Glycogen phosphorylase in glycogen-rich cells is involved in the energy supply for ion regulation in fish gill epithelia

Abstract

The molecular and cellular mechanisms behind glycogen metabolism and the energy metabolite translocation between mammal neurons and astrocytes have been well studied. A similar mechanism is proposed for rapid mobilization of local energy stores to support energy-dependent transepithelial ion transport in gills of the Mozambique tilapia (Oreochromis mossambicus). A novel gill glycogen phosphorylase isoform (tGPGG), which catalyzes the initial degradation of glycogen, was identified in branchial epithelial cells of O. mossambicus. Double in situ hybridization and immunocytochemistry demonstrated that tGPGG mRNA and glycogen were colocalized in glycogen-rich cells (GRCs), which surround ionocytes (labeled with a Na(+)-K(+)-ATPase antiserum) in gill epithelia. Concanavalin-A (a marker for the apical membrane) labeling indicated that GRCs and mitochondria-rich cells share the same apical opening. Quantitative real-time PCR analyses showed that tGPGG mRNA expression levels specifically responded to environmental salinity changes. Indeed, the glycogen content, glycogen phosphorylase (GP) protein level and total activity, and the density of tGPGG-expressing cells (i.e., GRCs) in fish acclimated to seawater (SW) were significantly higher than those in freshwater controls. Short-term acclimation to SW caused an evident depletion in the glycogen content of GRCs. Taken altogether, tGPGG expression in GRCs is stimulated by hyperosmotic challenge, and this may catalyze initial glycogen degradation to provide the adjacent ionocytes with energy to carry out iono- and osmoregulatory functions.

Metabolic substrates are not mobilized from the osmoregulatory organs (gills and kidney) of the estuarine pufferfishes Sphoeroides greeleyi and S. testudineus upon short-term salinity reduction

“…The hypothesis tested here was that the two species of pufferfishes, with distinct tolerances of seawater dilution, might differ in their short-term use of metabolic substrates stored in their main osmoregulatory organs, when challenged with salinity alteration. The disturbance in the osmotic homeostasis of these fish would impose a metabolic demand of the energetic substrates stored in their osmoregulatory organs, thus potentially more readily available (Tseng et al, 2007). This hypothesis is supported by previous reports that rapid alterations in transport mechanisms (including changes in Na + , K + -ATPase activity) ensue when estuarine fishes endure salinity changes in their environment (Mancera & McCormick, 2000;Sakamoto et al, 2000;Marshall, 2003;Wood & Laurent, 2003;Prodocimo et al, 2007).…”

“…Alternatively, the gills of the pufferfishes may provide the glucose they need, since they have glycogen levels ~20-100-fold higher than glycogen contents of the gills of Sparus auratus (Sangiao-Alvarellos et al, 2003Laíz-Carrión et al, 2002, measured using the same methodology (Keppler & Decker, 1974). Indeed, this mobilization of branchial glycogen has been recently demonstrated in the gills of the Mozambique tilapia (Tseng et al, 2007).…”

“…The energy requirement of the gills and kidney is partially maintained by using the metabolic substrates stored in these organs (Tseng et al, 2007). However, there is scant information about the mobilization of their metabolic substrates according to the salinity of acclimation in fish (Hansen et al, 1999;Laiz-Carrión et al, 2002Sangiao-Alvarellos et al, 2003.…”

“…The effects of short-term (hours) salinity changes on metabolic reserves of fish have been poorly investigated (Woo & Wu, 1982;Nakano et al, 1998;Tseng et al, 2007). In the freshwater euryhaline tilapia (Oreochromis mossambicus) liver glycogen content increased after 6 hours in 23‰ (Nakano et al, 1998), but rapid mobilization of the local reserves of branchial glycogen has been observed to fuel ion transport mechanisms in ionocytes of the gills of tilapia upon short-term (3 hours) increase in salinity (25‰) (Tseng et al, 2007).…”

“…In the freshwater euryhaline tilapia (Oreochromis mossambicus) liver glycogen content increased after 6 hours in 23‰ (Nakano et al, 1998), but rapid mobilization of the local reserves of branchial glycogen has been observed to fuel ion transport mechanisms in ionocytes of the gills of tilapia upon short-term (3 hours) increase in salinity (25‰) (Tseng et al, 2007). In the marine teleosts red grouper (Epinephelus akaara) and black sea bream (Mylio macrocephalus), shortterm (6 hours) exposure to 7‰ salinity (from 30‰) did not induce consumption of liver glycogen content (Woo & Wu, 1982).…”