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Effect of urea and low temperature on the expression and activity of flavin-containing monooxygenase in the liver and gill of rainbow trout (Oncorhynchus mykiss)

Fish Physiology and Biochemistry volume 25, pages 19–29 (2001)Cite this article

Abstract

Little is known about the physiological role of flavin containing monooxygenases (FMOs) in teleost fish. Recent studies have indicated induction during saltwater adaptation in several telost species including rainbow trout. A physiological product of FMOs, trimethylamine N-oxide (TMAO) and urea have also been shown to increase in rainbow trout muscle during saltwater adapatation. TMAO counteracts the denaturing effects of urea. In order to evaluate urea as a possible inducer of FMO expression and activity, adult rainbow trout were infused for 48 h with urea/saline solutions at a loading rate of 8 mmol urea/kg/day. To determine whether low temperature had any effect on FMO expression and activity, one group of animals was infused with urea and exposed to low temperature (2–3 °C) for 48 h. Gill FMO-catalyzed thiourea oxygenase activity was significantly induced by low temperature, with twice the activity observed at low temperature (1.116±0.356 nmol/min/mg) compared to urea infusion at 10 °C (0.585±0.282 nmol/min/mg). Low temperature without urea treatment caused a 50% increase in gill FMO activity. In the liver, urea infusion caused an increase in liver FMO activity (from 0.144±0.053 nmol/min/mg to 0.464±0.237 nmol/min/mg), but was unaffected by co-exposure to low temperature (0.523±219 nmol/min/mg). FMO expression and activity correlated with elevated tissue urea levels, but TMAO concentrations were not related. The interactions between urea, temperature and the tissue-specific induction of FMOs indicate FMOs may contribute to other physiological and cellular processes besides osmoregulation.

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References

  • Azuma, T., Chikushi, Y. and Itazawa, Y. 1998. Effects of acute drop of ambient temperature on respiration and blood circulation of porgy. Fish. Sci. 64: 270–275.

    CAS  Google Scholar 

  • Cohen, D.M., Gullands, S.R. and Chin W.W. 1996. Urea inducibility of egr-1 in murine inner medullary collecting duct cells is mediated by the serum response element and adjacent Ets motifs. J. Biol. Chem. 271: 12903–12908.

    Article  PubMed  CAS  Google Scholar 

  • Daikoku, T. 1977. Changes and effects of trimethylamine oxide in freshwater fishes, the guppies, Poecilia reticulata and the goldfish, Carassius auratus. Annot. Zool. Jpn. 50: 203–211.

    CAS  Google Scholar 

  • Daikoku, T.D., Arai, M., Murata, M. and Sakaguchi, M. 1987. Effects of dietary trimethylamine on the concentration of trimethylamine oxide in various tissues of the chum salmon, Oncorhynchus keta, in freshwater and seawater environments. Comp. Biochem. Physiol. 87A: 101–105.

    CAS  Google Scholar 

  • Daikoku, T.M., Murata, M. and Sakaguchi, M. 1988. Effects of intraperiotoneally injected and dietary trimethylamine on the biosynthesis of trimethylamine oxide in relation to seawater adaptation of the eel, Anguilla japonica and the Guppy, Poecilia reticulata. Comp. Biochem. Physiol. 89A: 261–264.

    CAS  Google Scholar 

  • El-Alfy, A., Larsen, B.K. and Schlenk, D. 2002. Effects of cortisol and growth hormone on the expression of flavin-containing monooxygenase expression and activity in rainbow trout. Mar. Environ. Res. In press.

  • Evans, D.H. 1993. Osmotic and Ionic regulation. In:The Physiology of Fishes. pp. 315–341. Edited by D.H. Evans. CRC Press, London.

    Google Scholar 

  • Gillett, M.B., Suko, J.R., Sontoso, F.R. and Yancey, R.H. 1997. Elevated levels of trimethylamine oxide in muscles of deep-sea Gadiform teleosts: A high-pressure adaptation? J. Exp. Zool. 279: 386–391.

    Article  CAS  Google Scholar 

  • Goldstein, L. and Dewitt-Harley, S. 1973. Trimethylamine oxidase of nurse shark liver and its relation to mammalian mixed function amine oxidase Comp. Biochem. Physiol. 89A: 261–264.

    Google Scholar 

  • Guo, W.-X.A. and Ziegler, D.M. 1991. Estimation of Flavin-Containing Monooxygenase Activity in Crude Tissue Preparations by Thiourea-Dependent Oxidation of Thiocholine. Analyt. Biochem. 198: 143–148.

    Article  PubMed  CAS  Google Scholar 

  • Kelly, R.H. and Yancey, P.H. 1999. High contents of trimethylamine oxide correlating with depth in deep-sea teleost fishes, skates, and decapod crustaceans. Biol. Bull. 196: 18–25.

    CAS  Google Scholar 

  • Korsgaard, B., Mommsen, T.P. and Wright, P.A. 1995. Nitrogen excretion in teleostean fish: Adaptive relationships to environment, ontogenesis, and viviparity. In: Nitrogen Metabolism and Excretion. pp. 259–287. Edited by P.J. Walsh and P. Wright. CRC Press, Boca Raton.

    Google Scholar 

  • Lang, D.H., Yeung, C.K., Peter, R.M., Ibarra, C., Gasser, R., Itagaki, K., Philpot, R.M. and Rettie, A.E. 1998. Isoform specificity of trimethylamine N-Oxygenation by human flavin-containing monooxygenase (FMO) and P450 enzymes: Selective catalysis by FMO3. Biochem. Pharmacol. 56: 1005–1012.

    Article  PubMed  CAS  Google Scholar 

  • Larsen, B. and Schlenk, D. 2001. Effect of salinity on flavincontaining monooxygenase expression and activity in rainbow trout (Oncorhynchus mykiss). J. Comp. Physiol. B. 171: 421–429.

    Article  PubMed  CAS  Google Scholar 

  • Lin, T.-Y. and Timasheff, S.N. 1994. Why do some organisms use a urea-methylamine mixture as osmolyte? Thermodynamic Compensation of urea and trimethylamine N-oxide interactions with protein. Biochemistry 33: 12695–12701.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, M.D. and Wood, C.M. 1998. Reabsorption of urea by the kidney of the freshwater rainbow trout. Fish. Physiol. Biochem. 18: 375–386.

    Article  CAS  Google Scholar 

  • Nigra, L. and Huxtable, R.J. 1992. Hepatic glutathione concentrations and the release of pyrrolic metabolites of the pyrrolizidine alkaloid monocrotaline, from the isolated perfused liver. Toxicon 30: 1195–1202.

    Article  PubMed  CAS  Google Scholar 

  • Pang, P.K.T., Griffith, R.W. and Atz, J.W. 1977. Osmoregulation in elasmobranchs. Am. Zool. 17: 365–377.

    CAS  Google Scholar 

  • Parab, S.N. and Rao, S.B. 1984. Distribution of trimethylamine oxide in somemarine and freshwater fish. Curr. Sci. 53: 307–309.

    CAS  Google Scholar 

  • Pärt, P., Wrightm P.A. and Wood, C.M. 1998. Urea and water permeability of dogfish (Squalus acanthias) gills. Comp. Biochem. Physiol. 119A: 117–123.

    Google Scholar 

  • Raymond, J.A. 1994. Seasonal variations of trimethylamine oxide and urea in the blood of a cold-adapted marine teleost, the rainbow smelt. Fish. Physiol. Biochem. 13: 13–22.

    Article  CAS  Google Scholar 

  • Raymond, J.A. 1998. Trimethylamine oxide and urea synthesis in rainbow smelt and some northern fishes. Physiol. Zool. 71: 515–523.

    PubMed  CAS  Google Scholar 

  • Raymond, J.A. and DeVries, A.L. 1998. Elevated concentrations and synthetic pathways of trimethylamine oxide and urea in some teleost fishes of McMurdo Sound, Antarctica Fish. Physiol. Biochem. 18: 387–398.

    CAS  Google Scholar 

  • Schlenk, D. 1998. Occurrence of flavin-containing monooxygenases in non-mammalian eukaryotic organisms. Comp. Biochem. Physiol. 121C: 185–195.

    CAS  Google Scholar 

  • Schlenk, D. and El-Alfy, A. 1998. Expression of branchial flavincontaining monooxygenase is directly correlated with salinityinduced aldicarb toxicity in the euryhaline fish (Oryzias latipes). Mar. Env. Res. 46: 103–106.

    Article  CAS  Google Scholar 

  • Schlenk, D. and Li-Schlenk, R. 1994. Characterization of liver flavin-containing monooxygenase of the dogfish shark (Squalus acanthias) and partial purification of liver flavin-containing monooxygenase of the silky shark (Carcharhinus falciformis) Comp. Biochem. Physiol. 109B: 655–664.

    CAS  Google Scholar 

  • Schlenk, D. and Buhler, D.R. 1991. Flavin-containing monooxygenase activity in liver microsomes from the rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 20: 13–24.

    Article  CAS  Google Scholar 

  • Schlenk, D., Peters, L., Shehin-Johnson, S., Hines, R.N. and Livingstone, D.R. 1995. Differential expression and activity of flavin-containing monooxygenases in euryhaline and stenohaline flatfishes indicates potential osmoregulatory role. Comp. Biochem. Physiol. 112C: 179–186.

    CAS  Google Scholar 

  • Schlenk, D., Peters, L.D. and Livingstone, D.R. 1996. Downregulation of piscine flavin-containing mono-oxygenase activity by decreased salinity in euryhaline flounder (Platichthys flesus). Mar. Env. Res. 42: 339–343.

    Article  CAS  Google Scholar 

  • Schlenk, D., El-Alfy, A. and Buhler D.R. 1997. Downregulation of hepatic flavin-containing monooxygenase activity by 17B-estradiol in rainbow trout (Oncorhynchus mykiss) Comp. Biochem. Physiol. 118C: 199–202.

    CAS  Google Scholar 

  • Shehin-Johnson, S.E., Williams, D.E., Larsen-Su, S., Stresser, D.M. and Hines, R.N. 1995. Tissue specific expression of flavin containing monooxygenase (FMO) forms 1 and 2 in the rabbit. J. Pharmacol. Exp. Therapeut. 272: 1293–1299.

    CAS  Google Scholar 

  • Shehin-Johnson, S.E. and Hines, R.N. 1996. Identification of tissue-specific DNAse I hypersensitive sites in the rabbit flavincontaining monooxygenase from 2 (FMO2) gene. Drug Metab. Disp. 24: 891–898.

    CAS  Google Scholar 

  • Suh, J.K. and Robertus, J.D. 2000. Yeast flavin-containing monooxygenases is induced by the unfolded protein response. Proc. Nat. Acad. Sci.97: 121–126.

    Article  PubMed  CAS  Google Scholar 

  • Walsh, P.J., Wood, C.M., Perry, S.F. and Thomas, S. 1994. Urea transport by hepatocytes and red blood cells of selected elasmobranch and teleost fishes J. Exp. Biol 193: 321–335.

    PubMed  CAS  Google Scholar 

  • Walsh, P.J. and Wood, C.M. 1996. Interactions of urea transport and synthesis in hepatocytes of the gulf toadfish Opsanus beta. Comp Biochem Physiol 113B: 411–416.

    CAS  Google Scholar 

  • Walsh, P.J. 1997. Evolution and regulation of urea synthesis and ureotely in (batrachoidid) fishes. Ann. Rev. Physiol. 59: 299–323.

    Article  CAS  Google Scholar 

  • Wekell, J.C. and Barnett, H. 1991. New method for analysis of trimethylamine oxide using ferrous sulfate and EDTA. J. Food Sci. 56: 132–138.

    Article  CAS  Google Scholar 

  • Wood, C.M. 1993. Ammonia and Urea Metabolism and Excretion In: The Physiology of Fishes. pp. 376–423. Edited by Evans. CRC Press, Boca Raton.

    Google Scholar 

  • Wood, C.M., Hopkins, T.W. and Walsh, P.J. 1997. Pulsatile urea excretion in the toadfish (Opsanus beta) is due to a pulsatile excretion mechanism, not a pulsatile production mechanism. J. Exp. Biol. 200: 1039–1046.

    PubMed  CAS  Google Scholar 

  • Wright, P.A., Pärt, P. and Wood C.M. 1995. Ammonia and urea excretion in the tidepool sculpin (Oligocottus maculosus): Sites of excretion, effects of reduced salinity and mechanisms of urea transport. Fish. Physiol. Biochem. 14: 111–123.

    Article  CAS  Google Scholar 

  • Yancey, P.H. and Somero, G.N. 1979. Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem. J. 183: 317–323.

    PubMed  CAS  Google Scholar 

  • Yancey, P.H. and Somero, G.N. 1980. Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes. J. Exp. Zool. 212: 205–213.

    Article  CAS  Google Scholar 

  • Yancey, P.H., Clark, M.E. and Hand, S.C. (1982) Living with water Stress: Evolution of Osmolyte Systems. Science 217: 1214–1222.

    PubMed  CAS  Google Scholar 

  • Zhang, Z., Yang, X.-Y. and Cohen, D.M. 1999. Urea-associated oxidative stress and Gadd153/CHOP induction. Am. J. Physiol. 276: F786–F793.

    PubMed  CAS  Google Scholar 

  • Ziegler, D.M. 1988. Flavin-containing monooxygenases: Catalytic mechanisms and substrate specificities. Drug Metab. Rev. 19: 1–32.

    PubMed  CAS  Google Scholar 

  • Ziegler, D.M. 1993. Recent studies on the structure and function of multisubstrate flavin-containing monooxygenases. Ann. Rev. Pharmacol. Toxicol. 33: 179–199.

    Article  CAS  Google Scholar 

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  1. Department of Environmental Sciences, University of California, Riverside, Riverside, CA , 92521, USA

    B.K. Larsen & D. Schlenk

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  1. B.K. Larsen
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  2. D. Schlenk
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Larsen, B., Schlenk, D. Effect of urea and low temperature on the expression and activity of flavin-containing monooxygenase in the liver and gill of rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry 25, 19–29 (2001). https://doi.org/10.1023/A:1019769026824

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  • DOI: https://doi.org/10.1023/A:1019769026824

  • FMO
  • low temperature
  • TMAO
  • urea

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