Identification of intestinal bicarbonate transporters involved in formation of carbonate precipitates to stimulate water absorption in marine teleost fish

Yukihiro Kurita, Tsutomu Nakada, Akira Kato, Hiroyuki Doi, Abinash C. Mistry, Min Hwang Chang, Michael F Romero, Shigehisa Hirose

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Abstract

Marine teleost fish precipitate divalent cations as carbonate deposits in the intestine to minimize the potential for excessive Ca 2+ entry and to stimulate water absorption by reducing luminal osmotic pressure. This carbonate deposit formation, therefore, helps maintain osmoregulation in the seawater (SW) environment and requires controlled secretion of HCO 3 - to match the amount of Ca 2+ entering the intestinal lumen. Despite its physiological importance, the process of HCO 3 - secretion has not been characterized at the molecular level. We analyzed the expression of two families of HCO 3 - transporters, Slc4 and Slc26, in fresh-water-and SW-acclimated euryhaline pufferfish, mefugu (Takifugu obscurus), and obtained the following candidate clones: NBCe1 (an Na +-HCO 3 - cotransporter) and Slc26a6A and Slc26a6B (putative Cl -/HCO 3 - exchangers). Heterologous expression in Xenopus oocytes showed that Slc26a6A and Slc26a6B have potent HCO 3 --transporting activity as electrogenic Cl -/nHCO 3 - exchangers, whereas mefugu NBCe1 functions as an electrogenic Na +-nHCO 3 - cotransporter. Expression of NBCe1 and Slc26a6A was highly induced in the intestine in SW and expression of Slc26a6B was high in the intestine in SW and fresh water, suggesting their involvement in HCO 3 - secretion and carbonate precipitate formation. Immunohistochemistry showed staining on the apical (Slc26a6A and Slc26a6B) and basolateral (NBCe1) membranes of the intestinal epithelial cells in SW. We therefore propose a mechanism for HCO 3 - transport across the intestinal epithelial cells of marine fish that includes basolateral HCO 3 - uptake (NBCe1) and apical HCO 3 - secretion (Slc26a6A and Slc26a6B).

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume294
Issue number4
DOIs
StatePublished - Apr 2008

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Keywords

  • Calcium carbonate
  • Intestine
  • NBC
  • Osmoregulation
  • Slc26

ASJC Scopus subject areas

  • Physiology

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