Granzyme B triggers a prolonged pressure to die in Bcl-2 overexpressing cells, defining a window of opportunity for effective treatment with ABT-737

Cell Death and Disease

Volumn 3, Issue 7, 2012, Pages

  Sutton, V R ^a,b   Sedelies, K ^a,b   Dewson, G ^b,c   Christensen, M E ^d   Bird, P I ^e   Johnstone, R W ^a,b,f   Kluck, R M ^b,c   Trapani, J A ^a,b,f   Waterhouse, N J ^d,g  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d MATER MEDICAL RESEARCH INSTITUTE   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f VICTORIAN COMPREHENSIVE CANCER CENTRE   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

ABT 737; apoptosis; Bcl 2; granzyme; lymphocyte; mitochondria

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; GRANZYME B; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; ABT-737; BIPHENYL DERIVATIVE; CYTOCHROME C; GRANZYME; NITROPHENOL; PIPERAZINE DERIVATIVE; SULFONAMIDE;

ARTICLE; CELL MEMBRANE PERMEABILITY; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL OUTER MEMBRANE PERMEABILIZATION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; APOPTOSIS; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECT; HELA CELL; IMMUNOLOGY; METABOLISM; MITOCHONDRION;

APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BIPHENYL COMPOUNDS; CELL MEMBRANE PERMEABILITY; CYTOCHROMES C; GRANZYMES; HELA CELLS; HUMANS; KILLER CELLS, NATURAL; MITOCHONDRIA; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; SULFONAMIDES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84864880328     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.73     Document Type: Article

References (37)

1. Waterhouse NJ, Trapani J.A. CTL: Caspases Terminate Life, but that's not the whole story. Tissue Antigens 2002; 59: 175-183.
2. Trapani JA, Sutton V.R. Granzyme B: pro-apoptotic, antiviral and antitumor functions. Curr Opin Immunol 2003; 15: 533-543.
3. Zitvogel L, Tesniere A, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol 2008; 8: 59-73.
4. Froelich CJ, Orth K, Turbov J, Seth P, Gottlieb R, Babior B et al. New paradigm for lymphocyte granule-mediated cytotoxicity. Target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis. J Biol Chem 1996; 271: 29073-29079.
5. Shi L, Mai S, Israels S, Browne K, Trapani JA, Greenberg A.H. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization. J Exp Med 1997; 185: 855-866.
6. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, Whisstock JC et al. The major human and mouse granzymes are structurally and functionally divergent. J Cell Biol 2006; 175: 619-630.
7. Sutton VR, Davis JE, Cancilla M, Johnstone RW, Ruefli AA, Sedelies K et al. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J Exp Med 2000; 192: 1403-1414.
8. Barry M, Heibein JA, Pinkoski MJ, Lee SF, Moyer RW, Green DR et al. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol Cell Biol 2000; 20: 3781-3794.
9. Pinkoski MJ, Waterhouse NJ, Heibein JA, Wolf BB, Kuwana T, Goldstein JC et al. Granzyme B-mediated apoptosis proceeds predominantly through a Bcl-2-inhibitable mitochondrial pathway. J Biol Chem 2001; 276: 12060-12067.
10. Alimonti JB, Shi L, Baijal PK, Greenberg AH. Granzyme B induces BID-mediated cytochrome c release and mitochondrial permeability transitionJ Biol Chem 2001; 276: 6974-6982.
11. 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.
12. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997; 275: 1132-1136.
13. Sutton VR, Vaux DL, Trapani J.A. Bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J Immunol 1997; 158: 5783-5790.
14. Sedelies KA, Ciccone A, Clarke CJ, Oliaro J, Sutton VR, Scott FL et al. Blocking granule-mediated death by primary human NK cells requires both protection of mitochondria and inhibition of caspase activity. Cell Death Differ 2008; 15: 708-717.
15. Sutton VR, Wowk ME, Cancilla M, Trapani J.A. Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors. Immunity 2003; 18: 319-329.
16. Lickliter JD, Cox J, McCarron J, Martinez NR, Schmidt CW, Lin H et al. Small-molecule Bcl-2 inhibitors sensitise tumour cells to immune-mediated destruction. Br J Cancer 2007; 96: 600-608.
17. Waterhouse NJ, Goldstein JC, von Ahsen O, Schuler M, Newmeyer DD, Green D.R. Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J Cell Biol 2001; 153: 319-328.
18. Waterhouse NJ, Sedelies KA, Sutton VR, Pinkoski MJ, Thia KY, Johnstone R et al. Functional dissociation of DeltaPsim and cytochrome c release defines the contribution of mitochondria upstream of caspase activation during granzyme B-induced apoptosis. Cell Death Differ 2006; 13: 607-618.
19. Kluck RM, Esposti MD, Perkins G, Renken C, Kuwana T, Bossy-Wetzel E et al. The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol. J Cell Biol 1999; 147: 809-822.
20. von Ahsen O, Renken C, Perkins G, Kluck RM, Bossy-Wetzel E, Newmeyer D.D. Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J Cell Biol 2000; 150: 1027-1036.
21. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S et al. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999; 144: 891-901.
22. Wei MC, Zong WX, Cheng EH, 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.
23. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer S.J. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 2001; 8: 705-711.
24. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams J.M. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005; 19: 1294-1305.
25. Ding J, Zhang Z, Roberts GJ, Falcone M, Miao Y, Shao Y et al. Bcl-2 and Bax interact via the BH1-3 groove-BH3 motif interface and a novel interface involving the BH4 motif. J Biol Chem 2010; 285: 28749-28763.
26. Dai H, Meng XW, Lee SH, Schneider PA, Kaufmann S.H. Context-dependent Bcl-2/Bak interactions regulate lymphoid cell apoptosis. J Biol Chem 2009; 284: 18311-18322.
27. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 2011; 44: 517-531.
28. Dewson G, Kratina T, Sim HW, Puthalakath H, Adams JM, Colman PM et al. To trigger apoptosis, Bak exposes its BH3 domain and homodimerizes via BH3:groove interactions. Mol Cell 2008; 30: 369-380.
29. Yecies D, Carlson NE, Deng J, Letai A. Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 2010; 115: 3304-3013.
30. Metkar SS, Wang B, Ebbs ML, Kim JH, Lee YJ, Raja SM et al. Granzyme B activates procaspase-3 which signals a mitochondrial amplification loop for maximal apoptosis. J Cell Biol 2003; 160: 875-885.
31. Breitschopf K, Zeiher AM, Dimmeler S. Ubiquitin-mediated degradation of the proapoptotic active form of bid. A functional consequence on apoptosis induction. J Biol Chem 2000; 275: 21648-21652.
32. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
33. Peng J, Tan C, Roberts GJ, Nikolaeva O, Zhang Z, Lapolla SM et al. tBid elicits a conformational alteration in membrane-bound Bcl-2 such that it inhibits Bax pore formation. J Biol Chem 2006; 281: 35802-35811.
34. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007; 315: 856-859.
35. Sun J, Bird CH, Buzza MS, McKee KE, Whisstock JC, Bird PI et al. Expression and purification of recombinant human granzyme B from Pichia pastoris. Biochem Biophys Res Commun 1999; 261: 251-255.
36. Bird CH, Sutton VR, Sun J, Hirst CE, Novak A, Kumar S et al. Selective regulation of apoptosis: the cytotoxic lymphocyte serpin proteinase inhibitor 9 protects against granzyme B-mediated apoptosis without perturbing the Fas cell death pathway. Mol Cell Biol 1998; 18: 6387-6398.
37. Kaufmann T, Tai L, Ekert PG, Huang DC, Norris F, Lindemann RK, Johnstone RW et al. The BH3-only protein bid is dispensable for DNA damage- and replicative stress-induced apoptosis or cell-cycle arrest. Cell 2007; 129: 423-433.