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

Abstract

Ruhr IM, Takei Y, Grosell M. The role of the rectum in osmoregulation and the potential effect of renoguanylin on SLC26a6 transport activity in the Gulf toadfish (Opsanus beta). Am J Physiol Regul Integr Comp Physiol 311: R179 -R191, 2016. First published March 30, 2016 doi:10.1152/ajpregu.00033.2016.-Teleosts living in seawater continually absorb water across the intestine to compensate for branchial water loss to the environment. The present study reveals that the Gulf toadfish (Opsanus beta) rectum plays a comparable role to the posterior intestine in ion and water absorption. However, the posterior intestine appears to rely more on SLC26a6 (a HCO 3 Ϫ /Cl Ϫ antiporter) and the rectum appears to rely on NKCC2 (SLC12a1) for the purposes of solute-coupled water absorption. The present study also demonstrates that the rectum responds to renoguanylin (RGN), a member of the guanylin family of peptides that alters the normal osmoregulatory processes of the distal intestine, by inhibited water absorption. RGN decreases rectal water absorption more greatly than in the posterior intestine and leads to net Na ϩ and Cl Ϫ secretion, and a reversal of the absorptive short-circuit current (ISC). It is hypothesized that maintaining a larger fluid volume within the distal segments of intestinal tract facilitates the removal of CaCO3 precipitates and other solids from the intestine. Indeed, the expression of the components of the Cl Ϫ -secretory response, apical CFTR, and basolateral NKCC1 (SLC12a2), are upregulated in the rectum of the Gulf toadfish after 96 h in 60 ppt, an exposure that increases CaCO3 precipitate formation relative to 35 ppt. Moreover, the downstream intracellular effects of RGN appear to directly inhibit ion absorption by NKCC2 and anion exchange by SLC26a6. Overall, the present findings elucidate key electrophysiological differences between the posterior intestine and rectum of Gulf toadfish and the potent regulatory role renoguanylin plays in osmoregulation. water secretion; Cl Ϫ secretion; HCO 3 Ϫ secretion; intestine; marine teleost; CFTR SEAWATER TELEOST FISH LIVE IN an environment that is hypertonic to their blood plasma, resulting in continual water loss through the gills (34). To compensate for this, seawater teleosts drink copious volumes of water that are continually desalinated by the esophagus and gastrointestinal tract to produce a fluid that is roughly isotonic to blood plasma (17, 34). The constant absorption of ions, by the intestine, is critical as it lowers luminal osmolality and allows for solute-coupled water absorption, and, thereby, compensating for branchial water loss (45,46 (53), a process coupled to the ion transport mechanisms described above. The seawater teleost rectum also plays a role in water absorption. For instance, in the sea bream (Sparus aurata) and Japanese eel (Anguilla japonica), fluid absorption by the rectum also occurs via aquaporins, but the rate of absorption is less than in the intestine (8,15,28,36). The rectum of the Gulf toadfish (Opsanus beta) also expres...

Dietary zinc addition influenced zinc and lipid deposition in the fore- and mid-intestine of juvenile yellow catfishPelteobagrus fulvidraco

“…Therefore, understanding the mechanisms of intestinal Zn uptake in fish is of considerable interest from both nutritional and toxicological perspectives. Studies suggested a morpho-functional specialisation of intestinal regions in fish with regard to ion transport (8)(9)(10) , and fish showed anterior-middle regionalisation of ion transport (11) . However, the mechanisms of absorption of mineral elements along the intestinal tract are far less understood (9,12) .…”

Molecular mechanisms for intestinal HCO3-secretion and its regulation by guanylin in seawater-acclimated eels

“…On the apical membrane of intestinal epithelial cells, Pat-1 may play an important role in HCO 3 - secretion as its stoichiometry is n HCO 3 - /1Cl - as shown in the euryhaline pufferfish, Takifugu obscurus (Kato et al, 2009), although there are conflicting reports on the stoichiometry of Pat-1 in mammals (see Alper and Sharma, 2013). In fact, pat1 is profoundly upregulated after transfer of this euryhaline pufferfish from FW to SW (Kurita et al, 2008) and after transfer of toadfish (Ruhr et al, 2016) and sea bream (Gregŏrio et al, 2013) from SW to concentrated SW. Consistently, mucosal DIDS, but not serosal DIDS, inhibited HCO 3 - secretion in the sanddab, Citharichthys sordidus (Grosell et al, 2001).…”

“…To assess the ion transporter target(s) of GN that lead to increased HCO 3 - secretion, various inhibitors were applied on either mucosal or serosal side of the intestinal epithelia in the Ussing chamber before or after GN administration. The inhibitors applied on the mucosal side were bumetanide, DPC and DNDS/DIDS since, in our earlier studies, GN inhibited NKCC2 and stimulated Cl - channel in the eel (Ando et al, 2014; Ando and Takei, 2015), and since UGN inhibited Pat-1 in the toadfish (Ruhr et al, 2016). DNDS/DIDS was also applied to the serosal side to evaluate the role of basolateral AE and NBC that transport HCO 3 - into the cell.…”

Renoguanylin stimulates apical CFTR translocation and decreases HCO3− secretion through PKA activity in the Gulf toadfish (Opsanus beta)

“…The combined effect of these processes, in addition to other ion-absorbing pathways, renders the fluid osmolality in the intestine similar to that of the extracellular fluids and allows for efficient water absorption that is coupled to Na + and Cl − absorption (Skadhauge, 1969(Skadhauge, , 1974. Even though net water absorption and the mechanisms that facilitate it are vital to the survival of teleosts living in seawater, recent studies reveal regionspecific areas of the intestine that display net secretory functions, at least periodically (Ruhr et al, 2014(Ruhr et al, , 2016.…”

“…In the Gulf toadfish, Opsanus beta (Goode and Bean, 1880), members of the homologous guanylin family of intestinal peptides [guanylin, uroguanylin and renoguanylin (RGN)] reverse ion absorption in the posterior intestine, but not in the anterior region (Ruhr et al, 2014). This reversal also corresponds to RGNstimulated water secretion in the posterior intestine and rectum, but not in the anterior intestine (Ruhr et al, 2014(Ruhr et al, , 2016. The switch from net ion absorption to net ion secretion (from mucosa-to-serosa to serosa-to-mucosa) seems to be caused primarily by inhibiting ion absorption by the Na + /K + /Cl − -cotransporter type 2 (NKCC2) and limiting HCO 3 − /Cl − exchange activity, as well as activating Cl − secretion through the apical cystic fibrosis transmembrane conductance regulator (CFTR) channel (Ruhr et al, 2014(Ruhr et al, , 2015(Ruhr et al, , 2016.…”