Freshwater Fish Gill Ion Transport: August Krogh to morpholinos and microprobes

Abstract

August Krogh proposed that freshwater fishes (and other freshwater animals) maintain body NaCl homoeostasis by extracting these ions from the environment via separate Na(+) /NH(4)(+) and Cl(-) /HCO(3)(-) exchangers in the gill epithelium. Subsequent data from other laboratories suggested that Na(+) uptake was more probably coupled to H(+) secretion via a vesicular proton pump (V-ATPase) electrically coupled to a Na(+) channel. However, despite uncertainty about electrochemical gradients, evidence has accrued that epithelial Na(+) /H(+) exchange indeed may be an alternative pathway for Na(+) uptake. The specific pathways for Na(+) uptake may be species and environment specific. An apical Cl(-) /HCO(3)(-) exchanger is generally accepted for most species (some species do not extract Cl(-) from freshwater), but the relative roles of anion exchanger-like (SLC4A1) vs. pendrin-like (SLC26Z4) exchangers are unknown, and also may be species specific. Most recently, data have supported the presence of an apical Na(+) + Cl(-) cotransporter (NCC-type), despite thermodynamic uncertainty. Ammonia extrusion may be via NH(3) diffusing through the paracellular junctions or NH(4) (+) substitution on both basolateral and apical ionic exchangers (Na(+) + K(+) -ATPase; Na(+) + K(+) + Cl(-) - cotransporter; and Na(+) /H(+) exchanger), but recent evidence suggests that Rhesus-glycoproteins mediate both basolateral and apical movement of ammonia.

Feeding induces translocation of vacuolar proton ATPase and pendrin to the membrane of leopard shark (Triakis semifasciata) mitochondrion-rich gill cells

“…The presence of NKA and VHA in two distinct cell populations separates elasmobranchs from teleost fishes. In freshwater teleosts, simultaneous expression of NKA and VHA is thought to drive Na + uptake and NH 3 excretion during osmoregulation and nitrogen balance (Evans, 2011), and has been shown in gills from rainbow trout (Galvez et al, 2002; Lin et al, 1994; Wilson et al, 2000a), killifish (Katoh et al, 2003), mudskipper (Wilson et al, 2000b), zebrafish (Liao et al, 2009), and several species of intertidal blennies (Uchiyama et al, 2012). Marine teleost gills also have several types of NKA-rich cells and although not widely reported, NKA and VHA may co-localize in the same cell as observed in a small population of branchial MR cells from longhorn sculpin (Catches et al, 2006).…”

Global Protein Expression Profiling of Zebrafish Organs Based on in Vivo Incorporation of Stable Isotopes

“…Recently, transporters such as vesicular proton pumps (V-ATPase), anion exchangers (SLC), Na + / K + ATPase transporter (NKA), and Na + /H + exchangers (NHE) were identified to regulate ammonia and ion homeostasis in freshwater fishes. 42 Here, we quantified more than ∼130 transporters and found several specific transporters which were exclusively expressed in gill tissue. The highest SILAC ratio was found for the ATPase atp1a1a.2 (Na + /K + transporting, alpha 1a polypeptide, tandem duplicate 2), an enzyme which regulates sodium and potassium exchange within the plasma membrane.…”

Prolactin and teleost ionocytes: New insights into cellular and molecular targets of prolactin in vertebrate epithelia

“…To date, several models have been proposed to explain how ionocytes facilitate ion uptake against strong electrochemical gradients (reviewed by Evans, 2011) and uncertainty regarding the cellular mechanisms of ion uptake has impeded progress towards understanding the specific actions of prolactin. Nonetheless, exogenous prolactin has been shown to stimulate ion uptake by cultured branchial epithelia (Zhou et al, 2003), suggesting that genes regulating freshwater-type ionocyte function might be good candidates as targets of prolactin.…”