Granzyme H induces cell death primarily via a Bcl-2-sensitive mitochondrial cell death pathway that does not require direct Bid activation

Molecular Immunology

Volumn 54, Issue 3-4, 2013, Pages 309-318

  Ewen, Catherine L ^a,b   Kane, Kevin P ^a   Bleackley, R Chris ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; Bcl 2 proteins; Caspases; DFF45; Granzymes

Indexed keywords

APOPTOSOME; BCL2 RELATED PROTEIN A1; CASPASE 3; FAS ANTIGEN; GRANZYME; PROTEIN BID;

APOPTOSIS; ARTICLE; CELL DEATH; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DNA DAMAGE; HUMAN; HUMAN CELL; IMMUNE EVASION; MITOCHONDRION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 84872740551     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.12.020     Document Type: Article

References (58)

1. Andrade F., Fellows E., Jenne D.E., Rosen A., Young C.S. Granzyme H destroys the function of critical adenoviral proteins required for viral DNA replication and granzyme B inhibition. EMBO Journal 2007, 26:2148-2157.
2. Anthony D.A., Andrews D.M., Chow M., Watt S.V., House C., Akira S., Bird P.I., Trapani J.A., Smyth M.J. A role for granzyme M in TLR4-driven inflammation and endotoxicosis. Journal of Immunology 2010, 185:1794-1803.
3. Barry M., Bleackley R.C. Cytotoxic T lymphocytes: all roads lead to death. Nature Reviews Immunology 2002, 2:401-409.
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. Molecular and Cellular Biology 2000, 20:3781-3794.
5. Boldin M.P., Goncharov T.M., Goltsev Y.V., Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996, 85:803-815.
6. Bovenschen N., de Koning P.J., Quadir R., Broekhuizen R., Damen J.M., Froelich C.J., Slijper M., Kummer J.A. NK cell protease granzyme M targets alpha-tubulin and disorganizes the microtubule network. Journal of Immunology 2008, 180:8184-8191.
7. Bratke K., Kuepper M., Bade B., Virchow J.C., Luttmann W. Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. European Journal of Immunology 2005, 35:2608-2616.
8. Brenner D., Mak T.W. Mitochondrial cell death effectors. Current Opinion in Cell Biology 2009, 21:871-877.
9. Chipuk J.E., Green D.R. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization?. Trends in Cell Biology 2008, 18:157-164.
10. Chowdhury D., Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annual Review of Immunology 2008, 26:389-420.
11. Chowdhury I., Tharakan B., Bhat G.K. Caspases - an update. Comparative Biochemistry and Physiology. Part B: Biochemistry and Molecular Biology 2008, 151:10-27.
12. Darmon A.J., Ley T.J., Nicholson D.W., Bleackley R.C. Cleavage of CPP32 by granzyme B represents a critical role for granzyme B in the induction of target cell DNA fragmentation. Journal of Biological Chemistry 1996, 271:21709-21712.
13. Darmon A.J., Nicholson D.W., Bleackley R.C. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 1995, 377:446-448.
14. 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 and Differentiation 2000, 7:973-983.
15. Fellows E., Gil-Parrado S., Jenne D.E., Kurschus F.C. Natural killer cell-derived human granzyme H induces an alternative, caspase-independent cell-death program. Blood 2007, 110:544-552.
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. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:7464-7469.
17. Goping I.S., Barry M., Liston P., Sawchuk T., Constantinescu G., Michalak K.M., Shostak I., Roberts D.L., Hunter A.M., Korneluk R., Bleackley R.C. Granzyme B-induced apoptosis requires both direct caspase activation and relief of caspase inhibition. Immunity 2003, 18:355-365.
18. Guo Y., Chen J., Shi L., Fan Z. Valosin-containing protein cleavage by granzyme K accelerates an endoplasmic reticulum stress leading to caspase-independent cytotoxicity of target tumor cells. Journal of Immunology 2010, 185:5348-5359.
19. Guo Y., Chen J., Zhao T., Fan Z. Granzyme K degrades the redox/DNA repair enzyme Ape1 to trigger oxidative stress of target cells leading to cytotoxicity. Molecular Immunology 2008, 45:2225-2235.
20. Han J., Goldstein L.A., Gastman B.R., Rabinovitz A., Wang G.Q., Fang B., Rabinowich H. Differential involvement of Bax and Bak in TRAIL-mediated apoptosis of leukemic T cells. Leukemia 2004, 18:1671-1680.
21. 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. Journal of Immunology 1999, 163:4683-4693.
22. 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. Journal of Experimental Medicine 2000, 192:1391-1402.
23. Hou Q., Zhao T., Zhang H., Lu H., Zhang Q., Sun L., Fan Z. Granzyme H induces apoptosis of target tumor cells characterized by DNA fragmentation and Bid-dependent mitochondrial damage. Molecular Immunology 2008, 45:1044-1055.
24. Hu D., Liu S., Shi L., Li C., Wu L., Fan Z. Cleavage of survivin by Granzyme M triggers degradation of the survivin-X-linked inhibitor of apoptosis protein (XIAP) complex to free caspase activity leading to cytolysis of target tumor cells. Journal of Biological Chemistry 2010, 285:18326-18335.
25. Joeckel L.T., Wallich R., Martin P., Sanchez-Martinez D., Weber F.C., Martin S.F., Borner C., Pardo J., Froelich C., Simon M.M. Mouse granzyme K has pro-inflammatory potential. Cell Death and Differentiation 2011, 18:1112-1119.
26. Johnson H., Scorrano L., Korsmeyer S.J., Ley T.J. Cell death induced by granzyme C. Blood 2003, 101:3093-3101.
27. Kagi D., Vignaux F., Ledermann B., Burki K., Depraetere V., Nagata S., Hengartner H., Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994, 265:528-530.
28. Kelly J.M., Waterhouse N.J., Cretney E., Browne K.A., Ellis S., Trapani J.A., Smyth M.J. Granzyme M mediates a novel form of perforin-dependent cell death. Journal of Biological Chemistry 2004, 279:22236-22242.
29. Kroemer G., Galluzzi L., Vandenabeele P., Abrams J., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., El-Deiry W.S., Golstein P., Green D.R., Hengartner M., Knight R.A., Kumar S., Lipton S.A., Malorni W., Nunez G., Peter M.E., Tschopp J., Yuan J., Piacentini M., Zhivotovsky B., Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death and Differentiation 2009, 16:3-11.
30. 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 1998, 94:491-501.
31. Lomonosova E., Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene 2008, 27(Suppl. 1):S2-S19.
32. Lowin B., Hahne M., Mattmann C., Tschopp J. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994, 370:650-652.
33. Lu H., Hou Q., Zhao T., Zhang H., Zhang Q., Wu L., Fan Z. Granzyme M directly cleaves inhibitor of caspase-activated DNase (CAD) to unleash CAD leading to DNA fragmentation. Journal of Immunology 2006, 177:1171-1178.
34. 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.
35. Mahrus S., Kisiel W., Craik C.S. Granzyme M is a regulatory protease that inactivates proteinase inhibitor 9, an endogenous inhibitor of granzyme B. Journal of Biological Chemistry 2004, 279:54275-54282.
36. Martinvalet D., Dykxhoorn D.M., Ferrini R., Lieberman J. Granzyme A cleaves a mitochondrial complex I protein to initiate caspase-independent cell death. Cell 2008, 133:681-692.
37. Meier M., Kwong P.C., Fregeau C.J., Atkinson E.A., Burrington M., Ehrman N., Sorensen O., Lin C.C., Wilkins J., Bleackley R.C. Cloning of a gene that encodes a new member of the human cytotoxic cell protease family. Biochemistry 1990, 29:4042-4049.
38. Muzio M., Chinnaiyan A.M., Kischkel F.C., O'Rourke K., Shevchenko A., Ni J., Scaffidi C., Bretz J.D., Zhang M., Gentz R., Mann M., Krammer P.H., Peter M.E., Dixit V.M. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death--inducing signaling complex. Cell 1996, 85:817-827.
39. Nakajima H., Park H.L., Henkart P.A. Synergistic roles of granzymes A and B in mediating target cell death by rat basophilic leukemia mast cell tumors also expressing cytolysin/perforin. Journal of Experimental Medicine 1995, 181:1037-1046.
40. Pardo J., Simon M.M., Froelich C.J. Granzyme A is a proinflammatory protease. Blood 2009, 114:3968. (author reply 3969-3970).
41. Pham C.T., Ley T.J. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:8627-8632.
42. Pinkoski M.J., Waterhouse N.J., Heibein J.A., Wolf B.B., Kuwana T., Goldstein J.C., Newmeyer D.D., Bleackley R.C., Green D.R. Granzyme B-mediated apoptosis proceeds predominantly through a Bcl-2-inhibitable mitochondrial pathway. Journal of Biological Chemistry 2001, 276:12060-12067.
43. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 1998, 391:96-99.
44. Sayers T.J., Brooks A.D., Ward J.M., Hoshino T., Bere W.E., Wiegand G.W., Kelly J.M., Smyth M.J. The restricted expression of granzyme M in human lymphocytes. Journal of Immunology 2001, 166:765-771.
45. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO Journal 1998, 17:1675-1687.
46. Sedelies K.A., Sayers T.J., Edwards K.M., Chen W., Pellicci D.G., Godfrey D.I., Trapani J.A. Discordant regulation of granzyme H and granzyme B expression in human lymphocytes. Journal of Biological Chemistry 2004, 279:26581-26587.
47. Sharif-Askari E., Alam A., Rheaume E., Beresford P.J., Scotto C., Sharma K., Lee D., DeWolf W.E., Nuttall M.E., Lieberman J., Sekaly R.P. Direct cleavage of the human DNA fragmentation factor-45 by granzyme B induces caspase-activated DNase release and DNA fragmentation. EMBO Journal 2001, 20:3101-3113.
48. Shi L., Wu L., Wang S., Fan Z. Granzyme F induces a novel death pathway characterized by Bid-independent cytochrome c release without caspase activation. Cell Death and Differentiation 2009, 16:1694-1706.
49. 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. Journal of Experimental Medicine 2000, 192:1403-1414.
50. Sutton V.R., Wowk M.E., 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.
51. Thomas D.A., Du C., Xu M., Wang X., Ley T.J. DFF45/ICAD can be directly processed by granzyme B during the induction of apoptosis. Immunity 2000, 12:621-632.
52. 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. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:14985-14990.
53. Veugelers K., Motyka B., Goping I.S., Shostak I., Sawchuk T., Bleackley R.C. Granule-mediated killing by granzyme B and perforin requires a mannose 6-phosphate receptor and is augmented by cell surface heparan sulfate. Molecular Biology of the Cell 2006, 17:623-633.
54. Wang S., Xia P., Shi L., Fan Z. FADD cleavage by NK cell granzyme M enhances its self-association to facilitate procaspase-8 recruitment for auto-processing leading to caspase cascade. Cell Death and Differentiation 2012, 19:605-615.
55. Waterhouse N.J., Sedelies K.A., Browne K.A., Wowk M.E., Newbold A., Sutton V.R., Clarke C.J., Oliaro J., Lindemann R.K., Bird P.I., Johnstone R.W., Trapani J.A. A central role for Bid in granzyme B-induced apoptosis. Journal of Biological Chemistry 2005, 280:4476-4482.
56. Waterhouse N.J., Trapani J.A. A new quantitative assay for cytochrome c release in apoptotic cells. Cell Death and Differentiation 2003, 10:853-855.
57. Zhao T., Zhang H., Guo Y., Fan Z. Granzyme K directly processes bid to release cytochrome c and endonuclease G leading to mitochondria-dependent cell death. Journal of Biological Chemistry 2007, 282:12104-12111.
58. Zhao T., Zhang H., Guo Y., Zhang Q., Hua G., Lu H., Hou Q., Liu H., Fan Z. Granzyme K cleaves the nucleosome assembly protein SET to induce single-stranded DNA nicks of target cells. Cell Death and Differentiation 2007, 14:489-499.