Apoptotic signaling by c-MYC

Oncogene

Volumn 27, Issue 50, 2008, Pages 6462-6472

  Hoffman, B ^a   Liebermann, D A ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Bcl 2 family; c MYC; Cancer; Death receptors; Mitochondria

Indexed keywords

ARF PROTEIN; ATM PROTEIN; BH3 PROTEIN; DEATH RECEPTOR; MYC PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

APOPTOSIS; BONE MARROW CELL; CANCER GROWTH; CARCINOGENESIS; CELL DIFFERENTIATION; CELL GROWTH; CELL SURVIVAL; CELL TYPE; GENE EXPRESSION; HUMAN; MITOCHONDRION; MYELOID LEUKEMIA; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; APOPTOSIS; CELL SURVIVAL; GENES, MYC; GENES, TUMOR SUPPRESSOR; HUMANS; MITOCHONDRIA; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 54949149565     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.312     Document Type: Review

References (91)

1. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S et al. (1985). The c-Myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
2. Adams JM, Harris AW, Strasser A, Ogilvy S, Cory S. (1999). Transgenic models of lymphoid neoplasia and development of a pan-hematopoietic vector. Oncogene 18: 5268-5277.
3. Adrain C, Martin SJ. (2006). Cell biology: double knockout blow for caspases. Science 311: 785-786.
4. Amanullah A, Liebermann DA, Hoffman B. (2000). p53-independent apoptosis associated with c-Myc-mediated block in myeloid cell differentiation. Oncogene 19: 2967-2977.
5. Amanullah A, Liebermann DA, Hoffman B. (2002). Deregulated c-Myc prematurely recruits both type I and II CD95/Fas apoptotic pathways associated with terminal myeloid differentiation. Oncogene 21: 1600-1610.
6. Amati B, Land H. (1994). Myc-Max-Mad: a transcription factor network controlling cell cycle progression, differentiation and death. Curr Opin Gene Dev 4: 102-108.
7. Amente S, Gargano B, Varrone F, Ruggiero L, Dominguez-Sola D, Lania L et al. (2006). p14ARF directly interacts with Myc through the Myc BoxII domain. Cancer Biol Ther 5: 287-291.
8. Amundson SA, Zhan Q, Penn LZ, Fornace Jr AJ. (1998). Myc suppresses induction of the growth arrest genes gadd34, gadd45, and gadd153 by DNA-damaging agents. Oncogene 17: 2149-2154.
9. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B et al. (2005). Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBOJ 24: 2096-2103.
10. Askew DS, Ashmun RA, Simmons B, Cleveland JL. (1991). Constitutive c-Myc expression in an IL-3 dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6: 1915-1922.
11. Askew DS, Ihle JN, Cleveland JL. (1993). Activation of apoptosis associated with enforced Myc expression in myeloid progenitor cells is dominant to the suppression of apoptosis by interleukin-3 or erythropoietin. Blood 82: 2079-2087.
12. Baudino TA, Cleveland JL. (2001). The max network gone mad. Mol Cell Biol 21: 691-702.
13. Bouchard C, Lee S, Laulus-Hock V, Loddenkemper C, Eilers M, Schmitt CA. (2007). FoxO transcription factors suppress Myc-driven lymphomagenesis via direct activation of Arf. Gene Dev 21: 2775-2787.
14. Brunner T, Kasibhatla S, Pinkoski MJ, Frutschi C, Yoo NJ, Echeverri F et al. (2000). Expression of Fas ligand in activated T cells is regulated by c-Myc. J Biol Chem 275: 9767-9772.
15. Cao X, Bennett RL, May WS. (2008). c-Myc and caspase-2 are involved in activating Bax during cytotoxic drug-induced apoptosis. J Biol Chem 283: 14490-14496.
16. Cavarretta IT, Neuwirt H, Untergasser G, Moser PL, Zaki MH, Steiner H et al. (2007). The antiapoptotic effect of IL-6 autocrine loop in a cellular model of advanced prostate cancer is mediated by Mcl-1. Oncogene 26: 2822-2832.
17. Corn PG, El-Deiry WS. (2007). Microassay analysis of p-53-dependent gene expression in response to hypoxia and DNA damage. Cancer Biol Ther 6: 1858-1866.
18. Conzen SD, Gottlob K, Kandel ES, Khanduri P, Wagner A, O'Leary M et al. (2000). Induction of cell cycle progression and acceleration of apoptosis are two separable functions of c-Myc: transrepression correlates with acceleration of apoptosis. Mol Cell Biol 20: 6008-6018.
19. D'Angelo S, Liebermann DA, Hoffman B. (2008). The c-Myc apoptotic response is not intrinsic to blocking terminal myeloid differentiation. J Cell Physiol 21: 120-127.
20. Dang CV, O'Donell KA, Zeller KI, Nguyen T, Osthus RC, Li F. (2006). The c-Myc target gene network. Semin Cancer Biol 16: 253-264.
21. Dang CV, O'Donnell KA, Juopperi T. (2005). The great Myc escape in tumorigenesis. Cancer Cell 8: 177-178.
22. Dansen TB, Whitfield J, Rostker F, Brown-Swigart L, Evan GI. (2006). Specific requirement for Bax, not Bak, in Myc-induced apoptosis and tumor suppression in vivo. J Biol Chem 281: 10890-10895.
23. Egle A, Harris AW, Bouillet P, Cory S. (2004). Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc Natl Acad Sci USA 101: 6164-6169.
24. Eischen CM, Packham G, Nip J, Fee BE, Hiebert SW, Zambetti GP et al. (2001b). Bcl-2 is an apoptotic target suppressed by both c-Myc and E2F-1. Oncogene 20: 6983-6993.
25. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. (1999). Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13: 2658-2669.
26. Eischen CM, Woo D, Roussel MF, Cleveland JL. (2001a). Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol Cell Biol 21: 5063-5070.
27. Eisenman RN. (2000). The max network: coordinated transcriptional regulation of cell growth and proliferation. Harvey Lect 96: 1-32.
28. Evan GI, Littlewood TD. (1993). The role of c-Myc in cell growth. Curr Opin Genet Dev 3: 44-49.
29. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M et al. (1992). Induction of apoptosis in fibroblasts by c-Myc protein. Cell 69: 119-128.
30. Felsher DW, Bishop JM. (1999). Transient excess of Myc activity can elicit genomic instability and tumorigenesis. Proc Natl Acad Sci USA 96: 3940-3944.
31. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. (2007). RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ 14: 400-410.
32. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, Elbim C. (2005). Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J Immunol 174: 3633-3642.
33. Gartel AL, Shchors K. (2003). Mechanisms of c-Myc-mediated transcriptional repression of growth arrest genes. Exp Cell Res 283: 17-21.
34. Guillouf C, Grana X, Selvakumaran M, Giordano A, Hoffman B, Liebermann DA. (1995). Dissection of the genetic programs of 53-mediated G1 growth arrest and apoptosis: Blocking p53-induced apoptosis unmasks G1 arrest. Blood 85: 2691-2698.
35. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C et al. (2005). Evasion of the p53 tumour surveillance network by tumour-derived Myc mutants. Nature 436: 807-811.
36. Henriksson M, Luscher B. (1996). Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 68: 109-182.
37. Hermeking H, Eick D. (1994). Mediation of c-Myc-induced apoptosis by p53. Science 265: 2091-2093.
38. Ho JS, Ma W, Mao DY, Benchimol S. (2005). p53-dependent transcriptional repression of c-Myc is required for G1 cell cycle arrest. Mol Cell Biol 25: 7423-7431.
39. Hoffman B, Anamullah A, Shafarenko M, Liebermann DA. (2002). The proto-oncogene c-Myc in hematopoietic development and leukemogenesis. Oncogene 21: 3414-3421.
40. Hoffman B, Liebermann DA. (1998). The proto-ocogene c-Myc and apoptosis. Oncogene 17: 3351-3357.
41. Hsu B, Marin MC, el-Naggar AK, Stephens LC, Brisbay S, McDonnell TJ. (1995). Evidence that c-Myc mediated apoptosis does not require wild-type p53 during lymphomagenesis. Oncogene 11: 175-179.
42. Hueber AO, Zornig M, Lyon D, Suda T, Nagata S, Evan GI. (1997). Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis. Science 278: 1246-1247.
43. Hurlin PJ, Huang J. (2006). The MAX-interacting transcription factor network. Semin Cancer Biol 16: 265-274.
44. Iaccarino I, Hancock D, Evan G, Downward J. (2003). c-Myc induces cytochrome c release in Rat1 fibroblasts by increasing outer mitochondrial membrane permeability in a Bid-dependent manner. Cell Death Differ 10: 599-608.
45. Jiang X, Tsang YH, Yu Q. (2007). c-Myc overexpression sensitizes Bim-mediated Bax activation for apoptosis induced by histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through regulating Bcl-2/Bcl-xL expression. Int J Biochem Cell Biol 39: 1016-1025.
46. Juin P, Hunt A, Littlewood T, Griffiths B, Swigart LB, Korsmeyer S et al. (2002). c-Myc functionally cooperates with Bax to induce apoptosis. Moll Cell Biol 22: 6158-6169.
47. Kasibhatla S, Beere HM, Brunner T, Echeverri F, Green DR. (2000). A 'non-canonical' DNA-binding element mediates the response of the Fas-ligand promoter to c-Myc. Curr Biol 10: 1205-1208.
48. Kelly PN, Puthalakath H, Adams JM, Strsasser A. (2007). Endogenous bcl-2 is not required for the development of Emu-Myc-induced B-cell lymphoma. Blood 109: 4907-4913.
49. Klefstrom J, Arighi E, Littlewood T, Jaattela M, Saksela E, Evan GI et al. (1997). Induction of TNF-sensitive cellular phenotype by c-Myc involves p53 and impaired NF-kappaB activation. EMBOJ 16: 7382-7392.
50. Knoepfler PS. (2007). Myc goes global: new tricks for an old oncogene. Cancer Res 67: 5061-5063.
51. Kobayashi S, Werneburg NW, Bronk SF, Kaufmann SH, Gores GJ. (2005). Interleukin-6 contributes to Mcl-1 up-regulation and TRAIL resistance via an Akt-signaling pathway in cholangiocarcinoma cells. Gastroenterology 128: 2054-2065.
52. Kreuz S, Siegmund D, Rumpf JJ, Samel D, Leverkus M, Janssen O. (2004). NFkappaB activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J Cell Biol 166: 369-380.
53. Lakhani SA, Masud A, Kuida K, Porter Jr GA, Booth CJ, Mehal WZ et al. (2006). Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311: 847-851.
54. Liebermann DA, Hoffman B. (2002). Myeloid differentiation (MyD)/growth arrest DNA damage (GADD) genes in tumor suppression, immunity and inflammation. Leukemia 16: 527-541.
55. Lindemans CA, Coffer PJ, Schellens IM, de Graaff PM, Kimpen JL, Koenderman L. (2006). Respiratory syncytial virus inhibits granulocyte apoptosis through a phosphatidylinositol 3-kinase and NF-kappaB-dependent mechanism. J Immunol 176: 5529-5537.
56. Luscher B, Larsson LG. (2007). The world according to Myc. EMBO reports 8: 1110-1114.
57. Luscher B. (2001). Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene 277: 1014.
58. Maclean KH, Keller UB, Rodriguez-Galindo C, Nilsson JA, Cleveland JL. (2003). c-Myc augments gamma irradiation-induced apoptosis by suppressing Bcl-XL. Mol Cell Biol 23: 7256-7270.
59. Meng F, Liu L, Chin PC, D'Mello SR. (2002). Akt is a downstream target of NF-kappa B. J Biol Chem 277: 29674-29680.
60. Meyer N, Kim SS, Penn LZ. (2006). The Oscar-worth role of Myc in apoptosis. Semin Cancer Biol 16: 275-287.
61. Meylan E, Tschopp J. (2005). The RIP kinases: crucial integrators of cellular stress. Trends Biochem Sci 30: 151-159.
62. Mitchell KO, Ricci MS, Miyashita T, Dicker DT, Jin Z, Reed JC et al. (2000). Bax is a transcriptional target and mediator of c-Myc-induced apoptosis. Cancer Res 60: 6318-6325.
63. Nieminen AI, Partanen JI, Jau A, Klefstrom J. (2007b). c-Myc primed mitochondria determine cellular sensitivity to TRAIL-induced apoptosis. EMBO J 26: 1055-1067.
64. Nieminen AI, Partanen JI, Klefstrom J. (2007a). C-Myc blazing a trail of death. Cell Cycle 6: 2464-2472.
65. Nikiforov MA, Riblett M, Tang WH, Gratchouck V, Zhuang D, Fernandez Y et al. (2007). Tumor cell-selective regulation of NOXA by c-Myc in response to proteasome inhibition. Proc Natl Acad Sci USA 104: 19488-19493.
66. Nilsson JA, Cleveland JL. (2003). Myc pathways provoking cell suicide and cancer. Oncogene 22: 9007-9021.
67. Oster SK, Ho CS, Soucie EL, Penn LZ. (2002). The Myc oncogene: marvelously complex. Adv Cancer Res 84: 81-154.
68. Oster SK, Mao DY, Kennedy J, Penn LZ. (2003). Functional analysis of the N-terminal domain of the Myc oncoprotein. Oncogene 22: 1998-2010.
69. Patel JH, McMahon SB. (2006). Targeting of Miz-1 is essential for Myc-mediated apoptosis. J Biol Chem 281: 3283-3289.
70. Patel JH, McMahon SB. (2007). BCL2 is a downstream effector of MIZ-1 essential for blocking c-Myc-induced apoptosis. J Biol Chem 282: 5-13.
71. Pauklin S, Kristjuhan A, maimets T, Jaks V. (2005). ART and ATM/ATR cooperate in p53-mediated apoptosis upon oncogenic stress. Biochem Biophys Res Commun 334: 386-394.
72. Pusapati RV, Rounbehler RJ, Hong S, Powers JT, Yan M, Kiguchi K et al. (2006). ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc Natl Acad Sci USA 103: 1446-1451.
73. Ricci MS, Jin Z, Dews M, Yu D, Thomas-Tikhonenko A, Dicker DT et al. (2004). Direct repression of FLIP expression by c-Myc is a major determinant of TRAIL sensitivity. Mol Cell Biol 24: 8541-8555.
74. Ricci MS, Kim SH, Ogi K, Plastaras JP, Ling J, Wang W et al. (2007). Reduction of TRAIL-induced Mcl-1 and cIAP2 by c-Myc or sorafenib sensitizes resistant human cancer cells to TRAIL-induced death. Cancer Cell 12: 66-80.
75. Rottman S, Luscher B. (2006). The mad side of the max network: antagonizing the function of myc and more. Curr Top Microbiol Immunol 302: 63-122.
76. Sakamuro D, Eviner V, Elliott KJ, Showe L, White E, Prendergast GC. (1995). c-Myc induces apoptosis in epithelial cells by both p53-dependent and p53-independent mechanisms. Oncogene 11: 2411-2418.
77. Sargent LM, Sanderson ND, Thorgeirsson SS. (1996). Ploidy and karyotypic alterations associated with early events in the development of hepatocarcinogenesis in transgenic mice harboring c-Myc and transforming growth factor alpha transgenes. Cancer Res 56: 2137-2142.
78. Sarker D, Fisher PB. (2006). Regulation of Myc function by ARF: checkpoint for Myc-induced oncogenesis. Cancer Biol Ther 5: 693-695.
79. Schmitt CA, McCurrach ME, De Stanchina E, Wallace-Brodeur RR, Lowe SW. (1999). INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev 13: 2670-2677.
80. Schulze-Bergkamen H, Brenner D, Krueger A, Suess D, Fas SC, Frey CR et al. (2004). Hepatocyte growth factor induces Mcl-1 in primary human hepatocytes and inhibits CD95-mediated apoptosis via Akt. Hepatology 39: 645-654.
81. Seoane J, Le HV, Massague J. (2002). Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419: 729-734.
82. Shi Y, Glynn JM, Guilbert WJ, Cotter TG, Bissonnette RP, Green DR. (1992). Role for c-Myc in activation-induced apoptotic cell death in T cell hybridomas. Science 257: 212-214.
83. Spencer CA, Groudine M. (1991). Control of c-Myc regulation in normal and neoplastic cells. Adv Cancer Res 56: 1-48.
84. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM et al. (2002). c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9: 1031-1044.
85. Vairapandi M, Balliet AG, Fornace A, Hoffman B, Liebermann DA. (1996). The differentiation primary response gene MyD118, related to Gadd45, encodes for a nuclear protein which interacts with PCNA and p21. Oncogene 12: 2579-2594.
86. Vesely DL, Hoffman B, Liebermann DA. (2007). Phosphatidylinositol 3-kinase/Akt signaling mediates interleukin-6 protection against p53-induced apoptosis in M1 myeloid leukemic cells. Oncogene 26: 3041-3050.
87. Vousden KH. (2002). Switching from life to death: the Miz-ing link between Myc and p53. Cancer Cell 2: 351-352.
88. Wagner AJ, Kokontis JM, Hay N. (1994). Myc-mediated apoptosis requires wild-type p53 in a manner independent of cell cycle arrest and the ability of p53 to induce p21waf1/cip1. Genes Dev 8: 2817-2830.
89. Wang Y, Engels IH, Knee DA, Nasoff M, Deveraux QL, Quon KC. (2004). Synthetic lethal targeting of Myc by activation of the DR5 death receptor pathway. Cancer Cell 5: 501-512.
90. Wu S, Cetinkaya C, Munoz-Alonso MJ, von der Lehr N, Bahram F, Beuger V et al. (2003). Myc represses differentiation-induced p21CIP1 expression via Miz-1-dependent interaction with the p21 core promoter. Oncogene 22: 351-360.
91. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ et al. (1998). Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 12: 2424-2433.