Human and mouse perforin are processed in part through cleavage by the lysosomal cysteine proteinase cathepsin L

Immunology. 2010 Oct;131(2):257-67. doi: 10.1111/j.1365-2567.2010.03299.x.

Abstract

The pore-forming protein perforin is synthesized as an inactive precursor in natural killer (NK) cells and cytotoxic T lymphocytes (CTLs), and becomes active when a short C-terminal peptide is cleaved within acidic lysosome-like cytotoxic granules. Although it was shown more than a decade ago that this cleavage is pH dependent and can be inhibited by the generic cysteine cathepsin inhibitor E-64d, no protease capable of processing the perforin C terminus has been identified. Neither is it known whether a single protease is responsible or the processing has inbuilt redundancy. Here, we show that incubation of human NK cells and primary antigen-restricted mouse CTLs with the cathepsin L (CatL) inhibitor L1 resulted in a marked inhibition of perforin-dependent target cell death and reduced perforin processing. In vitro, CatL preferentially cleaved a site on full-length recombinant perforin close to its C terminus. The NK cells of mice deficient in CatL showed a reduction but not a complete absence of processed perforin, indicating that cysteine proteases other than CatL are also able to process perforin. We conclude that granule-bound cathepsins are essential for processing perforin to its active form, and that CatL is an important, but not exclusive, participant in this process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biocatalysis / drug effects
  • Cathepsin L / antagonists & inhibitors
  • Cathepsin L / genetics
  • Cathepsin L / metabolism*
  • Cell Line, Tumor
  • Cysteine Proteinase Inhibitors / pharmacology
  • Cytotoxicity, Immunologic / drug effects
  • Cytotoxicity, Immunologic / genetics
  • Cytotoxicity, Immunologic / immunology
  • Egtazic Acid / pharmacology
  • Granzymes / metabolism
  • Humans
  • K562 Cells
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / metabolism
  • Leucine / analogs & derivatives
  • Leucine / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Ovalbumin / immunology
  • Peptide Fragments / immunology
  • Peptide Hydrolases / metabolism
  • Perforin
  • Pore Forming Cytotoxic Proteins / genetics
  • Pore Forming Cytotoxic Proteins / metabolism*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • T-Lymphocytes, Cytotoxic / drug effects
  • T-Lymphocytes, Cytotoxic / immunology

Substances

  • Cysteine Proteinase Inhibitors
  • OVA-8
  • PRF1 protein, human
  • Peptide Fragments
  • Pore Forming Cytotoxic Proteins
  • Recombinant Proteins
  • perforin 1, mouse
  • Perforin
  • Egtazic Acid
  • Ovalbumin
  • Peptide Hydrolases
  • Granzymes
  • CTSL protein, human
  • Cathepsin L
  • Ctsl protein, mouse
  • Leucine
  • aloxistatin