Hyaluronic acid or TNF-alpha plus fibronectin triggers granulocyte macrophage-colony-stimulating factor mRNA stabilization in eosinophils yet engages differential intracellular pathways and mRNA binding proteins

J Immunol. 2003 Dec 15;171(12):6780-7. doi: 10.4049/jimmunol.171.12.6780.

Abstract

Eosinophils (Eos) accumulate in airways and lung parenchyma of active asthmatics. GM-CSF is a potent inhibitor of Eos apoptosis both in vitro and in vivo and is produced by activated fibroblasts, mast cells, T lymphocytes as well as Eos. Cytokine release by Eos is preceded by GM-CSF mRNA stabilization induced by TNF-alpha plus fibronectin. Hyaluronic acid (HA) is a major extracellular matrix proteoglycan, which also accumulates in the lung during asthma exacerbations. In this study we have analyzed the effects of HA on Eos survival and GM-CSF expression. We demonstrate that like TNF-alpha plus fibronectin, HA stabilizes GM-CSF mRNA, increases GM-CSF secretion, and prolongs in vitro Eos survival. GM-CSF mRNA stabilization accounts for most of the observed GM-CSF mRNA accumulation and protein production. Unlike TNF-alpha plus fibronectin, GM-CSF mRNA stabilization induction by HA requires continuous extracellular signal-regulated kinase phosphorylation. Finally, to identify potential protein regulators responsible for GM-CSF mRNA stabilization, immunoprecipitation-RT-PCR studies revealed increased GM-CSF mRNA associated with YB-1, HuR, and heterogeneous nuclear ribonucleoprotein (hnRNP) C after TNF-alpha plus fibronectin but only hnRNP C after HA. Thus, our data suggest that both TNF-alpha plus fibronectin and HA, which are relevant physiological effectors in asthma, contributes to long-term Eos survival in vivo by enhancing GM-CSF production through two different posttranscriptional regulatory pathways involving extracellular signal-regulated kinase phosphorylation and RNA binding proteins YB-1, HuR, and hnRNP C.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adjuvants, Immunologic / pharmacology
  • Cell Survival / physiology
  • Drug Combinations
  • Eosinophils / cytology
  • Eosinophils / enzymology
  • Eosinophils / metabolism*
  • Eosinophils / physiology
  • Fibronectins / pharmacology*
  • Granulocyte-Macrophage Colony-Stimulating Factor / genetics
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Heterogeneous-Nuclear Ribonucleoprotein Group C / metabolism
  • Humans
  • Hyaluronan Receptors / physiology
  • Hyaluronic Acid / pharmacology*
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphorylation
  • Protein Binding / physiology
  • RNA Stability / physiology*
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / metabolism*
  • RNA-Binding Proteins / metabolism
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Up-Regulation / physiology

Substances

  • Adjuvants, Immunologic
  • Drug Combinations
  • Fibronectins
  • Heterogeneous-Nuclear Ribonucleoprotein Group C
  • Hyaluronan Receptors
  • RNA, Messenger
  • RNA-Binding Proteins
  • Tumor Necrosis Factor-alpha
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Hyaluronic Acid
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases