The Rel/NF-κb family directly activates expression of the apoptosis inhibitor BCl-x(L)

Molecular and Cellular Biology

Volumn 20, Issue 8, 2000, Pages 2687-2695

  Chen, Cailin ^a,e   Edelstein, Leonard C ^a,b   Gélinas, Céline ^a,c,d  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^d CABM   (United States)

^e JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ONCOPROTEIN; PROTEIN BCL 2; PROTEIN BCL X; TRANSCRIPTION FACTOR; BCL2L1 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL LINE; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; TRANSCRIPTION REGULATION; CELL DIFFERENTIATION; CELL DIVISION; GENETICS; HELA CELL;

APOPTOSIS; BCL-X PROTEIN; CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 0033621956     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.8.2687-2695.2000     Document Type: Article

References (69)

1. Adams, J. M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281:1322-1326.
2. Armstrong, R. C., T. Aja, J. Xiang, S. Gaur, J. F. Krebs, K. Hoang, X. Bai, S. J. Korsmeyer, D. S. Karanewsky, L. C. Fritz, and K. J. Tomaselli. 1996. Fas-induced activation of the cell death-related prutease CPP32 is inhibited by Bcl-2 and by ICE family protease inhibitors. J. Biol. Chem. 271:16850-16855.
3. Badrichani, A. Z., D. M. Stroka, G. Bilbao, D. T. Curiel, F. H. Bach, and C. Ferran. 1999. Bcl-2 and Bcl-xL serve an anti-inflammatory function in endothelial cells through inhibition of NF-κB. J. Clin. Investig. 103:543-553.
4. Bargou, R., F. Emmerich, D. Krappmann, K. Bommert, M. Mapara, W. Arnold, H. Royer, E. Grinstein, A. Greiner, C. Scheidereit, and B. Dorken. 1997. Constitutive nuclear factor-kappaB-RelA activation is required tor proliferation and survival of Hodgkin's disease tumor cells. J. Clin. Investig. 100:2961-2969.
5. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 274:782-784.
6. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature 376:167-170.
7. Boise, L., M. Gonzalez-Garcia, C. Postema, L. Ding, T. Lindsten, L. Turka, X. Mao, G. Nunez, and C. Thompson. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597-608.
8. Boise, L. H., and C. B. Thompson. 1997. Bcl-x(L) can inhibit apoptosis in cells that have undergone Fas-induced protease activation. Proc. Natl. Acad. Sci. USA 94:3759-3764.
9. Bours, V., E. Dejardin, F. Goujon-Letawe, M.-P. Merville, and V. Castronovo. 1994. The NF-κB transcription factor and cancer: high expression of NF-κB-and IκB-related proteins in tumor cell lines. Biochem. Pharmacol. 47:145-149.
10. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
11. Cabannes, E., G. Khan, F. Aillet, R. Jarrett, and R. Hay. 1999. Mutations in the IκBα gene in Hodgkin's disease suggest a tumour suppressor role for Ikappa B alpha. Oncogene 18:3063-3070.
12. Carrasco, D., F. Weih, and R. Bravo. 1994. Developmental expression of the mouse c-rel proto-oncogene in hematopoietic organs. Development 120: 2991-3004.
13. Chen, C., F. Agnès, and C. Gélinas. 1999. Mapping of a serine-rich domain essential for the transcriptional, antiapoptotic, and transforming activities of the v-Rel oncoprotein. Mol. Cell. Biol. 19:307-316.
14. Chinnaiyan, A., K. Orth, K. O'Rourke, H. Duan, G. Poirier, and V. Dixit. 1996. Molecular ordering of the cell death pathway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271: 4573-4576.
15. Chu, Z.-L., T. A. McKinsey, L. Liu, J. J. Gentry, M. H. Malim, and D. W. Ballard. 1997. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-κB control. Proc. Natl. Acad. Sci. USA 94:10057-10062.
16. Dejardin, E., G. Bonizzi, A. Bellahcene, V. Castronovo, M.-P. Merville, and V. Bours. 1995. Highly expressed p100/p52 (NFκB2) sequesters other NFκB-related proteins in the cytoplasm of human breast cancer cells. Oncogene 11:1835-1841.
17. Dragovich, T., C. M. Rudin, and C. B. Thompson. 1998. Signal transduction pathways that regulate cell survival and cell death. Oncogene 17:3207-3213.
18. Erhardt, P., and G. M. Cooper. 1996. Activation of the CPP32 apoptotic protease by distinct signaling pathways with differential sensitivity to Bcl-xL. J. Biol. Chem. 271:17601-17604.
19. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
20. Fujio, Y., K. Kunisada, H. Hirota, K. Yamauchi-Takihara, and T. Kishimoto. 1997. Signals through gp130 upregulate bcl-x gene expression via STAT1-binding cis-element in cardiac myocytes. J. Clin. Investig. 99:2898-2905.
21. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 89:5547-5551.
22. Grillot, D. A. M., M. González-Garcia, D. Ekhterae, L. Duan, N. Inohara, S. Ohta, M. F. Seldin, and G. Nunez. 1997. Genomic organization, promoter region analysis, and chromosome localization of the mouse bcl-x gene. J. Immunol. 158:4750-4757.
23. Grumont, R. J., I. J. Rourke, and S. Gerondakis. 1999. Rel-dependent induction of A1 transcription is required to protect B cells front antigen receptor ligation-induced apoptosis. Genes Dev. 13:400-411.
24. Hettmann, T., J. DiDonato, M. Karin, and J. M. Leiden. 1999. An essential role for nuclear factor kappaB in promoting double positive thymocyte apoptosis. J. Exp. Med. 189:145-158.
25. Houldsworth, J., S. Mathew, P. H. Rao, K. Dyomina, D. C. Louie, N. Parsa, K. Offit, and R. S. K. Chaganti. 1996. REL proto-oncogene is frequently amplified in extranodal diffuse large cell lymphoma. Blood 87:25-29.
26. Krajewska, M., S. Krajewski, J. Epstein, A. Shabaik, J. Sauvageot, K. Song, S. Kitada, and J. Reed. 1996. Immunohistochemical analysis of bcl-2, bax, bcl-x, and mcl-1 expression in prostate cancers. Am. J. Pathol. 148:1567-1576.
27. Krajewska, M., S. Moss, S. Krajewski, K. Song, P. Holt, and J. Reed. 1996. Elevated expression of Bcl-x and reduced Bak in primary colorectal adenocarcinomas. Cancer Res. 56:2422-2427.
28. Krajewski, S., M. Krajewska, A. Shabaik, H. G. Wang, S. Irie, L. Fong, and J. C. Reed. 1994. Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54:5501-5507.
29. Krappmann, D., F. Emmerich, U. Kordes, E, Scharschmidt, B. Dorken, and C. Scheidereit. 1999. Molecular mechanisms of constitutive NF-kappaB/Rel activation in Hodgkin/Reed-Sternberg cells. Oncogene 18:943-953.
30. Krikos, A., C. D. Laherty, and V. M. Dixit. 1992. Transcriptional activation of the tumor necrosis factor α-inducihle zinc linger protein. A20, is mediated by κB elements. J. Biol. Chem. 267:17971-17976.
31. Lee, H. H., H. Dadgostar, Q. Cheng, J. Shu, and G. Cheng. 1999. NF-κB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA 96:9136-9141.
32. Liu, Z., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87:565-576.
33. Lu, D., J. D. Thompson, G. K. Gorski, N. R. Rice, M. G. Mayer, and J. J. Yunis. 1991. Alterations at the rel locus in human lymphoma. Oncogene 6:1235-1241.
34. Luque, I., and C. Gélinas. 1997. Rel/NF-κB und IκB factors in oncogenesis. Semin. Cancer Biol. 8:103-111.
35. Miyazaki, T., Z. J. Liu, and T. Taniguchi. 1996. Selective cooperation of HTLV-I-encoded p40tax-1 with cellular oncoproteins in the induction of hematopoietic cell proliferation. Oncogene 12:2403-2408.
36. Ohta, K., K. Iwai, Y. Kasahara, N. Taniguchi, S. Krajewski, J. C. Reed, and T. Miyawaki. 1995. Immunoblot analysis of cellular expression of Bcl-2 family proteins, Bcl-2, Bax, Bcl-X and Mcl-1, in human peripheral blood and lymphoid tissues. Int. Immunol. 7:1817-1825.
37. Pallis, M., Y. M. Zhu, and N. H. Russell. 1997. Bcl-x(L) is heterogenously expressed by acute myeloblastic leukaemia cells and is associated with autonomous growth in vitro and with P-glvcoprotein expression. Leukemia 11:945-949.
38. Perez, D., and E. White. 1998. ElB 19K inhibits Fas-mediated apoptosis through FADD-dependent sequestration of FLICE. J. Cell Biol. 141:1255-1266.
39. Rao, P. H., J. Houldsworth, K. Dyomina, N. Z. Parsa, J. C. Cigudosa, D. C. Louie, L. Popplewell, K. Offit, S. C. Jhanwar, and R. S. K. Chaganti. 1998. Chromosomal and gene amplification in diffuse large B-cell lymphoma. Blood 92:234-240.
40. Rayet, B., and C. Gélinas. 1999. Aberrant rel/nfκb genes and activity in human cancer. Oncogene 18:6938-6947.
41. Reed, J. C. 1996. Mechanisms of Bcl-2 family protein function and dysfunction in health and disease. Behring Inst. Mitt. 97:72-100.
42. 1/S phase transition hy expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
43. Schneider, T. J., D. Grillot, L. C. Foote, G. E. Nunez, and T. L. Rothstein. 1997. Bcl-x protects primary B cells against Fas-mediated apoptosis. J. Immunol. 159:4834-4839.
44. Schott, A. F., I. J. Apel, G. Nunez, and M. F. Clarke. 1995. Bel-XL protects cancer cells from p53-mediated apoptosis. Oncogene 11:1389-1394.
45. L-dependent mechanism. Mol. Cell. Biol. 19:2624-2634.
46. Shimizu, S., Y. Eguchi, W. Kamiike, H. Matsuda, and Y. Tsujimoto. 1996. Bcl-2 expression prevents activation of the ICE proteasc cascade. Oncogene 12:2251-2257.
47. Socolovsky, M., A. E. J. Fallon, S. Wang, C. Brugnara, and H. F. Lodish. 1999. Fetal anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/-mice: a direct role for Stat5 in Bcl-XL induction. Cell 98:181-191.
48. Sovak, M., R. Bellas, D. Kim, G. Zanieski, A. Rogers, A. Traish, and G. Sonenshein. 1997. Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J. Clin. Investig. 100:2952-2960.
49. Srinivasan, A., F. Li, A. Wong, L. Kodandapani, R. Smidt, Jr., J. F. Krebs, L. C. Fritz, J. C. Wu, and K. J. Tomaselli. 1998. Bcl-xL functions downstream of caspase-8 to inhibit Fas-and tumor necrosis factor receptor 1-induced apoptosis of MCF7 breast carcinoma cells. J. Biol. Chem. 273:4511-4529.
50. Stehlik, C., R. de Martin, I. Kumabashiri, J. A. Schmid, B. R. Binder, and J. Lipp. 1998. Nuclear factor (NF)-kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J. Exp. Med. 188:211-216.
51. Tamatani, M., Y. H. Che, H. Matsuzaki, S. Ogawa, H. Okado, S.-I. Miyake, T. Mizuno, and M. Tohyama. 1999. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFκB activation in primary hippocampal neurons. J. Biol. Chem. 274:8531-8538.
52. L expression by human T-cell leukemia virus type 1 Tax through NF-κB in apoptosis-resistant T-cell transfectants with Tax. J. Virol. 73:7981-7987.
53. Tu, Y., S. Renner, F. Xu, A. Fleishman, J. Taylor, J. Weisz, R. Vescio, M. Rettig, J. Berenson, S. Krajewski, J. C. Reed, and A. Lichtenstein. 1998. Bcl-x expression in multiple myeloma: possible indicator of chemoresistance. Cancer Res. 58:256-262.
54. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-α-induced apoptosis by NF-κB. Science 274:787-789.
55. Van Antwerp, D. J., S. J. Martin, I. M. Verma, and D. R. Green. 1998. Inhibition of TNF-induced apoptosis by NF-κB. Trends Cell Biol. 8:107-111.
56. Wang, C.-Y., D. C. Guttridge, M. W. Mayo, and A. S. Baldwin, Jr. 1999. NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19:5923-5929.
57. Wang, C.-Y., M. W. Mayo, and A. S. Baldwin, Jr. 1996. TNF-and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science 274:784-787.
58. Wang, C.-Y., M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin, Jr. 1998. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680-1683.
59. While, D. W., A. Roy, and T. D. Gilmore. 1995. The v-Rel oncoprotein blocks apoptosis and proteolysis of IκBα in transformed chicken spleen cells. Oncogene 10:857-868.
60. White, E., P. Sabbatini, M. Debbas, W. S. M. Wold, D. I. Kusher, and L. R. Gooding. 1992. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor a. Mol. Cell. Biol. 12:2570-2580.
61. Wood, K., M. Roff, and R. Hay. 1998. Defective IκBα in Hodgkin cell lines with constitutively active NF-κB. Oncogene 16:2131-2139.
62. Wu, M., H. Lee, R. E. Bellas, S. L. Schauer, M. Arsura, D. Katz, M. J. FitzGerald, T. L. Rothstein, D. H. Sherr, and G. E. Sonenshein. 1996. Inhibition of NF-κB/Rel induces apoptosis of murine B cells. EMBO J. 15:4682-4690.
63. Wu, M. X., Z. Ao, K. V. S. Prasad, R. Wu, and S. F. Schlossman. 1998. IEX-IL, an apoptosis inhibitor involved in NF-κB-mediated cell survival. Science 281:998-1001.
64. Xu, X., and C. Gélinas. 1997. A mutant Rel-homology domain promotes transcription by p50/NF-κB1. Oncogene 14:1521-1530.
65. Yang, E., and S. J. Korsmeyer. 1996. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 88:386-401.
66. You, M., P.-T. Ku, R. Hrdlicková, and H. R. Bose, Jr. 1997. ch-IAP1, a member of the inhibitor-of-apoptosis protein family, is a mediator of the antiapoptotic activity of the v-Rel oncoprotein. Mol. Cell. Biol. 17:7328-7341.
67. Zong, W.-X., J. Bash, and C. Gélinas. 1998. Rel blocks both anti-Fas and TNFα-induced apoptosis and an intact Rel transactivation domain is essential for this effect. Cell Death Differ. 5:963-972.
68. Zong, W.-X., M. Farrell, J. Bash, and C. Gélinas. 1997. v-Rel prevents apoptosis in transformed lymphoid cells and blocks TNFα-induced cell death. Oncogene 15:971-980.
69. Zong, W. X., L. C. Edelstein, C. Chen, J. Bash, and C. Gélinas. 1999. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNFα-induced apoptosis. Genes Dev. 13:382-387.