Skip to main content Accessibility help
×
Home
Hostname: page-component-559fc8cf4f-rz424 Total loading time: 0.244 Render date: 2021-03-06T12:08:30.049Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

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
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
Corresponding
E-mail address:

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.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2011

Access options

Get access to the full version of this content by using one of the access options below.

References

Agius, C. Roberts, R.J. 2003. Melano-macrophage centres and their role in fish physiology. Journal of Fish Diseases, 26, 499509.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, 549563.Google 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, 83368342.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, 1049110496.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, 407420.CrossRefGoogle ScholarPubMed
DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science, 172, 11521155.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, 611621.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, 301315.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, 155201.Google Scholar
Fange, R. Nilsson, S. 1985. The fish spleen: structure and function. Experientia, 41, 152158.CrossRefGoogle ScholarPubMed
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, 18331839.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, 333338.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 40818 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, 177185.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/C0SC00194eCrossRefGoogle 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.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, 25892593.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, S65S77.CrossRefGoogle Scholar
Swanson, J.A. Hoppe, A.D. 2004. The coordination of signalling during Fc receptor-mediated phagocytosis. Journal of Leukocyte Biology, 76, 10931103.CrossRefGoogle Scholar
Valerio, P.F., Kao, M.H. Fletcher, G.L. 1992. Fish skin - an effective barrier to ice crystal propagation. Journal of Experimental Biology, 164, 135151.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, 740743.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, 518524.CrossRefGoogle Scholar

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 120
Total number of PDF views: 264 *
View data table for this chart

* Views captured on Cambridge Core between September 2016 - 6th March 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *