NF-κB in cancer: A marked target

Seminars in Cancer Biology

Volumn 13, Issue 2, 2003, Pages 107-114

  Lin, Anning ^a   Karin, Michael ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anti apoptosis; Cancer; NF B; Therapy; Transcription

Indexed keywords

CASPASE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR;

APOPTOSIS; CANCER; CANCER THERAPY; CARCINOGENESIS; CELL PROLIFERATION; DNA DAMAGE; ENZYME INHIBITION; REGULATORY MECHANISM; REVIEW; TUMOR CELL; TUMOR GROWTH; ANIMAL; DRUG ANTAGONISM; HUMAN; NEOPLASM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; HUMANS; NEOPLASMS; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 0037376895     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1044-579X(02)00128-1     Document Type: Review

References (90)

1. Bishop J.M. Molecular themes in oncogenesis. Cell. 64:1991;235-248.
2. Hunter T. Cooperation between oncogenes. Cell. 64:1991;249-270.
3. Cantley L.C.et al. Oncogenes and signal transduction. Cell. 64:1991;281-302.
4. Fisher D.E. Apoptosis in cancer therapy: crossing the threshold. Cell. 78:1994;539-542.
5. Evan G.I., Vousden K.H. Proliferation, cell cycle and apoptosis in cancer. Nature. 411:2001;342-348.
6. Johnstone R.W., Ruefli A.A., Lowe S.W. Apoptosis: a link between cancer genetics and chemotherapy. Cell. 108:2002;153-164.
7. Karin M., Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18:2000;621-663.
8. Ghosh S., Karin M. Missing pieces in the NF-κB puzzle. Cell. 109(Suppl.):2002;S81-S96.
9. Baldwin A.S. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB. J. Clin. Invest. 107:2001;241-246.
10. Karin M., Cao Y., Greten F.R., Li Z.W. NF-κB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer. 2:2002;301-310.
11. Gilmore T.D. Multiple mutations contribute to the oncogenicity of the retroviral oncoprotein v-Rel. Oncogene. 18:1999;6925-6937.
12. Karin M., Lin A. NF-κB at the crossroads of life and death. Nat. Immunol. 3:2002;221-227.
13. Baldwin A.S. Jr. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:1996;649-683.
14. Li Z.W.et al. The IKKβ subunit of IκB kinase (IKK) is essential for nuclear factor kappa B activation and prevention of apoptosis. J. Exp. Med. 189:1999;1839-1845.
15. Li Q., Van Antwerp D., Mercurio F., Lee K.F., Verma I.M. Severe liver degeneration in mice lacking the IκB kinase 2 gene. Science. 284:1999;321-325.
16. Tanaka M.et al. Embryonic lethality, liver degeneration, and impaired NF-κB activation in IKKβ-deficient mice. Immunity. 10:1999;421-429.
17. Senftleben U., Li Z.W., Baud V., Karin M. IKKβ is essential for protecting T cells from TNF-α-induced apoptosis. Immunity. 14:2001;217-230.
18. Solan N.J., Miyoshi H., Carmona E.M., Bren G.D., Paya C. RelB cellular regulation and transcriptional activity are regulated by p100. J. Biol. Chem. 277:2002;1405-1418.
19. Zhong H., SuYang H., Erdjument-Bromage H., Tempst P., Ghosh S. The transcriptional activity of NF-κB is regulated by the IκB-associated PKAc subunit through a cyclic AMP-independent mechanism. Cell. 89:1997;413-424.
20. Sizemore N., Leung S., Stark G.R. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-κB p65/RelA subunit. Mol. Cell. Biol. 19:1999;4798-4805.
21. Madrid L.V.et al. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-κB. Mol. Cell. Biol. 20:2000;1626-1638.
22. Beg A.A., Sha W.C., Bronson R.T., Ghosh S., Baltimore D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB. Nature. 376:1995;167-170.
23. Beg A.A., Baltimore D. An essential role for NF-κB in preventing TNF-α-induced cell death. Science. 274:1996;782-784.
24. Van Antwerp D.J., Marti S.J., Kafri T., Green D.R., Verma I.M. Suppression of TNF-α-induced apoptosis by NF-κB. Science. 274:1996;787-789.
25. Liu Z.G., Hsu H., Goeddel D.V., Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell. 87:1996;565-576.
26. Makris C.et al. Female mice heterozygous for IKKγ/NEMO deficiencies develop a dermatopathy similar to the human X-linked disorder incontinentia pigmenti. Mol. Cell. 5:2000;969-979.
27. Alcamo E.et al. Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-κB in leukocyte recruitment. J. Immunol. 167:2001;1592-1600.
28. Doi T.S.et al. Absence of tumor necrosis factor rescues RelA-deficient mice from embryonic lethality. Proc. Natl. Acad. Sci. U.S.A. 96:1999;2994-2999.
29. Horwitz B.H., Scott M.L., Cherry S.R., Bronson R.T., Baltimore D. Failure of lymphopoiesis after adoptive transfer of NF-κB-deficient fetal liver cells. Immunity. 6:1997;765-772.
30. Wang C.Y., Cusack J.C. Jr., Liu R., Baldwin A.S. Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-κB. Nat. Med. 5:1999;412-417.
31. Deveraux Q.L.et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17:1998;2215-2223.
32. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. Jr. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 281:1998;1680-1683.
33. Chu Z.L.et al. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-κB control. Proc. Natl. Acad. Sci. U.S.A. 94:1997;10057-10062.
34. Liston P.et al. Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature. 379:1996;349-353.
35. Takahashi R.et al. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem. 273:1998;7787-7790.
36. Deveraux Q.L.et al. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J. 18:1999;5242-5251.
37. Conte D., Liston P., Wong J.W., Wright K.E., Korneluk R.G. Thymocyte-targeted overexpression of XIAP transgene disrupts T lymphoid apoptosis and maturation. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5049-5054.
38. Harlin H., Reffey S.B., Duckett C.S., Lindsten T., Thompson C.B. Characterization of XIAP-deficient mice. Mol. Cell. Biol. 21:2001;3604-3608.
39. Stehlik C.et al. Nuclear factor (NF)-kappaB-regulated X-chromosome-linked IAP gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J. Exp. Med. 188:1998;211-216.
40. Tang G.et al. Inhibition of JNK activation through NF-κB target genes. Nature. 414:2001;313-317.
41. Yeh W.C.et al. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity. 12:2000;633-642.
42. Kreuz S., Siegmund D., Scheurich P., Wajant H. NF-κB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 21:2001;3964-3973.
43. Irmler M.et al. Inhibition of death receptor signals by cellular FLIP. Nature. 388:1997;190-195.
44. Shu H.B., Halpin D.R., Goeddel D.V. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity. 6:1997;751-763.
45. Baud V., Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol. 11:2001;372-377.
46. Lin E.Y., Orlofsky A., Berger M.S., Prystowsky M.B. Characterization of A1, a novel hemopoietic-specific early-response gene with sequence similarity to bcl-2. J. Immunol. 151:1993;979-988.
47. Wang C.Y., Guttridge D.C., Mayo M.W., Baldwin A.S. Jr. NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19:1999;5923-5929.
48. Lee H.H., Dadgostar H., Cheng Q., Shu J., Cheng G. 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. U.S.A. 96:1999;9136-9141.
49. Tsukahara T.et al. Induction of Bcl-x(L) expression by human T-cell leukemia virus type 1 Tax through NF-κB in apoptosis-resistant T-cell transfectants with Tax. J. Virol. 73:1999;7981-7987.
50. Khoshnan A.et al. The NF-κB cascade is important in Bcl-xL expression and for the anti-apoptotic effects of the CD28 receptor in primary human CD4+ lymphocytes. J. Immunol. 165:2000;1743-1754.
51. Chen C., Edelstein L.C., Gelinas C. The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell. Biol. 20:2000;2687-2695.
52. Grossmann M.et al. The anti-apoptotic activities of Rel and RelA required during B-cell maturation involve the regulation of Bcl-2 expression. EMBO J. 19:2000;6351-6360.
53. Bentires-Alj M.et al. Inhibition of the NF-κB transcription factor increases Bax expression in cancer cell lines. Oncogene. 20:2001;2805-2813.
54. Lee S.Y.et al. TRAF2 is essential for JNK but not NF-κB activation and regulates lymphocyte proliferation and survival. Immunity. 7:1997;703-713.
55. Verheij M.et al. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380:1996;75-79.
56. Natoli G.et al. Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science. 275:1997;200-203.
57. Tournier C.et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science. 288:2000;870-874.
58. De Smaele E.et al. Induction of gadd45β by NF-κB downregulates pro-apoptotic JNK signalling. Nature. 414:2001;308-313.
59. Javelaud D., Besancon F. NF-κB activation results in rapid inactivation of JNK in TNF-α-treated Ewing sarcoma cells: a mechanism for the anti-apoptotic effect of NF-κB. Oncogene. 20:2001;4365-4372.
60. Lenczowski J.M.et al. Lack of a role for Jun kinase and AP-1 in Fas-induced apoptosis. Mol. Cell. Biol. 17:1997;170-181.
61. Zhan Q, et al. Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 18:2892-900.
62. Lin A. Activation of the JNK signaling pathway: breaking the brake on apoptosis. BioEssays, in press.
63. Park JM, Greten FR, Li Z-W, Karin M. Macrophage apoptosis by anthrax lethal factor and p38 kinase inhibition. Science 2002, in press.
64. Lin Y., Devin A., Rodriguez Y., Liu Z.G. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13:1999;2514-2526.
65. Arch R.H., Gedrich R.W., Thompson C.B. Translocation of TRAF proteins regulates apoptotic threshold of cells. Biochem. Biophys. Res. Commun. 272:2000;936-945.
66. Leo E.et al. TRAF1 is a substrate of caspases activated during tumor necrosis factor receptor-alpha-induced apoptosis. J. Biol. Chem. 276:2001;8087-8093.
67. Schwenzer R.et al. The human tumor necrosis factor (TNF) receptor-associated factor 1 gene (TRAF1) is up-regulated by cytokines of the TNF ligand family and modulates TNF-induced activation of NF-κB and c-Jun N-terminal kinase. J. Biol. Chem. 274:1999;19368-19374.
68. Tang G., Yang J., Minemoto Y., Lin A. Blocking caspase-3-mediated proteolysis of IKKβ suppresses TNF-α-induced apoptosis. Mol. Cell. 8:2001;1005-1016.
69. Reuther J.Y., Baldwin A.S. Jr. Apoptosis promotes a caspase-induced amino-terminal truncation of IκBα that functions as a stable inhibitor of NF-κB. J. Biol. Chem. 274:1999;20664-20670.
70. Barkett M., Xue D., Horvitz H.R., Gilmore T.D. Phosphorylation of IκBα inhibits its cleavage by caspase CPP32 in vitro. J. Biol. Chem. 272:1997;29419-29422.
71. Levkau B.et al. xIAP induces cell-cycle arrest and activates nuclear factor-kappa B: new survival pathways disabled by caspase-mediated cleavage during apoptosis of human endothelial cells. Circ. Res. 88:2001;282-290.
72. Clem R.J.et al. c-IAP1 is cleaved by caspases to produce a proapoptotic C-terminal fragment. J. Biol. Chem. 276:2001;7602-7608.
73. Clem R.J.et al. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. U.S.A. 95:1998;554-559.
74. Fujita N., Nagahashi A., Nagashima K., Rokudai S., Tsuruo T. Acceleration of apoptotic cell death after the cleavage of Bcl-XL protein by caspase-3-like proteases. Oncogene. 17:1998;1295-1304.
75. Fadok V.A.et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101:1998;890-898.
76. Orth K.et al. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science. 290:2000;1594-1597.
77. Mills S.D.et al. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc. Natl. Acad. Sci. U.S.A. 94:1997;12638-12643.
78. Kasof G.M.et al. Tumor necrosis factor-alpha induces the expression of DR6, a member of the TNF receptor family, through activation of NF-κB. Oncogene. 20:2001;7965-7975.
79. Ravi R.et al. Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-κB. Nat. Cell Biol. 3:2001;409-416.
80. Zheng Y.et al. 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. 166:2001;4949-4957.
81. Furman R.R., Asgary Z., Mascarenhas J.O., Liou H.C., Schattner E.J. Modulation of NF-κB activity and apoptosis in chronic lymphocytic leukemia B cells. J. Immunol. 164:2000;2200-2206.
82. Bargou R.et al. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J. Clin. Invest. 100:1997;2961-2969.
83. Cahir-McFarland E., Kieff E. NF-κB inhibition in EBV-transformed lymphoblastoid cell lines. Rec. Results Cancer Res. 159:2002;44-48.
84. Wang C.Y., Mayo M.W., Baldwin A.S. Jr. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-κB. Science. 274:1996;784-787.
85. Kopp E., Ghosh S. Inhibition of NF-κB by sodium salicylate and aspirin. Science. 265:1994;956-959.
86. Yin M.J., Yamamoto Y., Gaynor R.B. The anti-inflammatory agents aspirin and salicylate inhibit the activity of IκB kinase β Nature. 396:1998;77-80.
87. Tsai S.H., Liang Y.C., Lin-Shiau S.Y., Lin J.K. Suppression of TNF-α-mediated NF-κB activity by myricetin and other flavonoids through downregulating the activity of IKK in ECV304 cells. J. Cell Biochem. 74:1999;606-615.
88. Jobin C.et al. Curcumin blocks cytokine-mediated NF-kappa B activation and proinflammatory gene expression by inhibiting inhibitory factor I-kappa B kinase activity. J. Immunol. 163:1999;3474-3483.
89. Mayo M.W.et al. Requirement of NF-κB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science. 278:1997;1812-1815.
90. Sovak M.A.et al. Aberrant nuclear factor-kappaB/Rel expression and the pathogenesis of breast cancer. J. Clin. Invest. 100:1997;2952-2960.