Site-specific effects of dietary salt intake on guanylin and uroguanylin mRNA expression in rat intestine

Carrithers, Stephen L.; Cai, Weiyan; Greenberg, Richard N.; Ott, Cobern E.

doi:10.1016/s0167-0115(02)00069-1

Cited by 37 publications

(31 citation statements)

References 26 publications

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“…Although the physiological function of the guanylin peptides in teleosts is still uncertain, studies have shown that they may play a role in long-term salinity adaptation. Indeed, GN and UGN mRNA expression increase following a 24-h transfer from freshwater (FW) to SW by at least twofold in the Japanese eel (Anguilla japonica) (12,39,67), a pattern also observed in the rat after salt loading of intestinal tissues (8,40,45). In mammalian tissues, GN and UGN either increase the secretory short-circuit current (I sc ) of the intestine or reverse an absorptive I sc , while in teleosts, these peptides have no effect on the anterior intestine of the Japanese eel, but do reverse the I sc of the mid and posterior intestine, resulting in a net serosa-to-mucosa flux of, presumably, Cl Ϫ ions (38,54,68).…”

mentioning

confidence: 77%

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

Ruhr

Bodinier

Mager

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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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.

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mentioning

confidence: 77%

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

Ruhr

Bodinier

Mager

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In mammals, guanylin and uroguanylin cause increased HCO 3 Ϫ secretion into the intestinal lumen; accordingly, it has been suggested that uroguanylin might play a role in defending the pH of the intestine, as acidic chyme enters from the stomach (11). Conversely, guanylin transcription and secretion are increased in rat intestinal tissues when perfused with high salt concentrations and decreased with low salt intake (7,29,32). Conceivably, in seawater teleosts, uroguanylin plays a more prominent role in digestion, and guanylin takes a more active part in osmoregulatory processes.…”

Section: Significance and Perspectivesmentioning

confidence: 99%

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

Ruhr

Takei

Grosell

2016

American Journal of Physiology-Regulatory, Integrative and Comp

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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...

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“…There is now additional evidence that guanylin and uroguanylin have both local intestinal (paracrine) and endocrine functions, forming a potential enteric-renal link to coordinate salt ingestion with natriuresis (for reviews, see Forte et al,. Circumstantial evidence suggests that both peptides, particularly uroguanylin, function as endocrine intestinal natriuretic hormones because (a) both circulate in the bloodstream (6)(7)(8); (b) high-salt intake increases uroguanylin and guanylin mRNA (9,10), as well as urinary excretion of uroguanylin (11); and (c) uroguanylin levels are increased in the circulation of patients with renal disease and congestive heart failure (12,13). In addition, the cellular localization of uroguanylin in enterocytes of the proximal small intestine is consistent with the luminal and systemic secretion of enteric uroguanylin (11,(14)(15)(16).…”

Section: Introductionmentioning

confidence: 99%

Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load

Lorenz¹,

Nieman²,

Sabo³

et al. 2003

J. Clin. Invest.

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Guanylin and uroguanylin, peptides synthesized in the intestine and kidney, have been postulated to have both paracrine and endocrine functions, forming a potential enteric-renal link to coordinate salt ingestion with natriuresis. To explore the in vivo role of uroguanylin in the regulation of sodium excretion, we created gene-targeted mice in which uroguanylin gene expression had been ablated. Northern and Western analysis confirmed the absence of uroguanylin message and protein in knockout mice, and cGMP levels were decreased in the mucosa of the small intestine. Ussing chamber analysis of jejunum revealed that Na+/H+ exchanger–mediated Na+ absorption and tissue conductance was not altered in the knockout animals, but short-circuit current, an index of electrogenic anion secretion, was reduced. Renal clearance measurements showed that uroguanylin deficiency results in impaired ability to excrete an enteral load of NaCl, primarily due to an inappropriate increase in renal Na+ reabsorption. Finally, telemetric recordings of blood pressure demonstrated increased mean arterial pressure in uroguanylin knockout animals that was independent of the level of dietary salt intake. Together, these findings establish a role for uroguanylin in an enteric-renal communication axis as well as a fundamental principle of this axis in the maintenance of salt homeostasis in vivo

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Site-specific effects of dietary salt intake on guanylin and uroguanylin mRNA expression in rat intestine

Cited by 37 publications

References 26 publications

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

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

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

Uroguanylin knockout mice have increased blood pressure and impaired natriuretic response to enteral NaCl load

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