Guanylin peptides regulate electrolyte and fluid transport in the Gulf toadfish (Opsanus beta) posterior intestine

Abstract

The physiological effects of guanylin (GN) and uroguanylin (UGN) on fluid and electrolyte transport in the teleost fish intestine have yet to be thoroughly investigated. In the present study, the effects of GN, UGN, and renoguanylin (RGN; a GN and UGN homolog) on short-circuit current ( Isc) and the transport of Cl−, Na+, bicarbonate (HCO3−), and fluid in the Gulf toadfish ( Opsanus beta) intestine were determined using Ussing chambers, pH-stat titration, and intestinal sac experiments. GN, UGN, and RGN reversed the Isc of the posterior intestine (absorptive-to-secretory), but not of the anterior intestine. RGN decreased baseline HCO3− secretion, but increased Cl− and fluid secretion in the posterior intestine. The secretory response of the posterior intestine coincides with the presence of basolateral NKCC1 and apical cystic fibrosis transmembrane conductance regulator (CFTR), the latter of which is lacking in the anterior intestine and is not permeable to HCO3− in the posterior intestine. However, the response to RGN by the posterior intestine is counterintuitive given the known role of the marine teleost intestine as a salt- and water-absorbing organ. These data demonstrate that marine teleosts possess a tissue-specific secretory response, apparently associated with seawater adaptation, the exact role of which remains to be determined.

Living with a leaky skin: upregulation of ion transport proteins during sloughing

“…Apical and basolateral surfaces of the skin were perfused with an oxygenated (95% O 2 and 5% CO 2 ) frog Ringer solution (mmol l −1 : NaCl 112, KCl 2.5, D-glucose 10, Na 2 HPO 4 2, CaCl 2 1, MgCl 2 1, Hepes salt 5, Hepes 5, at pH 7.4 with an osmolality of 230±20 mosmol l −1 ; Voyles et al, 2009), and temperature was maintained via a water bath set at 25±1°C. Electrophysiological parameters were measured as follows: (1) transepithelial potential (V T ) under open-circuit conditions by clamping the current to 0 μA and recording the resulting voltage (mV) with reference to the basolateral side, (2) active ion transport via clamping the voltage to 0 mV and recording the instantaneous short-circuit current (I sc ) response (μA cm 2 ) and (3) transepithelial resistance per unit area (Ω cm −2 ) by applying 3 s of 1 µA pulses across the epithelium every 60 s, or under voltageclamp conditions by applying 3 s of 1 mV at 60 s intervals (Ruhr et al, 2014). The inflections from the resulting change in I sc and V T during pulsing were used to calculate resistance using Ohm's law.…”

The role of the rectum in osmoregulation and the potential effect of renoguanylin on SLC26a6 transport activity in the Gulf toadfish (Opsanus beta)

“…These short-length hormones are expressed in the intestine and rectum of the Japanese eel, European eel (A. anguilla), and Gulf toadfish (41,47,48), and they are upstream regulators of apical guanylyl cyclase-C1 and -C2 (GC-C) receptors in the intestine (56). GC-C activation leads to increases in intracellular cGMP formation, whose downstream effects stimulate Cl Ϫ secretion by activation of the apical cystic fibrosis transmembrane conductance regulator (CFTR) and greatly inhibit ion and water absorption (3,4,6,40). In the Gulf toadfish and Japanese eel, the guanylin peptide effect appears restricted to the mid-and posterior intestine, by reversing the absorptive short-circuit current (I SC ) (from mucosa-to-serosa to serosa-tomucosa), mediated primarily by a switch from net Cl Ϫ absorpAddress for reprint requests and other correspondence: I. M. Ruhr,…”

“…However, recent studies have demonstrated the potential for inhibited fluid absorption by the intestine, initiated by the guanylin family of intestinal peptides [guanylin, uroguanylin, and renoguanylin (RGN)] (3,4,40,41). These short-length hormones are expressed in the intestine and rectum of the Japanese eel, European eel (A. anguilla), and Gulf toadfish (41,47,48), and they are upstream regulators of apical guanylyl cyclase-C1 and -C2 (GC-C) receptors in the intestine (56).…”

“…GC-C activation leads to increases in intracellular cGMP formation, whose downstream effects stimulate Cl Ϫ secretion by activation of the apical cystic fibrosis transmembrane conductance regulator (CFTR) and greatly inhibit ion and water absorption (3,4,6,40). In the Gulf toadfish and Japanese eel, the guanylin peptide effect appears restricted to the mid-and posterior intestine, by reversing the absorptive short-circuit current (I SC ) (from mucosa-to-serosa to serosa-tomucosa), mediated primarily by a switch from net Cl Ϫ absorp-tion to net secretion (4,40,41,55). This reversal leads to either fluid secretion or inhibited fluid absorption (3,4,40,41,55).…”

“…In the Gulf toadfish and Japanese eel, the guanylin peptide effect appears restricted to the mid-and posterior intestine, by reversing the absorptive short-circuit current (I SC ) (from mucosa-to-serosa to serosa-tomucosa), mediated primarily by a switch from net Cl Ϫ absorp-tion to net secretion (4,40,41,55). This reversal leads to either fluid secretion or inhibited fluid absorption (3,4,40,41,55). Moreover, the guanylin peptides, GC-C1, and GC-C2, are transcriptionally upregulated when freshwater-acclimated European and Japanese eels are transferred from freshwater to seawater (SW) (9,10,27,54,56), which suggests that the guanylin peptide system is important for seawater acclimatization.…”