Expression Profiles of Branchial FXYD Proteins in the Brackish Medaka Oryzias dancena: A Potential Saltwater Fish Model for Studies of Osmoregulation

Abstract

FXYD proteins are novel regulators of Na+-K+-ATPase (NKA). In fish subjected to salinity challenges, NKA activity in osmoregulatory organs (e.g., gills) is a primary driving force for the many ion transport systems that act in concert to maintain a stable internal environment. Although teleostean FXYD proteins have been identified and investigated, previous studies focused on only a limited group of species. The purposes of the present study were to establish the brackish medaka (Oryzias dancena) as a potential saltwater fish model for osmoregulatory studies and to investigate the diversity of teleostean FXYD expression profiles by comparing two closely related euryhaline model teleosts, brackish medaka and Japanese medaka (O. latipes), upon exposure to salinity changes. Seven members of the FXYD protein family were identified in each medaka species, and the expression of most branchial fxyd genes was salinity-dependent. Among the cloned genes, fxyd11 was expressed specifically in the gills and at a significantly higher level than the other fxyd genes. In the brackish medaka, branchial fxyd11 expression was localized to the NKA-immunoreactive cells in gill epithelia. Furthermore, the FXYD11 protein interacted with the NKA α-subunit and was expressed at a higher level in freshwater-acclimated individuals relative to fish in other salinity groups. The protein sequences and tissue distributions of the FXYD proteins were very similar between the two medaka species, but different expression profiles were observed upon salinity challenge for most branchial fxyd genes. Salinity changes produced different effects on the FXYD11 and NKA α-subunit expression patterns in the gills of the brackish medaka. To our knowledge, this report is the first to focus on FXYD expression in the gills of closely related euryhaline teleosts. Given the advantages conferred by the well-developed Japanese medaka system, we propose the brackish medaka as a saltwater fish model for osmoregulatory studies.

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

“…For example, pituitary hormones are essential for freshwater survival of Mozambique tilapia (Dharmamba and Maetz, 1972), while coho salmon ( Oncorhynchus kisutch ) and rainbow trout ( Salmo gairdneri ) can maintain osmotic balance in fresh water following hypophysectomy (Björnsson and Hansson, 1984; Björnsson et al, 1987). The functions of FXYD proteins in teleosts are becoming better resolved (Tipsmark, 2008; Wang et al, 2008; Saito et al, 2010; Yang et al, 2013), and based on how NKA enzyme activity is regulated during salinity challenges (McCormick, 1995), it is likely that prolactin will emerge as a key modulator of NKA kinetics upon freshwater transfer via FXYD-11. Links between prolactin and FXYD proteins clearly warrant further comparative study in euryhaline models such as spotted green pufferfish ( Tetraodon nigroviridis ) and medaka ( Oryzias dancena and O. latipes ) (Wang et al, 2008; Yang et al, 2013).…”

Early vertebrate origin and diversification of small transmembrane regulators of cellular ion transport

“…), while Tyr is mutated to Phe (FXFD) in FXYD3/4‐2 (fxyd9) of different Actinopterygii species (Tipsmark, ; Yang et al . ; Fig. ).…”

“…OdFXYD9 , OlFXYD9 ) (Yang et al . ) and suffixes denoting the species (e.g. FXYD9dr ) (Sweadner & Rael, ).…”

“…Some of the supposedly fish‐specific FXYDs (FXYD8–12) (Yang et al . ) could be orthologous to the mammalian FXYDs (FXYD1–7). Such uncertainties in the current FXYD classification hamper comparative studies of FXYD function in fishes and other lower vertebrates.…”

“…Secondly, evolutionary relationships between the fish and the mammalian FXYDs are unclear (Sweadner & Rael, 2000;Mahmmoud et al 2003;Tipsmark, 2008). Some of the supposedly fish-specific FXYDs (FXYD8-12) (Yang et al 2013) could be orthologous to the mammalian FXYDs (FXYD1-7). Such uncertainties in the current FXYD classification hamper comparative studies of FXYD function in fishes and other lower vertebrates.…”