Regulation of glycogen metabolism in gills and liver of the euryhaline tilapia (Oreochromis mossambicus) during acclimation to seawater
Tóm tắt
Glucose, which plays a central role in providing energy for metabolism, is primarily stored as glycogen. The synthesis and degradation of glycogen are mainly initialized by glycogen synthase (GS) and glycogen phosphorylase (GP),respectively. The present study aimed to examine the glycogen metabolism in fish liver and gills during acute exposure to seawater. In tilapia(Oreochromis mossambicus) gill, GP, GS and glycogen were immunocytochemically colocalized in a specific group of glycogen-rich (GR)cells, which are adjacent to the gill's main ionocytes, mitochondrion-rich(MR) cells. Na+/K+-ATPase activity in the gills, protein expression and/or activity of GP and GS and the glycogen content of the gills and liver were examined in tilapia after their acute transfer from freshwater(FW) to 25‰ seawater (SW). Gill Na+/K+-ATPase activity rapidly increased immediately after SW transfer. Glycogen content in both the gills and liver were significantly depleted after SW transfer, but the depletion occurred earlier in gills than in the liver. Gill GP activity and protein expression were upregulated 1–3 h post-transfer and eventually recovered to the normal level as determined in the control group. At the same time, GS protein expression was downregulated. Similar changes in liver GP and GS protein expression were also observed but they occurred later at 6–12 h post-transfer. In conclusion, GR cells are initially stimulated to provide prompt energy for neighboring MR cells that trigger ion-secretion mechanisms. Several hours later, the liver begins to degrade its glycogen stores for the subsequent energy supply.
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Ando, M., Mukuda, T. and Kozaka, T. (2003). Water metabolism in the eel acclimated to sea water: from mouth to intestine. Comp. Biochem. Physiol.136B,621-633.
Assem, H. and Hanke, W. (1979). Concentrations of carbohydrates during osmotic adjustment of the euryhaline teleost, Tilapia mossambica.Comp. Biochem. Physiol.64, 5-16.
Baba, O. (1993). Production of monoclonal antibody that recognizes glycogen and its application for immunohistochemistry. Kokubyo Gakkai Zasshi60,264-287.
Bacca, H., Huvet, A., Fabioux, C., Daniel, J. Y., Delaporte, M.,Pouvreau, S., Van Wormhoudt, A. and Moal, J. (2005). Molecular cloning and seasonal expression of oyster glycogen phosphorylase and glycogen synthase genes. Comp. Biochem. Physiol.140B,635-646.
Boeuf, G. and Payan, P. (2001). How should salinity influence fish growth? Comp. Biochem. Physiol.130C,411-423.
Bollen, M., Keppens, S. and Stalmans, W.(1998). Specific features of glycogen metabolism in the liver. Biochem. J.336,19-31.
Brown, A. M., Tekkok, S. B. and Ransom, B. R.(2003). Glycogen regulation and functional role in mouse white matter. J. Physiol.549,501-512.
Cohen, P. (1982). The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature296,613-620.
Evans, D. H., Piermarini, P. M. and Choe, K. P.(2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid–base regulation, and excretion of nitrogenous waste. Physiol. Rev.85, 97-177.
Febry, R. and Lutz, P. (1987). Energy partitioning in fish: the activity-related cost of osmoregulation in a euryhaline cichlid. J. Exp. Biol.128, 63-85.
Fernandez-Novell, J. M., Arino, J., Vilaro, S. and Guinovart, J. J. (1992). Glucose induces the translocation and the aggregation of glycogen synthase in rat hepatocytes. Biochem. J.281,443-448.
Frolow, J. and Milligan, C. L. (2004). Hormonal regulation of glycogen metabolism in white muscle slices from rainbow trout(Oncorhynchus mykiss Walbaum). Am. J. Physiol.287,R1344-R1353.
Garcia-Rocha, M., Roca, A., De La Iglesia, N., Baba, O.,Fernandez-Novell, J. M., Ferrer, J. C. and Guinovart, J. J.(2001). Intracellular distribution of glycogen synthase and glycogen in primary cultured rat hepatocytes. Biochem. J.357,17-24.
Greenberg, C. C., Jurczak, M. J., Danos, A. M. and Brady, M. J. (2006). Glycogen branches out: new perspectives on the role of glycogen metabolism in the integration of metabolic pathways.Am. J. Physiol.291, E1-E8.
Hardy, T. A. and Roach, P. J. (1993). Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation. J. Biol. Chem.268,23799-23805.
Higgins, D. G. and Sharp, P. M. (1988). CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene73,237-244.
Higgins, D. G., Thompson, J. D. and Gibson, T. J.(1996). Using CLUSTAL for multiple sequence alignments. Meth. Enzymol.266,383-402.
Hirose, S., Kaneko, T., Naito, N. and Takei, Y.(2003). Molecular biology of major components of chloride cells. Comp. Biochem. Physiol.136B,593-620.
Hoffman, J. and Katz, U. (1998). Glyconeogenesis and urea synthesis in the toad Bufo viridis during acclimation to water restriction. Physiol. Zool.71, 85-92.
Hwang, P. P. (1987). Tolerance and ultrastructural response of branchial chloride cells on salinity changes in euryhaline teleost, Oreochromis mossambicus.Mar. Biol.94,643-649.
Hwang, P. P., Sun, C. M. and Wu, S. M. (1989). Changes of plasma osmolality, chloride concentration, and gill Na,K-ATPase activity in tilapia, Oreochromis mossambicus, during seawater acclimation. Mar. Biol.100,295-299.
Hwang, P. P., Lee, T. H., Weng, C. F., Fang, M. J. and Cho, G. Y. (1999). Presence of Na-K-ATPase in mitochondria-rich cells in yolk-sac epithelium of larvae of the teleost, Oreochromis mossambicus.Physiol. Biochem. Zool.72,138-144.
Karlsson, J. (1979). Some features of glycogen metabolism in human skeletal muscle. Bibl. Nutr. Dieta27,121-125.
Kelly, S. P., Chow, I. N. and Woo, N. Y.(1999). Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. J. Exp. Zool.283,226-241.
Lee, T. H., Feng, S. H., Lin, C. H., Hwang, Y. H., Huang, C. L. and Hwang, P. P. (2003). Ambient salinity modulates the expression of sodium pumps in branchial mitochondria-rich cells of Mozambique tilapia, Oreochromis mossambicus.Zool. Sci.20, 29-36.
Mahrenholz, A. M., Wang, Y. H. and Roach, P. J.(1988). Catalytic site of rabbit glycogen synthase isozymes. Identification of an active site lysine close to the amino terminus of the subunit. J. Biol. Chem.263,10561-10567.
Marshall, W. S., Emberley, T. R., Singer, T. D., Bryson, S. E. and McCormick, S. D. (1999). Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J. Exp. Biol.202,1535-1544.
Milligan, C. L. (2003). A regulatory role for cortisol in muscle glycogen metabolism in rainbow trout Oncorhynchus mykiss Walbaum. J. Exp. Biol.206,3167-3173.
Morgan, J. D. and Iwama, G. K. (1991). Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow trout (Oncorhynchus mykiss) and fall Chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci.48,2083-2094.
Morgan, J. D. and Iwama, G. K. (1998). Salinity effects on oxygen consumption, gill Na+, K+-ATPase and ion regulation in juvenile coho salmon. J. Fish Biol.53,1110-1119.
Morgan, J. D., Sakamoto, T., Grau, E. G. and Iwama, G. K.(1997). Physiological and respiratory responses of the Mozambique tilapia (Oreochromis mossambicus) to salinity acclimation. Comp. Biochem. Physiol.117A,391-398.
Nakano, K., Tagawa, M., Takemura, A. and Hirano, T.(1998). Temporal changes in liver carbohydrate metabolism associated with seawater transfer in Oreochromis mossambicus.Comp. Biochem. Physiol.119B,721-728.
Nakao, T. (1974). Fine structure of the agranular cytoplasmic tubules in the lamprey chloride cells. Anat. Rec.178,49-61.
Newgard, C. B., Hwang, P. K. and Fletterick, R. J.(1989). The family of glycogen phosphorylases: structure and function. Crit. Rev. Biochem. Mol. Biol.24, 69-99.
Oliveira, G. T., Rossi, I. C., Kucharski, L. C. and Da Silva, R. S. (2004). Hepatopancreas gluconeogenesis and glycogen content during fasting in crabs previously maintained on a high-protein or carbohydrate-rich diet. Comp. Biochem. Physiol.137A,383-390.
Pederson, B. A., Cheng, C., Wilson, W. A. and Roach, P. J.(2000). Regulation of glycogen synthase. Identification of residues involved in regulation by the allosteric ligand glucose-6-P and by phosphorylation. J. Biol. Chem.275,27753-27761.
Perry, S. F. and Walsh, P. J. (1989). Metabolism of isolated fish gill cells: contribution of epithelial chloride cells. J. Exp. Biol.144,507-520.
Pfeiffer-Guglielmi, B., Fleckenstein, B., Jung, G. and Hamprecht, B. (2003). Immunocytochemical localization of glycogen phosphorylase isozymes in rat nervous tissues by using isozyme-specific antibodies. J. Neurochem.85, 73-81.
Pfeiffer-Guglielmi, B., Francke, M., Reichenbach, A. and Hamprecht, B. (2007). Glycogen phosphorylase isozymes and energy metabolism in the rat peripheral nervous system–an immunocytochemical study. Brain Res.1136,20-27.
Philpott, C. W. and Copeland, D. E. (1963). Fine structure of chloride cells from three species of Fundulus.J. Cell Biol.18,389-404.
Ransom, B. R. and Fern, R. (1997). Does astrocytic glycogen benefit axonal function and survival in CNS white matter during glucose deprivation? Glia21,134-141.
Roach, P. J. (1990). Control of glycogen synthase by hierarchal protein phosphorylation. FASEB J.4,2961-2968.
Roach, P. J., Cheng, C., Huang, D., Lin, A., Mu, J., Skurat, A. V., Wilson, W. and Zhai, L. (1998). Novel aspects of the regulation of glycogen storage. J. Basic Clin. Physiol. Pharmacol.9,139-151.
Sangiao-Alvarellos, S., Laiz-Carrion, R., Guzman, J. M., Martin del Rio, M. P., Miguez, J. M., Mancera, J. M. and Soengas, J. L.(2003). Acclimation of Sparus aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am. J. Physiol.285,R897-R907.
Sangiao-Alvarellos, S., Arjona, F. J., Martin del Rio, M. P.,Miguez, J. M., Mancera, J. M. and Soengas, J. L. (2005). Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus.J. Exp. Biol.208,4291-4304.
Sardella, B. A., Matey, V., Cooper, J., Gonzalez, R. J. and Brauner, C. J. (2004). Physiological, biochemical and morphological indicators of osmoregulatory stress in `California' Mozambique tilapia (Oreochromis mossambicus × O. urolepis hornorum) exposed to hypersaline water. J. Exp. Biol.207,1399-1413.
Smythe, C. and Cohen, P. (1991). The discovery of glycogenin and the priming mechanism for glycogen biogenesis. Eur. J. Biochem.200,625-631.
Soengas, J. L., Otero, J., Fuentes, J., Andres, M. D. and Aldegunde, M. (1991). Preliminary studies on carbohydrate metabolism changes in domesticated rainbow trout (Oncorhynchus mykiss) transferred to diluted seawater (12 p.p.t.). Comp. Biochem. Physiol.98B,53-57.
Soengas, J. L., Barciela, P., Fuentes, J., Otero, J., Andres, M. D. and Aldegunde, M. (1993). The effect of seawater transfer in liver carbohydrate metabolism of domesticated rainbow trout(Oncorhynchus mykiss). Comp. Biochem. Physiol.105B,337-343.
Tagaya, M., Nakano, K. and Fukui, T. (1985). A new affinity labeling reagent for the active site of glycogen synthase. Uridine diphosphopyridoxal. J. Biol. Chem.260,6670-6676.