NF-κB directly regulates fas transcription to modulate Fas-mediated apoptosis and tumor suppression

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25530-25540

  Liu, Feiyan ^a,b   Bardhan, Kankana ^a   Yang, Dafeng ^a   Thangaraju, Muthusamy ^a   Ganapathy, Vadivel ^a   Waller, Jennifer L ^a   Liles, Georgia B ^a,c   Lee, Jeffrey R ^a,c   Liu, Kebin ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-TUMORS; APOPTOSIS PATHWAYS; APOPTOTIC; CANCER DEVELOPMENT; CASPASES; CELLULAR RESPONSE; COLON CARCINOMA; COLORECTAL CANCER; DEATH-RECEPTOR; EXPERIMENTAL DATA; FAS PROTEIN; HUMAN CARCINOMA CELLS; INDUCED APOPTOSIS; MOUSE EMBRYO FIBROBLASTS; TRANSCRIPTION ACTIVATORS; TUMOR CELLS; TUMOR SUPPRESSION;

CELL CULTURE; CHEMICAL ACTIVATION; DISEASES; DRUG PRODUCTS; MAMMALS; TRANSCRIPTION; TUMORS; WELL STIMULATION;

CELL DEATH;

3 METHYLCHOLANTHRENE; AZOXYMETHANE; CASPASE 8; DEXTRAN SULFATE; FAS ANTIGEN; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER RECURRENCE; CARCINOMA CELL; CELL PROTECTION; COLON CARCINOMA; COLORECTAL CANCER; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; ENZYME ACTIVATION; FAS GENE; FASL GENE; FIBROBLAST; GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SARCOMA; TRANSCRIPTION REGULATION;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CASPASE 8; COLONIC NEOPLASMS; EMBRYO, MAMMALIAN; FAS LIGAND PROTEIN; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; METHYLCHOLANTHRENE; MICE; MICE, KNOCKOUT; NEOPLASMS, EXPERIMENTAL; NF-KAPPA B P52 SUBUNIT; PROMOTER REGIONS, GENETIC; SARCOMA; TRANSCRIPTION FACTOR RELA; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84864087098     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.356279     Document Type: Article

References (61)

1. Lavrik, I. N., and Krammer, P. H. (2012) Regulation of CD95/Fas signaling at the DISC. Cell Death Differ. 19, 36-41
2. Kaufmann, T., Strasser, A., and Jost, P. J. (2012) Fas death receptor signaling. Roles of Bid and XIAP. Cell Death Differ. 19, 42-50
3. Kober, A. M., Legewie, S., Pforr, C., Fricker, N., Eils, R., Krammer, P. H., and Lavrik, I. N. (2011) Caspase-8 activity has an essential role in CD95/ Fas-mediated MAPK activation. Cell Death Dis. 2, e212
4. Straus, S. E., Jaffe, E. S., Puck, J. M., Dale, J. K., Elkon, K. B., Rösen-Wolff, A., Peters, A. M., Sneller, M. C., Hallahan, C. W., Wang, J., Fischer, R. E., Jackson, C. M., Lin, A. Y., Bäumler, C., Siegert, E., Marx, A., Vaishnaw, A. K., Grodzicky, T., Fleisher, T. A., and Lenardo, M. J. (2001) The development of lymphomas in families with autoimmune lymphoproliferative syndrome with germ line Fas mutations and defective lymphocyte apoptosis. Blood 98, 194-200
5. Nikolov, N. P., Shimizu, M., Cleland, S., Bailey, D., Aoki, J., Strom, T., Schwartzberg, P. L., Candotti, F., and Siegel, R. M. (2010) Systemic autoimmunity and defective Fas ligand secretion in the absence of the Wiskott- Aldrich syndrome protein. Blood 116, 740-747
6. Lenardo, M. J., Oliveira, J. B., Zheng, L., and Rao, V. K. (2010) ALPS. Ten lessons from an international workshop on a genetic disease of apoptosis. Immunity 32, 291-295
7. Neven, B., Magerus-Chatinet, A., Florkin, B., Gobert, D., Lambotte, O., De Somer, L., Lanzarotti, N., Stolzenberg, M. C., Bader-Meunier, B., Aladjidi, N., Chantrain, C., Bertrand, Y., Jeziorski, E., Leverger, G., Michel, G., Suarez, F., Oksenhendler, E., Hermine, O., Blanche, S., Picard, C., Fischer, A., and Rieux-Laucat, F. (2011) A survey of 90 patients with autoimmune lymphoproliferative syndrome related to TNFRSF6 mutation. Blood 118, 4798-4807
8. Dowdell, K. C., Niemela, J. E., Price, S., Davis, J., Hornung, R. L., Oliveira, J. B., Puck, J. M., Jaffe, E. S., Pittaluga, S., Cohen, J. I., Fleisher, T. A., and Rao, V. K. (2010) Somatic FAS mutations are common in patients with genetically undefined autoimmune lymphoproliferative syndrome. Blood 115, 5164-5169
9. Park, W. S., Oh, R. R., Kim, Y. S., Park, J. Y., Lee, S. H., Shin, M. S., Kim, S. Y., Kim, P. J., Lee, H. K., Yoo, N. Y., and Lee, J. Y. (2001) Somatic mutations in the death domain of the Fas (Apo-1/CD95) gene in gastric cancer. J. Pathol. 193, 162-168 (Pubitemid 32118126)
10. Lei, D., Sturgis, E. M., Wang, L. E., Liu, Z., Zafereo, M. E., Wei, Q., and Li, G. (2010) FAS and FASLG genetic variants and risk for second primary malignancy in patients with squamous cell carcinoma of the head and neck. Cancer Epidemiol. Biomarkers Prev. 19, 1484-1491
11. Yang, M., Sun, T., Wang, L., Yu, D., Zhang, X., Miao, X., Liu, J., Zhao, D., Li, H., Tan, W., and Lin, D. (2008) Functional variants in cell death pathway genes and risk of pancreatic cancer. Clin. Cancer Res. 14, 3230-3236
12. Qiu, L. X., Shi, J., Yuan, H., Jiang, X., Xue, K., Pan, H. F., Li, J., and Zheng, M. H. (2009) FAS -1,377 G/A polymorphism is associated with cancer susceptibility. Evidence from 10,564 cases and 12,075 controls. Hum. Genet. 125, 431-435
13. Sunter, N. J., Scott, K., Hills, R., Grimwade, D., Taylor, S., Worrillow, L. J., Fordham, S. E., Forster, V. J., Jackson, G., Bomken, S., Jones, G., and Allan, J. M. (2012) A functional variant in the core promoter of the CD95 cell death receptor gene predicts prognosis in acute promyelocytic leukemia. Blood 119, 196-205
14. Sibley, K., Rollinson, S., Allan, J. M., Smith, A. G., Law, G. R., Roddam, P. L., Skibola, C. F., Smith, M. T., and Morgan, G. J. (2003) Functional FAS promoter polymorphisms are associated with increased risk of acute myeloid leukemia. Cancer Res. 63, 4327-4330 (Pubitemid 36950998)
15. Sung, W. W., Wang, Y. C., Cheng, Y. W., Lee, M. C., Yeh, K. T., Wang, L., Wang, J., Chen, C. Y., and Lee, H. (2011) A polymorphic-844T/C in FasL promoter predicts survival and relapse in non-small cell lung cancer. Clin. Cancer Res. 17, 5991-5999
16. Barnhart, B. C., Legembre, P., Pietras, E., Bubici, C., Franzoso, G., and Peter, M. E. (2004) CD95 ligand induces motility and invasiveness of apoptosis- resistant tumor cells. EMBO J. 23, 3175-3185 (Pubitemid 39093611)
17. Peter, M. E., Budd, R. C., Desbarats, J., Hedrick, S. M., Hueber, A. O., Newell, M. K., Owen, L. B., Pope, R. M., Tschopp, J., Wajant, H., Wallach, D., Wiltrout, R. H., Zörnig, M., and Lynch, D. H. (2007) The CD95 receptor. Apoptosis revisited. Cell 129, 447-450
18. Kleber, S., Sancho-Martinez, I., Wiestler, B., Beisel, A., Gieffers, C., Hill, O., Thiemann, M., Mueller, W., Sykora, J., Kuhn, A., Schreglmann, N., Letellier, E., Zuliani, C., Klussmann, S., Teodorczyk, M., Gröne, H. J., Ganten, T. M., Sültmann, H., Tüttenberg, J., von Deimling, A., Regnier- Vigouroux, A., Herold-Mende, C., and Martin-Villalba, A. (2008) Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 13, 235-248 (Pubitemid 351324880)
19. Chen, L., Park, S. M., Tumanov, A. V., Hau, A., Sawada, K., Feig, C., Turner, J. R., Fu, Y. X., Romero, I. L., Lengyel, E., and Peter, M. E. (2010) CD95 promotes tumor growth. Nature 465, 492-496
20. Karin, M. (2006) Nuclear factor-κB in cancer development and progression. Nature 441, 431-436
21. Karl, S., Pritschow, Y., Volcic, M., Häcker, S., Baumann, B., Wiesmüller, L., Debatin, K. M., and Fulda, S. (2009) Identification of a novel proapopotic function of NF-κB in the DNA damage response. J. Cell Mol. Med. 13, 4239-4256
22. Chen, F., and Castranova, V. (2007) Nuclear factor-κB, an unappreciated tumor suppressor. Cancer Res. 67, 11093-11098 (Pubitemid 350248529)
23. Vince, J. E., Wong, W. W., Khan, N., Feltham, R., Chau, D., Ahmed, A. U., Benetatos, C. A., Chunduru, S. K., Condon, S. M., McKinlay, M., Brink, R., Leverkus, M., Tergaonkar, V., Schneider, P., Callus, B. A., Koentgen, F., Vaux, D. L., and Silke, J. (2007) IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693 (Pubitemid 350103599)
24. Varfolomeev, E., Blankenship, J. W., Wayson, S. M., Fedorova, A. V., Kayagaki, N., Garg, P., Zobel, K., Dynek, J. N., Elliott, L. O., Wallweber, H. J., Flygare, J. A., Fairbrother, W. J., Deshayes, K., Dixit, V. M., and Vucic, D. (2007) IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell 131, 669-681 (Pubitemid 350087204)
25. Petersen, S. L., Wang, L., Yalcin-Chin, A., Li, L., Peyton, M., Minna, J., Harran, P., and Wang, X. (2007) Autocrine TNFα signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis. Cancer Cell 12, 445-456 (Pubitemid 350064365)
26. Chien, Y., Scuoppo, C., Wang, X., Fang, X., Balgley, B., Bolden, J. E., Premsrirut, P., Luo, W., Chicas, A., Lee, C. S., Kogan, S. C., and Lowe, S. W. (2011) Control of the senescence-associated secretory phenotype by NF- {kappa}B promotes senescence and enhances chemosensitivity. Genes Dev. 25, 2125-2136
27. Jing, H., Kase, J., Dörr, J. R., Milanovic, M., Lenze, D., Grau, M., Beuster, G., Ji, S., Reimann, M., Lenz, P., Hummel, M., Dörken, B., Lenz, G., Scheidereit, C., Schmitt, C. A., and Lee, S. (2011) Opposing roles of NF-κB in anti-cancer treatment outcome unveiled by cross-species investigations. Genes Dev. 25, 2137-2146
28. Jennewein, C., Karl, S., Baumann, B., Micheau, O., Debatin, K. M., and Fulda, S. (2012) Identification of a novel proapoptotic role of NF-κB in the regulation of TRAIL- and CD95-mediated apoptosis of glioblastoma cells. Oncogene 31, 1468-1474
29. Crescenzi, E., Pacifico, F., Lavorgna, A., De Palma, R., D'Aiuto, E., Palumbo, G., Formisano, S., and Leonardi, A. (2011) NF-κB-dependent cytokine secretion controls Fas expression on chemotherapy-induced premature senescent tumor cells. Oncogene 30, 2707-2717
30. Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., and Schreiber, R. D. (2001) IFNλ and lymphocytes prevent primary tumour development and shape tumor immunogenicity. Nature 410, 1107-1111 (Pubitemid 32391043)
31. Greten, F. R., Eckmann, L., Greten, T. F., Park, J. M., Li, Z. W., Egan, L. J., Kagnoff, M. F., and Karin, M. (2004) IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285-296 (Pubitemid 39061110)
32. Ryan, K. M., Ernst, M. K., Rice, N. R., and Vousden, K. H. (2000) Role of NF-κB in p53-mediated programmed cell death. Nature 404, 892-897 (Pubitemid 30230343)
33. Kew, R. R., Penzo, M., Habiel, D. M., and Marcu, K. B. (2012) The IKKα- dependent NF-κB p52/RelB noncanonical pathway is essential to sustain a CXCL12 autocrine loop in cells migrating in response to HMGB1. J. Immunol. 188, 2380-2386
34. O'Mahony, A., Lin, X., Geleziunas, R., and Greene, W. C. (2000) Activation of the heterodimeric IκB kinase α (IKKα)-IKKβ complex is directional. IKKα regulates IKKκ under both basal and stimulated conditions. Mol. Cell. Biol. 20, 1170-1178 (Pubitemid 30069237)
35. Liu, F., Hu, X., Zimmerman, M., Waller, J. L., Wu, P., Hayes-Jordan, A., Lev, D., and Liu, K. (2011) TNFα Cooperates with IFN-γ to Repress Bcl-xL Expression to Sensitize Metastatic Colon Carcinoma Cells to TRAIL-mediated apoptosis. PLoS One 6, e16241
36. Zimmerman, M., Yang, D., Hu, X., Liu, F., Singh, N., Browning, D., Ganapathy, V., Chandler, P., Choubey, D., Abrams, S. I., and Liu, K. (2010) IFN-γ up-regulates survivin and Ifi202 expression to induce survival and proliferation of tumor-specific T cells. PLoS One 5, e14076
37. Hu, X., Yang, D., Zimmerman, M., Liu, F., Yang, J., Kannan, S., Burchert, A., Szulc, Z., Bielawska, A., Ozato, K., Bhalla, K., and Liu, K. (2011) IRF8 regulates acid ceramidase expression to mediate apoptosis and suppresses myelogeneous leukemia. Cancer Res. 71, 2882-2891
38. Yang, D., Wang, S., Brooks, C., Dong, Z., Schoenlein, P. V., Kumar, V., Ouyang, X., Xiong, H., Lahat, G., Hayes-Jordan, A., Lazar, A., Pollock, R., Lev, D., and Liu, K. (2009) IFN regulatory factor 8 sensitizes soft tissue sarcoma cells to death receptor-initiated apoptosis via repression of FLICE-like protein expression. Cancer Res. 69, 1080-1088
39. Wingender, G., Krebs, P., Beutler, B., and Kronenberg, M. (2010) Antigenspecific cytotoxicity by invariant NKT cells in vivo is CD95/CD178-dependent and is correlated with antigenic potency. J. Immunol. 185, 2721-2729
40. + T-cell cytotoxicity. Cancer Res. 69, 6615-6623
41. Krammer, P. H. (1999) CD95(APO-1/Fas)-mediated apoptosis. Live and let die. Adv. Immunol. 71, 163-210
42. O'Reilly, L. A., Tai, L., Lee, L., Kruse, E. A., Grabow, S., Fairlie, W. D., Haynes, N. M., Tarlinton, D. M., Zhang, J. G., Belz, G. T., Smyth, M. J., Bouillet, P., Robb, L., and Strasser, A. (2009) Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 461, 659-663
43. Camus, M., Tosolini, M., Mlecnik, B., Pagès, F., Kirilovsky, A., Berger, A., Costes, A., Bindea, G., Charoentong, P., Bruneval, P., Trajanoski, Z., Fridman, W. H., and Galon, J. (2009) Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res. 69, 2685-2693
44. Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce- Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., Zinzindohoué, F., Bruneval, P., Cugnenc, P. H., Trajanoski, Z., Fridman, W. H., and Pagès, F. (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960-1964 (Pubitemid 44498003)
45. Krammer, P. H., Galle, P. R., Möller, P., and Debatin, K. M. (1998) CD95(APO-1/Fas)-mediated apoptosis in normal and malignant liver, colon, and hematopoietic cells. Adv. Cancer Res. 75, 251-273 (Pubitemid 28429038)
46. Ahn, E. Y., Pan, G., Vickers, S. M., and McDonald, J. M. (2002) IFN-gammaupregulates apoptosis-related molecules and enhances Fas-mediated apoptosis in human cholangiocarcinoma. Int. J. Cancer 100, 445-451
47. Zheng, Y., Ouaaz, F., Bruzzo, P., Singh, V., Gerondakis, S., and Beg, A. A. (2001) NF-κB RelA (p65) is essential for TNF-α-induced Fas expression but dispensable for both TCR-induced expression and activation-induced cell death. J. Immunol. 166, 4949-4957 (Pubitemid 32280705)
48. Staudt, L. M. (2010) Oncogenic activation of NF-κB. Cold Spring Harb. Perspect. Biol. 2, a000109
49. Ben-Neriah, Y., and Karin, M. (2011) Inflammation meets cancer, with NF-κB as the matchmaker. Nat. Immunol. 12, 715-723
50. Deng, Y., Ren, X., Yang, L., Lin, Y., and Wu, X. (2003) A JNK-dependent pathway is required for TNFα-induced apoptosis. Cell 115, 61-70 (Pubitemid 37255318)
51. Caldwell, S. A., Ryan, M. H., McDuffie, E., and Abrams, S. I. (2003) The Fas/Fas ligand pathway is important for optimal tumor regression in a mouse model of CTL adoptive immunotherapy of experimental CMS4 lung metastases. J. Immunol. 171, 2402-2412 (Pubitemid 37025547)
52. Sträter, J., Hinz, U., Hasel, C., Bhanot, U., Mechtersheimer, G., Lehnert, T., and Möller, P. (2005) Impaired CD95 expression predisposes for recurrence in curatively resected colon carcinoma. Clinical evidence for immunoselection and CD95L-mediated control of minimal residual disease. Gut 54, 661-665
53. Schillaci, R., Salatino, M., Cassataro, J., Proietti, C. J., Giambartolomei, G. H., Rivas, M. A., Carnevale, R. P., Charreau, E. H., and Elizalde, P. V. (2006) Immunization with murine breast cancer cells treated with antisense oligodeoxynucleotides to type I insulin-like growth factor receptor induced an antitumoral effect mediated by a CD8+ response involving Fas/Fas ligand cytotoxic pathway. J. Immunol. 176, 3426-3437 (Pubitemid 43363990)
54. Ikner, A., and Ashkenazi, A. (2011) TWEAK induces apoptosis through a death-signaling complex comprising receptor-interacting protein 1 (RIP1), Fas-associated death domain (FADD), and caspase-8. J. Biol. Chem. 286, 21546-21554
55. Owen-Schaub, L. B., van Golen, K. L., Hill, L. L., and Price, J. E. (1998) Fas and Fas ligand interactions suppress melanoma lung metastasis. J. Exp. Med. 188, 1717-1723 (Pubitemid 28516116)
56. Guillen-Ahlers, H., Suckow, M. A., Castellino, F. J., and Ploplis, V. A. (2010) Fas/CD95 deficiency in ApcMin/+ mice increases intestinal tumor burden. PLoS One 5, e9070
57. Ruiz-Ruiz, C., Robledo, G., Cano, E., Redondo, J. M., and Lopez-Rivas, A. (2003) Characterization of p53-mediated up-regulation of CD95 gene expression upon genotoxic treatment in human breast tumor cells. J. Biol. Chem. 278, 31667-31675 (Pubitemid 37048345)
58. Kägi, D., Ledermann, B., Bürki, K., Seiler, P., Odermatt, B., Olsen, K. J., Podack, E. R., Zinkernagel, R. M., and Hengartner, H. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369, 31-37 (Pubitemid 24144352)
59. Klein, U., and Ghosh, S. (2011) The two faces of NF-κB signaling in cancer development and therapy. Cancer Cell 20, 556-558
60. Bivona, T. G., Hieronymus, H., Parker, J., Chang, K., Taron, M., Rosell, R., Moonsamy, P., Dahlman, K., Miller, V. A., Costa, C., Hannon, G., and Sawyers, C. L. (2011) FAS and NF-κB signaling modulate dependence of lung cancers on mutant EGFR. Nature 471, 523-526
61. Bista, P., Zeng, W., Ryan, S., Bailly, V., Browning, J. L., and Lukashev, M. E. (2010) TRAF3 controls activation of the canonical and alternative NFκB by the lymphotoxin β receptor. J. Biol. Chem. 285, 12971-12978