Lack of interleukin-1α or interleukin-1β inhibits transformation of steatosis to steatohepatitis and liver fibrosis in hypercholesterolemic mice

J Hepatol. 2011 Nov;55(5):1086-94. doi: 10.1016/j.jhep.2011.01.048. Epub 2011 Feb 24.

Abstract

Background & aims: The identification of the cellular and molecular pathways that mediate the development of non-alcoholic steatohepatitis is of crucial importance. Cytokines produced by liver-resident and infiltrating inflammatory cells, play a pivotal role in liver inflammation. The role of the proinflammatory cytokines IL-1α and IL-1β in steatohepatitis remains elusive.

Methods: We employed IL-1α and IL-1β-deficient mice and transplanted marrow cells to study the role of liver-resident and bone marrow-derived IL-1 in steatosis and its progression to steatohepatitis.

Results: Atherogenic diet-induced steatohepatitis in wild-type mice was associated with 16 and 4.6 fold-elevations in mRNA levels of hepatic IL-1α and IL-1β, respectively. In mice deficient in either IL-1α or IL-1β the transformation of steatosis to steatohepatitis and liver fibrosis was markedly reduced. This protective effect in IL-1α-deficient mice was noted despite increased liver cholesterol levels. Deficiency of IL-1α markedly reduced plasma serum amyloid A and steady-state levels of mRNA coding for inflammatory genes (P-selectin, CXCL1, IL-6, and TNFα) as well as pro-fibrotic genes (MMP-9 and Collagen) and particularly a 50% decrease in TGFβ levels (p = 0.004). IL-1α mRNA levels were two-folds lower in IL-1β-deficient mice, and IL-1β transcripts were three-folds lower in IL-1α-deficient compared to wild-type mice. Hepatic cell derived IL-1α rather than from recruited bone marrow-derived cells was required for steatohepatitis development.

Conclusions: These data demonstrate the critical role of IL-1α and IL-1β in the transformation of steatosis to steatohepatitis and liver fibrosis in hypercholesterolemic mice. Therefore, the potential of neutralizing IL-1α and/or IL-1β to inhibit the development of steatohepatitis should be explored.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Chemokine CXCL1 / genetics
  • Chemokine CXCL1 / metabolism
  • Collagen / genetics
  • Collagen / metabolism
  • Diet, Atherogenic
  • Disease Progression
  • Fatty Liver / metabolism*
  • Fatty Liver / pathology
  • Gene Expression
  • Hepatitis / metabolism*
  • Hepatitis / pathology
  • Hypercholesterolemia / complications
  • Interleukin-1 / genetics
  • Interleukin-1 / metabolism
  • Interleukin-1alpha / deficiency*
  • Interleukin-1alpha / genetics
  • Interleukin-1alpha / metabolism
  • Interleukin-1beta / deficiency*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Liver Cirrhosis / metabolism*
  • Liver Cirrhosis / pathology
  • Male
  • Matrix Metalloproteinase 9 / genetics
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • P-Selectin / genetics
  • P-Selectin / metabolism
  • RNA, Messenger / metabolism*
  • Serum Amyloid A Protein / metabolism
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Chemokine CXCL1
  • Interleukin-1
  • Interleukin-1alpha
  • Interleukin-1beta
  • P-Selectin
  • RNA, Messenger
  • Serum Amyloid A Protein
  • Transforming Growth Factor beta
  • Tumor Necrosis Factor-alpha
  • Collagen
  • Matrix Metalloproteinase 9