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Synthesis and recycling of antifreeze glycoproteins in polar fishes

  • Clive W. Evans (a1), Linn Hellman (a1), Martin Middleditch (a1), Joanna M. Wojnar (a2), Margaret A. Brimble (a1) (a2) and Arthur L. Devries (a3)...

Evolutionary disparate Antarctic notothenioids and Arctic gadids have adapted to their freezing environments through the elaboration of essentially identical antifreeze glycoproteins (AFGPs). Here we show that this convergence of molecular identity, which evolved from unrelated parent genes, extends to convergence in physiological deployment. Both fish groups synthesize AFGPs in the exocrine pancreas from where they are discharged into the gut to inhibit the growth of ingested ice. Antifreeze glycoproteins not lost with the faeces are resorbed from the gut via the rectal epithelium, transported to the blood and ultimately secreted into the bile, from where they re-enter the gastrointestinal tract. Antifreeze glycoprotein recirculation conserves energy expenditure and explains how high levels of AFGPs reach the blood in notothenioids since, unlike Arctic gadids which also synthesize AFGP in the liver, AFGP secretion in notothenioids is directed exclusively towards the gastrointestinal lumen. Since AFGPs function by inhibiting ice crystal growth, ice must be present for them to function. The two fish groups are thus faced with an identical problem of how to deal with internal ice. Here we show that both accumulate AFGPs within ellipsoidal macrophages of the spleen, presumably adsorbed to phagocytosed ice crystals which are then held until a warming event ensues.

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Ahlgren, J.A., Cheng, C.-H.C., Schrag, J.D.DeVries, A.L. 1988. Freezing avoidance and the distribution of antifreeze glycopeptides in body fluids and tissues of Antarctic fish. Journal of Experimental Biology, 137, 549563.
Berge, G.E., Goodman, M., Espe, M.Lied, E. 2003. Intestinal absorption of amino acids in fish: kinetics and interaction of the in vitro uptake of L-methionine in Atlantic salmon (Salmo salar L.). Aquaculture, 229, 265273.
Bush, C.A.Feeney, R.E. 1986. Conformation of the glycotripeptide repeating unit of antifreeze glycoprotein of polar fish as determined from the fully assigned proton n.m.r. International Journal of Peptide Protein Research, 28, 386397.
Chen, L., DeVries, A.L.Cheng, C.-H.C. 1997a. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proceedings of the National Academy of Sciences of the United States of America, 94, 38113816.
Chen, L., DeVries, A.L.Cheng, C.-H.C. 1997b. Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proceedings of the National Academy of Sciences of the United States of America, 94, 38173822.
Cheng, C.-H.C. 1996. Genomic basis for antifreeze glycopeptide heterogeneity and abundance in Antarctic notothenioid fishes. In Ennion, S.&Goldspink, G., eds. Gene expression and manipulation in aquatic organisms. Cambridge: Cambridge University Press, 120.
Cheng, C.-H.C., Cziko, P.A.Evans, C.W. 2006. Non-hepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proceedings of the National Academy of Sciences of the United States of America, 103, 10 49110 496.
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 11521155.
DeVries, A.L. 1983. Antifreeze peptides and glycopeptides in cold-water fishes. Annual Review of Physiology, 45, 245260.
DeVries, A.L.Cheng, C.-H.C. 2005. Antifreeze proteins and organismal freezing avoidance in polar fishes. In Farrell, A.P.&Steffensen, J.F., eds. Fish physiology. San Diego, CA: Academic Press, 155201.
DeVries, A.L.Wohlschlag, D.E. 1969. Freezing resistance in some Antarctic fishes. Science, 163, 10731075.
Espenes, A., Press, C.M., Dannevig, B.H.Landsverk, T. 1994. Investigation of the structural and functional features of splenic ellipsoids in rainbow trout (Oncorhynchus mykiss). Cell Tissue Research, 279, 469474.
Evans, C.W., Hills, J.M.Dickson, J.M.J. 2000. Heavy metal pollution in Antarctica: a molecular ecotoxicological approach to exposure assessment. Journal of Fish Biology, 57, A8A19.
Evans, C.W., Gubala, V., Nooney, R., Williams, D.E., Brimble, M.A.DeVries, A.L. 2011. How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins. Antarctic Science, 23, 5764.
Fletcher, G.L., Hew, C.L.Davies, P.L. 2001. Antifreeze proteins of teleost fishes. Annual Review of Physiology, 63, 359390.
Hernandez-Blazquez, F.J.Cunha da Silva, J.R.M. 1998. Absorption of macromolecular proteins by the rectal epithelium of the Antarctic fish Notothenia neglecta. Canadian Journal of Zoology, 76, 12471253.
Hsiao, K.C., Cheng, C.-H.C., Fernandes, I.E., Detrich, H.W.DeVries, A.L. 1990. An antifreeze glycopeptide gene from the Antarctic cod Notothenia coriiceps neglecta encodes a polyprotein of high peptide copy number. Proceedings of the National Academy of Sciences of the United States of America, 87, 92659269.
Hudson, A.P., DeVries, A.L.Haschemeyer, A.E.V. 1979. Antifreeze glycoprotein biosynthesis in Antarctic fishes. Comparative Biochemistry and Physiology, 62B, 179183.
Hunt, B.M., Hoefling, K.Cheng, C.-H.C. 2003. Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarctic Science, 15, 333338.
McLean, E.Ash, R. 1987. Intact protein (antigen) absorption in fishes: mechanism and physiological significance. Journal of Fish Biology, 31, 219223.
McLean, E., Rønsholdt, B., Sten, C. Najamuddin 1999. Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts. Aquaculture, 177, 231247.
O'Grady, S.M., Schrag, J.D., Raymond, J.A.DeVries, A.L. 1982. Comparison of antifreeze glycopeptides from Arctic and Antarctic fishes. Journal of Experimental Zoology, 224, 177185.
Oliveira Ribeiro, C.A.Fanta, E. 2000. Microscopic morphology and histochemistry of the digestive system of a tropical freshwater fish Trichomycterus brasiliensis (Lütken) (Siluroidei, Trichomycteridae). Revista Brasileira de Zoologia, 17, 953971.
Peltier, R., Brimble, M.A., Wojnar, J.M., Williams, D.E., Evans, C.W.DeVries, A.L. 2010. Synthesis and antifreeze activity of fish antifreeze glycoproteins and their analogues. Chemical Science, 1, 538551.
Praebel, K., Hunt, B., Hunt, L.DeVries, A.L. 2009. The presence and quantification of splenic ice in the McMurdo Sound notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902). Comparative Biochemistry and Physiology, 154A, 564569.
Presnell, J.K., Schreibman, M.P.Humason, G.L. 1997. Humason's animal tissue techniques. Baltimore, MD: Johns Hopkins University Press, 572 pp.
Raymond, J.A.DeVries, A.L. 1977. Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proceedings of the National Academy of Sciences of the United States of America, 74, 25892593.
Schurmann, H.Christiansen, J.S. 1994. Behavioural thermoregulation and swimming activity of two arctic teleosts: the polar cod (Boreogadus saida) and the navaga (Eleginus navaga). Journal of Thermal Biology, 19, 207212.
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Antarctic Science
  • ISSN: 0954-1020
  • EISSN: 1365-2079
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