Hostname: page-component-5d59c44645-7l5rh Total loading time: 0 Render date: 2024-03-02T07:22:53.421Z Has data issue: false hasContentIssue false

Synthesis and recycling of antifreeze glycoproteins in polar fishes

Published online by Cambridge University Press:  02 April 2012

Clive W. Evans*
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Linn Hellman
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Martin Middleditch
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Joanna M. Wojnar
Affiliation:
School of Chemical Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Margaret A. Brimble
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand School of Chemical Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Arthur L. Devries
Affiliation:
Department of Animal Biology, University of Illinois at Urbana-Champaign, 524 Burrill Hall, 407 South Goodwin, Urbana, IL 61801, USA

Abstract

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.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 11521155.Google Scholar
DeVries, A.L. 1983. Antifreeze peptides and glycopeptides in cold-water fishes. Annual Review of Physiology, 45, 245260.Google Scholar
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.Google Scholar
DeVries, A.L.Wohlschlag, D.E. 1969. Freezing resistance in some Antarctic fishes. Science, 163, 10731075.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Fletcher, G.L., Hew, C.L.Davies, P.L. 2001. Antifreeze proteins of teleost fishes. Annual Review of Physiology, 63, 359390.Google Scholar
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.Google Scholar
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.Google Scholar
Hudson, A.P., DeVries, A.L.Haschemeyer, A.E.V. 1979. Antifreeze glycoprotein biosynthesis in Antarctic fishes. Comparative Biochemistry and Physiology, 62B, 179183.Google Scholar
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.Google Scholar
McLean, E.Ash, R. 1987. Intact protein (antigen) absorption in fishes: mechanism and physiological significance. Journal of Fish Biology, 31, 219223.Google Scholar
McLean, E., Rønsholdt, B., Sten, C. Najamuddin 1999. Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts. Aquaculture, 177, 231247.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Presnell, J.K., Schreibman, M.P.Humason, G.L. 1997. Humason's animal tissue techniques. Baltimore, MD: Johns Hopkins University Press, 572 pp.Google Scholar
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.Google Scholar
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.Google Scholar