Transforming growth factor-α inhibits the intrinsic pathway of c-Myc-induced apoptosis through activation of nuclear factor-κB in murine hepatocellular carcinomas

Molecular Cancer Research

Volumn 3, Issue 7, 2005, Pages 403-412

  Cavin, Lakita G ^a   Wang, Fang ^a   Factor, Valentina M ^b   Kaur, Swayamjot ^a   Venkatraman, Manickam ^a   Thorgeirsson, Snorri S ^b   Arsura, Marcello ^a  

^a UNIVERSITY OF TENNESSEE CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL XL; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR ALPHA; X LINKED INHIBITOR OF APOPTOSIS;

ADENOVIRUS; ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNE RESPONSE; LIVER CELL; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CASPASE 9; CASPASES; CELL LINE, TUMOR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; LIVER NEOPLASMS; MICE; MICE, TRANSGENIC; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MYC; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR ALPHA; UP-REGULATION;

ADENOVIRIDAE; MURINAE;

EID: 22944470236     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-04-0186     Document Type: Article

References (53)

1. Barkett M, Gilmore TD. Control of apoptosis by Rel/NF-κB transcription factors. Oncogene 1999;18:6910-24.
2. Kucharczak J, Simmons MJ, Fan Y, Gelinas C. To be, or not to be: NF-κB is the answer-role of Rel/NF-κB in the regulation of apoptosis. Oncogene 2003;22: 8961-82.
3. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S. Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev 1995;9:2723-35.
4. Ghosh S, Karin M. Missing pieces in the NF-κB puzzle. Cell 2002;109 Suppl:S81-96.
5. Pikarsky E, Porat RM, Stein I, et al. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature 2004;431:461-6.
6. Cavin LG, Venkatraman M, Factor VM, et al. Regulation of α-fetoprotein by nuclear factor-κB protects hepatocytes from tumor necrosis factor-α cytotoxicity during fetal liver development and hepatic oncogenesis. Cancer Res 2004;64: 7030-8.
7. Arsura M, Mercuric F, Oliver AL, Thorgeirsson SS, Sonenshein GE. Role of the IκB kinase complex in oncogenic Ras- and Raf-mediated transformation of rat liver epithelial cells. Mol Cell Biol 2000;20:5381-91.
8. Factor V, Oliver AL, Panta GR, Thorgeirsson SS, Sonenshein GE, Arsura M. Roles of Akt/PKB and IKK complex in constitutive induction of NF-κB in hepatocellular carcinomas of transforming growth factor α/c-myc transgenic mice. Hepatology 2001;34:32-41.
9. Arsura M, Panta GR, Bilyeu JD, et al. Transient activation of NF-κB through a TAK1/IKK kinase pathway by TGF-β1 inhibits AP-1/SMAD signaling and apoptosis: implications in liver tumor formation. Oncogene 2003; 22:412-25.
10. Cavin LG, Romieu-Mourez R, Panta GR, et al. Inhibition of CK2 activity by TGF-β1 promotes IκB-α protein stabilization and apoptosis of immortalized hepatocytes. Hepatology 2003;38:1540-51.
11. Lucito R, Schneider RJ. Hepatitis B virus X protein activates transcription factor NF-κB without a requirement for protein kinase C. J Virol 1992;66:983-91.
12. Tai DI, Tsai SL, Chang YH, et al. Constitutive activation of nuclear factor κB in hepatocellular carcinoma. Cancer 2000;89:2274-81.
13. Waris G, Livolsi A, Imbert V, Peyron JF, Siddiqui A. Hepatitis C virus NS5A and subgenomic replicon activate NF-κB via tyrosine phosphorylation of IκBα and its degradation by calpain protease. J Biol Chem 2003;278:40778-87.
14. Arsura M, Sonenshein GE. The role of c-myc and c-myb oncogenes in hematopoiesis and leukemogenesis. 1st ed. New York: John Wiley and Sons, Inc.; 2000. p. 521-50.
15. Grandori C, Cowley SM, James LP, Eisenman RN. The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 2000;16:653-99.
16. Yaswen P, Goyette M, Shank PR, Fausto N. Expression of c-Ki-ras, c-Ha-ras, and c-myc in specific cell types during hepatocarcinogenesis. Mol Cell Biol 1985; 5:780-6.
17. Moray T, Marchio A, Etiemble J, Trepo C, Tiollais P, Buendia MA. Rearrangement and enhanced expression of c-myc in hepatocellular carcinoma of hepatitis virus infected woodchucks. Nature 1986;324:276-9.
18. Nagy P, Evarts RP, Marsden E, Roach J, Thorgeirsson SS. Cellular distribution of c-myc transcripts during chemical hepatocarcinogenesis in rats. Cancer Res 1988;48:5522-7.
19. Gu JR, Hu LF, Cheng YC, Wan DF. Oncogenes in human primary hepatic cancer. J Cell Physiol 1986;4 Suppl:13-20.
20. Tiniakos D, Spandidos DA, Kakkanas A, Pintzas A, Pollice L, Tiniakos G. Expression of ras and myc oncogenes in human hepatocellular carcinoma and non-neoplastic liver tissues. Anticancer Res 1989;9:715-21.
21. Sandgren EP, Quaife CJ, Pinkert CA, Palmiter RD, Brinster RL. Oncogene-induced liver neoplasia in transgenic mice. Oncogene 1989;4:715-24.
22. Shachaf CM, Kopelman AM, Arvanitis C, et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004;431:1112-7.
23. Prendergast GC. Mechanisms of apoptosis by c-Myc. Oncogene 1999;18: 2967-87.
24. Nilsson JA, Cleveland JL. Myc pathways provoking cell suicide and cancer. Oncogene 2003;22:9007-21.
25. Murakami H, Sanderson ND, Nagy P, Marino PA, Merlino G, Thorgeirsson SS. Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: interaction of c-myc and transforming growth factor α in hepatic oncogenesis. Cancer Res 1993;53:1719-23.
26. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGF α overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990;61:1137-46.
27. Santoni-Rugiu E, Jensen MR, Thorgeirsson SS. Disruption of the pRb/E2F pathway and inhibition of apoptosis are major oncogenic events in liver constitutively expressing c-myc and transforming growth factor α. Cancer Res 1998;58:123-34.
28. Romashkova JA, Makarov SS. NF-κB is a target of AKT in anti-apoptotic PDGF signalling [see comments]. Nature 1999;401:86-90.
29. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase [see comments]. Nature 1999;401:82-5.
30. Yang CH, Murti A, Pfeffer SR, Kim JG, Donner DB, Pfeffer LM. Interferon α/β promotes cell survival by activating nuclear factor κB through phosphatidylinositol 3-kinase and Akt. J Biol Chem 2001;276:13756-61.
31. Pianetti S, Arsura M, Romieu-Mourez R, Coffey RJ, Sonenshein GE. Her-2/neu overexpression induces NF-κB via a PI3-kinase/Akt pathway involving calpain-mediated degradation of IκB-α that can be inhibited by the tumor suppressor PTEN. Oncogene 2001;20:1287-99.
32. Madrid LV, Mayo MW, Reuther JY, Baldwin AS Jr. Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen-activated protein kinase p38. J Biol Chem 2001;276:18934-40.
33. Mercuric F, Zhu H, Murray BW, et al. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation [see comments]. Science 1997;278: 860-6.
34. Ayer DE, Kretzner L, Eisenman RN. Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell 1993;72:211-22.
35. Sherr CJ. The INK4a/ARF network in tumour suppression. Nat Rev Mol Cell Biol 2001;2:731-7.
36. Juin P, Hueber AO, Littlewood T, Evan G. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev 1999;13: 1367-81.
37. L. Mol Cell Biol 2003;23:7256-70.
38. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ Jr, Sledge GW Jr. Constitutive activation of NF-κB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 1997;17:3629-39.
39. Sovak MA, Bellas RE, Kim DW, et al. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997;100: 2952-60.
40. Romieu-Mourez R, Landesman-Bollag E, Seldin DC, Traish AM, Mercuric F, Sonenshein GE. Roles of IKK kinases and protein kinase CK2 in activation of nuclear factor-κB in breast cancer. Cancer Res 2001;61: 3810-8.
41. Madrid LV, Wang CY, Guttridge DC, Schottelius AJ, Baldwin AS Jr, Mayo MW. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-κB. Mol Cell Biol 2000;20:1626-38.
42. Biswas DK, Cruz AP, Gansberger E, Pardee AB. Epidermal growth factor-induced nuclear factor κB activation: a major pathway of cell-cycle progression in estrogen-receptor negative breast cancer cells. Proc Natl Acad Sci U S A 2000; 97:8542-7.
43. Jeay S, Pianetti S, Kagan HM, Sonenshein GE. Lysyl oxidase inhibits ras-mediated transformation by preventing activation of NF-κB. Mol Cell Biol 2003; 23:2251-63.
44. Palamakumbura AH, Jeay S, Guo Y, et al. The pro-peptide domain of lysyl oxidase induces phenotypic reversion of Ras-transformed cells. J Biol Chem 2004;279:40593-600.
45. Eischen CM, Woo D, Roussel MF, Cleveland JL. Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol Cell Biol 2001;21:5063-70.
46. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 1999;13:2658-69.
47. Tanaka H, Matsumura I, Ezoe S, et al. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-κB activity that facilitates MnSOD-mediated ROS elimination. Mol Cell 2002;9:1017-29.
48. Arsura M, Wu M, Sonenshein GE. TGF β1 inhibits NF-κB/Rel activity inducing apoptosis of B cells: transcriptional activation of IκBα. Immunity 1996; 5:31-40.
49. Panta GR, Kaur S, Cavin LG, et al. ATM and the catalytic subunit of DNA-dependent protein kinase activate NF-κB through a common MEK/extracellular signal-regulated kinase/p90(rsk) signaling pathway in response to distinct forms of DNA damage. Mol Cell Biol 2004;24:1823-35.
50. Chen J, Willingham T, Margraf LR, Schreiber-Agus N, DePinho RA, Nisen PD. Effects of the MYC oncogene antagonist, MAD, on proliferation, cell cycling and the malignant phenotype of human brain tumour cells. Nat Med 1995;1:638-43.
51. Kupriyanova TA, Kandror KV. Akt-2 binds to Glut4-containing vesicles and phosphorylates their component proteins in response to insulin. J Biol Chem 1999;274:1458-64.
52. Roussel MF, Theodoras AM, Pagano M, Sherr CJ. Rescue of defective mitogenic signaling by D-type cyclins. Proc Natl Acad Sci U S A 1995;92: 6837-41.
53. Duyao MP, Buckler AJ, Sonenshein GE. Interaction of an NF-κB-like factor with a site upstream of the c-myc promoter. Proc Natl Acad Sci U S A 1990;87: 4727-31.