Regulation of apical h +-atpase activity and intestinal HCO 3 - secretion in marine fish osmoregulation

S. Guffey, A. Esbaugh, Martin Grosell

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42 Citations (Scopus)

Abstract

The absorption of Cl - and water from ingested seawater in the marine fish intestine is accomplished partly through Cl -/HCO 3 - exchange. Recently, a H - pump (vacuolar-type H +-ATPase) was found to secrete acid into the intestinal lumen, and it may serve to titrate luminal HCO 3 - and facilitate further Cl -/HCO 3 - exchange, especially in the posterior intestine, where adverse concentration gradients could limit Cl -/HCO 3 - exchange. The H + pump is expressed in all intestinal segments and in gill tissue of gulf toadfish (Opsanus beta) maintained in natural seawater. After acute transfer of toadfish to 60 ppt salinity, H + pump expression increased 20-fold in the posterior intestine. In agreement with these observations was a fourfold-increased H +- ATPase activity in the posterior intestine of animals acclimated to 60 ppt salinity. Interestingly, Na +-K +-ATPase activity was elevated in the anterior intestine and gill, but not in the posterior intestine. Apical acid secretion by isolated intestinal tissue mounted in Ussing chambers fitted with pH-stat titration systems increased after acclimation to hypersalinity in the anterior and posterior intestine, titrating >20% of secreted bicarbonate. In addition, net base secretion increased in hypersalinity-acclimated fish and was ~70% dependent on serosal HCO 3 -. Protein localization by immunohistochemistry confirmed the presence of the vacuolar-type H +-ATPase in the apical region of intestinal enterocytes. These results show that the H + pump, especially in the posterior intestine, plays an important role in hypersaline osmoregulation and that it likely has significant effects on HCO 3 - accumulation in the intestinal lumen and, therefore, the continued absorption of Cl - and water.

Original languageEnglish
Pages (from-to)1682-1691
Number of pages10
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume301
Issue number6
DOIs
StatePublished - Dec 1 2011

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Osmoregulation
Intestines
Adenosine Triphosphatases
Fishes
Proton Pumps
Batrachoidiformes
Vacuolar Proton-Translocating ATPases
Salinity
Seawater
Intestinal Secretions
Acids
Proton-Translocating ATPases
Water
Enterocytes
Acclimatization
Bicarbonates
Immunohistochemistry

Keywords

  • Ion transport
  • Ph-stat titration
  • Posterior intestine
  • Salinity
  • Water absorption

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

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title = "Regulation of apical h +-atpase activity and intestinal HCO 3 - secretion in marine fish osmoregulation",
abstract = "The absorption of Cl - and water from ingested seawater in the marine fish intestine is accomplished partly through Cl -/HCO 3 - exchange. Recently, a H - pump (vacuolar-type H +-ATPase) was found to secrete acid into the intestinal lumen, and it may serve to titrate luminal HCO 3 - and facilitate further Cl -/HCO 3 - exchange, especially in the posterior intestine, where adverse concentration gradients could limit Cl -/HCO 3 - exchange. The H + pump is expressed in all intestinal segments and in gill tissue of gulf toadfish (Opsanus beta) maintained in natural seawater. After acute transfer of toadfish to 60 ppt salinity, H + pump expression increased 20-fold in the posterior intestine. In agreement with these observations was a fourfold-increased H +- ATPase activity in the posterior intestine of animals acclimated to 60 ppt salinity. Interestingly, Na +-K +-ATPase activity was elevated in the anterior intestine and gill, but not in the posterior intestine. Apical acid secretion by isolated intestinal tissue mounted in Ussing chambers fitted with pH-stat titration systems increased after acclimation to hypersalinity in the anterior and posterior intestine, titrating >20{\%} of secreted bicarbonate. In addition, net base secretion increased in hypersalinity-acclimated fish and was ~70{\%} dependent on serosal HCO 3 -. Protein localization by immunohistochemistry confirmed the presence of the vacuolar-type H +-ATPase in the apical region of intestinal enterocytes. These results show that the H + pump, especially in the posterior intestine, plays an important role in hypersaline osmoregulation and that it likely has significant effects on HCO 3 - accumulation in the intestinal lumen and, therefore, the continued absorption of Cl - and water.",
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T1 - Regulation of apical h +-atpase activity and intestinal HCO 3 - secretion in marine fish osmoregulation

AU - Guffey, S.

AU - Esbaugh, A.

AU - Grosell, Martin

PY - 2011/12/1

Y1 - 2011/12/1

N2 - The absorption of Cl - and water from ingested seawater in the marine fish intestine is accomplished partly through Cl -/HCO 3 - exchange. Recently, a H - pump (vacuolar-type H +-ATPase) was found to secrete acid into the intestinal lumen, and it may serve to titrate luminal HCO 3 - and facilitate further Cl -/HCO 3 - exchange, especially in the posterior intestine, where adverse concentration gradients could limit Cl -/HCO 3 - exchange. The H + pump is expressed in all intestinal segments and in gill tissue of gulf toadfish (Opsanus beta) maintained in natural seawater. After acute transfer of toadfish to 60 ppt salinity, H + pump expression increased 20-fold in the posterior intestine. In agreement with these observations was a fourfold-increased H +- ATPase activity in the posterior intestine of animals acclimated to 60 ppt salinity. Interestingly, Na +-K +-ATPase activity was elevated in the anterior intestine and gill, but not in the posterior intestine. Apical acid secretion by isolated intestinal tissue mounted in Ussing chambers fitted with pH-stat titration systems increased after acclimation to hypersalinity in the anterior and posterior intestine, titrating >20% of secreted bicarbonate. In addition, net base secretion increased in hypersalinity-acclimated fish and was ~70% dependent on serosal HCO 3 -. Protein localization by immunohistochemistry confirmed the presence of the vacuolar-type H +-ATPase in the apical region of intestinal enterocytes. These results show that the H + pump, especially in the posterior intestine, plays an important role in hypersaline osmoregulation and that it likely has significant effects on HCO 3 - accumulation in the intestinal lumen and, therefore, the continued absorption of Cl - and water.

AB - The absorption of Cl - and water from ingested seawater in the marine fish intestine is accomplished partly through Cl -/HCO 3 - exchange. Recently, a H - pump (vacuolar-type H +-ATPase) was found to secrete acid into the intestinal lumen, and it may serve to titrate luminal HCO 3 - and facilitate further Cl -/HCO 3 - exchange, especially in the posterior intestine, where adverse concentration gradients could limit Cl -/HCO 3 - exchange. The H + pump is expressed in all intestinal segments and in gill tissue of gulf toadfish (Opsanus beta) maintained in natural seawater. After acute transfer of toadfish to 60 ppt salinity, H + pump expression increased 20-fold in the posterior intestine. In agreement with these observations was a fourfold-increased H +- ATPase activity in the posterior intestine of animals acclimated to 60 ppt salinity. Interestingly, Na +-K +-ATPase activity was elevated in the anterior intestine and gill, but not in the posterior intestine. Apical acid secretion by isolated intestinal tissue mounted in Ussing chambers fitted with pH-stat titration systems increased after acclimation to hypersalinity in the anterior and posterior intestine, titrating >20% of secreted bicarbonate. In addition, net base secretion increased in hypersalinity-acclimated fish and was ~70% dependent on serosal HCO 3 -. Protein localization by immunohistochemistry confirmed the presence of the vacuolar-type H +-ATPase in the apical region of intestinal enterocytes. These results show that the H + pump, especially in the posterior intestine, plays an important role in hypersaline osmoregulation and that it likely has significant effects on HCO 3 - accumulation in the intestinal lumen and, therefore, the continued absorption of Cl - and water.

KW - Ion transport

KW - Ph-stat titration

KW - Posterior intestine

KW - Salinity

KW - Water absorption

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JO - American Journal of Physiology - Cell Physiology

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