The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency

J Immunol. 2003 Jan 15;170(2):805-15. doi: 10.4049/jimmunol.170.2.805.

Abstract

Granzyme B (grB) is a serine proteinase released by cytotoxic lymphocytes (CLs) to kill abnormal cells. GrB-mediated apoptotic pathways are conserved in nucleated cells; hence, CLs require mechanisms to protect against ectopic or misdirected grB. The nucleocytoplasmic serpin, proteinase inhibitor 9 (PI-9), is a potent inhibitor of grB that protects cells from grB-mediated apoptosis in model systems. Here we show that PI-9 is present in CD4(+) cells, CD8(+) T cells, NK cells, and at lower levels in B cells and myeloid cells. PI-9 is up-regulated in response to grB production and degranulation, and associates with grB-containing granules in activated CTLs and NK cells. Intracellular complexes of PI-9 and grB are evident in NK cells, and overexpression of PI-9 enhances CTL potency, suggesting that cytoplasmic grB, which may threaten CL viability, is rapidly inactivated by PI-9. Because dendritic cells (DCs) acquire characteristics similar to those of target cells to activate naive CD8(+) T cells and therefore may also require protection against grB, we investigated the expression of PI-9 in DCs. PI-9 is evident in thymic DCs (CD3(-), CD4(+), CD8(-), CD45(+)), tonsillar DCs, and DC subsets purified from peripheral blood (CD16(+) monocytes and CD123(+) plasmacytoid DCs). Furthermore, PI-9 is expressed in monocyte-derived DCs and is up-regulated upon TNF-alpha-induced maturation of monocyte-derived DCs. In conclusion, the presence and subcellular localization of PI-9 in leukocytes and DCs are consistent with a protective role against ectopic or misdirected grB during an immune response.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adjuvants, Immunologic / biosynthesis
  • Adjuvants, Immunologic / blood
  • Adjuvants, Immunologic / genetics
  • Adjuvants, Immunologic / physiology
  • Antigen-Presenting Cells / cytology*
  • Antigen-Presenting Cells / metabolism
  • Cell Degranulation / immunology*
  • Cell Differentiation / immunology
  • Cell Line
  • Cells, Cultured
  • Cytotoxicity, Immunologic* / genetics
  • Dendritic Cells / classification
  • Dendritic Cells / metabolism
  • Granzymes
  • Humans
  • Intracellular Fluid / enzymology
  • Intracellular Fluid / metabolism
  • Leukocytes / metabolism
  • Serine Endopeptidases / biosynthesis
  • Serine Endopeptidases / metabolism*
  • Serine Proteinase Inhibitors / biosynthesis*
  • Serine Proteinase Inhibitors / blood
  • Serine Proteinase Inhibitors / genetics
  • Serine Proteinase Inhibitors / physiology
  • Serpins / biosynthesis*
  • Serpins / blood
  • Serpins / genetics
  • Serpins / physiology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*
  • T-Lymphocytes, Cytotoxic / enzymology
  • T-Lymphocytes, Cytotoxic / immunology*
  • Up-Regulation / genetics
  • Up-Regulation / immunology*

Substances

  • Adjuvants, Immunologic
  • SERPINB9 protein, human
  • Serine Proteinase Inhibitors
  • Serpins
  • GZMB protein, human
  • Granzymes
  • Serine Endopeptidases