Genome-wide analysis displays marked induction of EBI3/IL-27B in IL-18-activated AML-derived KG1 cells: Critical role of two κB binding sites in the human EBI3 promotor

Molecular Immunology

Volumn 45, Issue 10, 2008, Pages 2869-2880

  Poleganov, Marco A ^a   Bachmann, Malte ^a   Pfeilschifter, Josef ^a   Mühl, Heiko ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

EBI3; Interleukin 18; Interleukin 27; NF B

Indexed keywords

CCL1 CHEMOKINE; CHEMOKINE; CXCL11 CHEMOKINE; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 27; INTERLEUKIN 27B; MESSENGER RNA; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; BINDING SITE; CELL ACTIVATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPSTEIN BARR VIRUS INDUCED GENE 3; GENOME ANALYSIS; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA TRANSLATION; UPREGULATION; VIRUS GENE;

BINDING SITES; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; INTERLEUKIN-17; INTERLEUKIN-18; INTERLEUKINS; LEUKEMIA, MYELOID, ACUTE; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS (GENETICS);

ANIMALIA; HUMAN HERPESVIRUS 4; MURINAE;

EID: 41849129854     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2008.01.021     Document Type: Article

References (65)

1. Aguayo A., Kantarjian H., Manshouri T., Gidel C., Estey E., Thomas D., Koller C., Estrov Z., O'Brien S., Keating M., Freireich E., and Albitar M. Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 96 (2000) 2240-2245
2. Akamatsu S., Arai N., Hanaya T., Arai S., Tanimoto T., Fujii M., Kohno K., Micallef M.J., Ikeda M., and Kurimoto M. Antitumor activity of interleukin-18 against the murine T-cell leukemia/lymphoma EL-4 in syngeneic mice. J. Immunother. 25 Suppl 1 (2002) S28-S34 1997
3. Amadi-Obi A., Yu C.R., Liu X., Mahdi R.M., Clarke G.L., Nussenblatt R.B., Gery I., Lee Y.S., and Egwuagu C.E. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13 (2007) 711-718
4. Bachmann M., Dragoi C., Poleganov M.A., Pfeilschifter J., and Mühl H. Interleukin-18 directly activates T-bet expression and function via p38 mitogen-activated protein kinase and nuclear factor-kappaB in acute myeloid leukemia-derived predendritic KG-1 cells. Mol. Cancer Ther. 6 (2007) 723-731
5. Batten M., and Ghilardi N. The biology and therapeutic potential of interleukin 27. J. Mol. Med. 85 (2007) 661-672
6. Batten M., Li J., Yi S., Kljavin N.M., Danilenko D.M., Lucas S., Lee J., de Sauvage F.J., and Ghilardi N. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7 (2006) 929-936
7. Boraschi D., and Dinarello C.A. IL-18 in autoimmunity: review. Eur. Cytokine Netw. 17 (2006) 224-252
8. Brender C., Tannahill G.M., Jenkins B.J., Fletcher J., Columbus R., Saris C.J., Ernst M., Nicola N.A., Hilton D.J., Alexander W.S., and Starr R. Suppressor of cytokine signaling 3 regulates CD8 T-cell proliferation by inhibition of interleukins 6 and 27. Blood 110 (2007) 2528-2536
9. Cao R., Farnebo J., Kurimoto M., and Cao Y. Interleukin-18 acts as an angiogenesis and tumor suppressor. Faseb J. 13 (1999) 2195-2202
10. Carrascal M.T., Mendoza L., Valcarcel M., Salado C., Egilegor E., Telleria N., Vidal-Vanaclocha F., and Dinarello C.A. Interleukin-18 binding protein reduces b16 melanoma hepatic metastasis by neutralizing adhesiveness and growth factors of sinusoidal endothelium. Cancer Res. 63 (2003) 491-497
11. Chandrasekar B., Mummidi S., Mahimainathan L., Patel D.N., Bailey S.R., Imam S.Z., Greene W.C., and Valente A.J. Interleukin-18-induced human coronary artery smooth muscle cell migration is dependent on NF-kappaB- and AP-1-mediated matrix metalloproteinase-9 expression and is inhibited by atorvastatin. J. Biol. Chem. 281 (2006) 15099-15109
12. Charo I.F., and Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354 (2006) 610-621
13. Chen Y., Langrish C.L., McKenzie B., Joyce-Shaikh B., Stumhofer J.S., McClanahan T., Blumenschein W., Churakovsa T., Low J., Presta L., Hunter C.A., Kastelein R.A., and Cua D.J. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J. Clin. Invest. 116 (2006) 1317-1326
14. Colgan J., and Rothman P. All in the family: IL-27 suppression of T(H)-17 cells. Nat. Immunol. 7 (2006) 899-901
15. Coughlin C.M., Salhany K.E., Wysocka M., Aruga E., Kurzawa H., Chang A.E., Hunter C.A., Fox J.C., Trinchieri G., and Lee W.M. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J. Clin. Invest. 101 (1998) 1441-1452
16. Curti A., Pandolfi S., Aluigi M., Isidori A., Alessandrini I., Chiodoni C., Testoni N., Colombo M.P., Baccarani M., and Lemoli R.M. Interleukin-12 production by leukemia-derived dendritic cells counteracts the inhibitory effect of leukemic microenvironment on T cells. Exp. Hematol. 33 (2005) 1521-1530
17. Devergne O., Hummel M., Koeppen H., Le Beau M.M., Nathanson E.C., Kieff E., and Birkenbach M. A novel interleukin-12 p40-related protein induced by latent Epstein-Barr virus infection in B lymphocytes. J. Virol. 70 (1996) 1143-1153
18. Dinarello C.A. Biologic basis for interleukin-1 in disease. Blood 87 (1996) 2095-2147
19. Dinarello C.A. The paradox of pro-inflammatory cytokines in cancer. Cancer Metastasis Rev. 25 (2006) 307-313
20. Ghezzi P., and Cerami A. Tumor necrosis factor as a pharmacological target. Mol. Biotechnol. 31 (2005) 239-244
21. Gollob J.A., Mier J.W., Veenstra K., McDermott D.F., Clancy D., Clancy M., and Atkins M.B. Phase I trial of twice-weekly intravenous interleukin 12 in patients with metastatic renal cell cancer or malignant melanoma: ability to maintain IFN-gamma induction is associated with clinical response. Clin. Cancer Res. 6 (2000) 1678-1692
22. Gutzmer R., Langer K., Mommert S., Wittmann M., Kapp A., and Werfel T. Human dendritic cells express the IL-18R and are chemoattracted to IL-18. J. Immunol. 171 (2003) 6363-6371
23. Hisada M., Kamiya S., Fujita K., Belladonna M.L., Aoki T., Koyanagi Y., Mizuguchi J., and Yoshimoto T. Potent antitumor activity of interleukin-27. Cancer Res. 64 (2004) 1152-1156
24. Hofstetter H.H., Ibrahim S.M., Koczan D., Kruse N., Weishaupt A., Toyka K.V., and Gold R. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol. 237 (2005) 123-130
25. Houtenbos I., Westers T.M., Ossenkoppele G.J., and van de Loosdrecht A.A. Leukemia-derived dendritic cells: towards clinical vaccination protocols in acute myeloid leukemia. Haematologica 91 (2006) 348-355
26. Hunter C.A. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5 (2005) 521-531
27. Hussong J.W., Rodgers G.M., and Shami P.J. Evidence of increased angiogenesis in patients with acute myeloid leukemia. Blood 95 (2000) 309-313
28. Inoue K., Sugiyama H., Ogawa H., Yamagami T., Azuma T., Oka Y., Miwa H., Kita K., Hiraoka A., Masaoka T., et al. Expression of the interleukin-6 (IL-6), IL-6 receptor, and gp130 genes in acute leukemia. Blood 84 (1994) 2672-2680
29. Karin M. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation. J. Biol. Chem. 274 (1999) 27339-27342
30. Kastelein R.A., Hunter C.A., and Cua D.J. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 25 (2007) 221-242
31. Kessler T., Fehrmann F., Bieker R., Berdel W.E., and Mesters R.M. Vascular endothelial growth factor and its receptor as drug targets in hematological malignancies. Curr. Drug Targets 8 (2007) 257-268
32. Kirkwood J.M., Kefford R., Logan T., Mainwaring P.N., Millward M., Pavlick A.C., Dar M.M., Kathman S., Laubscher K., and Bell W. Phase II trial of iboctadekin (rhIL-18) on a daily X 5 schedule in metastatic melanoma (MM). J. Clin. Oncol. 24 (2006) 10043
33. Kojima H., Aizawa Y., Yanai Y., Nagaoka K., Takeuchi M., Ohta T., Ikegami H., Ikeda M., and Kurimoto M. An essential role for NF-kappa B in IL-18-induced IFN-gamma expression in KG-1 cells. J. Immunol. 162 (1999) 5063-5069
34. Laning J., Kawasaki H., Tanaka E., Luo Y., and Dorf M.E. Inhibition of in vivo tumor growth by the beta chemokine, TCA3. J. Immunol. 153 (1994) 4625-4635
35. Larousserie F., Bardel E., Pflanz S., Arnulf B., Lome-Maldonado C., Hermine O., Bregeaud L., Perennec M., Brousse N., Kastelein R., and Devergne O. Analysis of interleukin-27 (EBI3/p28) expression in Epstein-Barr virus- and human T-cell leukemia virus type 1-associated lymphomas: heterogeneous expression of EBI3 subunit by tumoral cells. Am. J. Pathol. 166 (2005) 1217-1228
36. Li J., Mbow M.L., Sun L., Li L., Yang G., Griswold D.E., Schantz A., Shealy D.J., Goletz T.J., Wan J., and Peritt D. Induction of dendritic cell maturation by IL-18. Cell Immunol. 227 (2004) 103-108
37. Maaser C., Egan L.J., Birkenbach M.P., Eckmann L., and Kagnoff M.F. Expression of Epstein-Barr virus-induced gene 3 and other interleukin-12-related molecules by human intestinal epithelium. Immunology 112 (2004) 437-445
38. Mashino K., Sadanaga N., Tanaka F., Ohta M., Yamaguchi H., and Mori M. Effective strategy of dendritic cell-based immunotherapy for advanced tumor-bearing hosts: the critical role of Th1-dominant immunity. Mol. Cancer Ther. 1 (2002) 785-794
39. Morishima N., Owaki T., Asakawa M., Kamiya S., Mizuguchi J., and Yoshimoto T. Augmentation of effector CD8+ T cell generation with enhanced granzyme B expression by IL-27. J. Immunol. 175 (2005) 1686-1693
40. Mühl H., and Pfeilschifter J. Anti-inflammatory properties of pro-inflammatory interferon-gamma. Int. Immunopharmacol. 3 (2003) 1247-1255
41. Mühl H., and Pfeilschifter J. Interleukin-18 bioactivity: a novel target for immunopharmacological anti-inflammatory intervention. Eur. J. Pharmacol. 500 (2004) 63-71
42. Niedbala W., Wei X.Q., Cai B., Hueber A.J., Leung B.P., McInnes I.B., and Liew F.Y. IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur. J. Immunol. 37 (2007) 3021-3029
43. Nold M., Goede A., Eberhardt W., Pfeilschifter J., and Mühl H. IL-18 initiates release of matrix metalloproteinase-9 from peripheral blood mononuclear cells without affecting tissue inhibitor of matrix metalloproteinases-1: suppression by TNF alpha blockage and modulation by IL-10. Naunyn Schmiedebergs Arch. Pharmacol. 367 (2003) 68-75
44. Oniki S., Nagai H., Horikawa T., Furukawa J., Belladonna M.L., Yoshimoto T., Hara I., and Nishigori C. Interleukin-23 and interleukin-27 exert quite different antitumor and vaccine effects on poorly immunogenic melanoma. Cancer Res. 66 (2006) 6395-6404
45. Owaki T., Asakawa M., Kamiya S., Takeda K., Fukai F., Mizuguchi J., and Yoshimoto T. IL-27 suppresses CD28-mediated [correction of medicated] IL-2 production through suppressor of cytokine signaling 3. J. Immunol. 176 (2006) 2773-2780
46. Padro T., Bieker R., Ruiz S., Steins M., Retzlaff S., Burger H., Buchner T., Kessler T., Herrera F., Kienast J., Muller-Tidow C., Serve H., Berdel W.E., and Mesters R.M. Overexpression of vascular endothelial growth factor (VEGF) and its cellular receptor KDR (VEGFR-2) in the bone marrow of patients with acute myeloid leukemia. Leukemia 16 (2002) 1302-1310
47. Padro T., Ruiz S., Bieker R., Burger H., Steins M., Kienast J., Buchner T., Berdel W.E., and Mesters R.M. Increased angiogenesis in the bone marrow of patients with acute myeloid leukemia. Blood 95 (2000) 2637-2644
48. Panoskaltsis N. Dendritic cells in MDS and AML-cause, effect or solution to the immune pathogenesis of disease?. Leukemia 19 (2005) 354-357
49. Pflanz S., Timans J.C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W.M., Mattson J.D., Wagner J.L., To W., Zurawski S., McClanahan T.K., Gorman D.M., Bazan J.F., de Waal Malefyt R., Rennick D., and Kastelein R.A. IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 16 (2002) 779-790
50. Puren A.J., Fantuzzi G., Gu Y., Su M.S., and Dinarello C.A. Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-CD14+ human blood mononuclear cells. J. Clin. Invest. 101 (1998) 711-721
51. Ruckes T., Saul D., Van Snick J., Hermine O., and Grassmann R. Autocrine antiapoptotic stimulation of cultured adult T-cell leukemia cells by overexpression of the chemokine I-309. Blood 98 (2001) 1150-1159
52. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17 (1989) 6419
53. Schuch G., Oliveira-Ferrer L., Loges S., Laack E., Bokemeyer C., Hossfeld D.K., Fiedler W., and Ergun S. Antiangiogenic treatment with endostatin inhibits progression of AML in vivo. Leukemia 19 (2005) 1312-1317
54. Shimizu M., Shimamura M., Owaki T., Asakawa M., Fujita K., Kudo M., Iwakura Y., Takeda Y., Luster A.D., Mizuguchi J., and Yoshimoto T. Antiangiogenic and antitumor activities of IL-27. J. Immunol. 176 (2006) 7317-7324
55. Spiekermann K., Biethahn S., Wilde S., Hiddemann W., and Alves F. Constitutive activation of STAT transcription factors in acute myelogenous leukemia. Eur. J. Haematol. 67 (2001) 63-71
56. Strengell M., Matikainen S., Siren J., Lehtonen A., Foster D., Julkunen I., and Sareneva T. IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J. Immunol. 170 (2003) 5464-5469
57. Strieter R.M., Burdick M.D., Mestas J., Gomperts B., Keane M.P., and Belperio J.A. Cancer CXC chemokine networks and tumour angiogenesis. Eur. J. Cancer 42 (2006) 768-778
58. Torre D., Speranza F., Martegani R., Pugliese A., Castelli F., Basilico C., and Biondi G. Circulating levels of IL-18 in adult and paediatric patients with HIV-1 infection. Aids 14 (2000) 2211-2212
59. Vidal-Vanaclocha F., Fantuzzi G., Mendoza L., Fuentes A.M., Anasagasti M.J., Martin J., Carrascal T., Walsh P., Reznikov L.L., Kim S.H., Novick D., Rubinstein M., and Dinarello C.A. IL-18 regulates IL-1beta-dependent hepatic melanoma metastasis via vascular cell adhesion molecule-1. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 734-739
60. Wheeler R.D., and Owens T. The changing face of cytokines in the brain: perspectives from EAE. Curr. Pharm. Des. 11 (2005) 1031-1037
61. Wirtz S., Becker C., Fantini M.C., Nieuwenhuis E.E., Tubbe I., Galle P.R., Schild H.J., Birkenbach M., Blumberg R.S., and Neurath M.F. EBV-induced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kappa B activation. J. Immunol. 174 (2005) 2814-2824
62. Wormald S., and Hilton D.J. The negative regulatory roles of suppressor of cytokine signaling proteins in myeloid signaling pathways. Curr. Opin. Hematol. 14 (2007) 9-15
63. Xu B., Dong C.Y., Zhang F., Lin Y.M., Wu K.F., and Ma X.T. Synergistic antileukemia effect of combinational gene therapy using murine beta-defensin 2 and IL-18 in L1210 murine leukemia model. Gene Ther. 14 (2007) 1181-1187
64. Yamada G., Shijubo N., Shigehara K., Okamura H., Kurimoto M., and Abe S. Increased levels of circulating interleukin-18 in patients with advanced tuberculosis. Am. J. Respir. Crit. Care Med. 161 (2000) 1786-1789
65. Zhang B., Wu K.F., Lin Y.M., Ma X.T., Rao Q., Zheng G.G., Cao Z.Y., Li G., and Song Y.H. Gene transfer of pro-IL-18 and IL-1beta converting enzyme cDNA induces potent antitumor effects in L1210 cells. Leukemia 18 (2004) 817-825