Acute hypoxia induces HIF-independent monocyte adhesion to endothelial cells through increased intercellular adhesion molecule-1 expression: the role of hypoxic inhibition of prolyl hydroxylase activity for the induction of NF-kappa B

J Immunol. 2010 Aug 1;185(3):1786-93. doi: 10.4049/jimmunol.0903244. Epub 2010 Jun 23.

Abstract

Myeloid cells recruited to sites of bacterial inflammation are exposed to low oxygen tension, hypoxia, and high concentrations of inflammatory cytokines that significantly affect myeloid cell function. Therefore, we analyzed the direct consequences of acute and severe hypoxia on monocytic adhesion to the endothelium in coculture experiments. Marked upregulation of monocytic ICAM-1, but no other monocytic adhesion molecule, was responsible for an approximately 50-fold increase in adhesion of the monocytic cells THP-1 to human and rat endothelial cells. ICAM-1 expression was rapidly induced after the onset of severe hypoxia, but it decreased after 4 h. Knockdown of ICAM-1 by siRNA in endothelial and monocytic cells abolished the adhesion, indicating that ICAM-1 expression on both cell types was indispensable for hypoxia-induced adhesion of monocytes to the endothelium. siRNA-mediated knockdown of hypoxia inducible factor (HIF)-1alpha, HIF-2alpha, and the NF-kappaB family member p65 revealed that hypoxic upregulation of ICAM-1 resulted from hypoxic NF-kappaB induction but not from activation of HIFs. Within the leukocyte-adhesion cascade, our results provide evidence for prolyl hydroxylase-dependent but HIF-independent activation of hypoxia-induced monocyte-endothelial adhesion and assign a new function to monocytic ICAM-1 under acute hypoxic conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Disease
  • Amino Acids, Dicarboxylic / pharmacology
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / antagonists & inhibitors
  • Basic Helix-Loop-Helix Transcription Factors / physiology
  • Cell Adhesion / immunology
  • Cell Hypoxia / immunology*
  • Cell Line
  • Cell Line, Tumor
  • Coculture Techniques
  • Endothelium, Vascular / cytology*
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / immunology*
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / antagonists & inhibitors
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology*
  • Intercellular Adhesion Molecule-1 / biosynthesis*
  • Intercellular Adhesion Molecule-1 / genetics
  • Intercellular Adhesion Molecule-1 / physiology
  • Monocytes / cytology
  • Monocytes / enzymology
  • Monocytes / immunology*
  • NF-kappa B / biosynthesis*
  • Procollagen-Proline Dioxygenase / antagonists & inhibitors*
  • Procollagen-Proline Dioxygenase / metabolism
  • RNA, Messenger / biosynthesis
  • Rats
  • Up-Regulation / immunology

Substances

  • Amino Acids, Dicarboxylic
  • Basic Helix-Loop-Helix Transcription Factors
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • NF-kappa B
  • RNA, Messenger
  • Intercellular Adhesion Molecule-1
  • endothelial PAS domain-containing protein 1
  • Procollagen-Proline Dioxygenase
  • oxalylglycine