Smac/DIABLO release from mitochondria and XIAP inhibition are essential to limit clonogenicity of Type i tumor cells after TRAIL receptor stimulation

Cell Death and Differentiation

Volumn 17, Issue 10, 2010, Pages 1613-1623

  Maas, C ^a   Verbrugge, I ^a,b   De Vries, E ^a   Savich, G ^a,c   Van De Kooij, L W ^a   Tait, S W G ^a,d   Borst, J ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

death receptor; inhibitor of apoptosis proteins; mitochondria; TRAIL; type I

Indexed keywords

CASPASE 3; CASPASE 9; PROTEIN BCL 2; PROTEIN BID; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; X LINKED INHIBITOR OF APOPTOSIS;

ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL SURVIVAL; CELL TYPE; CLONOGENESIS; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; ENZYME INHIBITION; EXCITATION AND STIMULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN SECRETION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL;

APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASE 9; CELL LINE, TUMOR; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA INTERFERENCE; TNF-RELATED APOPTOSIS-INDUCING LIGAND; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 77956702972     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2010.39     Document Type: Article

References (40)

1. Peter ME, Krammer PH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ 2003; 10: 26-35.
2. Luo X, Budihardjo I, Zou H, Slaughter 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: 481-490.
3. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15: 2922-2933.
4. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli K et al. Two CD95 (APO-1/ Fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
5. Yin X-M, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B et al. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature 1999; 400: 886-891.
6. Strasser A, Harris AW, Huang DCS, Krammer PH, Cory S. Bcl-2 and fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J 1995; 14: 6136-6147.
7. L. Proc Natl Acad Sci USA 1999; 96: 14871-14876.
8. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DCS et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009; 460: 1035-1039.
9. Lacronique V, Mignon A, Fabre M, Violet B, Rouquet N, Molina T et al. Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 1996; 2: 80-86.
10. Barnhart BC, Alappat EC, Peter ME. The CD95 Type I/Type II model. Sem Immunol 2003; 15: 185-193.
11. Algeciras-Schimnich A, Pietras EM, Barnhart BC, Legembre P, Vijayan S, Holbeck SL et al. Two CD95 tumor classes with different sensitivities to anti-tumor drugs. Proc Natl Acad Sci USA 2003; 100: 11445-11450.
12. Albeck JG, Burke JM, Aldridge BB, Zhang M, Luaffneburger DA, Sorger PK. Quantitative analysis of pathways controlling extrinsic apoptosis in single cells. Mol Cell 2008; 30: 11-25.
13. Eckelmann BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006; 7: 988-994.
14. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
15. Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K, Takahasi R. A serine protease, HtrA2 is released from the mitochondria and interacts with XIAP, inducing cell death. Mol Cell 2001; 8: 613-621.
16. Ekert PG, Silke J, Hawkins CJ, Verhagen AM, Vaux DL. DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase-9. J Cell Biol 2001; 152: 483-490.
17. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J et al. A conserved XIAP interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001; 410: 112-116.
18. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J 1998; 17: 2215-2223.
19. Sun X-M, Bratton SB, Butterworth M, MacFarlane M, Cohen G. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J Biol Chem 2002; 277: 11345-11351.
20. Tait SWG, de Vries E, Maas C, Keller A, D'Santos C, Borst J. Apoptosis induction by Bid requires unconventional ubiquitination and degradation of its N-terminal fragment. J Cell Biol 2007; 179: 1453-1466.
21. Ganten TM, Haas TL, Sykora J, Stahl H, Sprick MR, Fas SC et al. Enhanced caspase-8 recruitment to and activation at the DISC is critical for sensitisation of human hepatocellular carcinoma cells to TRAIL-induced apoptosis by chemotherapeutic drugs. Cell Death Differ 2004; 11: S86-S96.
22. Berns K, Hijmans ME, Mullenders J, Brummelkamp TR, Velds A, Heimerikx M et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 2004; 428: 431-437.
23. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS et al. Differential requirement for Caspase 9 in apoptotic pathways in vivo. Cell 1998; 94: 339-352.
24. Chauhan D, Neri P, Velankar M, Podar K, Hideshima T, Fulciniti M et al. Targeting mitochondrial factor Smac/DIABLO as therapy for multiple myeloma (MM). Blood 2007; 109: 1220-1227.
25. Van de Craen M, Declercq W, Van den Brande I, Fiers W, Vandenabeele P. The proteolytic procaspase activation network: an in vitro analysis. Cell Death Differ 1999; 6: 1117-1124.
26. Han Z, Hendrickson EA, Bremner TA, Wyche JH. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J Biol Chem 1997; 272: 13432-13436.
27. Spencer S, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009; 459: 428-433.
28. Wei MC, Zong W-X, Cheng E, Lindsten T, Panoutsakopoulou V, Ross AJ et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
29. Lindsten T, Ross AJ, King A, Zong W-X, Rathmell JC, Shiels HA et al. The combined functions of proapoptotic Bcl-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol Cell 2000; 6: 1389-1399.
30. Weant AE, Michalek RD, Khan IU, Holbrook BC, Willingham MC, Grayson JM. Apoptosis regulators Bim and Fas function concurrently to control autoimmunity and CD8+ T cell contraction. Immunity 2008; 28: 218-230.
31. Cretney E, Takeda K, Yagita H, Galccum M, Peschon JJ, Smyth MK. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002; 168:1356-1361.
32. Grosse-Wilde A, Voloshanenko O, Bailey SL, Longton GM, Schaefer U, Csernok AI etal. TRAIL-R deficiency in mice enhances lymph node metastasis without affecting primary tumor development. J Clin Invest 2008; 118:100-110.
33. Ashkenazi A, Holland P, Eckhardt G. Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol 2008; 26: 3621-3630.
34. Kuida K, Haydar TF, Kuna C-Y, Gu Y, Taya C, Karasuyama H et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking Caspase-9. Cell1998; 94: 325-337.
35. Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R et al. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 1998; 94: 739-750.
36. Shawgo ME, Shelton SN, Robertson JD. Caspase-9 activation is not required for Fas-mediated apoptosis in Type II Jurkat cells. J Biol Chem 2009; 284: 33447-33455.
37. Li S, Zhao Y, He X, Kim T-H, Kuharsky DK, Rabinowich H etal. Relief of extrinsic pathway of inhibition by the Bid-dependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis. J Biol Chem 2002; 277: 26912-26920.
38. Ndozangue-Touriguine O, Sebbagh M, Merino D, Micheau O, Bertoglio J, Breard J. A mitochondrial block and expression of XIAP lead to resistance to TRAIL-induced apoptosis during progression to metastasis of a colon carcinoma. Oncogene 2008; 27: 6012-6022.
39. Varfolomeev E, Vucic D. Unexpected roles of c-IAPs in apoptotic and NF-KB signaling pathways. Cell Cycle 2008; 7:1511-1521.
40. Gaither A, Porter D, Yao Y, Borawski J, Yang G, Donovan J etal. A Smac mimetic rescue screen reveals roles for inhibitor of apoptosis proteins in tumor necrosis factor a signaling. Cancer Res 2007; 67:11493-11498.