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PMID: 21187373 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation.

De Maria A, Bozzano F, Cantoni C, Moretta L

Abstract

The two major functions of human natural killer (NK) cells are conventionally associated with distinct cell subsets. Thus, cytolytic activity is mostly confined to the CD56(dim)CD16(+) subset, whereas cytokine production is generally assigned to CD56(bright)CD16(+/-) cells. In this study, we reevaluated the functional capabilities of these NK subsets with regard to the production of IFN-γ at different time points after cell triggering via NKp46 and NKp30 activating receptors. Different from previous studies, cytokine production was also assessed at early intervals. We show that CD56(dim) NK cells produce IFN-γ already at 2 to 4 h, whereas no cytokine production is detected beyond 16 h. In contrast, CD56(bright) cells release IFN-γ only at late time intervals (>16 h after stimulation). The rapid IFN-γ production by CD56(dim) NK cells is in line with the presence of IFN-γ mRNA in freshly isolated cells. Rapid IFN-γ production was also induced by combinations of IL-2, IL-12, and IL-15. Our data indicate that not only cytolytic activity but also early IFN-γ production is a functional property of CD56(dim) NK cells. Thus, this subset can assure a rapid and comprehensive NK cell intervention during the early phases of innate responses.

MeSH Terms
Animals CD3 Complex/biosynthesis CD56 Antigen/biosynthesis Cytokines/metabolism Interferon-gamma/metabolism Interleukin-12/metabolism Interleukin-15/metabolism Interleukin-2/metabolism Killer Cells, Natural/cytology Leukocytes, Mononuclear/cytology Mice Mice, Transgenic Receptors, IgG/biosynthesis,genetics Reverse Transcriptase Polymerase Chain Reaction Time Factors
Chemicals
CD3 Complex CD56 Antigen Cytokines Interleukin-15 Interleukin-2 Receptors, IgG Interleukin-12 Interferon-gamma
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
De Maria Andrea
Infectious Diseases Unit, Istituto Nazionale per la Ricerca sul Cancro, 16132 Genoa, Italy. de-maria@unige.it
Bozzano Federica
Cantoni Claudia
Moretta Lorenzo
References (26)
26 references, click to expand
  1. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs.
    Proc Natl Acad Sci U S A. 2004 Nov 23;101(47):16606-11 PMID: 15536127
  2. Unravelling natural killer cell function: triggering and inhibitory human NK receptors.
    EMBO J. 2004 Jan 28;23(2):255-9 PMID: 14685277
  3. NK cells at the interface between innate and adaptive immunity.
    Cell Death Differ. 2008 Feb;15(2):226-33 PMID: 17541426
  4. Human natural killer cells.
    Blood. 2008 Aug 1;112(3):461-9 PMID: 18650461
  5. Significant NK cell activation associated with decreased cytolytic function in peripheral blood of HIV-1-infected patients.
    Eur J Immunol. 2004 Aug;34(8):2313-21 PMID: 15259029
  6. Killer immunoglobulin-like receptors.
    Curr Opin Immunol. 2004 Oct;16(5):626-33 PMID: 15342010
  7. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity.
    Blood. 2003 Apr 15;101(8):3052-7 PMID: 12480696
  8. Regulation of human NK-cell cytokine and chemokine production by target cell recognition.
    Blood. 2010 Mar 18;115(11):2167-76 PMID: 19965656
  9. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells.
    J Exp Med. 2002 Feb 4;195(3):343-51 PMID: 11828009
  10. Surface NK receptors and their ligands on tumor cells.
    Semin Immunol. 2006 Jun;18(3):151-8 PMID: 16730454
  11. CD56brightCD16- killer Ig-like receptor- NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation.
    J Immunol. 2007 Apr 15;178(8):4947-55 PMID: 17404276
  12. Human NK cells: from HLA class I-specific killer Ig-like receptors to the therapy of acute leukemias.
    Immunol Rev. 2008 Aug;224:58-69 PMID: 18759920
  13. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells.
    Eur J Immunol. 1999 May;29(5):1656-66 PMID: 10359120
  14. Rapid response to Con A by CD4+CD45R- rat memory lymphocytes as compared to CD4+CD45R+ lymphocytes.
    Cell Immunol. 1989 Apr 1;119(2):317-26 PMID: 2522820
  15. Cellular ligands of activating NK receptors.
    Trends Immunol. 2005 Apr;26(4):221-6 PMID: 15797513
  16. Increased natural cytotoxicity receptor expression and relevant IL-10 production in NK cells from chronically infected viremic HCV patients.
    Eur J Immunol. 2007 Feb;37(2):445-55 PMID: 17273991
  17. Functionally relevant decreases in activatory receptor expression on NK cells are associated with pulmonary tuberculosis in vivo and persist after successful treatment.
    Int Immunol. 2009 Jul;21(7):779-91 PMID: 19461127
  18. NK cells: a lesson from mismatched hematopoietic transplantation.
    Trends Immunol. 2002 Sep;23(9):438-44 PMID: 12200065
  19. The interaction between NK cells and dendritic cells in bacterial infections results in rapid induction of NK cell activation and in the lysis of uninfected dendritic cells.
    Eur J Immunol. 2003 Feb;33(2):306-13 PMID: 12548561
  20. Regulatory role of NKp44, NKp46, DNAM-1 and NKG2D receptors in the interaction between NK cells and trophoblast cells. Evidence for divergent functional profiles of decidual versus peripheral NK cells.
    Int Immunol. 2008 Nov;20(11):1395-405 PMID: 18815119
  21. Effector and regulatory events during natural killer-dendritic cell interactions.
    Immunol Rev. 2006 Dec;214:219-28 PMID: 17100887
  22. Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression.
    Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11918-23 PMID: 20547831
  23. NK cell and DC interactions.
    Trends Immunol. 2004 Jan;25(1):47-52 PMID: 14698284
  24. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44).
    Eur J Immunol. 2003 Sep;33(9):2410-8 PMID: 12938217
  25. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton.
    J Exp Med. 1995 Feb 1;181(2):577-84 PMID: 7836913
  26. Early liaisons between cells of the innate immune system in inflamed peripheral tissues.
    Trends Immunol. 2005 Dec;26(12):668-75 PMID: 16198147
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-01-11
Epub
2010-00-27
Pages
728-32
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3021076
Subset
IM
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