The proinflammatory cytokine interleukin-18 alters multiple signaling pathways to inhibit natural killer cell death

Journal of Interferon and Cytokine Research

Volumn 26, Issue 10, 2006, Pages 706-718

  Hodge, Deborah L ^a   Subleski, Jeff J ^a   Reynolds, Della A ^a   Buschman, Matthew D ^a   Schill, William B ^b   Burkett, Mark W ^c   Malyguine, Anatoli M ^c   Young, Howard A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b LEETOWN SCIENCE CENTER   (United States)

^c SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYTOKINE; HELENALIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 2; MESSENGER RNA; STAUROSPORINE; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; INHIBITOR OF APOPTOSIS PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; INFLAMMATION; MEMBRANE POTENTIAL; MITOCHONDRION; NATURAL KILLER CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; WESTERN BLOTTING; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECT; GENETICS; IMMUNOLOGY; METABOLISM;

APOPTOSIS; CELLS, CULTURED; HUMANS; INFLAMMATION MEDIATORS; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-18; KILLER CELLS, NATURAL; NF-KAPPA B; RECEPTORS, TUMOR NECROSIS FACTOR; RNA, MESSENGER; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 1; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33750588974     PISSN: 10799907     EISSN: None     Source Type: Journal    
DOI: 10.1089/jir.2006.26.706     Document Type: Article

References (54)

1. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 1994;76:977-987.
2. Shi L, Kraut RP, Aebersold R, Greenberg AH. A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 1992;175:553-566.
3. Balaji KN, Schaschke N, Machleidt W, Catalfamo M, Henkart PA. Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J. Exp. Med. 2002;196:493-503.
4. Jiang SB, Ojcius DM, Persechini PM, Young JD. Resistance of cytolytic lymphocytes to perforin-mediated killing. Inhibition of perforin binding activity by surface membrane proteins. J. Immunol. 1990;144:998-1003.
5. Muller C, Tschopp J. Resistance of CTL to perforin-mediated lysis. Evidence for a lymphocyte membrane protein interacting with perforin. J. Immunol. 1994;153:2470-2478.
6. Hunter CA, Timans J, Pisacane P, Menon S, Cai G, Walker W, Aste-Amezaga M, Chizzonite R, Bazan JF, Kastelein RA. Comparison of the effects of interleukin-1 alpha, interleukin-1 beta and interferon-gamma-inducing factor on the production of interferon-gamma by natural killer. Eur. J. Immunol 1997;27:2787-2792.
7. Kohno K, Kataoka J, Ohtsuki T, Suemoto Y, Okamoto I, Usui M, Ikeda M, Kurimoto M. IFN-gamma-inducing factor (IGIF) is a co-stimulatory factor on the activation of Th1 but not Th2 cells and exerts its effect independently of IL-12. J. Immunol. 1997;158: 1541-1550.
8. Stoll S, Muller G, Kurimoto M, Saloga J, Tanimoto T, Yamauchi H, Okamura H, Knop J, Enk AH. Production of IL-18 (IFN-gamma-inducing factor) messenger RNA and functional protein by murine keratinocytes. J. Immunol. 1997;159:298-302.
9. Stoll S, Jonuleit H, Schmitt E, Muller G, Yamauchi H, Kurimoto M, Knop J, Enk AH. Production of functional IL-18 by different subtypes of murine and human dendritic cells (DC): DC-derived IL-18 enhances IL-12-dependent Th1 development. Eur. J. Immunol. 1998;28:3231-3239.
10. Dao T, Ohashi K, Kayano T, Kurimoto M, Okamura H. Interferon-gamma- inducing factor, a novel cytokine, enhances Fas ligand-mediated cytotoxicity of murine T helper 1 cells. Cell. Immunol. 1996;173:230-235.
11. Fehniger TA, Shah MH, Turner MJ, VanDeusen JB, Whitman SP, Cooper MA, Suzuki K, Wechser M, Goodsaid F, Caligiuri MA. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 1999;162:4511-4520.
12. Okamoto M, Kato S, Oizumi K, Kinoshita M, Inoue Y, Hoshino K, Akira S, McKenzie AN, Young HA, Hoshino T. Interleukin 18 (IL-18) in synergy with 1L-2 induces lethal lung injury in mice: a potential role for cytokines, chemokines, and natural killer cells in the pathogenesis of interstitial pneumonia. Blood 2002;99:1289-1298.
13. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T, Torigoe K, Okura T, Nukada Y, Hattori K. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995;378:88-91.
14. Tsutsui H, Nakanishi K, Matsui K, Higashino K, Okamura H, Miyazawa Y, Kaneda K. IFN-gamma-inducing factor up-regulates Fas ligand-mediated cytotoxic activity of murine natural killer cell clones. J. Immunol. 1996;157:3967-3973.
15. Micallef MJ, Tanimoto T, Kohno K, Ikeda M, Kurimoto M. Interleukin 18 induces the sequential activation of natural killer cells and cytotoxic T lymphocytes to protect syngeneic mice from transplantation with Meth A sarcoma. Cancer Res. 1997;57:4557-4563.
16. Street SE, Trapani JA, MacGregor D, Smyth MJ. Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J. Exp. Med. 2002;196:129-134.
17. Leite-de-Moraes MC, Herbelin A, Gouarin C, Koezuka Y, Schneider E, Dy M. Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J. Immunol. 2000;165: 4367-4371.
18. Schneider E, Tonanny MB, Lisbonne M, Leite-de-Moraes M, Dy M. Pro-Th1 cytokines promote Fas-dependent apoptosis of immature peripheral basophils. J. Immunol. 2004;172:5262-5268.
19. Chandrasekar B, Vemula K, Surabhi RM, Li-Weber M, Owen-Schaub LB, Jensen LE, Mummidi S. Activation of intrinsic and extrinsic proapoptotic signaling pathways in interleukin-18-mediated human cardiac endothelial cell death. J. Biol. Chem. 2004; 279:20221-20233.
20. Hodge DL, Schill WB, Wang JM, Blanca I, Reynolds DA, Ortaldo JR, Young HA. IL-2 and IL-12 alter NK cell responsiveness to IFN-gamma-inducible protein 10 by downregulating CXCR3 expression. J. Immunol. 2002;168:6090-6098.
21. Timonen T, Reynolds CW, Ortaldo JR, Herberman RB. Isolation of human and rat natural killer cells. J. Immunol. Methods 1982; 51:269-277.
22. Hodge DL, Martinez A, Julias JG, Taylor LS, Young HA. Regulation of nuclear gamma interferon gene expression by interleukin 12 (IL-12) and IL-2 represents a novel form of posttranscriptional control. Mol. Cell. Biol. 2002;22:1742-1753.
23. Khaled AR, Kim K, Hofmeister R, Muegge K, Durum SK. Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proc. Natl. Acad. Sci. USA 1999;96:14476-14481.
24. Derby E, Reddy V, Kopp W, Nelson E, Baseler M, Sayers T, Malyguine A. Three-color flow cytometric assay for the study of the mechanisms of cell-mediated cytotoxicity. Immunol. Lett. 2001; 78:35-39.
25. Duckett CS, Gedrich RW, Gilfillan MC, Thompson CB. Induction of nuclear factor kappaB by the CD30 receptor is mediated by TRAF1 and TRAF2. Mol. Cell. Biol. 1997;17:1535-1542.
26. Micheau O, Lens S, Gaide O, Alevizopoulos K, Tschopp J. NF-kappaB signals induce the expression of c-FLIP. Mol. Cell. Biol. 2001;21:5299-5305.
27. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and C-IAP2 to suppress caspase-8 activation. Science 1998;281:1680-1683.
28. Matsumoto S, Tsuji-Takayama K, Aizawa Y, Koide K, Takeuchi M, Ohta T, Kurimoto M. Interleukin-18 activates NF-kappaB in murine T helper type 1 cells. Biochem. Biophys. Res. Commun. 1997;234:454-457.
29. Dunn IF, Sannikova TY, Geha RS, Tsitsikov EN. Identification and characterization of two CD40-inducible enhancers in the mouse TRAF1 gene locus. Mol. Immunol. 2000;37:961-973.
30. Naume B, Shalaby R, Lesslauer W, Espevik T. Involvement of the 55- and 75-kDa tumor necrosis factor receptors in the generation of lymphokine-activated killer cell activity and proliferation of natural killer cells. J. Immunol. 1991;146:3045-3048.
31. Rothe M, Wong SC, Henzel WJ, Goeddel DV. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell 1994;78:681-692.
32. Tsitsikov EN, Laouini D, Dunn IF, Sannikova TY, Davidson L, Alt FW, Geha RS. TRAF1 is a negative regulator of TNF signaling, enhanced TNF signaling in TRAF1-deficient mice. Immunity 2001;15:647-657.
33. Rothstein TL, Mage M, Jones G, McHugh LL. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J. Immunol. 1978;121:1652-1656.
34. Atkinson EA, Barry M, Darmon AJ, Shostak I, Turner PC, Moyer RW, Bleackley RC. Cytotoxic T lymphocyte-assisted suicide. Caspase 3 activation is primarily the result of the direct action of granzyme B. J. Biol. Chem. 1998;273:21261-21266.
35. Warren HS. NK cell proliferation and inflammation. Immunol. Cell Biol. 1996;74:473-480.
36. Wiltrout RH. Regulation and antimetastatic functions of liver-associated natural killer cells. Immunol. Rev. 2000;174:63-76.
37. Eischen CM, Schilling JD, Lynch DH, Krammer PH, Leibson PJ. Fc receptor-induced expression of Fas ligand on activated NK cells facilitates cell-mediated cytotoxicity and subsequent autocrine NK cell apoptosis. J. Immunol. 1996;156:2693-2699.
38. Jewett A, Bonavida B. MHC-class I antigens regulate both the function and the survival of human peripheral blood NK cells: role of endogenously secreted TNF-alpha. Clin. Immunol. 2000;96:19-28.
39. Spaggiari GM, Contini P, Dondero A, Carosio R, Puppo F, Indiveri F, Zocchi MR, Poggi A. Soluble HLA class I induces NK cell apoptosis upon the engagement of killer-activating HLA class I receptors through FasL-Fas interaction. Blood 2002;100:4098-4107.
40. Jewett A, Bonavida B. Target-induced inactivation and cell death by apoptosis in a subset of human NK cells. J. Immunol. 1996;156: 907-915.
41. Ortaldo JR, Mason AT, O'Shea JJ. Receptor-induced death in human natural killer cells: involvement of CD16. J. Exp. Med. 1995; 181:339-344.
42. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, Alnemri ES, Salvesen GS, Reed JC. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 1998;17:2215-2223.
43. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC, Salvesen GS. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001;104:791-800.
44. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM, Alnemri ES, Fairman R, Shi Y. Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell 2003;11:519-527.
45. Huang H, Joazeiro CA, Bonfoco E, Kamada S, Leverson JD, Hunter T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J. Biol. Chem. 2000;275:26661-26664.
46. Fotin-Mleczek M, Henkler F, Hausser A, Glauner H, Samel D, Graness A, Scheurich P, Mauri D, Wajant H. Tumor necrosis factor receptor-associated factor (TRAF) 1 regulates CD40-induced TRAF2-mediated NF-kappaB activation. J. Biol. Chem. 2004;279: 677-685.
47. Arron JR, Pewzner-Jung Y, Walsh MC, Kobayashi T, Choi Y. Regulation of the subcellular localization of tumor necrosis factor receptor-associated factor (TRAF)2 by TRAF1 reveals mechanisms of TRAF2 signaling. J. Exp. Med. 2002;196:923-934.
48. Hudig D, Gregg NJ, Kam CM, Powers JC. Lymphocyte granule-mediated cytolysis requires serine protease activity. Biochem. Biophys. Res. Commun. 1987;149:882-888.
49. Podack ER, Dennert G. Assembly of two types of tubules with putative cytolytic function by cloned natural killer cells. Nature 1983;302:442-445.
50. Waterhouse NJ, Trapani JA. CTL: caspases terminate life, but that's not the whole story. Tissue Antigens 2002;59:175-183.
51. Sarin A, Williams MS, Alexander-Miller MA, Berzofsky JA, Zacharchuk CM, Henkart PA. Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity 1997;6:209-215.
52. Sun J, Bird CH, Sutton V, McDonald L, Coughlin PB, De Jong TA, Trapani JA, Bird PI. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 1996;271:27802-27809.
53. Bird CH, Sutton VR, Sun J, Hirst CE, Novak A, Kumar S, Trapani JA, Bird PI. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol. Cell. Biol. 1998;18:6387-6398.
54. Hirst CE, Buzza MS, Bird CH, Warren HS, Cameron PU, Zhang M, Ashton-Rickardt PG, Bird PI. 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;170:805-815.