The mechanisms and physiological relevance of glycocalyx degradation in hepatic ischemia/reperfusion injury

Antioxid Redox Signal. 2014 Sep 1;21(7):1098-118. doi: 10.1089/ars.2013.5751. Epub 2014 Feb 19.

Abstract

Significance: Hepatic ischemia/reperfusion (I/R) injury is an inevitable side effect of major liver surgery that can culminate in liver failure. The bulk of I/R-induced liver injury results from an overproduction of reactive oxygen and nitrogen species (ROS/RNS), which inflict both parenchymal and microcirculatory damage. A structure that is particularly prone to oxidative attack and modification is the glycocalyx (GCX), a meshwork of proteoglycans and glycosaminoglycans (GAGs) that covers the lumenal endothelial surface and safeguards microvascular homeostasis. ROS/RNS-mediated degradation of the GCX may exacerbate I/R injury by, for example, inducing vasoconstriction, facilitating leukocyte adherence, and directly activating innate immune cells.

Recent advances: Preliminary experiments revealed that hepatic sinusoids contain a functional GCX that is damaged during murine hepatic I/R and major liver surgery in patients. There are three ROS that mediate GCX degradation: hydroxyl radicals, carbonate radical anions, and hypochlorous acid (HOCl). HOCl converts GAGs in the GCX to GAG chloramides that become site-specific targets for oxidizing and reducing species and are more efficiently fragmented than the parent molecules. In addition to ROS/RNS, the GAG-degrading enzyme heparanase acts at the endothelial surface to shed the GCX.

Critical issues: The GCX seems to be degraded during major liver surgery, but the underlying cause remains ill-defined.

Future directions: The relative contribution of the different ROS and RNS intermediates to GCX degradation in vivo, the immunogenic potential of the shed GCX fragments, and the role of heparanase in liver I/R injury all warrant further investigation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Glycocalyx / metabolism*
  • Humans
  • Liver / metabolism*
  • Liver / pathology*
  • Liver Diseases / metabolism*
  • Liver Diseases / pathology*
  • Reactive Nitrogen Species / metabolism
  • Reactive Oxygen Species / metabolism
  • Reperfusion Injury / metabolism*
  • Reperfusion Injury / pathology*

Substances

  • Reactive Nitrogen Species
  • Reactive Oxygen Species