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. 2016 Jul 1;311(1):R179-91. doi: 10.1152/ajpregu.00033.2016. Epub 2016 Mar 30.

Abstract

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 HCO3 (-)/Cl(-) 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(+) and Cl(-) 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(-)-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.

Keywords: CFTR; Cl− secretion; HCO3− secretion; intestine; marine teleost; water secretion.

MeSH terms

  • Adenine Nucleotide Translocator 3 / metabolism*
  • Animals
  • Batrachoidiformes / metabolism*
  • Bicarbonates / metabolism
  • Biological Transport, Active / drug effects
  • Calcium Carbonate / pharmacology
  • Chlorides / metabolism
  • Gastrointestinal Hormones / pharmacology*
  • Intestinal Mucosa / metabolism
  • Intestines / drug effects
  • Natriuretic Peptides / pharmacology*
  • Osmoregulation / drug effects*
  • Rectum / drug effects*
  • Sodium / metabolism
  • Solute Carrier Family 12, Member 1 / metabolism
  • Water / metabolism

Substances

  • Adenine Nucleotide Translocator 3
  • Bicarbonates
  • Chlorides
  • Gastrointestinal Hormones
  • Natriuretic Peptides
  • Solute Carrier Family 12, Member 1
  • Water
  • guanylin
  • Sodium
  • Calcium Carbonate