Short-term TNFα shedding is independent of cytoplasmic phosphorylation or furin cleavage of ADAM17

Biochim Biophys Acta. 2013 Dec;1833(12):3355-3367. doi: 10.1016/j.bbamcr.2013.10.005. Epub 2013 Oct 14.

Abstract

Proteolysis of transmembrane molecules is an irreversible post-translational modification enabling autocrine, paracrine and endocrine signaling of many cytokines. The pro-inflammatory activities of membrane bound TNFα (pro-TNFα) strongly depend on ectodomain shedding mediated by the A Disintegrin And Metalloprotease family member ADAM17. Despite the well-documented role of ADAM17 in pro-TNFα cleavage during inflammation, little is known about its regulation. Mitogen-activated protein kinase-induced phosphorylation of the ADAM17 cytoplasmic tail has been described to be required for proper activation. To address, if pro-TNFα shedding depends on cytosolic phosphorylation we analyzed ADAM17 mutants lacking the cytoplasmic domain. ADAM17 mediated shedding of pro-TNFα was induced by PMA, Anisomycin and the phosphatase inhibitors Cantharidin and Calyculin A. Deletion of the entire cytoplasmic portion of ADAM17 abolished furin-dependent proteolytic maturation and pro-TNFα cleavage. Interestingly, we could exclude that resistance to proconvertase processing is the reason for the enzymatic inactivity of ADAM17 lacking the cytoplasmic portion as furin-resistant ADAM17 mutants rescued genetic ADAM17 deficiency after mitogen-activated protein kinase activation. Adding only 6 cytoplasmic amino acids completely restored ADAM17 maturation and shedding of pro-TNFα as well as of both TNF-receptors Finally, we showed that a pro-TNFα mutant lacking the cytoplasmic portion was also shed from the cell surface. We conclude that pro-TNFα cleavage by its major sheddase ADAM17 does not depend on cytosolic phosphorylation and/or interaction. These results have general implications on understanding the activation mechanism controlling the activity of ADAM17.

Keywords: A Disintegrin And Metalloprotease; ADAM; ADAM17; ADAM17(ex/ex) cells; ADAM17-hypomorphic cells; CHX; Cell surface trafficking; Cycloheximide; EGF; Epidermal Growth Factor; Furin; GPI; ICD; Intracellular domain; LPA; MAPK; PMA; Phosphorylation; TNF receptor; TNF-α; TNFR; TNFα; Tumor Necrosis Factor-α; glycosylphosphatidylinositol; intracellular domain; lysophosphatidic acid; mEF; mitogen-activated protein kinase; murine embryonic fibroblast; phorbol 12-myristate 13-acetate.

MeSH terms

  • ADAM Proteins / chemistry
  • ADAM Proteins / metabolism*
  • ADAM17 Protein
  • Animals
  • Cell Line
  • Cytoplasm / metabolism*
  • Furin / metabolism*
  • Humans
  • Mice
  • Mutant Proteins / metabolism
  • Phosphorylation
  • Protein Multimerization
  • Protein Processing, Post-Translational
  • Protein Structure, Tertiary
  • Protein Transport
  • Proteolysis
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • Mutant Proteins
  • Tumor Necrosis Factor-alpha
  • Furin
  • ADAM Proteins
  • ADAM17 Protein
  • ADAM17 protein, human
  • Adam17 protein, mouse