The differential role of renoguanylin in osmoregulation and apical Cl<sup>−</sup>/HCO<sup>−</sup><inf>3</inf> exchange activity in the posterior intestine of the gulf toadfish (Opsanus beta)

Ilan M. Ruhr, Edward M. Mager, Yoshio Takei, Martin Grosell

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

The guanylin family of peptides are effective regulators of intestinal physiology in marine teleosts. In the distal intestinal segments, they inhibit or reverse fluid absorption by inhibiting the absorptive shortcircuit current (I<inf>sc</inf>). The present findings demonstrate that mRNA from guanylin and uroguanylin, as well as at least one isoform of the guanylin peptide receptor, apical guanylyl cyclase-C (GC-C), was highly expressed in the intestine and rectum of the Gulf toadfish (Opsanus beta). In the posterior intestine, GC-C, as well as the cystic fibrosis transmembrane conductance regulator and basolateral Na<sup>+</sup>/ K<sup>+</sup>/2Cl<sup>−</sup> cotransporter, which comprise a Cl<sup>−</sup>-secretory pathway, were transcriptionally upregulated in 60 parts per thousand (ppt). The present study also shows that, in intestinal tissues from Gulf toadfish held in 35 ppt, renoguanylin (RGN) expectedly causes net Cl<sup>−</sup> secretion, inhibits both the absorptive Isc and fluid absorption, and decreases HCO<inf>3</inf><sup>−</sup> secretion. Likewise, in intestinal tissues from Gulf toadfish acclimated to 60 ppt, RGN also inhibits the absorptive I<inf>sc</inf> and fluid absorption but to an even greater extent, corresponding with the mRNA expression data. In contrast, RGN does not alter Cl<sup>−</sup> flux and, instead, elevates HCO<sup>−</sup><inf>3</inf> secretion in the 60-ppt group, suggesting increased apical Cl<sup>−</sup>/HCO<sup>−</sup><inf>3</inf> exchange activity by SLC26a6. Overall, these findings reinforce the hypotheses that the guanylin peptide system is important for salinity acclimatization and that the secretory response could facilitate the removal of solids, such as CaCO<inf>3</inf> precipitates, from the intestine.

Original languageEnglish (US)
Pages (from-to)R399-R409
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume309
Issue number4
DOIs
StatePublished - Aug 18 2015

Fingerprint

Batrachoidiformes
Osmoregulation
Intestines
Cystic Fibrosis Transmembrane Conductance Regulator
Messenger RNA
Peptides
Peptide Receptors
Secretory Pathway
Acclimatization
Salinity
Rectum
Protein Isoforms
guanylin

Keywords

  • Fluid Secretion
  • HCO<sup>–</sup><inf>3</inf> secretion
  • Hypersalinity
  • Marine teleost
  • Osmoregulation

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

@article{590af3370ccf4bafb587c75de29c9b20,
title = "The differential role of renoguanylin in osmoregulation and apical Cl−/HCO−3 exchange activity in the posterior intestine of the gulf toadfish (Opsanus beta)",
abstract = "The guanylin family of peptides are effective regulators of intestinal physiology in marine teleosts. In the distal intestinal segments, they inhibit or reverse fluid absorption by inhibiting the absorptive shortcircuit current (Isc). The present findings demonstrate that mRNA from guanylin and uroguanylin, as well as at least one isoform of the guanylin peptide receptor, apical guanylyl cyclase-C (GC-C), was highly expressed in the intestine and rectum of the Gulf toadfish (Opsanus beta). In the posterior intestine, GC-C, as well as the cystic fibrosis transmembrane conductance regulator and basolateral Na+/ K+/2Cl− cotransporter, which comprise a Cl−-secretory pathway, were transcriptionally upregulated in 60 parts per thousand (ppt). The present study also shows that, in intestinal tissues from Gulf toadfish held in 35 ppt, renoguanylin (RGN) expectedly causes net Cl− secretion, inhibits both the absorptive Isc and fluid absorption, and decreases HCO3− secretion. Likewise, in intestinal tissues from Gulf toadfish acclimated to 60 ppt, RGN also inhibits the absorptive Isc and fluid absorption but to an even greater extent, corresponding with the mRNA expression data. In contrast, RGN does not alter Cl− flux and, instead, elevates HCO−3 secretion in the 60-ppt group, suggesting increased apical Cl−/HCO−3 exchange activity by SLC26a6. Overall, these findings reinforce the hypotheses that the guanylin peptide system is important for salinity acclimatization and that the secretory response could facilitate the removal of solids, such as CaCO3 precipitates, from the intestine.",
keywords = "Fluid Secretion, HCO<sup>–</sup><inf>3</inf> secretion, Hypersalinity, Marine teleost, Osmoregulation",
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year = "2015",
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pages = "R399--R409",
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TY - JOUR

T1 - The differential role of renoguanylin in osmoregulation and apical Cl−/HCO−3 exchange activity in the posterior intestine of the gulf toadfish (Opsanus beta)

AU - Ruhr, Ilan M.

AU - Mager, Edward M.

AU - Takei, Yoshio

AU - Grosell, Martin

PY - 2015/8/18

Y1 - 2015/8/18

N2 - The guanylin family of peptides are effective regulators of intestinal physiology in marine teleosts. In the distal intestinal segments, they inhibit or reverse fluid absorption by inhibiting the absorptive shortcircuit current (Isc). The present findings demonstrate that mRNA from guanylin and uroguanylin, as well as at least one isoform of the guanylin peptide receptor, apical guanylyl cyclase-C (GC-C), was highly expressed in the intestine and rectum of the Gulf toadfish (Opsanus beta). In the posterior intestine, GC-C, as well as the cystic fibrosis transmembrane conductance regulator and basolateral Na+/ K+/2Cl− cotransporter, which comprise a Cl−-secretory pathway, were transcriptionally upregulated in 60 parts per thousand (ppt). The present study also shows that, in intestinal tissues from Gulf toadfish held in 35 ppt, renoguanylin (RGN) expectedly causes net Cl− secretion, inhibits both the absorptive Isc and fluid absorption, and decreases HCO3− secretion. Likewise, in intestinal tissues from Gulf toadfish acclimated to 60 ppt, RGN also inhibits the absorptive Isc and fluid absorption but to an even greater extent, corresponding with the mRNA expression data. In contrast, RGN does not alter Cl− flux and, instead, elevates HCO−3 secretion in the 60-ppt group, suggesting increased apical Cl−/HCO−3 exchange activity by SLC26a6. Overall, these findings reinforce the hypotheses that the guanylin peptide system is important for salinity acclimatization and that the secretory response could facilitate the removal of solids, such as CaCO3 precipitates, from the intestine.

AB - The guanylin family of peptides are effective regulators of intestinal physiology in marine teleosts. In the distal intestinal segments, they inhibit or reverse fluid absorption by inhibiting the absorptive shortcircuit current (Isc). The present findings demonstrate that mRNA from guanylin and uroguanylin, as well as at least one isoform of the guanylin peptide receptor, apical guanylyl cyclase-C (GC-C), was highly expressed in the intestine and rectum of the Gulf toadfish (Opsanus beta). In the posterior intestine, GC-C, as well as the cystic fibrosis transmembrane conductance regulator and basolateral Na+/ K+/2Cl− cotransporter, which comprise a Cl−-secretory pathway, were transcriptionally upregulated in 60 parts per thousand (ppt). The present study also shows that, in intestinal tissues from Gulf toadfish held in 35 ppt, renoguanylin (RGN) expectedly causes net Cl− secretion, inhibits both the absorptive Isc and fluid absorption, and decreases HCO3− secretion. Likewise, in intestinal tissues from Gulf toadfish acclimated to 60 ppt, RGN also inhibits the absorptive Isc and fluid absorption but to an even greater extent, corresponding with the mRNA expression data. In contrast, RGN does not alter Cl− flux and, instead, elevates HCO−3 secretion in the 60-ppt group, suggesting increased apical Cl−/HCO−3 exchange activity by SLC26a6. Overall, these findings reinforce the hypotheses that the guanylin peptide system is important for salinity acclimatization and that the secretory response could facilitate the removal of solids, such as CaCO3 precipitates, from the intestine.

KW - Fluid Secretion

KW - HCO<sup>–</sup><inf>3</inf> secretion

KW - Hypersalinity

KW - Marine teleost

KW - Osmoregulation

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DO - 10.1152/ajpregu.00118.2015

M3 - Article

C2 - 26017493

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