Fish Physiology and Biochemistry

, Volume 6, Issue 2, pp 121–127 | Cite as

Antifreeze proteins in the urine of marine fish

  • Garth L. Fletcher
  • Madonna J. King
  • Ming H. Kao
  • Margaret A. Shears
Article

Abstract

Several species of marine teleosts have evolved blood plasma antifreeze polypeptides which enable them to survive in ice-laden seawater. Four distinct antifreeze protein classes differing in carbohydrate content, amino acid composition, protein sequence and secondary structure are currently known. Although all of these antifreezes are relatively small (2.6–33 kd) it was generally thought that they were excluded from the urine by a variety of glomerular mechanisms. In the present study antifreeze polypeptides were found in the bladder urine of winter flounder (Pseudopleuronectes americanus), sea raven (Hemitripterus americanus), ocean pout (Macrozoarces americanus) and Atlantic cod (Gadus morhua). Since the plasma of each of these fish contains a different antifreeze class it would appear that all four classes of antifreeze can enter the urine. The major antifreeze components in the urine of winter flounder were found to be identical to the major plasma components in terms of high performance liquid chromatography retention times and amino acid composition. It is concluded that plasma antifreeze peptides need not be chemically modified before they can enter the urine.

Keywords

kidney peptides freeze-resistance Pseudopleuronectes sp. Hemitripes sp. Macrozoarces sp. Gadus sp. 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Boyd, R.B. and DeVries, A.L. 1983. The seasonal distribution of anionic binding sites in the basement membrane of the kidney glomerulus of the winter flounder,Pseudopleuronectes americanus Cell Tiss. Res. 234: 271–277.Google Scholar
  2. Chang, R.L.S., Deen, W.M., Robertson, C.F. and Brenner, B.M. 1975. Permselectivity of the glomerular capillary wall to macromolecules. III. Restricted transport of polyanions. Kidney Int. 8: 212–218.Google Scholar
  3. Davies, P.L., Hew, C.L. and Fletcher, G.L. 1988. Fish antifreeze proteins: Physiology and evolutionary biology. Can. J. Zool. In press.Google Scholar
  4. DeVries, A.L. 1982. Biological antifreeze agents in cold water fishes. Comp. Biochem. Physiol. 73A: 627–640.Google Scholar
  5. DeVries, A.L., Komatsu, S.K. and Feeney, R.E.. 1970. Chemical and physical properties of freezing-point-depressing glycoproteins from Antarctic fishes. J. Biol. Chem. 245: 2901–2908.Google Scholar
  6. Dobbs, G.H., Lin, Y., DeVries, A.L. 1974. Aglomerularism in Antarctic fish. Science 185: 793–794.Google Scholar
  7. Duman, J.G. and DeVries, A.L. 1976. Isolation, characterization, and physical properties of protein antifreezes from the winter flounder,Pseudopleuronectes americanus. Comp. Biochem. Physiol. 54B: 375–380.Google Scholar
  8. Eastman, J.T., Boyd, R.B. and DeVries, A.L. 1987. Renal corpuscle development in boreal fishes with and without antifreezes. Fish Physiol. Biochem. 4: 89–100.Google Scholar
  9. Eastman, J.T. and DeVries, A.L. 1986. Renal glomerular evolution in Antarctic notothenioid fishes. J. Fish Biol. 29: 649–662.Google Scholar
  10. Eastman, J.T., DeVries, A.L., Coalson, R.E., Nordquist, R.E. and Boyd, R.B. 1979. Renal conservation of antifreeze peptide in Antarctic eelpout,Rhigophila dearborni. Nature, Lond. 282: 217–218.Google Scholar
  11. Fletcher, G.L. 1977. Circannual cycles of blood plasma freezing point and Na+ and Cl concentrations in Newfoundland winter flounder (Pseudopleuronectes americanus): correlation with water temperature and photoperiod. Can. J. Zool. 55: 789–795.Google Scholar
  12. Fletcher, G.L., Hew, C.L. and Joshi, S.B. 1982. Isolation and characterization of antifreeze glycoproteins from the frost fish,Microgadus tomcod. Can. J. Zool. 60: 348–355.Google Scholar
  13. Fletcher, G.L., Kao, M.H. and Fourney, R.M. 1986. Antifreeze peptides confer freezing resistance to fish. Can. J. Zool. 64: 1897–1901.Google Scholar
  14. Fletcher, G.L. and King, M.J. 1978. Seasonal dynamics of Cu2+, Zn2+, Ca2+ and Mg2+ in gonads and liver of winter flounder (Pseudopleuronectes americanus): Evidence for summer storage of Zn2+ for winter gonad development. Can. J. Zool. 56: 284–290.Google Scholar
  15. Fletcher, G.L., King, M.J. and Kao, M.H. 1987. Low temperature regulation of antifreeze glycopeptide levels in Atlantic cod (Gadus morhua). Can. J. Zool. 65: 227–233.Google Scholar
  16. Fourney, R.M., Hew, C.L., Joshi, S.B. and Kao, M.H. 1984a. Heterogeneity of antifreeze polypeptides from the winter flounder,Pseudopleuronectes americanus. Can. J. Zool. 62: 28–32.Google Scholar
  17. Fourney, R.M., Hew, C.L., Joshi, S.B., and Fletcher, G.L. 1984b. Comparison of antifreeze polypeptides from Newfoundland, Nova Scotia, New Brunswick and Long Island winter flounder. Comp. Biochem. Physiol. 78B: 791–796.Google Scholar
  18. Hew, C.L. and Fletcher, G.L. 1985. Biochemical adaptation to the freezing environment-structure, biosynthesis and regulation of fish antifreeze polypeptides.In Circulation, Respiration, and Metabolism. pp. 553–563. Edited by R. Gilles. Springer-Verlag, Berlin.Google Scholar
  19. Hew, C.L., Joshi, S., Wang, N.C., Kao, M.H. and Ananthanarayanan, V.S. 1985. Structures of shorthorn sculpin antifreeze polypeptides. Eur. J. Biochem. 151: 167–172.Google Scholar
  20. Hew, C.L., Slaughter, D., Fletcher, G.L. and Joshi, S.B. 1981. Antifreeze glycoproteins in the plasma of Newfoundland Atlantic cod (Gadus morhua). Can. J. Zool. 59: 2186–2192.Google Scholar
  21. Hew, C.L., Slaughter, D., Joshi, S.B., Fletcher, G.L. and Ananthanarayanan, V.S. 1984. Antifreeze polypeptides from the Newfoundland ocean pout,Macrozoarces americanus: Presence of multiple and compositionally diverse components. J. Comp. Physiol. 155: 81–88.Google Scholar
  22. Hew, C.L., Wang, N.C., Yan, S., Cai, H., Sclater, A. and Fletcher, G.L. 1986. Biosynthesis of antifreeze polypeptides in winter flounder. Characterization and seasonal occurrence of precursor polypeptides. Eur. J. Biochem. 160: 267–272.Google Scholar
  23. Kao, M.H., Fletcher, G.L., Wang, N.C. and Hew, C.L. 1986. The relationship between molecular weight and antifreeze polypeptide activity in marine fish. Can. J. Zool. 64: 578–582.Google Scholar
  24. Ng, N.F., Trinh, K.Y. and Hew, C.L. 1986. Structure of an antifreeze polypeptide precursor from the sea raven,Hemitripterus americanus. J. Biol. Chem. 261: 15690–15695.Google Scholar
  25. Osuga, D.T. and Feeney, R.E. 1978. Antifreeze glycoproteins from Arctic fish. J. Biol. Chem. 253: 5338–5343.Google Scholar
  26. Petzel, D.H. and DeVries, A.L. 1979. Renal handling of peptide antifreeze in northern fishes. Bull. MDIBL 19: 17–19.Google Scholar
  27. Petzel, D.H. and DeVries, A.L. 1980. Renal handling of anionic and cationic antifreeze peptides in the glomerular winter flounder. Bull. MDIBL. 20: 17–18.Google Scholar
  28. Petzel, D.H. and DeVries, A.L. 1981. Functional morphology of the flounder glomerular capillary wall. Bull. MDIBL. 21: 35–37.Google Scholar
  29. Pickett, M., Scott, G., Davies, P., Wang, M., Joshi, S. and Hew, C. 1984. Sequence of an antifreeze protein precursor. Eur. J. Biochem. 143: 35–38.Google Scholar
  30. Renfro, J.L., 1980. Relationship between renal fluid and Mg secretion in a glomerular marine teleost. Am. J. Physiol. 238: F92-F98.Google Scholar
  31. Yang, D.S.C., Sax, M., Chakrabartty, A. and Hew, C.L. 1988. Crystal structure of an antifreeze polypeptide and its mechanistic implications. Nature, Lond. In press.Google Scholar

Copyright information

© Kugler Publication 1989

Authors and Affiliations

  • Garth L. Fletcher
    • 1
  • Madonna J. King
    • 1
  • Ming H. Kao
    • 1
  • Margaret A. Shears
    • 1
  1. 1.Marine Laboratory, Ocean Sciences CentreMemorial University of NewfoundlandSt. John'sCanada

Personalised recommendations