Advertisement

Fish Physiology and Biochemistry

, Volume 37, Issue 3, pp 681–692 | Cite as

Influence of increased environmental water salinity on gluconeogenesis in the air-breathing walking catfish, Clarias batrachus

  • Nirmalendu Saha
  • Lucy M. Jyrwa
  • Manas Das
  • Kuheli Biswas
Article

Abstract

The present study was aimed at determining the effect of hypertonicity due to increased environmental water salinity on gluconeogenesis in air-breathing walking catfish (Clarias batrachus). In situ exposure to hypertonic saline solution (150 mM NaCl) led to a significant stimulation of glucose efflux due to gluconeogenesis from the liver after 7 days with further elevation after 14 days in the presence of each of the three potential gluconeogenic substrates (lactate, pyruvate, and glutamate). This was accompanied by significant increase of activities of three key gluconeogenic enzymes, namely phosphoenolpyruvate carboxykinase (PEPCK), fructose 1,6-biphosphatase (FBPase), and glucose 6-phosphatase (G6Pase) in liver and kidney by about twofold to threefold. Environmental hypertonicity also led to a significant elevation in the levels of PEPCK, FBPase, and G6Pase enzyme proteins in both the tissues by about 2- to 2.75-fold, accompanied by a significant elevation in the level of PEPCK mRNA by about 2- to 2.5-fold after 7 days, and further enhancement to about 3.5- to 4-fold after 14 days. Thus, the upregulation of PEPCK, FBPase. and G6Pase activities appears to be a result of transcriptional regulation of these genes. The induction of gluconeogenesis under environmental hypertonicity, which this catfish faces regularly in its natural habitat, possibly occurs as a consequence of changes in hydration status/cell volume of different cell types. This would certainly assist in maintaining glucose homeostasis, and also for a proper energy supply to support metabolic demands for ion transport and other altered metabolic processes under various environmental hypertonic stress-related insults.

Keywords

Hypertonic stress Phosphoenolpyruvate carboxykinase Fructose 1, 6-biphosphatase Glucose 6-phosphatase Hydration status Gluconeogenesis Clarias batrachus 

Notes

Acknowledgments

This study was supported by the DSA programme to the Department of Zoology and the UPE-Biosciences project to the North-Eastern Hill University, Shillong by the University Grants Commission, New Delhi. The financial support as a research fellowship to LMJ from the Council of Scientific and Industrial Research (CSIR), New Delhi is gratefully acknowledged.

References

  1. Beale EG, Hammer RE, Antoine B, Forest C (2004) Disregulated glyceroneogenesis: PCK1 as a candidate diabetes and obesity genes. Trends Endocrinol Metab 15:129–135PubMedCrossRefGoogle Scholar
  2. Bergmeyer HU, Bernt E, Schmidt E, Stork H (1974) d-glucose. Determination with hexokinase and glucose-6-phosphate dehydrogenase. In: Bergmeyer HU, Bergmeyer J, Graßl M (eds) Methods of enzymatic analysis. Academic Press, New York, pp 1196–1201Google Scholar
  3. Bianchini L, Fossat B, Porthe-Nibelle J, Ellory JC, Lahlou B (1988) Effects of hyposmotic shock on ion fluxes in isolated trout hepatocytes. J Exp Biol 137:303–318PubMedGoogle Scholar
  4. Biswas K, Khongsngi JL, Häussinger D, Saha N (2009) Influence of cell volume changes on autophagic proteolysis in the perfused liver of air-breathing walking catfish (Clarias batrachus). J Exp Zool A 311:115–124Google Scholar
  5. Biswas K, Jyrwa LM, Häussinger D, Saha N (2010) Influence of cell volume changes on protein synthesis in isolated hepatocytes of air-breathing walking catfish (Clarias batrachus). Fish Physiol Biochem 36:17–27PubMedCrossRefGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  7. Carneiro NM, Amaral AD (1982) Effects of insulin and glucagon on plasma glucose level and glycogen content in the organs of the freshwater teleost, Pimelodus maculates. Gen Comp Endocrinol 49:115–121CrossRefGoogle Scholar
  8. De la Higuera M, Cardenas P (1986) Hormonal effects on gluconeogenesis from (U-14C) glutamate in rainbow trout Salmo gairdneri. Comp Biochem Physiol B 85:517–521CrossRefGoogle Scholar
  9. Enes P, Panserat S, Kaushik S, Oliva-Teles A (2009) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35:519–539PubMedCrossRefGoogle Scholar
  10. Espelt MV, Mut PN, Amodeo G, Krumschnabel G, Schwarzbaum PJ (2003) Volumetric and ionic responses of goldfish hepatocytes to anisotonic exposure and energetic limitation. J Exp Biol 206:513–522Google Scholar
  11. Fiske CH, Subbarow Y (1957) Method for estimation of phosphate. In: Colowick SP, Kaplin NO (eds) Methods in enzymology, vol 3. Academic Press, New York, pp 843–844Google Scholar
  12. Fugelli K, Thoroed SM (1986) Taurine transport associated with cell volume regulation in flounder erythrocytes under anisosmotic conditions. J Physiol 374:245–261PubMedGoogle Scholar
  13. Goswami C, Saha N (1998) Glucose, pyruvate and lactate efflux by perfused liver of a teleost, Clarias batrachus during aniso-osmotic exposure. Comp Biochem Physiol A 119:999–1007CrossRefGoogle Scholar
  14. Goswami C, Saha N (2006) Cell volume regulation in the perfused liver of a freshwater air-breathing catfish Clarias batrachus under aniso-osmotic conditions: Roles of inorganic ions and taurine. J Biosci 31:589–598PubMedCrossRefGoogle Scholar
  15. Goswami C, Datta S, Biswas K, Saha N (2004) Cell volume changes affect gluconeogenesis in the perfused liver of the catfish Clarias batrachus. J Biosci 29:337–347PubMedCrossRefGoogle Scholar
  16. Hallgren NK, Busty ER, Mommsen TP (2003) Cell volume affects glycogen phosphorylase activity in fish hepatocytes. J Comp Physiol B 173:591–599PubMedCrossRefGoogle Scholar
  17. Hanson RW, Reshef L (1997) Regulation of Phosphoenolpyruvate carboxykinase (GTP) gene expression. Annu Rev Biochem 66:581–611PubMedCrossRefGoogle Scholar
  18. Häussinger D (1996) The role of cellular hydration in the regulation of cell function. Biochem J 321:697–710Google Scholar
  19. Hayashi S, Ooshiro Z (1979) Gluconeogenesis in isolated liver cells of the eel, Anguilla japonica. J Comp Physiol B 132:343–350Google Scholar
  20. Haynes JK, Goldstein L (1993) Volume-regulatory amino acid transport in erythrocytes of the little skate, Raja erinacea. Am J Physiol 265:R173–R179PubMedGoogle Scholar
  21. Houde VP, Brûlė S, Festuccia WT, Blanchard PG, Bellmann K, Deshaies Y, Marette A (2010) Chronic rapamycine treatment causes glucose intolerance and hyperlipidemia by upregulating hepatic gluconeogenesis and impairing lipid deposition in adipose tissue. Diabetes 59:1338–1348PubMedCrossRefGoogle Scholar
  22. Kanli H, Norderhus E (1998) Cell volume regulation in proximal renal tubules from trout (Salmo trutta). J Exp Biol 201:1405–1419PubMedGoogle Scholar
  23. Lionetto MG, Giordona ME, Nicolardi G, Schettino T (2001) Hypertonicity stimulates Cl(−) transport in the intestine of fresh water acclimated eel, Anguilla anguilla. Cell Physiol Biochem 11:41–54PubMedCrossRefGoogle Scholar
  24. Lionetto MG, Giordano ME, De Nuccio F, Nicolardi G, Hoffmann EK, Schettino T (2005) Hypotonicity induced K+ and anion conductive pathways activation in eel intestinal epithelium. J Exp Biol 208:749–760PubMedCrossRefGoogle Scholar
  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  26. Mommsen TP, Walsh PJ, Moon TW (1985) Gluconeogenesis in hepatocytes and kidney of Atlantic salmon. Mol Physiol 8:89–100Google Scholar
  27. Moon TW, Foster GD (1995) Tissue carbohydrate metabolism, gluconeogenesis and hormonal and environmental influences. In: Hochachka PW, Mommsen TP (eds) Molecular biology and biochemistry of fishes, vol 4. Elsevier, Amsterdam, pp 65–100Google Scholar
  28. Moon TW, Johnston IA (1980) Starvation and the activities of glycolytic and gluconeogenic enzymes in skeletal muscles and liver of the plaice, Pleuronectes platessa. J Comp Physiol B 136:31–38CrossRefGoogle Scholar
  29. Munshi JSD, Ghosh TK (1994) Metabolic wheel hypothesis as applied to air-breathing fishes of India. In: Singh HR (ed) Advances in fish biology, vol 1. Hindustan, Delhi, pp 70–78Google Scholar
  30. Newsome WP, Warskulat U, Noe B, Wettstein M, Stoll B, Gerok W, Häussinger D (1994) Modulation of phosphoenolpyruvate carboxykinase mRNA levels by the hepatocellular hydration state. Biochem J 304:555–560PubMedGoogle Scholar
  31. Nordlie RC, Arion WJ (1966) Glucose-6-phosphatase: In: Wood WA (ed) Methods of enzymology, vol 9. Academic Press, New York, pp 619–624Google Scholar
  32. Pafundo DE, Osvaldo C, Faillace MP, Gerhard K, Schwarzbaum PJ (2008) Kinetics of ATP release and cell volume regulation of hyposmotically challenged goldfish hepatocytes. Am J Physiol 294:R220–R233Google Scholar
  33. Panserat S, Capilla E, Gutierrez J, Frappart PO, Vachot C, Plagnes-Juan AguirreP, Breque J, Kaushik S (2001) Glucokinase is highly induced and glucose-6-phosphatase poorly repressed in liver of rainbow trout (Onchorhynchus mykiss) by a single meal with glucose. Comp Biochem Physiol B 128:275–283PubMedCrossRefGoogle Scholar
  34. Perlman DF, Goldstein L (1999) Organic osmolytes channels in cell volume regulation in vertebrates. J Exp Biol 283:173–180Google Scholar
  35. Renaud JM, Moon TW (1980) Characterization of gluconeogenesis in hepatocytes isolated from the American eel, Anguilla rostrata Le Sueur. J Comp Physiol B 135:115–125CrossRefGoogle Scholar
  36. Saha N, Goswami C (2004) Effects of anisotonicity on pentose-phosphate pathway, oxidised glutathione release and t-butylhydroperoxide-induced oxidative stress in the perfused liver of air- breathing catfish, Clarias batrachus. J Biosci 29:179–187PubMedCrossRefGoogle Scholar
  37. Saha N, Ratha BK (2007) Functional ureogenesis and adaptation to ammonia metabolism in Indian freshwater air-breathing catfishes. Fish Physiol Biochem 33:283–295CrossRefGoogle Scholar
  38. Saha N, Stoll B, Lang F, Häussinger D (1992) Effects of anisotonic cell volume modulation on glutathione-S-conjugate release, t-butylhydroperoxide metabolism and the pentose-phosphate shunt in the perfused rat liver. Eur J Biochem 209:437–444PubMedCrossRefGoogle Scholar
  39. Saha N, Dkhar J, Ratha BK (1995) Induction of ureogenesis in the perfused liver of a freshwater teleost Heteropneustes fossilis, infused with different concentrations of ammonium chloride. Comp Biochem Physiol B 112:733–741CrossRefGoogle Scholar
  40. Saurez RK, Mommsen TP (1987) Gluconeogenesis in teleost fishes. Can J Zool 65:1869–1882CrossRefGoogle Scholar
  41. Schliess F, Richter L, vom Dahl S, Häussinger D (2006) Cell hydration and mTOR-dependent signalling. Acta Physiol (Oxf) 187:223–229CrossRefGoogle Scholar
  42. Sen TK (1985) The fish fauna of Assam and neighbouring North-Eastern States of India. Records of the zoological survey of India. Calcutta, Miscellaneous Publication, p 217Google Scholar
  43. Weiergräber OH, Häussinger D (2000) Hepatocellular hydration: signal transduction and functional implications. Cell Physiol Biochem 10:409–416PubMedCrossRefGoogle Scholar
  44. Weldon SL, Rando A, Matathias AS, Hod Y, Kalonick PA, Savon S, Cook JS, Hanson RW (1990) Mitochondrial phosphoenolpyruvate carboxykinase from the chicken: comparison of the cDNA protein sequences with the cytosolic isoenzymes. J Biol Chem 265:7308–7317Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Nirmalendu Saha
    • 1
  • Lucy M. Jyrwa
    • 1
  • Manas Das
    • 1
  • Kuheli Biswas
    • 1
  1. 1.Biochemical Adaptation Lab., Department of ZoologyNorth-Eastern Hill UniversityShillongIndia

Personalised recommendations