Granzyme B-activated p53 interacts with Bcl-2 to promote cytotoxic lymphocyte-mediated apoptosis

Journal of Immunology

Volumn 194, Issue 1, 2015, Pages 418-428

  Safta, Thouraya Ben ^a,b,c   Ziani, Linda ^a,b,c   Favre, Loetitia ^a,b,c   Lamendour, Lucille ^a,b,c   Gros, Gwendoline ^a,b,c   Mami Chouaib, Fathia ^a,b,c   Martinvalet, Denis ^d   Chouaib, Salem ^a,b,c   Thiery, Jerome ^a,b,c  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYTOCHROME C; GRANZYME B; PROCASPASE 3; PROCASPASE 9; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEIN P53; BAX PROTEIN, HUMAN; BENZOTHIAZOLE DERIVATIVE; BID PROTEIN, HUMAN; GRANZYME; GZMB PROTEIN, HUMAN; PIFITHRIN; SMALL INTERFERING RNA; TOLUENE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL PERMEABILITY; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CYTOTOXIC T LYMPHOCYTE; GENETICS; IMMUNOLOGY; MCF 7 CELL LINE; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NATURAL KILLER CELL; RNA INTERFERENCE; SECRETION (PROCESS); TUMOR CELL LINE;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BENZOTHIAZOLES; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASE 3; CELL LINE, TUMOR; CYTOCHROMES C; ENZYME ACTIVATION; GRANZYMES; HUMANS; KILLER CELLS, NATURAL; MCF-7 CELLS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; RNA INTERFERENCE; RNA, SMALL INTERFERING; T-LYMPHOCYTES, CYTOTOXIC; TOLUENE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84919663269     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401978     Document Type: Article

References (54)

1. Lieberman, J. 2003. The ABCs of granule-mediated cytotoxicity: New weapons in the arsenal. Nat. Rev. Immunol. 3: 361-370.
2. Chowdhury, D., and J. Lieberman. 2008. Death by a thousand cuts: Granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26: 389-420.
3. Anthony, D. A., D. M. Andrews, S. V. Watt, J. A. Trapani, and M. J. Smyth. 2010. Functional dissection of the granzyme family: Cell death and inflammation. Immunol. Rev. 235: 73-92.
4. Ewen, C. L., K. P. Kane, and R. C. Bleackley. 2012. A quarter century of granzymes. Cell Death Differ. 19: 28-35.
5. Thiery, J., D. Keefe, S. Boulant, E. Boucrot, M. Walch, D. Martinvalet, I. S. Goping, R. C. Bleackley, T. Kirchhausen, and J. Lieberman. 2011. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat. Immunol. 12: 770-777.
6. Thiery, J., D. Keefe, S. Saffarian, D. Martinvalet, M. Walch, E. Boucrot, T. Kirchhausen, and J. Lieberman. 2010. Perforin activates clathrin- and dynamin-dependent endocytosis, which is required for plasma membrane repair and delivery of granzyme B for granzyme-mediated apoptosis. Blood 115: 1582-1593.
7. Thiery, J., and J. Lieberman. 2014. Perforin: A key pore-forming protein for immune control of viruses and cancer. Subcell. Biochem. 80: 197-220.
8. Heibein, J. A., I. S. Goping, M. Barry, M. J. Pinkoski, G. C. Shore, D. R. Green, and R. C. Bleackley. 2000. Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members bid and Bax. J. Exp. Med. 192: 1391-1402.
9. Sutton, V. R., J. E. Davis, M. Cancilla, R. W. Johnstone, A. A. Ruefli, K. Sedelies, K. A. Browne, and J. A. Trapani. 2000. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J. Exp. Med. 192: 1403-1414.
10. Sutton, V. R., M. E. Wowk, M. Cancilla, and J. A. Trapani. 2003. Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors. Immunity 18: 319-329.
11. Wang, G. Q., E. Wieckowski, L. A. Goldstein, B. R. Gastman, A. Rabinovitz, A. Gambotto, S. Li, B. Fang, X. M. Yin, and H. Rabinowich. 2001. Resistance to granzyme B-mediated cytochrome c release in Bak-deficient cells. J. Exp. Med. 194: 1325-1337.
12. Pinkoski, M. J., N. J. Waterhouse, J. A. Heibein, B. B. Wolf, T. Kuwana, J. C. Goldstein, D. D. Newmeyer, R. C. Bleackley, and D. R. Green. 2001. Granzyme B-mediated apoptosis proceeds predominantly through a Bcl-2- inhibitable mitochondrial pathway. J. Biol. Chem. 276: 12060-12067.
13. Thomas, D. A., L. Scorrano, G. V. Putcha, S. J. Korsmeyer, and T. J. Ley. 2001. Granzyme B can cause mitochondrial depolarization and cell death in the absence of BID, BAX, and BAK. Proc. Natl. Acad. Sci. USA 98: 14985-14990.
14. Darmon, A. J., D. W. Nicholson, and R. C. Bleackley. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377: 446-448.
15. Sharif-Askari, E., A. Alam, E. Rhéaume, P. J. Beresford, C. Scotto, K. Sharma, D. Lee, W. E. DeWolf, M. E. Nuttall, J. Lieberman, and R. P. Sékaly. 2001. Direct cleavage of the human DNA fragmentation factor-45 by granzyme B induces caspase-Activated DNase release and DNA fragmentation. EMBO J. 20: 3101-3113.
16. Thomas, D. A., C. Du, M. Xu, X. Wang, and T. J. Ley. 2000. DFF45/ICAD can be directly processed by granzyme B during the induction of apoptosis. Immunity 12: 621-632.
17. Andrade, F., S. Roy, D. Nicholson, N. Thornberry, A. Rosen, and L. Casciola- Rosen. 1998. Granzyme B directly and efficiently cleaves several downstream caspase substrates: Implications for CTL-induced apoptosis. Immunity 8: 451-460.
18. Zhang, D., P. J. Beresford, A. H. Greenberg, and J. Lieberman. 2001. Granzymes A and B directly cleave lamins and disrupt the nuclear lamina during granulemediated cytolysis. Proc. Natl. Acad. Sci. USA 98: 5746-5751.
19. Goping, I. S., T. Sawchuk, D. A. Underhill, and R. C. Bleackley. 2006. Identification of alpha-tubulin as a granzyme B substrate during CTL-mediated apoptosis. J. Cell Sci. 119: 858-865.
20. Meslin, F., A. Hamaï, B. Mlecnik, F. Rosselli, C. Richon, A. Jalil, G. Wemhoff, J. Thiery, J. Galon, and S. Chouaib. 2011. hSMG-1 is a granzyme B-Associated stress-responsive protein kinase. J. Mol. Med. 89: 411-421.
21. Meslin, F., J. Thiery, C. Richon, A. Jalil, and S. Chouaib. 2007. Granzyme B-induced cell death involves induction of p53 tumor suppressor gene and its activation in tumor target cells. J. Biol. Chem. 282: 32991-32999.
22. el-Deiry, W. S., S. E. Kern, J. A. Pietenpol, K. W. Kinzler, and B. Vogelstein. 1992. Definition of a consensus binding site for p53. Nat. Genet. 1: 45-49.
23. Junttila, M. R., and G. I. Evan. 2009. p53-A Jack of all trades but master of none. Nat. Rev. Cancer 9: 821-829.
24. Moll, U. M., S. Wolff, D. Speidel, and W. Deppert. 2005. Transcriptionindependent pro-Apoptotic functions of p53. Curr. Opin. Cell Biol. 17: 631-636.
25. Galluzzi, L., E. Morselli, O. Kepp, I. Vitale, M. Pinti, and G. Kroemer. 2011. Mitochondrial liaisons of p53. Antioxid. Redox Signal. 15: 1691-1714.
26. Speidel, D. 2010. Transcription-independent p53 apoptosis: An alternative route to death. Trends Cell Biol. 20: 14-24.
27. Mihara, M., S. Erster, A. Zaika, O. Petrenko, T. Chittenden, P. Pancoska, and U. M. Moll. 2003. p53 has a direct apoptogenic role at the mitochondria. Mol. Cell 11: 577-590.
28. Chipuk, J. E., T. Kuwana, L. Bouchier-Hayes, N. M. Droin, D. D. Newmeyer, M. Schuler, and D. R. Green. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 303: 1010-1014.
29. Leu, J. I., P. Dumont, M. Hafey, M. E. Murphy, and D. L. George. 2004. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat. Cell Biol. 6: 443-450.
30. Yang, X. H., T. L. Sladek, X. Liu, B. R. Butler, C. J. Froelich, and A. D. Thor. 2001. Reconstitution of caspase 3 sensitizes MCF-7 breast cancer cells to doxorubicin- and etoposide-induced apoptosis. Cancer Res. 61: 348-354.
31. Dufour, E., G. Carcelain, C. Gaudin, C. Flament, M. F. Avril, and F. Faure. 1997. Diversity of the cytotoxic melanoma-specific immune response: Some CTL clones recognize autologous fresh tumor cells and not tumor cell lines. J. Immunol. 158: 3787-3795.
32. Dorothée, G., H. Echchakir, B. Le Maux Chansac, I. Vergnon, F. El Hage, A. Moretta, A. Bensussan, S. Chouaib, and F. Mami-Chouaib. 2003. Functional and molecular characterization of a KIR3DL2/p140 expressing tumor-specific cytotoxic T lymphocyte clone infiltrating a human lung carcinoma. Oncogene 22: 7192-7198.
33. Thiery, J., M. Walch, D. K. Jensen, D. Martinvalet, and J. Lieberman. 2010. Isolation of cytotoxic T cell and NK granules and purification of their effector proteins. Curr. Protoc. Cell Biol. Chapter 3: Unit 3.37.
34. Kam, C. M., D. Hudig, and J. C. Powers. 2000. Granzymes (lymphocyte serine proteases): Characterization with natural and synthetic substrates and inhibitors. Biochim. Biophys. Acta 1477: 307-323.
35. Leers, M. P., W. Kölgen, V. Björklund, T. Bergman, G. Tribbick, B. Persson, P. Björklund, F. C. Ramaekers, B. Björklund, M. Nap, et al. 1999. Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis. J. Pathol. 187: 567-572.
36. Strom, E., S. Sathe, P. G. Komarov, O. B. Chernova, I. Pavlovska, I. Shyshynova, D. A. Bosykh, L. G. Burdelya, R. M. Macklis, R. Skaliter, et al. 2006. Smallmolecule inhibitor of p53 binding to mitochondria protects mice from gamma radiation. Nat. Chem. Biol. 2: 474-479.
37. Gudkov, A. V., and E. A. Komarova. 2005. Prospective therapeutic applications of p53 inhibitors. Biochem. Biophys. Res. Commun. 331: 726-736.
38. Hsu, Y. T., and R. J. Youle. 1997. Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272: 13829-13834.
39. Llambi, F., T. Moldoveanu, S. W. Tait, L. Bouchier-Hayes, J. Temirov, L. L. McCormick, C. P. Dillon, and D. R. Green. 2011. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell 44: 517-531.
40. Volkmann, N., F. M. Marassi, D. D. Newmeyer, and D. Hanein. 2014. The rheostat in the membrane: BCL-2 family proteins and apoptosis. Cell Death Differ. 21: 206-215.
41. Westphal, D., R. M. Kluck, and G. Dewson. 2014. Building blocks of the apoptotic pore: How Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ. 21: 196-205.
42. Cheng, E. H., M. C. Wei, S. Weiler, R. A. Flavell, T. W. Mak, T. Lindsten, and S. J. Korsmeyer. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8: 705-711.
43. Willis, S. N., L. Chen, G. Dewson, A. Wei, E. Naik, J. I. Fletcher, J. M. Adams, and D. C. Huang. 2005. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19: 1294-1305.
44. Sohn, D., V. Graupner, D. Neise, F. Essmann, K. Schulze-Osthoff, and R. U. Jänicke. 2009. Pifithrin-Alpha protects against DNA damage-induced apoptosis downstream of mitochondria independent of p53. Cell Death Differ. 16: 869-878.
45. Lovell, J. F., L. P. Billen, S. Bindner, A. Shamas-Din, C. Fradin, B. Leber, and D. W. Andrews. 2008. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135: 1074-1084.
46. Edlich, F., S. Banerjee, M. Suzuki, M. M. Cleland, D. Arnoult, C. Wang, A. Neutzner, N. Tjandra, and R. J. Youle. 2011. Bcl-x(L) retrotranslocates Bax from the mitochondria into the cytosol. Cell 145: 104-116.
47. Schellenberg, B., P. Wang, J. A. Keeble, R. Rodriguez-Enriquez, S. Walker, T. W. Owens, F. Foster, J. Tanianis-Hughes, K. Brennan, C. H. Streuli, and A. P. Gilmore. 2013. Bax exists in a dynamic equilibrium between the cytosol and mitochondria to control apoptotic priming. Mol. Cell 49: 959-971.
48. Billen, L. P., C. L. Kokoski, J. F. Lovell, B. Leber, and D. W. Andrews. 2008. Bcl-XL inhibits membrane permeabilization by competing with Bax. PLoS Biol. 6: E147.
49. Hagn, F., C. Klein, O. Demmer, N. Marchenko, A. Vaseva, U. M. Moll, and H. Kessler. 2010. BclxL changes conformation upon binding to wild-type but not mutant p53 DNA binding domain. J. Biol. Chem. 285: 3439-3450.
50. Sot, B., S. M. Freund, and A. R. Fersht. 2007. Comparative biophysical characterization of p53 with the pro-Apoptotic BAK and the anti-Apoptotic BCL-xL. J. Biol. Chem. 282: 29193-29200.
51. Petros, A. M., A. Gunasekera, N. Xu, E. T. Olejniczak, and S. W. Fesik. 2004. Defining the p53 DNA-binding domain/Bcl-x(L)-binding interface using NMR. FEBS Lett. 559: 171-174.
52. Tomita, Y., N. Marchenko, S. Erster, A. Nemajerova, A. Dehner, C. Klein, H. Pan, H. Kessler, P. Pancoska, and U. M. Moll. 2006. WT p53, but not tumorderived mutants, bind to Bcl2 via the DNA binding domain and induce mitochondrial permeabilization. J. Biol. Chem. 281: 8600-8606.
53. Cristofanon, S., and S. Fulda. 2012. ABT-737 promotes tBid mitochondrial accumulation to enhance TRAIL-induced apoptosis in glioblastoma cells. Cell Death Dis. 3: E432.
54. Sutton, V. R., K. Sedelies, G. Dewson, M. E. Christensen, P. I. Bird, R. W. Johnstone, R. M. Kluck, J. A. Trapani, and N. J. Waterhouse. 2012. 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 Dis. 3: E344.