Co-inhibition of NF-κB and JNK is synergistic in TNF-expressing human AML

Journal of Experimental Medicine

Volumn 211, Issue 6, 2014, Pages 1093-1108

  Volk, Andrew ^a   Li, Jing ^b   Xin, Junping ^c   You, Dewen ^c   Zhang, Jun ^b   Liu, Xinli ^b   Xiao, Yechen ^c   Breslin, Peter ^a,c,d   Li, Zejuan ^e   Wei, Wei ^c   Schmidt, Rachel ^c   Li, Xingyu ^b   Zhang, Zhou ^f   Kuo, Paul C ^c   Nand, Sucha ^d   Zhang, Jianke ^g   Chen, Jianjun ^e   Zhang, Jiwang ^a,c  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b SHANGHAI NORMAL UNIVERSITY   (China)

^c LOYOLA UNIVERSITY HEALTH SYSTEM   (United States)

^d LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^g THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CELL DEATH; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTHRACENES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; GENE EXPRESSION REGULATION, LEUKEMIC; HL-60 CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; K562 CELLS; LEUKEMIA, MONOCYTIC, ACUTE; LEUKEMIA, MYELOID, ACUTE; LEUKEMIA, MYELOMONOCYTIC, ACUTE; LEUKEMIA, PROMYELOCYTIC, ACUTE; MICE; MICE, KNOCKOUT; NF-KAPPA B; NITRILES; RECEPTORS, TUMOR NECROSIS FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SULFONES; TRANSCRIPTION FACTOR AP-1; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS;

EID: 84901808678     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130990     Document Type: Article

References (61)

1. Anderson, G.M., M.T. Nakada, and M. DeWitte. 2004. Tumor necrosis factor-α in the pathogenesis and treatment of cancer. Curr. Opin. Pharmacol. 4:314-320. http://dx.doi.org/10.1016/j.coph.2004.04.004.
2. Balkwill, F. 2006. TNF-α in promotion and progression of cancer. Cancer Metastasis Rev. 25:409-416. http://dx.doi.org/10.1007/s10555-006-9005-3.
3. Balkwill, F. 2009. Tumour necrosis factor and cancer. Nat. Rev. Cancer. 9:361-371. http://dx.doi.org/10.1038/nrc2628.
4. Bettermann, K., M. Vucur, J. Haybaeck, C. Koppe, J. Janssen, F. Heymann, A. Weber, R. Weiskirchen, C. Liedtke, N. Gassler, et al. 2010. TAK1 suppresses a NEMO-dependent but NF-κB-independent pathway to liver cancer. Cancer Cell. 17:481-496. http://dx.doi.org/10.1016/j.ccr.2010.03.021.
5. Bode, A.M., and Z. Dong. 2007. The functional contrariety of JNK. Mol. Carcinog. 46:591-598. http://dx.doi.org/10.1002/mc.20348.
6. Chen, F. 2012. JNK-induced apoptosis, compensatory growth, and cancer stem cells. Cancer Res. 72:379-386. http://dx.doi.org/10.1158/0008-5472.CAN-11-1982.
7. Chen, N., M. Nomura, Q.B. She, W.Y. Ma, A.M. Bode, L. Wang, R.A. Flavell, and Z. Dong. 2001. Suppression of skin tumorigenesis in c-Jun NH(2)-terminal kinase-2-deficient mice. Cancer Res. 61:3908-3912.
8. Cordero, J.B., J.P. Macagno, R.K. Stefanatos, K.E. Strathdee, R.L. Cagan, and M. Vidal. 2010. Oncogenic Ras diverts a host TNF tumor suppressor activity into tumor promoter. Dev. Cell. 18:999-1011. http://dx.doi.org/ 10.1016/j.devcel.2010.05.014.
9. DiDonato, J.A., F. Mercurio, and M. Karin. 2012. NF-κB and the link between inflammation and cancer. Immunol. Rev. 246:379-400. http://dx.doi.org/10.1111/j.1600-065X.2012.01099.x.
10. Dufour, C., A. Corcione, J. Svahn, R. Haupt, V. Poggi, A.N. Béka'ssy, R. Scimè, A. Pistorio, and V. Pistoia. 2003. TNF-α and IFN-γ are overexpressed in the bone marrow of Fanconi anemia patients and TNF-α suppresses erythropoiesis in vitro. Blood. 102:2053-2059. http://dx.doi.org/10.1182/blood-2003-01-0114.
11. Dybedal, I., D. Bryder, A. Fossum, L.S. Rusten, and S.E. Jacobsen. 2001. Tumor necrosis factor (TNF)-mediated activation of the p55 TNF receptor negatively regulates maintenance of cycling reconstituting human hematopoietic stem cells. Blood. 98:1782-1791. http://dx.doi.org/10.1182/blood.V98.6.1782.
12. Egberts, J.H., V. Cloosters, A. Noack, B. Schniewind, L. Thon, S. Klose, B. Kettler, C. von Forstner, C. Kneitz, J. Tepel, et al. 2008. Anti-tumor necrosis factor therapy inhibits pancreatic tumor growth and metastasis. Cancer Res. 68:1443-1450. http://dx.doi.org/10.1158/0008-5472.CAN-07-5704.
13. Feoktistova, M., P. Geserick, B. Kellert, D.P. Dimitrova, C. Langlais, M. Hupe, K. Cain, M. MacFarlane, G. Häcker, and M. Leverkus. 2011. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell. 43: 449-463. http://dx.doi.org/10.1016/j.molcel.2011.06.011.
14. V617F positive cells in myeloproliferative neoplasms. Blood. 118:6392-6398. http://dx.doi.org/10.1182/blood-2011-04-348144.
15. Gallipoli, P., F. Pellicano, H. Morrison, K. Laidlaw, E.K. Allan, R. Bhatia, M. Copland, H.G. Jørgensen, and T.L. Holyoake. 2013. Autocrine TNF-α production supports CML stem and progenitor cell survival and enhances their proliferation. Blood. 122:3335-3339. http://dx.doi.org/10.1182/ blood-2013-02-485607.
16. Grivennikov, S.I., and M. Karin. 2011. Inflammatory cytokines in cancer: tumour necrosis factor and interleukin 6 take the stage. Ann. Rheum. Dis. 70:i104-i108. http://dx.doi.org/10.1136/ard.2010.140145.
17. Günther, C., E. Martini, N. Wittkopf, K. Amann, B. Weigmann, H. Neumann, M.J. Waldner, S.M. Hedrick, S. Tenzer, M.F. Neurath, and C. Becker. 2011. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature. 477:335-339. http://dx.doi.org/10.1038/nature10400.
18. Guzman, M.L., S.J. Neering, D. Upchurch, B. Grimes, D.S. Howard, D.A. Rizzieri, S.M. Luger, and C.T. Jordan. 2001. Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood. 98:2301-2307. http://dx.doi.org/10.1182/blood.V98.8.2301.
19. He, S., L. Wang, L. Miao, T. Wang, F. Du, L. Zhao, and X. Wang. 2009. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell. 137:1100-1111. http://dx.doi.org/10.1016/j.cell.2009.05.021.
20. Hernandez-Ilizaliturri, F.J., G. Deeb, P.L. Zinzani, S.A. Pileri, F. Malik, W.R. Macon, A. Goy, T.E. Witzig, and M.S. Czuczman. 2011. Higher response to lenalidomide in relapsed/refractory diffuse large B-cell lymphoma in nongerminal center B-cell-like than in germinal center B-cell-like phenotype. Cancer. 117:5058-5066. http://dx.doi.org/10.1002/cncr.26135.
21. Hess, P., G. Pihan, C.L. Sawyers, R.A. Flavell, and R.J. Davis. 2002. Survival signaling mediated by c-Jun NH(2)-terminal kinase in transformed B lymphoblasts. Nat. Genet. 32:201-205. http://dx.doi.org/10.1038/ng946.
22. Kaiser, W.J., J.W. Upton, A.B. Long, D. Livingston-Rosanoff, L.P. Daley-Bauer, R. Hakem, T. Caspary, and E.S. Mocarski. 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature. 471:368-372. http://dx.doi.org/10.1038/nature09857.
23. Kamata, H., S. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin. 2005. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell. 120:649-661. http://dx.doi.org/10.1016/j.cell.2004.12.041.
24. Ke, H., R. Harris, J.L. Coloff, J.Y. Jin, B. Leshin, P. Miliani de Marval, S. Tao, J.C. Rathmell, R.P. Hall, and J.Y. Zhang. 2010. The c-Jun NH2-terminal kinase 2 plays a dominant role in human epidermal neoplasia. Cancer Res. 70:3080-3088. http://dx.doi.org/10.1158/0008-5472.CAN-09-2923.
25. Kim, Y.S., M.J. Morgan, S. Choksi, and Z.G. Liu. 2007. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol. Cell. 26:675-687. http://dx.doi.org/ 10.1016/j.molcel.2007.04.021.
26. Knight, B., G.C. Yeoh, K.L. Husk, T. Ly, L.J. Abraham, C. Yu, J.A. Rhim, and N. Fausto. 2000. Impaired preneoplastic changes and liver tumor formation in tumor necrosis factor receptor type 1 knockout mice. J. Exp. Med. 192:1809-1818. http://dx.doi.org/10.1084/jem.192.12.1809.
27. Kuo, H.P., Z. Wang, D.F. Lee, M. Iwasaki, J. Duque-Afonso, S.H. Wong, C.H. Lin, M.E. Figueroa, J. Su, I.R. Lemischka, and M.L. Cleary. 2013. Epigenetic roles of MLL oncoproteins are dependent on NF-κB. Cancer Cell. 24:423-437. http://dx.doi.org/10.1016/j.ccr.2013.08.019.
28. Li, J., D.P. Sejas, X. Zhang, Y. Qiu, K.J. Nattamai, R. Rani, K.R. Rathbun, H. Geiger, D.A. Williams, G.C. Bagby, and Q. Pang. 2007. TNF-α induces leukemic clonal evolution ex vivo in Fanconi anemia group C murine stem cells. J. Clin. Invest. 117:3283-3295. http://dx.doi.org/10.1172/JCI31772.
29. Lim, K.H., Y. Yang, and L.M. Staudt. 2012. Pathogenetic importance and therapeutic implications of NF-κB in lymphoid malignancies. Immunol. Rev. 246:359-378. http://dx.doi.org/10.1111/j.1600-065X.2012.01105.x.
30. Liu, J., and A. Lin. 2005. Role of JNK activation in apoptosis: a double-edged sword. Cell Res. 15:36-42. http://dx.doi.org/10.1038/sj.cr.7290262.
31. Luedde, T., N. Beraza, V. Kotsikoris, G. van Loo, A. Nenci, R. De Vos, T. Roskams, C. Trautwein, and M. Pasparakis. 2007. Deletion of NEMO/ IKKγ in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell. 11:119-132. http://dx.doi.org/10.1016/j.ccr.2006.12.016.
32. Lv, L., P. Kerzic, G. Lin, A.R. Schnatter, L. Bao, Y. Yang, H. Zou, H. Fu, X. Ye, S.A. Gross, et al. 2007. The TNF-α 238A polymorphism is associated with susceptibility to persistent bone marrow dysplasia following chronic exposure to benzene. Leuk. Res. 31:1479-1485. http://dx.doi.org/10.1016/j.leukres.2007.01.014.
33. Maeda, S., H. Kamata, J.L. Luo, H. Leffert, and M. Karin. 2005. IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell. 121:977-990. http://dx.doi.org/10.1016/j.cell.2005.04.014.
34. Mantovani, A., P. Allavena, A. Sica, and F. Balkwill. 2008. Cancer-related inflammation. Nature. 454:436-444. http://dx.doi.org/10.1038/nature07205.
35. Molnár, L., T. Berki, A. Hussain, P. Németh, and H. Losonczy. 2000. Detection of TNFα expression in the bone marrow and determination of TNFα production of peripheral blood mononuclear cells in myelodysplastic syndrome. Pathol. Oncol. Res. 6:18-23. http://dx.doi.org/10.1007/ BF03032653.
36. Moore, R.J., D.M. Owens, G. Stamp, C. Arnott, F. Burke, N. East, H. Holdsworth, L. Turner, B. Rollins, M. Pasparakis, et al. 1999. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med. 5:828-831. http://dx.doi.org/10.1038/10552.
37. Naugler, W.E., and M. Karin. 2008. NF-κB and cancer-identifying targets and mechanisms. Curr. Opin. Genet. Dev. 18:19-26. http://dx.doi.org/10.1016/j.gde.2008.01.020.
38. Oberst, A., C.P. Dillon, R. Weinlich, L.L. McCormick, P. Fitzgerald, C. Pop, R. Hakem, G.S. Salvesen, and D.R. Green. 2011. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature. 471:363-367. http://dx.doi.org/10.1038/nature09852.
39. Oguma, K., H. Oshima, and M. Oshima. 2010. Inflammation, tumor necrosis factor and Wnt promotion in gastric cancer development. Future Oncol. 6:515-526. http://dx.doi.org/10.2217/fon.10.13.
40. Papa, S., F. Zazzeroni, C. Bubici, S. Jayawardena, K. Alvarez, S. Matsuda, D.U. Nguyen, C.G. Pham, A.H. Nelsbach, T. Melis, et al. 2004. Gadd45 β mediates the NF-κB suppression of JNK signalling by targeting MKK7/ JNKK2. Nat. Cell Biol. 6:146-153. http://dx.doi.org/10.1038/ncb1093.
41. Perkins, N.D. 2012. The diverse and complex roles of NF-κB subunits in cancer. Nat. Rev. Cancer. 12:121-132.
42. Popivanova, B.K., K. Kitamura, Y. Wu, T. Kondo, T. Kagaya, S. Kaneko, M. Oshima, C. Fujii, and N. Mukaida. 2008. Blocking TNF-α in mice reduces colorectal carcinogenesis associated with chronic colitis. J. Clin. Invest. 118:560-570.
43. Ren, G., X. Zhao, Y. Wang, X. Zhang, X. Chen, C. Xu, Z.R. Yuan, A.I. Roberts, L. Zhang, B. Zheng, et al. 2012. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFα. Cell Stem Cell. 11:812-824. http://dx.doi.org/10.1016/j.stem.2012.08.013.
44. Sakon, S., X. Xue, M. Takekawa, T. Sasazuki, T. Okazaki, Y. Kojima, J.H. Piao, H. Yagita, K. Okumura, T. Doi, and H. Nakano. 2003. NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J. 22:3898-3909. http://dx.doi.org/10.1093/emboj/cdg379.
45. Sakurai, H., S. Suzuki, N. Kawasaki, H. Nakano, T. Okazaki, A. Chino, T. Doi, and I. Saiki. 2003. Tumor necrosis factor-α-induced IKK phosphorylation of NF-κB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J. Biol. Chem. 278:36916-36923. http://dx.doi.org/10.1074/jbc.M301598200.
46. Sakurai, T., S. Maeda, L. Chang, and M. Karin. 2006. Loss of hepatic NF-κB activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc. Natl. Acad. Sci. USA. 103:10544-10551. http://dx.doi.org/10.1073/pnas.0603499103.
47. Sethi, G., B. Sung, and B.B. Aggarwal. 2008. TNF: a master switch for inflammation to cancer. Front. Biosci. 13:5094-5107. http://dx.doi.org/10.2741/3066.
48. Shaulian, E. 2010. AP-1-The Jun proteins: Oncogenes or tumor suppressors in disguise? Cell. Signal. 22:894-899. http://dx.doi.org/10.1016/j.cellsig.2009.12.008.
49. Skaug, B., X. Jiang, and Z.J. Chen. 2009. The role of ubiquitin in NF-κB regulatory pathways. Annu. Rev. Biochem. 78:769-796. http://dx.doi.org/ 10.1146/annurev.biochem.78.070907.102750.
50. Stifter, G., S. Heiss, G. Gastl, A. Tzankov, and R. Stauder. 2005. Over-expression of tumor necrosis factor-alpha in bone marrow biopsies from patients with myelodysplastic syndromes: relationship to anemia and prognosis. Eur. J. Haematol. 75:485-491. http://dx.doi.org/10.1111/j.1600-0609.2005.00551.x.
51. Sykes, S.M., S.W. Lane, L. Bullinger, D. Kalaitzidis, R. Yusuf, B. Saez, F. Ferraro, F. Mercier, H. Singh, K.M. Brumme, et al. 2011. AKT/FOXO signaling enforces reversible differentiation blockade in myeloid leukemias. Cell. 146:697-708. http://dx.doi.org/10.1016/j.cell.2011.07.032.
52. Tenev, T., K. Bianchi, M. Darding, M. Broemer, C. Langlais, F. Wallberg, A. Zachariou, J. Lopez, M. MacFarlane, K. Cain, and P. Meier. 2011. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell. 43:432-448. http://dx.doi.org/ 10.1016/j.molcel.2011.06.006.
53. Tsimberidou, A.M., and F.J. Giles. 2002. TNF-α targeted therapeutic approaches in patients with hematologic malignancies. Expert Rev. Anticancer Ther. 2:277-286. http://dx.doi.org/10.1586/14737140.2.3.277.
54. Tsimberidou, A.M., E. Estey, S. Wen, S. Pierce, H. Kantarjian, M. Albitar, and R. Kurzrock. 2008. The prognostic significance of cytokine levels in newly diagnosed acute myeloid leukemia and high-risk myelodysplastic syndromes. Cancer. 113:1605-1613. http://dx.doi.org/10.1002/ cncr.23785.
55. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NF-κB transcription factors in the immune system. Annu. Rev. Immunol. 27:693-733. http://dx.doi.org/10.1146/annurev.immunol.021908.132641.
56. Wang, L., F. Du, and X. Wang. 2008. TNF-α induces two distinct caspase-8 activation pathways. Cell. 133:693-703. http://dx.doi.org/10.1016/j.cell.2008.03.036.
57. Xiao, Y., H. Li, J. Zhang, A. Volk, S. Zhang, W. Wei, S. Zhang, P. Breslin, and J. Zhang. 2011. TNF-α/Fas-RIP-1-induced cell death signaling separates murine hematopoietic stem cells/progenitors into 2 distinct populations. Blood. 118:6057-6067. http://dx.doi.org/10.1182/blood-2011-06-359448.
58. Zhang, J.Y., C.L. Green, S. Tao, and P.A. Khavari. 2004. NF-κB RelA opposes epidermal proliferation driven by TNFR1 and JNK. Genes Dev. 18:17-22. http://dx.doi.org/10.1101/gad.1160904.
59. Zhang, J.Y., A.E. Adams, T.W. Ridky, S. Tao, and P.A. Khavari. 2007. Tumor necrosis factor receptor 1/c-Jun-NH2-kinase signaling promotes human neoplasia. Cancer Res. 67:3827-3834. http://dx.doi.org/10.1158/0008-5472.CAN-06-4017.
60. Zhang, D.W., J. Shao, J. Lin, N. Zhang, B.J. Lu, S.C. Lin, M.Q. Dong, and J. Han. 2009. RIP3, an energy metabolism regulator that switches TNFinduced cell death from apoptosis to necrosis. Science. 325:332-336. http://dx.doi.org/10.1126/science.1172308.
61. Zhang, H., X. Zhou, T. McQuade, J. Li, F.K. Chan, and J. Zhang. 2011. Functional complementation between FADD and RIP1 in embryos and lymphocytes. Nature. 471:373-376. http://dx.doi.org/10.1038/nature09878.