Molecular analysis of the methylprednisolone-mediated inhibition of NK-cell function: Evidence for different susceptibility of IL-2- versus IL-15-activated NK cells

Blood

Volumn 109, Issue 9, 2007, Pages 3767-3775

  Chiossone, Laura ^a   Vitale, Chiara ^b,d   Cottalasso, Francesca ^b   Moretti, Sara ^a   Azzarone, Bruno ^c   Moretta, Lorenzo ^a,b   Mingari, Maria Cristina ^b,d  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c HÔPITAL PAUL BROUSSE   (France)

^d UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; JANUS KINASE 3; MEMBRANE PROTEIN; METHYLPREDNISOLONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PROTEIN 2B4; PROTEIN NKP46; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL FUNCTION; CELL KILLING; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG BLOOD LEVEL; DRUG INHIBITION; GENETIC CROSS; GENETIC LINKAGE; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 33947379469     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-07-037846     Document Type: Article

References (63)

1. Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187-376.
2. Moretta L, Ciccone E, Mingari MC, Biassoni R, Moretta A. Human natural killer cells: origin, clonality, specificity, and receptors. Adv Immunol. 1994;55:341-380.
3. Moretta A, Bottino C, Vitale M, et al. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol. 1996;14:619-648.
4. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999;17:875-904.
5. Moretta A, Bottino C, Vitale M, et al. Activating receptors and co-receptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol. 2001;19:197-223.
6. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol. 2001;11:41-49.
7. Moretta L, Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 2004;23:255-259.
8. Orloff DG, Ra CS, Frank SJ, Klausner R, Kinet JP. Family of disulphide-linked dimers containing the ζ and ε chains of the T-cell receptor and the γ chain of Fc receptors. Nature. 1990;347:189-191.
9. Moretta A, Biassoni R, Bottino C, Mingari MC, Moretta L. Natural cytotoxicity receptors that trigger human NK-cell-mediated cytolysis. Immunol Today. 2000;21:228-234.
10. Bauer S, Groh V, Wu J, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MIC A. Science. 1999;285:727-729.
11. Pende D, Cantoni C, Rivera P, et al. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of non-epithelial origin. Eur J Immunol. 2001;31:1076-1086.
12. Bottino C, Moretta L, Pende D, Vitale M, Moretta A. Learning how to discriminate between friends and enemies, a lesson from natural killer cells. Mol Immunol. 2004;41:569-575.
13. Bottino C, Castriconi R, Pende D, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med. 2003;198:557-567.
14. Sivori S, Parolini S, Falco M, et al. 2B4 functions as a co-receptor in human NK cell activation. Eur J Immunol. 2000;30:787-793.
15. Vitale M, Falco M, Castriconi R, et al. Identification of NKp80, a novel triggering molecule expressed by human NK cells. Eur J Immunol. 2001;31:233-242.
16. Parolini S, Bottino C, Falco M, et al. X-linked ly-MePDNhoproliferative disease: 2B4 molecules displaying inhibitory rather than activating function are responsible for the inability of natural killer cells to kill Epstein-Barr virus-infected cells. J Exp Med. 2000;192:337-346.
17. Bottino C, Falco M, Parolini S, et al. NTB-A [correction of GNTB-A], a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease. J Exp Med. 2001;194:235-246.
18. Vitale C, Chiossone L, Cantoni C, et al. The corticosteroid-induced inhibitory effect on NK cell function reflects downregulation and/or dysfunction of triggering receptors involved in natural cytotoxicity. Eur J Immunol. 2004;34:3028-3038.
19. Clark AR, Lasa M. Crosstalk between glucocorticoids and mitogen-activated protein kinase signaling pathways. Curr Opin Pharmacol. 2003;3:404-411.
20. Wang Z, Malone MH, He H, McColl KS, Distelhorst CW. Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoid-induced apoptosis. J Biol Chem. 2003;278:23861-23867.
21. Watson CE, Archer TK. Chromatin and steroid receptor-mediated transcription. In: Freedman LP, ed. Molecular Biology of Steroid and Nuclear Hormone Receptors. Boston, MA: Birkhauser; 1998:209-235.
22. Ashwell JD, Lu FW, Vacchio MS. Glucocorticoids in T cell development and function. Annu Rev Immunol. 2000;18:309-345.
23. Webster JI, Tonelli L, Sternberg EM. Neuroendocrine regulation of immunity. Annu Rev Immunol. 2002;20:125-163.
24. Berrebi D, Bruscoli S, Cohen N, et al. Synthesis of glucocorticoid- induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood. 2003;101:729-738.
25. Ayroldi E, Migliorati G, Bruscoli S, et al. Modulation of T-cell activation by the glucocorticoid induced leucine zipper factor via inhibition of nuclear factor kappa B. Blood. 2001;98:743-753.
26. Mittelstadt PR, Ashwell JD. Inhibition of AP-1 by the glucocorticoid-inducible protein GILZ. J Biol Chem. 2001;276:29603-29610.
27. Kassel O, Sancono A, Kratzschmar J, Kreft B, Stassen M, Cato AC. Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J. 2001;20:7108-7116.
28. Wei S, Gamero AM, Liu JH, et al. Control of lytic function by mitogen-activated protein kinase/extracellular regulatory kinase 2 (ERK2) in a human natural killer cell line: identification of perforin and granzyme B mobilization by functional ERK2. J Exp Med.1998;187:1753-1765.
29. Trotta R, Puorro KA, Paroli M, et al. Dependence of both spontaneous and antibody-dependent, granule exocytosis-mediated NK cell cytotoxicity on extracellular signal-regulated kinases. J Immunol. 1998;161:6648-6656.
30. Djeu JY, Jiang K, Wei S. A view to a kill: signals triggering cytotoxicity. Clin Cancer Res. 2002;8:636-640.
31. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood. 2001;97:14-32.
32. Waldmann TA, Tagaya Y. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol. 1999;17:19-49.
33. Colucci F, Caligiuri MA, Di Santo JP. What does it take to make a natural killer? Nat Rev Immunol. 2003;3:413-425.
34. Fehniger TA, Cooper MA, Caligiuri MA. Interleukin-2 and interleukin-15: immunotherapy for cancer. Cytokine Growth Factor Rev. 2002;13:169-183.
35. Pende D, Parolini S, Pessino A, et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med. 1999;190:1505-1516.
36. Cantoni C, Bottino C, Vitale M, et al. NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J Exp Med. 1999;189:787-796.
37. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of protein from proteins from polycrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979;76:4350-4354.
38. Schluns KS, Lefrancois L. Cytokine control of memory T-cell development and survival. Nat Rev Immunol. 2003;3:269-279.
39. Leonard WJ, O'Shea JJ. Jaks and STATs: biological iMePDNlications. Annu Rev Immunol. 1998;16:293-322.
40. Yu CR, Lin JX, Fink DW, Akira S, Bloom ET, Yamauchi A. Differential utilization of Janus kinase-signal transducer and activator of transcription signaling pathways in the stimulation of human natural killer cells by IL-2, IL-12 and IFN-α. J Immunol. 1996;157:126-137.
41. Sivori S, Pende D, Bottino C, et al. 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;29:1656-1666.
42. Bianchi M, Meng C, Ivashkiv LB. Inhibition of IL-2-induced Jak-STAT signaling by glucocorticoids. Proc Natl Acad Sci U S A. 2000;97:9573-9578.
43. Tsitoura DC, Rothman PB. Enhancement of MEK/ERK signaling promotes glucocorticoid resistance in CD4+ T cells. J Clin Invest. 2004;113:619-627.
44. Goleva E, Kisich KO, Leung DYM. A role for STAT5 in the pathogenesis of IL-2-induced glucocorticoid resistance. J Immunol. 2002;169:5934-5940.
45. Pipitone N, Sinha N, Theodoridis E, et al. The glucocorticoid inhibition of LFA-1 and CD2 expression by human mononuclear cells is reversed by IL-2, IL-7 and IL-15 Eur J Immunol. 2001;31:2135-2142.
46. Imada K, Bloom ET, Nakajima H, et al. Stat5b is essential for natural killer cell-mediated proliferation and cytotoxicity. J Exp Med. 1998;188:2067-2074
47. Gaffen SL, Lay SY, Ha M, et al. Distinct tyrosine residues within the interleukin-2 receptor β chain drive signal transduction specificity, redundancy and diversity. J Biol Chem. 1996;271:21381-21390.
48. Ascherman DP, Migone TS, Friedman MC, Leonard WJ. Interleukin-2 (IL-2)-mediated induction of the IL-receptor α chain gene: critical role of two functionally redundant tyrosine residues in the IL-2 receptor β chain cytoplasmic domain as suggestion that these residues mediate more than STAT5 activation. J Biol Chem. 1997;272:8704-8709.
49. Giron-Michel J, Caignard A, Fogli M, et al. Differential STAT3, STAT5, and NF-kappaB activation in human hematopoietic progenitors by endogenous interleukin-15: implications in the expression of functional molecules. Blood. 2003;102:109-117.
50. Waldmann TA, Dubois S, Tagaya Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity. 2001;14:105-110.
51. Cooper MA, Bush JE, Fehniger TA, et al. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood. 2002;100:3633-3638.
52. Ranson T, Vosshenrich CA, Corcuff E, Richard O, Muller W, Di Santo JP. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood. 2003;101:4887-4893.
53. Burkett PR, Koka R, Chien M, Chai S, Boone DL, Ma A. Coordinate expression and trans presentation of interleukin (IL)-15R-α- and IL-15 supports natural killer cell and memory CD8+ T cell homeostasis. J Exp Med. 2004;200:825-834.
54. Budagian V, Bulanova E, Orinska Z, et al. A promiscuous liaison between IL-15 receptor and Axl receptor tyrosine kinase in cell death control. EMBO J. 2005;24:4260-4270.
55. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202:1001-1012.
56. Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood. 2006;107:159-166.
57. Upshaw JL, Schoon RA, Dick CJ, Billadeau DD, Leibson PJ. The isoforms of phospholipase C- are differentially used by distinct human NK activating receptors J Immunol. 2005;175:213-218.
58. Andrade MVM, Hiragun T, Beaven MA. Dexamethasone suppresses antigen-induced activation of phosohatidylinositol 3-kinase and downstream responses in mast cells. J Immunol. 2004;172:7254-7262.
59. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1:31-39.
60. Davis DM, Dustin ML. What is the importance of the immunological synapse? Trends in Immunology. 2004;25:323-327.
61. Farag SS, Fehniger TA, Ruggeri L, Velardi A, Caligiuri MA. Natural killer cell receptors: new biology and insights into the graft-versus leukemia effect. Blood. 2002;100:1935-1947.
62. Ruggeri L, Mancusi A, Capanni M, Martelli MF, Velardi A. Exploitation of alloreactive NK cells in adoptive immunotherapy of cancer. Curr Opin Immunol. 2005;17:211-217.
63. Costello RT, Fauriat C, Sivori S, Marcenaro E, Olive D. NK cells: innate immunity against hematological malignancies? Trends Immunol. 2004;25:328-333.