Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors

Immunity

Volumn 18, Issue 3, 2003, Pages 319-329

  Sutton, Vivien R ^a   Wowk, Michelle E ^a   Cancilla, Michael ^b,c   Trapani, Joseph A ^a,c  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

^c EXELIXIS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOCHROME C; GRANZYME B; MITOCHONDRIAL PROTEIN; PROTEIN BCL 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LINE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION;

EID: 0037341354     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(03)00050-5     Document Type: Article

References (64)

1. Adrain C., Creagh E.M., Martin S.J. Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 20:2001;6627-6636.
2. Alimonti J.B., Shi L., Baijal P.K., Greenberg A.H. Granzyme B induces BID-mediated cytochrome c release and mitochondrial permeability transition. J. Biol. Chem. 276:2001;6974-6982.
3. Andrade F., Roy S., Nicholson D., Thornberry N., Rosen A., Casciola-Rosen L. Granzyme B directly and efficiently cleaves several downstream caspase substrates. implications for CTL-induced apoptosis Immunity. 8:1998;451-460.
4. Barry M., Heibein J.A., Pinkoski M.J., Lee S.F., Moyer R.W., Green D.R., Bleackley R.C. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol. Cell. Biol. 20:2000;3781-3794.
5. Browne K.A., Blink E., Sutton V.R., Froelich C.J., Jans D.A., Trapani J.A. Cytosolic delivery of granzyme B by bacterial toxins. evidence that endosomal disruption, in addition to transmembrane pore formation, is an important function of perforin Mol. Cell. Biol. 19:1999;8604-8615.
6. Casciola-Rosen L., Andrade F., Ulanet D., Wong W.B., Rosen A. Cleavage by granzyme B is strongly predictive of autoantigen status. implications for initiation of autoimmunity J. Exp. Med. 190:1999;815-826.
7. Chai J., Du C., Wu J.W., Kyin S., Wang X., Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature. 406:2000;855-862.
8. Chai J., Shiozaki E., Srinivasula S.M., Wu Q., Datta P., Alnemri E.S., Shi Y., Dataa P. Structural basis of caspase-7 inhibition by XIAP. Cell. 104:2001;769-780.
9. Clem R.J., Miller L.K. Control of programmed cell death by the baculovirus genes p35 and iap. Mol. Cell. Biol. 14:1994;5212-5222.
10. Davis J.E., Sutton V.R., Smyth M.J., Trapani J.A. Dependence of granzyme B-mediated cell death on a pathway regulated by Bcl-2 or its viral homolog, BHRF1. Cell Death Differ. 7:2000;973-983.
11. Deveraux Q.L., Reed J.C. IAP family proteins - suppressors of apoptosis. Genes Dev. 13:1999;239-252.
12. Deveraux Q.L., Leo E., Stennicke H.R., Welsh K., Salvesen G.S., Reed J.C. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J. 18:1999;5242-5251.
13. 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. 102:2000;33-42.
14. Ekert P.G., Silke J., Hawkins C.J., Verhagen A.M., Vaux D.L. DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase 9. J. Cell Biol. 152:2001;483-490.
15. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:2000;929-935.
16. Fernandes-Alnemri T., Armstrong R.C., Krebs J., Srinivasula S.M., Wang L., Bullrich F., Fritz L.C., Trapani J.A., Tomaselli K.J., Litwack G., Alnemri E.S. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl. Acad. Sci. USA. 93:1996;7464-7469.
17. Grinberg M., Sarig R., Zaltsman Y., Frumkin D., Grammatikakis N., Reuveny E., Gross A. tBID homooligomerizes in the mitochondrial membrane to induce apoptosis. J. Biol. Chem. 277:2002;12237-12245.
18. Gross A., Yin X.M., Wang K., Wei M.C., Jockel J., Milliman C., Erdjument-Bromage H., Tempst P., Korsmeyer S.J. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274:1999;1156-1163.
19. Hegde R., Srinivasula S.M., Zhang Z., Wassell R., Mukattash R., Cilenti L., DuBois G., Lazebnik Y., Zervos A.S., Fernandes-Alnemri T., Alnemri E.S. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 277:2002;432-438.
20. Heibein J.A., Barry M., Motyka B., Bleackley R.C. Granzyme B-induced loss of mitochondrial inner membrane potential (Delta Psi m) and cytochrome c release are caspase independent. J. Immunol. 163:1999;4683-4693.
21. Heibein J.A., Goping I.S., Barry M., Pinkoski M.J., Shore G.C., Green D.R., Bleackley R.C. Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members bid and Bax. J. Exp. Med. 192:2000;1391-1402.
22. Heusel J.W., Wesselschmidt R.L., Shresta S., Russell J.H., Ley T.J. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell. 76:1994;977-987.
23. Huang D.C., Hahne M., Schroeter M., Frei K., Fontana A., Villunger A., Newton K., Tschopp J., Strasser A. Activation of Fas by FasL induces apoptosis by a mechanism that cannot be blocked by Bcl-2 or Bcl-x(L). Proc. Natl. Acad. Sci. USA. 96:1999;14871-14876.
24. Huang Y., Park Y.C., Rich R.L., Segal D., Myszka D.G., Wu H. Structural basis of caspase inhibition by XIAP. differential roles of the linker versus the BIR domain Cell. 104:2001;781-790.
25. Kagi D., Ledermann B., Burki K., Seiler P., Odermatt B., Olsen K.J., Podack E.R., Zinkernagel R.M., Hengartner H. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 369:1994;31-37.
26. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
27. Li L.Y., Luo X., Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 412:2001;95-99.
28. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts. requirement for dATP and cytochrome c Cell. 86:1996;147-157.
29. Liu Z., Sun C., Olejniczak E.T., Meadows R.P., Betz S.F., Oost T., Herrmann J., Wu J.C., Fesik S.W. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature. 408:2000;1004-1008.
30. 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. 94:1998;481-490.
31. Madesh M., Antonsson B., Srinivasula S.M., Alnemri E.S., Hajnoczky G. Rapid kinetics of tBid-induced cytochrome c and Smac/DIABLO release and mitochondrial depolarization. J. Biol. Chem. 277:2002;5651-5659.
32. Martin S.J., Amarante-Mendes G.P., Shi L., Chuang T.H., Casiano C.A., O'Brien G.A., Fitzgerald P., Tan E.M., Bokoch G.M., Greenberg A.H., Green D.R. The cytotoxic cell protease granzyme B initiates apoptosis in a cell-free system by proteolytic processing and activation of the ICE/CED-3 family protease, CPP32, via a novel two-step mechanism. EMBO J. 15:1996;2407-2416.
33. Martins L.M., Iaccarino I., Tenev T., Gschmeissner S., Totty N.F., Lemoine N.R., Savopoulos J., Gray C.W., Creasy C.L., Dingwall C., Downward J. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J. Biol. Chem. 277:2002;439-444.
34. Metkar S.S., Wang B., Aguilar-Santelises M., Raja S.M., Uhlin-Hansen L., Podack E., Trapani J.A., Froelich C.J. Cytotoxic cell granule-mediated apoptosis. perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation Immunity. 16:2002;417-428.
35. Mullbacher A., Hla R.T., Museteanu C., Simon M.M. Perforin is essential for control of ectromelia virus but not related poxviruses in mice. J. Virol. 73:1999;1665-1667. a.
36. Mullbacher A., Waring P., Tha Hla R., Tran T., Chin S., Stehle T., Museteanu C., Simon M.M. Granzymes are the essential downstream effector molecules for the control of primary virus infections by cytolytic leukocytes. Proc. Natl. Acad. Sci. USA. 96:1999;13950-13955. b.
37. Odake S., Kam C.M., Narasimhan L., Poe M., Blake J.T., Krahenbuhl O., Tschopp J., Powers J.C. Human and murine cytotoxic T lymphocyte serine proteases. subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins Biochemistry. 30:1991;2217-2227.
38. Parrish J., Li L., Klotz K., Ledwich D., Wang X., Xue D. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature. 412:2001;90-94.
39. Riedl S.J., Fuentes-Prior P., Renatus M., Kairies N., Krapp S., Huber R., Salvesen G.S., Bode W. Structural basis for the activation of human procaspase-7. Proc. Natl. Acad. Sci. USA. 98:2001;14790-14795.
40. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 391:1998;96-99.
41. Sarin A., Williams M.S., Alexander-Miller M.A., Berzofsky J.A., Zacharchuk C.M., Henkart P.A. Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity. 6:1997;209-215.
42. Schendel S.L., Azimov R., Pawlowski K., Godzik A., Kagan B.L., Reed J.C. Ion channel activity of the BH3 only Bcl-2 family member, BID. J. Biol. Chem. 274:1999;21932-21936.
43. Sharif-Askari, E., Alam, A., Rheaume, E., Beresford, P.J., Scotto, C., DeWolf, W.E., Nuttall, M.E., Lieberman, J., and Sekaly, R. (2001). Direct cleavage of the human DNA fragmentation factor-45 by granzyme B induces caspase-activated DNase release and DNA fragmentation. EMBO J. 20, 3101-3013.
44. Smyth M.J., Thia K.Y., Street S.E., MacGregor D., Godfrey D.I., Trapani J.A. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J. Exp. Med. 192:2000;755-760.
45. Srinivasula S.M., Datta P., Fan X.J., Fernandes-Alnemri T., Huang Z., Alnemri E.S. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J. Biol. Chem. 275:2000;36152-36157.
46. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., Lee R.A., Robbins P.D., Fernandes-Alnemri T., Shi Y., Alnemri E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature. 410:2001;112-116.
47. Stennicke H.R., Deveraux Q.L., Humke E.W., Reed J.C., Dixit V.M., Salvesen G.S. Caspase-9 can be activated without proteolytic processing. J. Biol. Chem. 274:1999;8359-8362.
48. Street S.E., Trapani J.A., MacGregor D., Smyth M.J. Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J. Exp. Med. 196:2002;129-134.
49. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M.et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-446.
50. Sutton V.R., Davis J.E., Cancilla M., Johnstone R.W., Ruefli A.A., Sedelies K., Browne K.A., Trapani J.A. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J. Exp. Med. 192:2000;1403-1414.
51. Sutton V.R., Vaux D.L., Trapani J.A. Bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J. Immunol. 158:1997;5783-5790.
52. Takahashi R., Deveraux Q., Tamm I., Welsh K., Assa-Munt N., Salvesen G.S., Reed J.C. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem. 273:1998;7787-7790.
53. Thomas D.A., Scorrano L., Putcha G.V., Korsmeyer S.J., Ley T.J. Granzyme B can cause mitochondrial depolarization and cell death in the absence of BID, BAX, and BAK. Proc. Natl. Acad. Sci. USA. 98:2001;14985-14990.
54. Trapani J.A., Browne K.A., Dawson M., Smyth M.J. Immunopurification of functional Asp-ase (natural killer cell granzyme B) using a monoclonal antibody. Biochem. Biophys. Res. Commun. 195:1993;910-920.
55. Trapani J.A., Jans D.A., Jans P.J., Smyth M.J., Browne K.A., Sutton V.R. Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perforin are caspase-dependent, but cell death is caspase-independent. J. Biol. Chem. 273:1998;27934-27938.
56. Trapani J.A., Davis J., Sutton V.R., Smyth M.J. Proapoptotic functions of cytotoxic lymphocyte granule constituents in vitro and in vivo. Curr. Opin. Immunol. 12:2000;323-329.
57. van den Broek M.E., Kagi D., Ossendorp F., Toes R., Vamvakas S., Lutz W.K., Melief C.J., Zinkernagel R.M., Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184:1996;1781-1790.
58. Van Loo G., Saelens X., Matthijssens F., Schotte P., Beyaert R., Declercq W., Vandenabeele P. Caspases are not localized in mitochondria during life or death. Cell Death Differ. 9:2002;1207-1211.
59. Verhagen A.M., Ekert P.G., Pakusch M., Silke J., Connolly L.M., Reid G.E., Moritz R.L., Simpson R.J., Vaux D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:2000;43-53.
60. Verhagen A.M., Silke J., Ekert P.G., Pakusch M., Kaufmann H., Connolly L.M., Day C.L., Tikoo A., Burke R., Wrobel C.et al. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 277:2002;445-454.
61. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., Korsmeyer S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14:2000;2060-2071.
62. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK. a requisite gateway to mitochondrial dysfunction and death Science. 292:2001;727-730.
63. Wu G., Chai J., Suber T.L., Wu J.W., Du C., Wang X., Shi Y. Structural basis of IAP recognition by Smac/DIABLO. Nature. 408:2000;1008-1012.
64. Yang X., Stennicke H.R., Wang B., Green D.R., Janicke R.U., Srinivasan A., Seth P., Salvesen G.S., Froelich C.J. Granzyme B mimics apical caspases. Description of a unified pathway for trans-activation of executioner caspase-3 and -7. J. Biol. Chem. 273:1998;34278-34283.