and to our fisherman, John Planes. Also thanks to Alyssa Weinrauch (University of Alberta) for assisting with running glucose assays and Galyna Graham (Ulster University) for help with peptide purification. This work was funded by NSERC Discovery Grants to WGA (311909) and PJW who are also supported by the Canada Research Chair Program. A portion of this study was also made possible by a JEB Travel Fellowship to CAD.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H.V. Carey.
Rights and permissions
About this article
Cite this article
Deck, C.A., Anderson, W.G., Conlon, J.M. et al. The activity of the rectal gland of the North Pacific spiny dogfish Squalus suckleyi is glucose dependent and stimulated by glucagon-like peptide-1. J Comp Physiol B 187, 1155–1161 (2017). https://doi.org/10.1007/s00360-017-1102-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-017-1102-9