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

Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance
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DOI:
10.1073/pnas.0603796103
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发表时间:
2006-07-05
影响因子:
11.1
通讯作者:
Evans, Clive W.
Evans, Clive W.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Cheng, Chi-Hing C.;Cziko, Paul A.;Evans, Clive W.

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系统发育多样的极地和亚极地海洋硬骨鱼进化抗冻蛋白(AFP)或抗冻糖蛋白(AFGPs),以避免接种冻结的内部冰。自第一个鱼类抗冻蛋白(AF)被发现以来的三十多年里,许多关于硬骨鱼抗冻性的研究表明,肝脏AF的合成和在循环中的分布是防止血液和鱼类结冰的关键。我们已经发现了一个重要的转折,这个长期持有的范例:在南极notothenioids的任何生命阶段的肝脏合成AFGPs的完全缺乏,这表明肝脏在这些鱼类的防冻中没有发挥作用。相反,我们发现胰腺外分泌是所有生命阶段AFGP合成和分泌的主要部位,胰腺AFGP通过胰管进入肠腔,以防止摄入的冰使低渗肠液成核。AFGP似乎在肠道环境中保持未降解,并且肠道AFGP同种型的组成和相对丰度与血清AFGP几乎相同。因此,完整的胰腺来源的肠AFGP的重吸收,而不是肝脏,是在notothenioid鱼循环AFGP的可能来源。我们研究了不同的北方鱼类类群和南极洲的鳗鱼肝合成的血源性AF,发现他们也表达分泌胰腺AF各自的类型。这种功能生理学的进化趋同强调了迄今为止在很大程度上未被认识到的重要性,肠道防冻在极地硬骨鱼防冻避免,特别是在长期冰冷的南极沃茨。
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.