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How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins

Published online by Cambridge University Press:  15 September 2010

Clive W. Evans ,
Vladimir Gubala ,
Robert Nooney ,
David E. Williams ,
Margaret A. Brimble  and
Arthur L. Devries
Clive W. Evans*
Affiliation:
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
Vladimir Gubala
Affiliation:
Biomedical Diagnostics Institute, Dublin City University, Glasnevin, Dublin 9, Ireland
Robert Nooney
Affiliation:
Biomedical Diagnostics Institute, Dublin City University, Glasnevin, Dublin 9, Ireland
David E. Williams
Affiliation:
Department of Chemistry, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand MacDiarmid Institute for Advanced Materials and Nanotechnology, 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 Department of Chemistry, 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 Sth. Goodwin, Urbana, IL 61801, USA
*
[email protected]
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Abstract

Antarctic fishes survive freezing through the secretion of antifreeze glycoproteins (AFGPs), which bind to ice crystals to inhibit their growth. This mode of action implies that ice crystals must be present internally for AFGPs to function. The entry and internal accumulation of ice is likely to be lethal, however, so how do fishes survive in its presence? We propose a novel function for the interaction between internal ice and AFGPs, namely the promotion of ice uptake by splenic phagocytes. We show here that i) external mucus of Antarctic notothenioids contains AFGPs and thus has a potential protective role against ice entry, ii) AFGPs are distributed widely through the extracellular space ensuring that they are likely to come into immediate contact with ice that penetrates their protective barriers, and iii) using AFGP-coated nanoparticles as a proxy for AFGP adsorbed onto ice, we suggest that internal ice crystals are removed from the circulation through phagocytosis, primarily in the spleen. We argue that intracellular sequestration in the spleen minimizes the risks associated with circulating ice and enables the fish to store the ice until it can be dealt with at a later date, possibly by melting during a seasonal warming event.

Keywords

AFGPnanoparticlesnotothenioidPagothenia borchgrevinkiphagocytosis
Type
Biological Sciences
Information
Antarctic Science , Volume 23 , Issue 1 , February 2011 , pp. 57 - 64
Copyright
Copyright © Antarctic Science Ltd 2011

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References

Agius, C. Roberts, R.J. 2003. Melano-macrophage centres and their role in fish physiology. Journal of Fish Diseases, 26, 499–509.CrossRefGoogle Scholar
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, 549–563.CrossRefGoogle ScholarPubMed
Bagwe, R.P., Yang, C., Hilliard, L.R. Tan, W. 2004. Optimisation of dye-doped silica nanoparticles prepared using a reverse microemulsion method. Langmuir, 20, 8336–8342.CrossRefGoogle 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, 10491–10496.CrossRefGoogle Scholar
Cziko, P.A., Evans, C.W., Cheng, C.-H.C. DeVries, A.L. 2006. Freezing resistance of antifreeze-deficient larval Antarctic fish. Journal of Experimental Biology, 209, 407–420.CrossRefGoogle ScholarPubMed
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 1152–1155.CrossRefGoogle ScholarPubMed
DeVries, A.L. 1988. The role of antifreeze glycopeptides and peptides in the freezing avoidance of Antarctic fishes. Comparative Biochemistry and Physiology, 90B, 611–621.Google Scholar
DeVries, A.L. Cheng, C.-H.C. 1992. The role of antifreeze glycopeptides and peptides in the survival of cold-water fishes. In Somero, G.N., Osmond, C.B. & Bolis, C.L., eds. Water and life. Berlin: Springer, 301–315.CrossRefGoogle 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, vol 22. San Diego, CA: Academic Press, 155–201.Google Scholar
Fange, R. Nilsson, S. 1985. The fish spleen: structure and function. Experientia, 41, 152–158.Google Scholar
Gon, O. Heemstra, P.C. 1990. Fishes of the Southern Ocean. Grahamstown: JLB Smith Institute of Ichthyology. 462 pp.Google Scholar
Gubala, V., Le Guevel, X., Nooney, R., Williams, D.E. MacCraith, B. 2010. A comparison of mono and multivalent linkers and their effect on the colloidal stability of nanoparticle and immunoassays performance. Talanta, 81, 1833–1839.CrossRefGoogle ScholarPubMed
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, 333–338.CrossRefGoogle Scholar
Jensen, L.D.E., Cao, R., Hedlund, E.-M., Söll, I., Lundberg, J.O., Hauptmann, G., Steffensen, J.F. Cao, Y. 2009. Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish. Proceedings of the National Academy of Sciences of the United States of America, 106, 18 408–18 413.CrossRefGoogle 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, 177–185.CrossRefGoogle 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, 10.1039/C0SC00194eGoogle 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, 564–569.CrossRefGoogle 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, 2589–2593.CrossRefGoogle ScholarPubMed
Romano, N., Ceccariglia, S., Abelli, L., Baldassini, M.R., Picchietti, S., Mazzini, M. Mastrolia, L. 2004. Adaptation of fish lymphomyeloid organs to polar water. Chemistry and Ecology, 20, S65–S77.CrossRefGoogle Scholar
Swanson, J.A. Hoppe, A.D. 2004. The coordination of signalling during Fc receptor-mediated phagocytosis. Journal of Leukocyte Biology, 76, 1093–1103.CrossRefGoogle ScholarPubMed
Valerio, P.F., Kao, M.H. Fletcher, G.L. 1992. Fish skin - an effective barrier to ice crystal propagation. Journal of Experimental Biology, 164, 135–151.Google Scholar
Verdier, J.M., Ewart, K.V., Griffith, M. Hew, C.L. 1996. An immune response to ice crystals in North Atlantic fishes. European Journal of Biochemistry, 241, 740–743.CrossRefGoogle ScholarPubMed
Yao, G., Wang, L., Wu, Y., Smith, J., Xu, J., Zhao, W., Lee, E. Tan, W. 2006. FloDots: luminescent particles. Analytical and Bioanalytical Chemistry, 385, 518–524.CrossRefGoogle Scholar