Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance

Phylogenetically diverse polar and subpolar marine teleost fishes have evolved antifreeze proteins (AFPs) or antifreeze glycoproteins (AFGPs) to avoid inoculative freezing by internalized ice. For over three decades since the first fish antifreeze (AF) protein was discovered, many studies of teleost...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences
Main Authors: Cheng, CHC, Cziko, PA, Evans, CW
Format: Article in Journal/Newspaper
Language:English
Published: National Academy of Sciences 2006
Subjects:
antifreeze glycoprotein-null liver
antifreeze paradigm shift
evolutionary adaptation
intestinal freeze avoidance
functional convergence
ANTARCTIC EEL POUT
PEPTIDE HETEROGENEITY
INTESTINAL FLUID
MCMURDO SOUND
PROTEIN
GLYCOPROTEIN
EVOLUTION
ABSORPTION
WATER
GENE
Antarctic
McMurdo Sound
The Antarctic
Antarc*
Online Access:http://hdl.handle.net/2292/12762
https://doi.org/10.1073/pnas.0603796103
Description
Summary:Phylogenetically diverse polar and subpolar marine teleost fishes have evolved antifreeze proteins (AFPs) or antifreeze glycoproteins (AFGPs) to avoid inoculative freezing by internalized ice. For over three decades since the first fish antifreeze (AF) protein was discovered, many studies of teleost freezing avoidance showed hepatic AF synthesis and distribution within the circulation as pivotal in preventing the blood, and therefore the fish, from freezing. We have uncovered an important twist to this long-held paradigm: the complete absence of liver synthesis of AFGPs in any life stage of the Antarctic notothenioids, indicating that the liver plays no role in the freezing avoidance in these fishes. Instead, we found the exocrine pancreas to be the major site of AFGP synthesis and secretion in all life stages, and that pancreatic AFGPs enter the intestinal lumen via the pancreatic duct to prevent ingested ice from nucleating the hyposmotic intestinal fluids. AFGPs appear to remain undegraded in the intestinal milieu, and the composition and relative abundance of intestinal AFGP isoforms are nearly identical to serum AFGPs. Thus, the reabsorption of intact pancreas-derived intestinal AFGPs, and not the liver, is the likely source of circulatory AFGPs in notothenioid fishes. We examined diverse northern fish taxa and Antarctic eelpouts with hepatic synthesis of bloodborne AF and found that they also express secreted pancreatic AF of their respective types. The evolutionary convergence of this functional physiology underscores the hitherto largely unrecognized importance of intestinal freezing prevention in polar teleost freezing avoidance, especially in the chronically icy Antarctic waters.

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