Modeling the intra- and extracellular cytokine signaling pathway under heat stroke in the liver

PLoS One. 2013 Sep 5;8(9):e73393. doi: 10.1371/journal.pone.0073393. eCollection 2013.

Abstract

Heat stroke (HS) is a life-threatening illness induced by prolonged exposure to a hot environment that causes central nervous system abnormalities and severe hyperthermia. Current data suggest that the pathophysiological responses to heat stroke may not only be due to the immediate effects of heat exposure per se but also the result of a systemic inflammatory response syndrome (SIRS). The observation that pro- (e.g., IL-1) and anti-inflammatory (e.g., IL-10) cytokines are elevated concomitantly during recovery suggests a complex network of interactions involved in the manifestation of heat-induced SIRS. In this study, we measured a set of circulating cytokine/soluble cytokine receptor proteins and liver cytokine and receptor mRNA accumulation in wild-type and tumor necrosis factor (TNF) receptor knockout mice to assess the effect of neutralization of TNF signaling on the SIRS following HS. Using a systems approach, we developed a computational model describing dynamic changes (intra- and extracellular events) in the cytokine signaling pathways in response to HS that was fitted to novel genomic (liver mRNA accumulation) and proteomic (circulating cytokines and receptors) data using global optimization. The model allows integration of relevant biological knowledge and formulation of new hypotheses regarding the molecular mechanisms behind the complex etiology of HS that may serve as future therapeutic targets. Moreover, using our unique modeling framework, we explored cytokine signaling pathways with three in silico experiments (e.g. by simulating different heat insult scenarios and responses in cytokine knockout strains in silico).

Publication types

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

MeSH terms

  • Animals
  • Computer Simulation
  • Cytokines / analysis
  • Cytokines / blood
  • Cytokines / immunology*
  • Gene Expression Regulation
  • Heat Stroke / complications*
  • Heat Stroke / genetics
  • Heat Stroke / immunology*
  • Liver / immunology*
  • Liver / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Models, Immunological
  • RNA, Messenger / analysis
  • RNA, Messenger / genetics
  • Receptors, Interleukin / genetics
  • Signal Transduction*
  • Systemic Inflammatory Response Syndrome / etiology*
  • Systemic Inflammatory Response Syndrome / genetics
  • Systemic Inflammatory Response Syndrome / immunology*
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • Cytokines
  • RNA, Messenger
  • Receptors, Interleukin
  • Tumor Necrosis Factor-alpha

Grants and funding

The authors acknowledge the financial support provided by the Institute for Collaborative Biotechnologies through grants W911NF-09-0001 and W911QY-09-P-0709 from the U.S. Army Research Office. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Army or the Department of Defense. Citations of commercial organizations and trade names in this report do not constitute an official Department of the Army endorsement or approval of the products or services of these organizations. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.