MUC1 oncoprotein blocks death receptor-mediated apoptosis by inhibiting recruitment of caspase-8

Cancer Research

Volumn 68, Issue 15, 2008, Pages 6136-6144

  Agata, Naoki ^a   Ahmad, Rehan ^a   Kawano, Takeshi ^a   Raina, Deepak ^a,b   Kharbanda, Surender ^a,b   Kufe, Donald ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Department of Genus Oncology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; DEATH RECEPTOR; FAS LIGAND; MUCIN 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; CA 15-3 ANTIGEN; MUC1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CANCER CELL; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; DRUG ANTAGONISM; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

APOPTOSIS; BASE SEQUENCE; CA-15-3 ANTIGEN; CASPASE 8; CELL LINE, TUMOR; ENZYME ACTIVATION; HUMANS; RECEPTORS, DEATH DOMAIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 51049090388     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0464     Document Type: Article

References (52)

1. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998;281:1305-8.
2. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003;114:181-90.
3. Schneider-Brachert W, Tchikov V, Neumeyer J, et al. Compartmentalization of TNF receptor 1 signaling: internalized TNF receptosomes as death signaling vesicles. Immunity 2004;21:415-28.
4. Boldin M, Goncharov T, Goltsev Y, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell-death. Cell 1996;85:803-15.
5. Muzio M, Chinnaiyan AM, Kischkel FC, et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996;85:817-27.
6. Stennicke H, Jurgenmeier J, Shin H, et al. Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 1998;273:27084-90.
7. Li H, Zhu H, Xu C-j, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the fas pathway of apotosis. Cell 1998;94:491-501.
8. Luo X, Budiharjo H, Zou H, Slauhter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481-90.
9. Scaffidi C, Kirchhoff S, Krammer PH, Peter ME. Apoptosis signaling in lymphocytes. Curr Opin Immunol 1999;11:277-85.
10. Kufe D, Inghirami G, Abe M, et al. Differential reactivity of a novel monoclonal antibody (DF3) with human malignant versus benign breast tumors. Hybridoma 1984;3:223-32.
11. Ligtenberg MJ, Kruijshaar L, Buijs F, et al. Cell-associated episialin is a complex containing two proteins derived from a common precursor. J Biol Chem 1992;267:6171-7.
12. Macao B, Johansson DG, Hansson GC, Hard T. Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 2006;13:71-6.
13. Levitin F, Stern O, Weiss M, et al. The MUC1 SEA module is a self-cleaving domain. J Biol Chem 2005; 280:33374-86.
14. Gendler S, Taylor-Papadimitriou J, Duhig T, Rothbard J, Burchell JA. A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 1988;263:12820-3.
15. Siddiqui J, Abe M, Hayes D, et al. Isolation and sequencing of a cDNA coding for the human DF3 breast carcinoma-associated antigen. Proc Natl Acad Sci U S A 1988;85:2320-3.
16. Li Y, Liu D, Chen D, Kharbanda S, Kufe D. Human DF3/MUC1 carcinoma-associated protein functions as an oncogene. Oncogene 2003;22:6107-10.
17. Li Y, Yu W-H, Ren J, et al. Heregulin targets γ-catenin to the nucleolus by a mechanism dependent on the DF3/MUC1 protein. Mol Cancer Res 2003;1:765-75.
18. Wei X, Xu H, Kufe D. Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer Cell 2005;7:167-78.
19. Wei X, Xu H, Kufe D. MUC1 oncoprotein stabilizes and activates estrogen receptor α. Mol Cell 2006;21: 295-305.
20. Huang L, Chen D, Liu D, et al. MUC1 oncoprotein blocks GSK3β-mediated phosphorylation and degradation of β-catenin. Cancer Res 2005;65:10413-22.
21. Wen Y, Caffrey T, Wheelock M, Johnson K, Hollingsworth M. Nuclear association of the cytoplasmic tail of MUC1 and β-catenin. J Biol Chem 2003;278:38029-39.
22. Ren J, Agata N, Chen D, et al. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anti-cancer agents. Cancer Cell 2004;5:163-75.
23. Ren J, Bharti A, Raina D, et al. MUC1 oncoprotein is targeted to mitochondria by heregulin-induced activation of c-Src and the molecular chaperone HSP90. Oncogene 2006;25:20-31.
24. Ren J, Raina D, Chen W, et al. MUC1 oncoprotein functions in activation of fibroblast growth factor receptor signaling. Mol Cancer Res 2006;4:873-83.
25. Merlo G, Siddiqui J, Cropp C, et al. DF3 tumor-associated antigen gene is located in a region on chromosome 1q frequently altered in primary human breast cancer. Cancer Res 1989;49:6966-71.
26. Li Y, Kuwahara H, Ren J, Wen G, Kufe D. The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3β and β-catenin. J Biol Chem 2001;276:6061-4.
27. Li Y, Bharti A, Chen D, Gong J, Kufe D. Interaction of glycogen synthase kinase 3β with the DF3/MUC1 carcinoma-associated antigen and β-catenin. Mol Cell Biol 1998;18:7216-24.
28. Ren J, Li Y, Kufe D. Protein kinase C δ regulates function of the DF3/MUC1 carcinoma antigen in β-catenin signaling. J Biol Chem 2002;277:17616-22.
29. Raina D, Ahmad R, Kumar S, et al. MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J 2006;25:3774-83.
30. Yamamoto M, Bharti A, Li Y, Kufe D. Interaction of the DF3/MUC1 breast carcinoma-associated antigen and β-catenin in cell adhesion. J Biol Chem 1997;272: 12492-4.
31. Ahmad R, Raina D, Trivedi V, et al. MUC1 oncoprotein activates the IκB kinase β complex and constitutive NF-κB signaling. Nat Cell Biol 2007;9:1419-27.
32. Yin L, Kufe D. Human MUC1 carcinoma antigen regulates intracellular oxidant levels and the apoptotic response to oxidative stress. J Biol Chem 2003;278:35458-64.
33. Yin L, Huang L, Kufe D. MUC1 oncoprotein activates the FOXO3a transcription factor in a survival response to oxidative stress. J Biol Chem 2004;279:45721-7.
34. Yin L, Kharbanda S, Kufe D. Mucin 1 oncoprotein blocks hypoxia-inducible factor 1α activation in a survival response to hypoxia. J Biol Chem 2007;282:257-66.
35. Bodmer JL, Holler N, Reynard S, et al. TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat Cell Biol 2000;2:241-3.
36. Scaffidi C, Volkland J, Blomberg I, et al. Phosphorylation of FADD/MORT1 at serine 194 and association with a 70-kDa cell cycle-regulated protein kinase. J Immunol 2000;164:1236-42.
37. Soule HD, Maloney TM, Wolman SR, et al. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 1990;50:6075-86.
38. Muthuswamy SK, Li D, Lelievre S, Bissell MJ, Brugge JS. ErbB2, but not ErbB1, reinitiates proliferation and induces luminal repopulation in epithelial acini. Nat Cell Biol 2001;3:785-92.
39. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol 2007;39:1462-75.
40. Chaturvedi R, Srivastava RK, Hisatsune A, et al. Augmentation of Fas ligand-induced apoptosis by MUC1 mucin. Int J Oncol 2005;26:1169-76.
41. Han DK, Chaudhary PM, Wright ME, et al. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclXL and initiates cell death. Proc Natl Acad Sci U S A 1997;94:11333-8.
42. Xu G, Cirilli M, Huang Y, et al. Covalent inhibition revealed by the crystal structure of the caspase-8/p35 complex. Nature 2001;410:494-7.
43. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997;326:1-16.
44. Budd RC, Yeh WC, Tschopp J. cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 2006;6:196-204.
45. Kreuz S, Siegmund D, Rumpf JJ, et al. NFκB activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J Cell Biol 2004;166:369-80.
46. Su H, Bidere N, Zheng L, et al. Requirement for caspase-8 in NF-κB activation by antigen receptor. Science 2005;307:1465-8.
47. Park SM, Schickel R, Peter ME. Nonapoptotic functions of FADD-binding death receptors and their signaling molecules. Curr Opin Cell Biol 2005;17:610-6.
48. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997;388: 190-5.
49. Srinivasula SM, Ahmad M, Ottilie S, et al. FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J Biol Chem 1997;272: 18542-5.
50. Goltsev YV, Kovalenko AV, Arnold E, et al. CASH, a novel caspase homologue with death effector domains. J Biol Chem 1997;272:19641-4.
51. Dyomin VG, Palanisamy N, Lloyd KO, et al. MUC1 is activated in a B-cell lymphoma by the t(1;14)(q21;q32) translocation and is rearranged and amplified in B-cell lymphoma subsets. Blood 2000;95: 2666-71.
52. Brossart P, Schneider A, Dill P, et al. The epithelial tumor antigen MUC1 is expressed in hematological malignancies and is recognized by MUC1-specific cytotoxic T-lymphocytes. Cancer Res 2001;29:6846-50.