Cytotoxicity of CD56 bright NK cells towards autologous activated CD4 + T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Nielsen, Natasja ^a,c   Ødum, Niels ^b   Ursø, Birgitte ^a   Lanier, Lewis L ^c   Spee, Pieter ^a  

^a NOVO NORDISK A S   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CD56 ANTIGEN; CD94 ANTIGEN; HLA E ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 7; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NATURAL KILLER CELL RECEPTOR NKG2A; NATURAL KILLER CELL RECEPTOR NKG2D; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; INTEGRIN; KLRK1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY D; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTOTOXICITY; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; ANIMAL; CHEMISTRY; CYTOLOGY; FLOW CYTOMETRY; HUMAN; INFLAMMATION; METABOLISM; METHODOLOGY; MONONUCLEAR CELL; MOUSE; STATISTICAL MODEL;

ANIMALS; ANTIGENS, CD56; CD4-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; HUMANS; INFLAMMATION; INTEGRINS; INTERLEUKIN-7; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE; MODELS, STATISTICAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84857489390     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031959     Document Type: Article

References (71)

1. Trinchieri G, (1989) Biology of natural killer cells. Adv Immunol 47: 187-376.
2. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S, (2008) Functions of natural killer cells. Nat Immunol 9: 503-510.
3. Lanier LL, (2005) NK cell recognition. Annu Rev Immunol 23: 225-274.
4. Ljunggren HG, Karre K, (1990) In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 11: 237-244.
5. Zhang B, Yamamura T, Kondo T, Fujiwara M, Tabira T, (1997) Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J Exp Med 186: 1677-1687.
6. Nilsson N, Bremell T, Tarkowski A, Carlsten H, (1999) Protective role of NK1.1+ cells in experimental Staphylococcus aureus arthritis. Clin Exp Immunol 117: 63-69.
7. Leavenworth JW, Wang X, Wenander CS, Spee P, Cantor H, (2011) Mobilization of natural killer cells inhibits development of collagen-induced arthritis. Proc Natl Acad Sci U S A 108: 14584-14589.
8. Fort MM, Leach MW, Rennick DM, (1998) A role for NK cells as regulators of CD4+ T cells in a transfer model of colitis. J Immunol 161: 3256-3261.
9. Lu L, Ikizawa K, Hu D, Werneck MB, Wucherpfennig KW, et al. (2007) Regulation of activated CD4+ T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity 26: 593-604.
10. Leavenworth JW, Schellack C, Kim HJ, Lu L, Spee P, et al. (2010) Analysis of the cellular mechanism underlying inhibition of EAE after treatment with anti-NKG2A F(ab')2. Proc Natl Acad Sci U S A 107: 2562-2567.
11. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH, (1986) The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol 136: 4480-4486.
12. Tak PP, Kummer JA, Hack CE, Daha MR, Smeets TJ, et al. (1994) Granzyme-positive cytotoxic cells are specifically increased in early rheumatoid synovial tissue. Arthritis Rheum 37: 1735-1743.
13. Ottaviani C, Nasorri F, Bedini C, de PO, Girolomoni G, et al. (2006) CD56brightCD16(-) NK cells accumulate in psoriatic skin in response to CXCL10 and CCL5 and exacerbate skin inflammation. Eur J Immunol 36: 118-128.
14. Marcenaro S, Gallo F, Martini S, Santoro A, Griffiths GM, et al. (2006) Analysis of natural killer-cell function in familial hemophagocytic lymphohistiocytosis (FHL): defective CD107a surface expression heralds Munc13-4 defect and discriminates between genetic subtypes of the disease. Blood 108: 2316-2323.
15. Kastrukoff LF, Lau A, Wee R, Zecchini D, White R, et al. (2003) Clinical relapses of multiple sclerosis are associated with 'novel' valleys in natural killer cell functional activity. J Neuroimmunol 145: 103-114.
16. Saraste M, Irjala H, Airas L, (2007) Expansion of CD56Bright natural killer cells in the peripheral blood of multiple sclerosis patients treated with interferon-beta. Neurol Sci 28: 121-126.
17. Vandenbark AA, Huan J, Agotsch M, La TD, Goelz S, et al. (2009) Interferon-beta-1a treatment increases CD56bright natural killer cells and CD4+CD25+ Foxp3 expression in subjects with multiple sclerosis. J Neuroimmunol 215: 125-128.
18. Takao S, Ishikawa T, Yamashita K, Uchiyama T, (2010) The rapid induction of HLA-E is essential for the survival of antigen-activated naive CD4 T cells from attack by NK cells. J Immunol 185: 6031-6040.
19. Roy S, Barnes PF, Garg A, Wu S, Cosman D, et al. (2008) NK cells lyse T regulatory cells that expand in response to an intracellular pathogen. J Immunol 180: 1729-1736.
20. Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, et al. (2007) Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK- cell lysis. Blood 110: 606-615.
21. Andresen L, Hansen KA, Jensen H, Pedersen SF, Stougaard P, et al. (2009) Propionic acid secreted from propionibacteria induces NKG2D ligand expression on human-activated T lymphocytes and cancer cells. J Immunol 183: 897-906.
22. Magri G, Muntasell A, Romo N, Saez-Borderias A, Pende D, et al. (2011) NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood 117: 848-856.
23. Della CM, Vitale M, Carlomagno S, Ferlazzo G, Moretta L, et al. (2003) The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 33: 1657-1666.
24. Schulz U, Kreutz M, Multhoff G, Stoelcker B, Kohler M, et al. (2010) Interleukin-10 promotes NK cell killing of autologous macrophages by stimulating expression of NKG2D ligands. Scand J Immunol 72: 319-331.
25. Lunemann A, Lunemann JD, Roberts S, Messmer B, da Silva RB, et al. (2008) Human NK cells kill resting but not activated microglia via NKG2D- and NKp46-mediated recognition. J Immunol 181: 6170-6177.
26. Mittendorf EA, Storrer CE, Shriver CD, Ponniah S, Peoples GE, (2005) Evaluation of the CD107 cytotoxicity assay for the detection of cytolytic CD8+ cells recognizing HER2/neu vaccine peptides. Breast Cancer Res Treat 92: 85-93.
27. Betts MR, Koup RA, (2004) Detection of T-cell degranulation: CD107a and b. Methods Cell Biol 75: 497-512.
28. Becknell B, Caligiuri MA, (2005) Interleukin-2, interleukin-15, and their roles in human natural killer cells. Adv Immunol 86: 209-239.
29. Fehniger TA, Bluman EM, Porter MM, Mrozek E, Cooper MA, et al. (2000) Potential mechanisms of human natural killer cell expansion in vivo during low-dose IL-2 therapy. J Clin Invest 106: 117-124.
30. Zwirner NW, Domaica CI, (2010) Cytokine regulation of natural killer cell effector functions. Biofactors 36: 274-288.
31. Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW, (2007) Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J Immunol 179: 3472-3479.
32. Biron CA, Sonnenfeld G, Welsh RM, (1984) Interferon induces natural killer cell blastogenesis in vivo. J Leukoc Biol 35: 31-37.
33. Takeda K, Tsutsui H, Yoshimoto T, Adachi O, Yoshida N, et al. (1998) Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8: 383-390.
34. Stanietsky N, Simic H, Arapovic J, Toporik A, Levy O, et al. (2009) The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc Natl Acad Sci U S A 106: 17858-17863.
35. Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M, (2004) Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol 172: 3994-3998.
36. Helander TS, Timonen T, (1998) Adhesion in NK cell function. Curr Top Microbiol Immunol 230: 89-99.
37. Bryceson YT, Ljunggren HG, Long EO, (2009) Minimal requirement for induction of natural cytotoxicity and intersection of activation signals by inhibitory receptors. Blood 114: 2657-2666.
38. Brooks CR, Elliott T, Parham P, Khakoo SI, (2006) The inhibitory receptor NKG2A determines lysis of vaccinia virus-infected autologous targets by NK cells. J Immunol 176: 1141-1147.
39. Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, et al. (2004) NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 172: 123-129.
40. Zamai L, Ahmad M, Bennett IM, Azzoni L, Alnemri ES, et al. (1998) Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J Exp Med 188: 2375-2380.
41. Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, et al. (2001) CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol 31: 3121-3127.
42. Nagler A, Lanier LL, Cwirla S, Phillips JH, (1989) Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol 143: 3183-3191.
43. Ellis TM, Fisher RI, (1989) Functional heterogeneity of Leu 19"bright"+ and Leu 19"dim"+ lymphokine-activated killer cells. J Immunol 142: 2949-2954.
44. Dadmarz R, Bockstoce DC, Golub SH, (1994) Interleukin-7 selectively enhances natural kill cytotoxicity mediated by the CD56bright natural killer subpopulation. Lymphokine Cytokine Res 13: 349-357.
45. Mottonen M, Isomaki P, Luukkainen R, Lassila O, (2002) Regulation of CD154-induced interleukin-12 production in synovial fluid macrophages. Arthritis Res 4: R9.
46. Gracie JA, Forsey RJ, Chan WL, Gilmour A, Leung BP, et al. (1999) A proinflammatory role for IL-18 in rheumatoid arthritis. J Clin Invest 104: 1393-1401.
47. Groh V, Bruhl A, El-Gabalawy H, Nelson JL, Spies T, (2003) Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc Natl Acad Sci U S A 100: 9452-9457.
48. van Roon JA, Verweij MC, Wijk MW, Jacobs KM, Bijlsma JW, et al. (2005) Increased intraarticular interleukin-7 in rheumatoid arthritis patients stimulates cell contact-dependent activation of CD4(+) T cells and macrophages. Arthritis Rheum 52: 1700-1710.
49. Niu X, He D, Zhang X, Yue T, Li N, et al. (2010) IL-21 regulates Th17 cells in rheumatoid arthritis. Hum Immunol 71: 334-341.
50. Vales-Gomez M, Chisholm SE, Cassady-Cain RL, Roda-Navarro P, Reyburn HT, (2008) Selective induction of expression of a ligand for the NKG2D receptor by proteasome inhibitors. Cancer Res 68: 1546-1554.
51. Molinero LL, Domaica CI, Fuertes MB, Girart MV, Rossi LE, et al. (2006) Intracellular expression of MICA in activated CD4 T lymphocytes and protection from NK cell-mediated MICA-dependent cytotoxicity. Hum Immunol 67: 170-182.
52. Eagle RA, Traherne JA, Ashiru O, Wills MR, Trowsdale J, (2006) Regulation of NKG2D ligand gene expression. Hum Immunol 67: 159-169.
53. El-Sherbiny YM, Meade JL, Holmes TD, McGonagle D, Mackie SL, et al. (2007) The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res 67: 8444-8449.
54. Barber DF, Faure M, Long EO, (2004) LFA-1 contributes an early signal for NK cell cytotoxicity. J Immunol 173: 3653-3659.
55. Ardolino M, Zingoni A, Cerboni C, Cecere F, Soriani A, et al. (2011) DNAM-1 ligand expression on Ag-stimulated T lymphocytes is mediated by ROS-dependent activation of DNA-damage response: relevance for NK-T cell interaction. Blood 117: 4778-4786.
56. Eagle RA, Jafferji I, Barrow AD, (2009) Beyond Stressed Self: Evidence for NKG2D Ligand Expression on Healthy Cells. Curr Immunol Rev 5: 22-34.
57. Wilson JL, Heffler LC, Charo J, Scheynius A, Bejarano MT, et al. (1999) Targeting of human dendritic cells by autologous NK cells. J Immunol 163: 6365-6370.
58. Ferlazzo G, Morandi B, D'Agostino A, Meazza R, Melioli G, et al. (2003) 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 33: 306-313.
59. Rabinovich BA, Li J, Shannon J, Hurren R, Chalupny J, et al. (2003) Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol 170: 3572-3576.
60. Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, et al. (2007) Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK- cell lysis. Blood 110: 606-615.
61. Bielekova B, Catalfamo M, Reichert-Scrivner S, Packer A, Cerna M, et al. (2006) Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2Ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc Natl Acad Sci U S A 103: 5941-5946.
62. Li Z, Lim WK, Mahesh SP, Liu B, Nussenblatt RB, (2005) Cutting edge: in vivo blockade of human IL-2 receptor induces expansion of CD56(bright) regulatory NK cells in patients with active uveitis. J Immunol 174: 5187-5191.
63. Kastrukoff LF, Morgan NG, Zecchini D, White R, Petkau AJ, et al. (1998) A role for natural killer cells in the immunopathogenesis of multiple sclerosis. J Neuroimmunol 86: 123-133.
64. Carrega P, Morandi B, Costa R, Frumento G, Forte G, et al. (2008) Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer 112: 863-875.
65. Dalbeth N, Gundle R, Davies RJ, Lee YC, McMichael AJ, et al. (2004) CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J Immunol 173: 6418-6426.
66. Katchar K, Soderstrom K, Wahlstrom J, Eklund A, Grunewald J, (2005) Characterisation of natural killer cells and CD56+ T-cells in sarcoidosis patients. Eur Respir J 26: 77-85.
67. Schierloh P, Yokobori N, Aleman M, Musella RM, Beigier-Bompadre M, et al. (2005) Increased susceptibility to apoptosis of CD56dimCD16+ NK cells induces the enrichment of IFN-gamma-producing CD56bright cells in tuberculous pleurisy. J Immunol 175: 6852-6860.
68. Dalbeth N, Callan MF, (2007) Phenotypic and functional analysis of synovial natural killer cells. Methods Mol Med 136: 149-163.
69. de Matos CT, Berg L, Michaelsson J, Fellander-Tsai L, Karre K, et al. (2007) Activating and inhibitory receptors on synovial fluid natural killer cells of arthritis patients: role of CD94/NKG2A in control of cytokine secretion. Immunology 122: 291-301.
70. Chen S, Kawashima H, Lowe JB, Lanier LL, Fukuda M, (2005) Suppression of tumor formation in lymph nodes by L-selectin-mediated natural killer cell recruitment. J Exp Med 202: 1679-1689.
71. Cooper MA, Fehniger TA, Caligiuri MA, (2001) The biology of human natural killer-cell subsets. Trends Immunol 22: 633-640.