Air-breathing catfish, Clarias batrachus upregulates glutamine synthetase and carbamyl phosphate synthetase III during exposure to high external ammonia

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 147, Issue 3, 2007, Pages 520-530

  Saha, Nirmalendu ^a   Datta, Shritapa ^a   Kharbuli, Zaiba Y ^a   Biswas, Kuheli ^a   Bhattacharjee, Arundhati ^a  

^a NORTH EASTERN HILL UNIVERSITY   (India)

Author keywords

Ammonia; Ammonium chloride; Cortisol; Glutamine; Ornithine urea cycle; Urea; Ureogenesis

Indexed keywords

AMMONIA; AMMONIUM CHLORIDE; CARBAMOYL PHOSPHATE SYNTHASE; GLUTAMATE AMMONIA LIGASE; GLUTAMINE; HYDROCORTISONE; ORNITHINE; UREA;

AIR BREATHING SPECIES; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATFISH; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; ENZYME REGULATION; LIVER PERFUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UREA CYCLE;

CLARIAS; CLARIAS BATRACHUS;

EID: 34249026032     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2007.03.007     Document Type: Article

References (67)

1. Anderson P.M. Urea and glutamine synthesis: environmental influences on nitrogen excretion. Fish Physiol. 20 (2001) 239-277
2. Anderson P.M., and Walsh P.J. Sub-cellular localization and biochemical properties of the enzymes of carbamyl phosphate and urea synthesis in the batrachoidid fishes Opsanus beta, Opsanus tau and Porichthys notatus. J. Exp. Biol. 198 (1995) 755-766
3. Anderson P.M., Broderius M.A., Fong K.C., Tsui K.N.T., Chew S.F., and Ip Y.K. Glutamine synthetase expression in liver, muscle, stomach and intestine of Bostrichthys sinensis in response to exposure to a high exogenous ammonia concentration. J. Exp. Biol. 205 (2002) 2053-2065
4. Arillo A., Margiocco C., Medlodia F., Mensi P., and Schenone G. Ammonia toxicity mechanisms in fish: studies on rainbow trout (Salmo gairdneri Richardson). Ecotoxicol. Environ. Saf. 5 (1981) 316-328
5. Bergmeyer H.U. Methods of Enzymatic Analysis (1974), Academic Press, New York
6. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
7. Campbell J.W. Excretory nitrogen metabolism. In: Prosser C.L. (Ed). Environmental and Metabolic Animal Physiology (1991), Wiley-Liss Inc., New York 277-324
8. Casey C.A., and Anderson P.M. Subcellular location of glutamine synthetase and urea cycle enzymes in liver of spiny dogfish (Squalus acanthias). J. Biol. Chem. 257 (1982) 8449-8453
9. Chakravorty J., Saha N., and Ratha B.K. A unique pattern of tissue distribution and sub-cellular localization of glutamine synthetase in a freshwater air-breathing teleost, Heteropneustes fossilis (Bloch). Biochem. Int. 19 (1989) 519-527
10. Chew S.F., Wong M.Y., Tam W.L., and Ip Y.K. The snakehead Channa asiatica accumulates alanine during aerial exposure, but is incapable of sustaining locomotory activities on land through partial amino acid catabolism. J. Exp. Biol. 206 (2003) 693-704
11. Dabrowska H., and Wlasow T. Sublethal effect of ammonia on certain biochemical and haematological indicators in common carp. Comp. Biochem. Physiol. 83C (1986) 179-184
12. Dutta H.M., and Munshi J.S.D. Functional morphology of air-breathing fishes. A review. Proc. Indian Acad. Sci., Anim. Sci. 94 (1985) 359-375
13. Essex-Fraser P.A., Steele S.L., Bernier N.J., Murray B.W., Stevens E.D., and Wright P.A. Expression of four glutamine synthetase genes in the early stages of development of rainbow trout (Oncorhynchus mykiss) in relation to nitrogen metabolism. J. Biol. Chem. 280 (2005) 20268-20273
14. Fahrner J., Labruyere W.T., Gaunitz C., Moorman A.F.M., Gebhardt R., and Lamers W.H. Identification and functional characterization of regulatory elements of the glutamine synthetase gene from rat liver. Eur. J. Biochem. 213 (1993) 1067-1073
15. Felskie A.K., Anderson P.M., Guiguen Y., Postlethwait J., and Chung B. Expression and activity of carbamyl phosphate synthetase III and ornithine urea cycle enzymes in various tissues of four fish species. Comp. Biochem. Physiol. B 119 (1998) 355-364
16. French C.J., Mommsen T.P., and Hochachka P.W. Amino acid utilization in isolated hepatocytes from rainbow trout. Eur. J. Biochem. 123 (1981) 311-317
17. Hopkins T.E., Wood C.M., and Walsh P.J. Interactions of cortisol and nitrogen metabolism in the ureogenic gulf toadfish Opsanus beta. J. Exp. Biol. 198 (1995) 2229-2235
18. Ip Y.K., Chew S.F., Leong I.A.W., Jin Y., Lim C.B., and Wu R.S.S. The sleeper Bostrichthys sinensis (Family Eleotridae) stores glutamine and reduces ammonia production during aerial exposure. J. Comp. Physiol. 171B (2001) 357-367
19. Ip Y.K., Chew S.F., and Randall D.J. Ammonia toxicity, tolerance and excretion. Fish Physiol. 20 (2001) 109-148
20. Ip Y.K., Lim C.B., Chew S.F., Wilson J.M., and Randall D.J. Partial amino acid catabolism leading to the formation of alanine in Periophthalmodon schlosseri (mudskipper): a strategy that facilitates the use of amino acids as an energy source during locomotory activity on land. J. Exp. Biol. 204 (2001) 1615-1624
21. Ip Y.K., Tay A.S.L., Lee K.H., and Chew S.F. Strategies for surviving high concentrations of environmental ammonia in the swamp eel Monopterus albus. Physiol. Biochem. Zool. 77 (2004) 390-405
22. Ip Y.K., Zubaidah R.M., Liew P.C., Loong A.M., Hiong K.C., Wong W.P., and Chew S.F. African sharptooth catfish Clarias gariepinus does not detoxify ammonia to urea or amino acids but actively excretes ammonia during exposure to environmental ammonia. Physiol. Biochem. Zool. 77 (2004) 242-254
23. Ip Y.K., Law I.Y., Wong W.P., Lee S.L.M., and Chew S.F. The African sharptooth catfish Clarias gariepinus can tolerate high levels of ammonia in its tissue and organ during four days of aerial exposure. Physiol. Biochem. Zool. 78 (2005) 630-640
24. Iwata K., Kajimura M., and Sakamoto T. Functional ureogenesis in the gobiid fish, Mugilobius abei. J. Exp. Biol. 203 (2000) 3703-3715
25. Jordon J. The influence of body weight on gas exchange in the air-breathing fish, Clarias batrachus. Comp. Biochem. Physiol. A 53 (1976) 305-310
26. Jow L.Y., Chew S.F., Lim C.B., Anderson P.M., and Ip Y.K. The marble goby Oxyeleotris marmoratus activates hepatic glutamine synthetase and detoxifies ammonia to glutamine during air exposure. J. Exp. Biol. 202 (1999) 237-245
27. Julsrud E.A., Walsh P.J., and Anderson P.M. N-Acetyl-l-glutamate and the urea cycle in the gulf toadfish (Opsanus beta) and other fish. Arch. Biochem. Biophys. 250 (1998) 55-60
28. Kong H.K., Edberg D.D., Salo W.L., Wright P.A., and Anderson P.M. Nitrogen excretion and expression of carbamoylphosphate synthetase III activity and mRNA in extrahepatic tissues of largemouth bass (Micropterus salmoides). Arch. Biochem. Biophys. 350 (1998) 157-168
29. Korsgaard B., Mommsen T.P., and Wright P.A. Nitrogen excretion in teleostean fishes: adaptive relationships to environment, ontogenesis, and viviparity. In: Walsh J., and Wright P.W. (Eds). Nitrogen Metabolism and Excretion (1995), CRC Press, New York 259-287
30. Korte J.J., Salo W.L., Cabrera V.M., Wright P.A., Felskie A.K., and Anderson P.M. Expression of carbamoyl-phosphate synthetase III mRNA during the early stages of development and in muscle of adult rainbow trout (Oncorhynchus mykiss). J. Biol. Chem. 272 (1997) 6270-6277
31. Kun E., and Kearney E.B. Ammonia. In: Bergmeyer H.U. (Ed). Methods of Enzymatic Analysis vol. IV (1974), Academic Press, New York 1802-1806
32. Levi G., Morisi G., Coletti A., and Catanzaro R. Free amino acids in fish brain: normal levels and changes upon exposure to high ammonia concentrations in vivo and upon incubation of brain slices. Comp. Biochem. Physiol. A 49 (1974) 623-636
33. Martinelle K., and Haggstrom L. Mechanisms of ammonia and ammonium ion toxicity in animal cells: transport across cell membranes. J. Biotechnol. 30 (1993) 339-350
34. McDonald M.D., and Wood C.M. The effect of chronic cortisol elevation on urea metabolism and excretion in the rainbow trout (Oncorhychus mykiss). J. Comp. Physiol. 174B (2004) 71-81
35. Mommsen T.P., and Walsh P.J. Evolution of urea synthesis in vertebrates: the piscine connection. Science 243 (1989) 72-75
36. Mommsen T.P., Vijayan M.M., and Moon T.W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fish. 9 (1999) 211-268
37. Mommsen T.P., Busby E.R., von Schalburg K.R., Evans J.C., Osachoff H.L., and Elliott M.E. Glutamine synthetase in tilapia gastrointestinal tract: zonation, cDNA and induction by cortisol. J. Comp. Physiol. 173B (2003) 419-427
38. Mommsen T.P., Osachoff H.L., and Elliott M.E. Metabolic zonation in teleost gastrointestinal tract. Effect of fasting and cortisol in tilapia. J. Comp. Physiol. 173B (2003) 409-418
39. Moore R.B., and Kauffman N.G. Simultaneous determination of citrulline and urea using diacetyl monoxime. Anal. Biochem. 33 (1970) 263-272
40. Murray B.W., Busby E.R., Mommsen T.P., and Wright P.A. Evolution of glutamine synthetase in vertebrates: multiple glutamine synthetase genes expressed in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 206 (2003) 1511-1521
41. 3 concentrations of 446 and 36 μM, respectively. Fish Physiol. Biochem. 19 (1998) 59-69
42. Randall D.J., Wood C.M., Perry S.F., Bergman H., Maloiy G.M.O., Mommsen T.P., and Wright P.A. Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337 (1989) 165-166
43. Rao G.R., Tripathi S.D., and Sahu A.K. Breeding and seed production of the Asian catfish Clarias batrachus (Linnaeus). Manual Series. Central Institute of Freshwater Aquaculture, Bhubaneswar, India vol. 3 (1994) 1-47
44. Read L.T. The presence of high ornithine-urea cycle enzymes activity in the teleost Opsanus tau. Comp. Biochem. Physiol. B 39 (1971) 409-419
45. Saha N., and Das L. Stimulation of ureogenesis in the perfused liver of an Indian air-breathing catfish, Clarias batrachus, infused with different concentrations of ammonium chloride. Fish Physiol. Biochem. 21 (1999) 303-311
46. Saha N., and Ratha B.K. Active ureogenesis in a freshwater air-breathing teleost, Heteropneustes fossilis. J. Exp. Zool. 241 (1987) 137-141
47. Saha N., and Ratha B.K. Comparative study of ureogenesis in freshwater, air-breathing teleosts. J. Exp. Zool 252 (1989) 1-8
48. Saha N., and Ratha B.K. Ureogenesis in Indian air-breathing teleosts: adaptation to environmental constraints. Comp. Biochem. Physiol. A 120 (1998) 195-208
49. Saha N., Dkhar J., and Ratha B.K. Induction of ureogenesis in perfused liver of a freshwater teleost, Heteropneustes fossilis, infused with different concentrations of ammonium chloride. Comp. Biochem. Physiol. B 112 (1995) 733-741
50. Saha N., Das L., and Dutta S. Types of carbamyl phosphate synthetases and subcellular localization of urea cycle and related enzymes in air-breathing walking catfish, Clarias batrachus. J. Exp. Zool. 283 (1999) 121-130
51. Saha N., Dutta S., and Häussinger D. Changes in free amino acid synthesis in the perfused liver of an air-breathing catfish, Clarias batrachus infused with ammonium chloride: a strategy to adapt under hyperammonia stress. J. Exp. Zool. 286 (2000) 13-23
52. Saha N., Das L., Dutta S., and Goswami U.C. Role of ureogenesis in the mud-dwelled singhi catfish (Heteropneustes fossilis) under condition of water shortage. Comp. Biochem. Physiol. B 128 (2001) 137-146
53. Saha N., Dutta S., and Bhattacharjee A. 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. B 133 (2002) 235-250
54. Saha N., Datta S., Biswas K., and Kharbuli Z.Y. Role of ureogenesis in tackling problems of ammonia toxicity during exposure to higher ambient ammonia in the air-breathing walking catfish Clarias batrachus. J. Biosci. 28 (2003) 733-742
55. Tay A.S.L., Chew S.F., and Ip Y.K. The swamp eel Monopterus albus reduces endogenous ammonia production and detoxifies ammonia to glutamine during 144h of aerial exposure. J. Exp. Biol. 206 (2003) 2473-2486
56. Vijayan M.M., Mommsen T.P., Glemet H.C., and Moon T.W. Metabolic effects of cortisol treatment in a marine teleost, the sea raven. J. Exp. Biol. 199 (1996) 1509-1514
57. Walsh P.J. Purification and properties of hepatic glutamine synthetases from the ureotelic gulf toadfish, Opsanus beta. Comp. Biochem. Physiol. B 115 (1996) 523-532
58. Walsh P.J., and Milligan C.L. Effects of feeding and confinement on nitrogen metabolism and excretion in the gulf toadfish Opsanus beta. J. Exp. Biol. 198 (1995) 1559-1566
59. Walsh J.P., Danulat E., and Mommsen T.P. Variation in urea excretion in the gulf toadfish Opsanus beta. Mar. Biol. 106 (1990) 323-328
60. Walsh P.J., Tucker B.C., and Hopkins T.E. Effects of confinement and crowding on ureogenesis in the gulf toadfish Opsanus beta. J. Exp. Biol. 191 (1994) 195-206
61. Walsh P.J., Mayer G.D., Medina M., Bernstein M.L., Barimo J.F., and Mommsen T.P. A second glutamine synthetase gene with expression in the gills of the gulf toadfish (Opsanus beta). J. Exp. Biol. 206 (2003) 1523-1533
62. Wang X., and Walsh P.J. High ammonia tolerance in fishes of the family Batrachoididae (toadfish and midshipmen). Aquat. Toxicol. 50 (2000) 205-221
63. Webb J.T., and Brown G.W. Some properties and occurrence of glutamine synthetase in fish. Comp. Biochem. Physiol. B 54 (1976) 171-175
64. Wilkie M.P. Mechanism of ammonia excretion across fish gills. Comp. Biochem. Physiol. A 118 (1997) 39-50
65. Wood C.M. Ammonia and urea metabolism and excretion. In: Evans D.H. (Ed). The Physiology of Fishes (1993), CRC Press, Boca Raton 379-425
66. Wright P.A. Nitrogen excretion: three end products, many physiological roles. J. Exp. Biol. 198 (1995) 273-281
67. Zhang H., and Young A.P. A single upstream glucocorticoid response element juxtaposed to an AP1/ATF/CRE-like site renders the chicken glutamine synthetase gene hormonally inducible in transfected retina. J. Biol. Chem 266 (1991) 24332-24338