Role of Taurine in Cellular Volume Regulation in Erythrocytes of Air-Breathing Catfish (Clarias magur) Under Osmotic Stress


The present study investigated the role of taurine in cellular volume regulation of erythrocytes isolated from freshwater air-breathing magur catfish (Clarias magur) under osmotic stress. Exposure of erythrocytes, pre-loaded with or without taurine, to hypotonic medium (− 80 mOsmol/L) led to a significant decrease in taurine level in the erythrocytes due to efflux of taurine through a band 3 transporter protein present in the plasma membrane with a slight increase in cellular volume of erythrocytes by 12–13%, whereas incubation of erythrocytes with hypertonic medium (+ 80 mOsmol/L) with taurine caused a significant uptake of taurine by the erythrocytes through the Na+-dependent pathway but without any loss of taurine from the erythrocytes which was accompanied by a slight decrease in the cellular volume of erythrocytes by 11–12%. Furthermore, a direct correlation between the osmosensitive cellular volume and taurine release could be established in the erythrocytes of magur catfish under hypotonic stress (r = 0.9921). In conclusion, the erythrocytes of air-breathing magur catfish do possess a very efficient taurine-dependent volume regulatory mechanism to resist the changes in cellular volume under anisotonic conditions as a unique adaptational strategy to defend against the osmosensitive changes in cellular volume of erythrocytes.

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  1. 1.

    Wehner F, Olsen H, Tinel H et al (2003) Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. In: Reviews of physiology, biochemistry and pharmacology. Reviews of physiology, biochemistry and pharmacology, vol 148. Springer, Berlin, Heidelberg, pp 1–80

  2. 2.

    Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193–277.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Kwon HM, Handler JS (1995) Cell volume regulated transporters of compatible osmolytes. Curr Opin Cell Biol 7:465–471.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Haga Y, Kondo H, Kumagai A et al (2015) Isolation, molecular characterization of cysteine sulfinic acid decarboxylase (CSD) of red sea bream Pagrus major and yellowtail Seriola quinqueradiata and expression analysis of CSD from several marine fish species. Aquaculture 449:8–17.

    CAS  Article  Google Scholar 

  6. 6.

    Suyama M, Yoshizawa Y (1973) Free amino acid composition of the skeletal muscle of migratory fish. Nippon Suisan Gakkaishi 39:1339–1343.

    CAS  Article  Google Scholar 

  7. 7.

    Perlman DF, Goldstein L (1999) Organic osmolyte channels in cell volume regulation in vertebrates. J Exp Zool 283:725–733.;2-%23

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Häussinger D (1996) The role of cellular hydration in the regulation of cell function. Biochem J 313:697–710.

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Motais R (1991) Red cell volume regulation: the pivotal role of ionic strength in controlling swelling-dependent transport systems. Biochim Biophys Acta Gen Subj 1075:169–180.

    CAS  Article  Google Scholar 

  10. 10.

    Fugelli K, Thoroed SM (1986) Taurine transport associated with cell volume regulation in flounder erythrocytes under anisosmotic conditions. J Physiol 374:245–261.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Cossins AR, Weaver YR, Lykkeboe G, Nielsen OB (1994) Role of protein phosphorylation in control of K flux pathways of trout red blood cells. Am J Physiol 267:C1641–C1650.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Sen TK (1985) The fish fauna of Assam and the neighbouring North-Eastern States of India. In: Records of the zoological survey of India. Miscellaneous Publication, Calcutta, p 217

  13. 13.

    Banerjee B, Koner D, Lal P, Saha N (2017) Unique mitochondrial localization of arginase 1 and 2 in hepatocytes of air-breathing walking catfish, Clarias batrachus and their differential expression patterns under hyper-ammonia stress. Gene 622:13–22.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Goswami C, Saha N (1998) Glucose, pyruvate and lactate efflux by the perfused liver of a teleost, Clarias batrachus during aniso-osmotic exposure. Comp Biochem Physiol Part A Mol Integr Physiol 119:999–1007.

    Article  Google Scholar 

  15. 15.

    Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781.

    Article  Google Scholar 

  16. 16.

    Fujiwara M, Ishida Y, Nimura N et al (1987) Postcolumn fluorometric detection system for liquid chromatographic analysis of amino and imino acids using o-phthalaldehyde/N-acetyl-l-cysteine reagent. Anal Biochem 166:72–78.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Saha N, Dutta S, Häussinger D (2000) Changes in free amino acid synthesis in the perfused liver of an air-breathing walking catfish, Clarias batrachus infused with ammonium chloride: a strategy to adapt under hyperammonia stress. J Exp Zool 286:13–23.;2-X

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Thoroed SM, Fugelli K (1994) Free amino compounds and cell volume regulation in erythrocytes from different marine fish species under hypoosmotic conditions: the role of a taurine channel. J Comp Physiol B 164:1–10.

    CAS  Article  Google Scholar 

  19. 19.

    El-Sayed A-FM (2014) Is dietary taurine supplementation beneficial for farmed fish and shrimp? A comprehensive review. Rev Aquac 6:241–255.

    Article  Google Scholar 

  20. 20.

    Saha N, Dutta S, Bhattacharjee A (2002) Role of amino acid metabolism in an air-breathing catfish, Clarias batrachus in response to exposure to a high concentration of exogenous ammonia. Comp Biochem Physiol Part B Biochem Mol Biol 133:235–250.

    Article  Google Scholar 

  21. 21.

    Goldstein L, Davis EM (1994) Taurine, betaine, and inositol share a volume-sensitive transporter in skate erythrocyte cell membrane. Am J Physiol 267:R426–R431.

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Goldstein L, Musch MW (1994) Volume-activated amino acid transport and cell signaling in skate erythrocytes. J Exp Zool 268:133–138.

    CAS  Article  Google Scholar 

  23. 23.

    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 31:589–598.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Warskulat U, Wettstein M, Häussinger D (1997) Osmoregulated taurine transport in H4IIE hepatoma cells and perfused rat liver. Biochem J.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Chamberlin ME, Strange K (1989) Anisosmotic cell volume regulation: a comparative view. Am J Physiol Physiol 257:C159–C173.

    CAS  Article  Google Scholar 

  26. 26.

    Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101–163.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Burg MB (1995) Molecular basis of osmotic regulation. Am J Physiol Ren Physiol 268:F983–F996.

    CAS  Article  Google Scholar 

  28. 28.

    Wettstein M, Häussinger D (2000) Taurine attenuates cold ischemia-reoxygenation injury in rat liver. Transplantation 69:2290–2296

    CAS  Article  Google Scholar 

  29. 29.

    Saha N, Goswami C (2004) Effects of anisotonicity on pentose-phosphate pathway, oxidized glutathione release and t-butylhydroperoxide-induced oxidative stress in the perfused liver of air-breathing catfish, Clarias batrachus. J Biosci 29:179–187.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Shennan DB (2008) Swelling-induced taurine transport: relationship with chloride channels, anion-exchangers and other swelling-activated transport pathways. Cell Physiol Biochem 21:015–028.

    CAS  Article  Google Scholar 

  31. 31.

    Goldstein L, Perlman DF (1995) Nitrogen metabolism, excretion, osmoregulation, and cell volume regulation. In: Walsh PJ, Wright P (eds) Nitrogen metabolism and excretion. CRC Press, Boca-Raton, pp 91–104

    Google Scholar 

  32. 32.

    Fincham DA, Wolowyk MW, Young JD (1987) Volume-sensitive taurine transport in fish erythrocytes. J Membr Biol 96:45–56.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Goldstein L, Brill S (1990) Isosmotic swelling of skate (Raja erinacea) red blood cells causes a volume regulatory release of intracellular taurine. J Exp Zool 253:132–138.

    Article  Google Scholar 

  34. 34.

    Motais R, Fiévet B, Borgese F, Garcia-Romeu F (1997) Association of the band 3 protein with a volume-activated, anion and amino acid channel: a molecular approach. J Exp Biol 200:361–367

    CAS  PubMed  Google Scholar 

  35. 35.

    Hubert EM, Musch MW, Goldstein L (2000) Inhibition of volume-stimulated taurine efflux and tyrosine kinase activity in the skate red blood cell. Pflügers Arch 440:132–139.

    CAS  Article  PubMed  Google Scholar 

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This study was supported by a project sanctioned to the corresponding author by the Science and Engineering Research Board, New Delhi, and the DSA programme to the Department of Zoology, Shillong, by the University Grants Commission, New Delhi.

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Correspondence to Nirmalendu Saha.

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Significance Statement

The present study demonstrated that under hypertonic stress, taurine gets accumulated and under hypotonic stress, excess taurine is released out from the erythrocyte of Clarias magur to maintain the cellular volume as a physiological adaptation.

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Banerjee, B., Koner, D., Lal, P. et al. Role of Taurine in Cellular Volume Regulation in Erythrocytes of Air-Breathing Catfish (Clarias magur) Under Osmotic Stress. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 89, 1389–1397 (2019).

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  • Hypotonicity
  • Hypertonicity
  • Anisotonicity
  • Cellular water content
  • 4,4′-Di-isothiocyanatostilbene-2,2′-disulphonic acid
  • Band 3 protein transporter