Low salt intake down-regulates the guanylin signaling pathway in rat distal colon

Li, Zhiping; Knowles, Joshua W.; Goyeau, Dominique; Prabhakar, Subhash; Short, Douglas B.; Perkins, Ashley; Goy, Michael F.

doi:10.1016/s0016-5085(96)70037-9

Cited by 46 publications

(26 citation statements)

References 31 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).…”

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confidence: 81%

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: 81%

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 the rat distal colon, high sodium diet did not change the expression of guanylin, but low sodium diet down-regulates its expression (44). In the mouse kidney, however, high oral salt intake increases the expression of uroguanylin (45).…”

Section: A Novel Guanylin Family In Eel-mentioning

confidence: 92%

A Novel Guanylin Family (Guanylin, Uroguanylin, and Renoguanylin) in Eels

Yuge

Inoue

Hyodo

et al. 2003

Journal of Biological Chemistry

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As the intestine is an essential organ for fish osmoregulation, the intestinal hormone guanylins may perform major functions, especially in euryhaline fish such as eels and salmonids. From the intestine of an eel, we identified cDNAs encoding three distinct guanylin-like peptides. Based on the sequence of mature peptide and sites of production, we named them guanylin, uroguanylin, and renoguanylin. Renoguanylin is a novel peptide that possesses the characteristics of both guanylin and uroguanylin and was abundantly expressed in the kidney. By immunohistochemistry, guanylin was localized exclusively in goblet cells, but not enterochromaffin cells, of the intestine. After transfer of eels from fresh water to seawater, mRNA expression of guanylin and uroguanylin did not change for 3 h, but it increased after 24 h. The increase was profound (2-6-fold) after adaptation to seawater. The expression of uroguanylin was also up-regulated in the kidney of seawater-adapted eels, but that of renoguanylin was not so prominent as other guanylins in both intestine and kidney. Collectively, the novel eel guanylin family appears to have important functions for seawater adaptation, particularly long-term adaptation. Eel guanylin may be secreted from goblet cells into the lumen with mucus in response to increased luminal osmolality and act on the epithelium to regulate water and salt absorption.

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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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Low salt intake down-regulates the guanylin signaling pathway in rat distal colon

Cited by 46 publications

References 31 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

A Novel Guanylin Family (Guanylin, Uroguanylin, and Renoguanylin) in Eels

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

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