Extracellular 2'5'-oligoadenylate synthetase 2 mediates T-cell receptor CD3-ζ chain down-regulation via caspase-3 activation in oral cancer

Immunology. 2016 Feb;147(2):251-64. doi: 10.1111/imm.12560. Epub 2015 Dec 27.

Abstract

Decreased expression of CD3-ζ chain, an adaptor protein associated with T-cell signalling, is well documented in patients with oral cancer, but the mechanistic justifications are fragmentary. Previous studies in patients with oral cancer have shown that decreased expression of CD3-ζ chain was associated with decreased responsiveness of T cells. Tumours are known to induce localized as well as systemic immune suppression. This study provides evidence that oral tumour-derived factors promote immune suppression by down-regulating CD3-ζ chain expression. 2'5'-Oligoadenylate synthetase 2 (OAS2) was identified by the proteomic approach and our results established a causative link between CD3-ζ chain down-regulation and OAS2 stimulation. The surrogate situation was established by over-expressing OAS2 in a HEK293 cell line and cell-free supernatant was collected. These supernatants when incubated with T cells resulted in down-regulation of CD3-ζ chain, which shows that the secreted OAS2 is capable of regulating CD3-ζ chain expression. Incubation of T cells with cell-free supernatants of oral tumours or recombinant human OAS2 (rh-OAS2) induced caspase-3 activation, which resulted in CD3-ζ chain down-regulation. Caspase-3 inhibition/down-regulation using pharmacological inhibitor or small interfering RNA restored down-regulated CD3-ζ chain expression in T cells induced by cell-free tumour supernatant or rh-OAS2. Collectively these results show that OAS2 leads to impairment in CD3-ζ chain expression, so offering an explanation that might be applicable to the CD3-ζ chain deficiency observed in cancer and diverse disease conditions.

Keywords: CD3-ζ chain; T cells; humans; tumour immunology; tumour-secreted factors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2',5'-Oligoadenylate Synthetase / genetics
  • 2',5'-Oligoadenylate Synthetase / metabolism*
  • CD3 Complex / immunology
  • CD3 Complex / metabolism*
  • Case-Control Studies
  • Caspase 3 / genetics
  • Caspase 3 / metabolism*
  • Cell Line, Tumor
  • Down-Regulation
  • Enzyme Activation
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Humans
  • Lymphocytes, Tumor-Infiltrating / enzymology*
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Mouth Neoplasms / enzymology*
  • Mouth Neoplasms / genetics
  • Mouth Neoplasms / immunology
  • Mouth Neoplasms / pathology
  • Paracrine Communication
  • Proteomics / methods
  • RNA Interference
  • Recombinant Proteins / metabolism
  • Signal Transduction
  • T-Lymphocytes / enzymology*
  • T-Lymphocytes / immunology
  • Time Factors
  • Transfection
  • Tumor Cells, Cultured

Substances

  • CD3 Complex
  • CD3 antigen, zeta chain
  • Recombinant Proteins
  • OAS2 protein, human
  • 2',5'-Oligoadenylate Synthetase
  • CASP3 protein, human
  • Caspase 3