Endocrine regulation of carbonate precipitate formation in marine fish intestine by Stanniocalcin and PTHrP

Abstract

In marine fish, high epithelial bicarbonate secretion by the intestine generates luminal carbonate precipitates of divalent cations that play a key role in water and ion homeostasis. In vitro studies highlight the involvement of the calciotropic hormones PTHrP (parathyroid hormone-related protein) and stanniocalcin (STC) in the regulation of epithelial bicarbonate transport. The present study tested the hypothesis that calciotropic hormones have a regulatory role in carbonate precipitate formation in vivo. Sea bream (Sparus aurata) juveniles received single intraperitoneal injections of piscine PTHrP(1-34), the PTH/PTHrP receptor antagonist PTHrP(7-34) or purified sea bream STC, or were passively immunized with polyclonal rabbit antisera raised against sea bream STC (STC-Ab). Endocrine effects on the expression of the basolateral sodium bicarbonate cotransporter (Slc4a4.A), the apical anion exchangers Slc26a6.A and Slc26a3.B, and the V-type proton pump β-subunit (Atp6v1b) in the anterior intestine were evaluated. In keeping with their calciotropic nature, the hypocalcaemic factors PTHrP(7-34) and STC upregulated gene expression of all transporters. In contrast, the hypercalcaemic factor PTHrP(1-34) and STC antibodies downregulated transporters involved in the bicarbonate secretion cascade. Changes in intestine luminal precipitate contents provoked by calcaemic endocrine factors validated these results: 24 h postinjection either PTHrP(1-34) or immunization with STC-Ab reduced the carbonate precipitate content in the sea bream intestine. In contrast, the PTH/PTHrP receptor antagonist PTHrP(7-34) increased not only the precipitated fraction but also the concentration of HCO 3 -equivalents in the intestinal fluid. These results confirm the hypothesis that calciotropic hormones have a regulatory role in carbonate precipitate formation in vivo in the intestine of marine fish. Furthermore, they illustrate for the first time in fish the counteracting effect of PTHrP and STC, and reveal an unexpected contribution of calcaemic factors to acid-base balance.

A proteinaceous organic matrix regulates carbonate mineral production in the marine teleost intestine

“…It has been well demonstrated that intestinal bicarbonate and calcium concentrations, the substrates required for CaCO 3 formation, are controlled via various mechanisms, which can affect the rate of CaCO 3 formation. Regulators of intestinal bicarbonate include the guanylin peptides 31 and prolactin 32 , where calciotropic hormones such as parathyroid hormone-related protein (PTHrP) and stanniocalcin (STC) can modify both luminal bicarbonate and calcium concentrations 33 34 . Additionally, the presence of calcium itself can modify the rate of intestinal bicarbonate secretion 35 .…”

Regulation of Bicarbonate Secretion in Marine Fish Intestine by the Calcium-Sensing Receptor

“…There are recent studies that suggest a relationship between calcium transport and HCO 3 − secretion in the intestine of marine fish in terms of regulation by endocrine factors or environmental effects [ 5 , 10 , 23 , 35 , 49 , 50 ]. The single common factor to all studies above cited is calcium.…”

“…Drinking is necessary to compensate osmotic water losses [ 1 , 2 , 3 ], therefore water replacement by drinking becomes essential to sustain osmotic regulation [ 4 ]. Several studies have reported the involvement of endocrine and environmental factors in the regulation of the amount of water ingestion by seawater fish [ 4 , 5 , 6 , 7 , 8 , 9 , 10 ].…”

“…Several hormones, such as stanniocalcin (STC), calcitonin, somatolactin (SL), parathyroid hormone-related protein (PTHrP) and, parathyroid hormone (PTH) are linked in the control of calcium transport in fish [ 5 , 7 , 30 , 31 , 32 , 33 , 34 ]. And recently, in the sea bream [ 10 , 35 ] it was demonstrated that the internal modulation of epithelial HCO 3 − secretion and the associated carbonate precipitation are under endocrine control highlighting a novel physiological role for calcium regulation.…”

PTH Reloaded: A New Evolutionary Perspective

“…In pufferfish and zebrafish two pth3 were identified and cloned, pth3a/pth3b (Power et al, 2000 ; Canario et al, 2006 ; Yan et al, 2012 ), however only pth3a has been identified in seabream (Flanagan et al, 2000 ). Recent studies have outlined the importance of Pth3 in fish ion balance (Gregório et al, 2014 ). The increase of circulating Pth3 in seabream stimulates the calcium uptake through gills and intestine (Guerreiro et al, 2001 ; Abbink et al, 2006 ; Fuentes and Figueiredo, 2006 ).…”