Transglutaminase II/microRNA-218/-181a loop regulates positive feedback relationship between allergic inflammation and tumor metastasis

J Biol Chem. 2014 Oct 24;289(43):29483-505. doi: 10.1074/jbc.M114.603480. Epub 2014 Sep 8.

Abstract

The molecular mechanism of transglutaminase II (TGaseII)-mediated allergic inflammation remains largely unknown. TGaseII, induced by antigen stimulation, showed an interaction and co-localization with FcϵRI. TGaseII was necessary for in vivo allergic inflammation, such as triphasic cutaneous reaction, passive cutaneous anaphylaxis, and passive systemic anaphylaxis. TGaseII was necessary for the enhanced metastatic potential of B16F1 melanoma cells by passive systemic anaphylaxis. TGaseII was shown to be a secreted protein. Recombinant TGaseII protein increased the histamine release and β-hexosaminidase activity, and enhanced the metastatic potential of B16F1 mouse melanoma cells. Recombinant TGaseII protein induced the activation of EGF receptor and an interaction between EGF receptor and FcϵRI. Recombinant TGaseII protein displayed angiogenic potential accompanied by allergic inflammation. R2 peptide, an inhibitor of TGaseII, exerted negative effects on in vitro and in vivo allergic inflammation by regulating the expression of TGaseII and FcϵRI signaling. MicroRNA (miR)-218 and miR-181a, decreased during allergic inflammation, were predicted as negative regulators of TGaseII by microRNA array and TargetScan analysis. miR-218 and miR-181a formed a negative feedback loop with TGaseII and regulated the in vitro and in vivo allergic inflammation. TGaseII was necessary for the interaction between mast cells and macrophages during allergic inflammation. Mast cells and macrophages, activated during allergic inflammation, were responsible for the enhanced metastatic potential of tumor cells that are accompanied by allergic inflammation. In conclusion, the TGaseII/miR-218/-181a feedback loop can be employed for the development of anti-allergy therapeutics.

Keywords: Allergic Inflammation; Angiogenesis; Gene Regulation; Macrophage; Mast Cell; MicroRNA-181a; MicroRNA-218; Transglutaminase II; Tumor Metastasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens / metabolism
  • Base Sequence
  • Cell Movement / drug effects
  • ErbB Receptors / metabolism
  • Feedback, Physiological* / drug effects
  • Female
  • GTP-Binding Proteins / antagonists & inhibitors
  • GTP-Binding Proteins / metabolism*
  • Hypersensitivity / complications
  • Hypersensitivity / genetics
  • Hypersensitivity / pathology*
  • Inflammation / complications
  • Inflammation / genetics
  • Inflammation / pathology*
  • Macrophage Activation / drug effects
  • Male
  • Mast Cells / drug effects
  • Mast Cells / metabolism
  • Melanoma / blood supply
  • Melanoma / genetics
  • Melanoma / metabolism
  • Melanoma / pathology*
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs / metabolism*
  • Molecular Sequence Data
  • Neoplasm Metastasis
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / pathology
  • Passive Cutaneous Anaphylaxis / genetics
  • Peptides / pharmacology
  • Protein Binding / drug effects
  • Protein Glutamine gamma Glutamyltransferase 2
  • Receptors, IgE / metabolism
  • Skin / pathology
  • Transglutaminases / antagonists & inhibitors
  • Transglutaminases / metabolism*

Substances

  • Antigens
  • Fc-epsilon receptor I beta-chain, mouse
  • MIRN218 microRNA, mouse
  • MicroRNAs
  • Peptides
  • Receptors, IgE
  • mirn181 microRNA, mouse
  • Protein Glutamine gamma Glutamyltransferase 2
  • Transglutaminases
  • ErbB Receptors
  • GTP-Binding Proteins