Caspase-dependent inhibition of mousepox replication by gzmB

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Pardo, Julián ^a,b   Gálvez, Eva Ma ^c   Koskinen, Aulikki ^d   Simon, Markus M ^e   Lobigs, Mario ^d   Regner, Matthias ^d   Müllbacher, Arno ^d  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b FUNDACIÓN ARAID   (Spain)

^c INSTITUTO DE CARBOQUÍMICA   (Spain)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^e MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; CASPASE 7; GRANZYME A; GRANZYME B; PROTEIN BAK; PROTEIN BAX; PROTEIN BID; CALRETICULIN; GRANZYME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ECTROMELIA VIRUS; EMBRYO; ENZYME DEFICIENCY; ENZYME INHIBITION; EX VIVO STUDY; FIBROBLAST; MOUSE; MOUSEPOX; NONHUMAN; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS TITRATION; WILD TYPE; ANIMAL; C57BL MOUSE; CYTOTOXIC T LYMPHOCYTE; GENETICS; MALE; METABOLISM; TRANSGENIC MOUSE; VIROLOGY;

ECTROMELIA VIRUS; MUS;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CALRETICULIN; CASPASE 3; CASPASE 7; CASPASES; ECTROMELIA VIRUS; ECTROMELIA, INFECTIOUS; FIBROBLASTS; GRANZYMES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTES, CYTOTOXIC;

EID: 70449395448     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007512     Document Type: Article

References (61)

1. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284: 555-556.
2. Russell JH, Ley TJ (2002) Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 20: 323-370.
3. Rouvier E, Luciani MF, Golstein P (1993) Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity. J Exp Med 177: 195-200.
4. Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V, et al. (1994) Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265: 528-530.
5. Ashton-Rickardt PG (2005) The granule pathway of programmed cell death. Crit Rev Immunol 25: 161-182.
6. Bossi G, Griffiths GM (2005) CTL secretory lysosomes: biogenesis and secretion of a harmful organelle. Semin Immunol 17: 87-94.
7. Voskoboinik I, Smyth MJ, Trapani JA (2006) Perforin-mediated target-cell death and immune homeostasis. Nat Rev Immunol 6: 940-952.
8. Simon MM, Kramer MD (1994) Granzyme A. Methods Enzymol 244: 68-79.
9. Lieberman J, Fan Z (2003) Nuclear war: the granzyme A-bomb. Curr Opin Immunol 15: 553-559.
10. Trapani JA, Sutton VR (2003) Granzyme B: pro-apoptotic, antiviral and antitumor functions. Curr Opin Immunol 15: 533-543.
11. Tschopp J (1994) Granzyme B. Methods Enzymology 244: 80-87.
12. Kagi D, Ledermann B, Burki K, Seiler P, Odermatt B, et al. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369: 31-37.
13. Mullbacher A, Hla RT, Museteanu C, Simon MM (1999) Perforin is essential for control of ectromelia virus but not related poxviruses in mice. J Virol 73: 1665-1667.
14. Müllbacher A, Waring P, Hia RT, Tran T, Chin S, et al. (1999) Granzymes are the essential downstream effector molecules for the control of primary virus infections by cytolytic leukocytes. Proc Natl Acad Sci U S A 96: 13950-13955.
15. Pereira RA, Simon MM, Simmons A (2000) Granzyme A, a noncytolytic component of CD8(+) cell granules, restricts the spread of herpes simplex virus in the peripheral nervous systems of experimentally infected mice. J Virol 74: 1029-1032.
16. Riera L, Gariglio M, Valente G, Mullbacher A, Museteanu C, et al. (2000) Murine cytomegalovirus replication in salivary glands is controlled by both perforin and granzymes during acute infection. Eur J Immunol 30: 1350-1355.
17. Wang Y, Lobigs M, Lee E, Mullbacher A (2004) Exocytosis and Fas mediated cytolytic mechanisms exert protection from West Nile virus induced encephalitis in mice. Immunol Cell Biol 82: 170-173.
18. Pardo J, Balkow S, Anel A, Simon MM (2002) Granzymes are essential for natural killer cell-mediated and perf-facilitated tumor control. Eur J Immunol 32: 2881-2887.
19. Revell PA, Grossman WJ, Thomas DA, Cao X, Behl R, et al. (2005) Granzyme B and the downstream granzymes C and/or F are important for cytotoxic lymphocyte functions. J Immunol 174: 2124-2131.
20. Smyth MJ, Thia KY, Street SE, MacGregor D, Godfrey DI, et al. (2000) Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 192: 755-760.
21. van den Broek ME, Kagi D, Ossendorp F, Toes R, Vamvakas S, et al. (1996) Decreased tumor surveillance in perforin-deficient mice. J Exp Med 184: 1781-1790.
22. van den Broek MF, Kagi D, Zinkernagel RM, Hengartner H (1995) Perforin dependence of natural killer cell-mediated tumor control in vivo. Eur J Immunol 25: 3514-3516.
23. Turk B, Stoka V (2007) Protease signalling in cell death: caspases versus cysteine cathepsins. FEBS Lett 581: 2761-2767.
24. Chipuk JE, Green DR (2006) Dissecting p53-dependent apoptosis. Cell Death Differ 13: 994-1002.
25. Adams JM, Cory S (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26: 1324-1337.
26. Benedict CA, Norris PS, Ware CF (2002) To kill or be killed: viral evasion of apoptosis. Nat Immunol 3: 1013-1018.
27. Boya P, Roumier T, Andreau K, Gonzalez-Polo RA, Zamzami N, et al. (2003) Mitochondrion-targeted apoptosis regulators of viral origin. Biochem Biophys Res Commun 304: 575-581.
28. Callus BA, Vaux DL (2007) Caspase inhibitors: viral, cellular and chemical. Cell Death Differ 14: 73-78.
29. Dobbelstein M, Shenk T (1996) Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J Virol 70: 6479-6485.
30. Macen JL, Garner RS, Musy PY, Brooks MA, Turner PC, et al. (1996) Differential inhibition of the Fas- and granule-mediated cytolysis pathways by the orthopoxvirus cytokine response modifier A/SPI-2 and SPI-1 protein. Proc Natl Acad Sci U S A 93: 9108-9113.
31. Pickup DJ, Ink BS, Hu W, Ray CA, Joklik WK (1986) Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine proteases. Proc Natl Acad Sci U S A 83: 7698-7702.
32. Fischer SF, Ludwig H, Holzapfel J, Kvansakul M, Chen L, et al. (2006) Modified vaccinia virus Ankara protein F1L is a novel BH3-domain-binding protein and acts together with the early viral protein E3L to block virus-associated apoptosis. Cell Death Differ 13: 109-118.
33. Wasilenko ST, Banadyga L, Bond D, Barry M (2005) The vaccinia virus F1L protein interacts with the proapoptotic protein Bak and inhibits Bak activation. J Virol 79: 14031-14043.
34. Postigo A, Cross JR, Downward J, Way M (2006) Interaction of F1L with the BH3 domain of Bak is responsible for inhibiting vaccinia-induced apoptosis. Cell Death Differ.
35. Aoyagi M, Zhai D, Jin C, Aleshin AE, Stec B, et al. (2007) Vaccinia virus N1L protein resembles a B cell lymphoma-2 (Bcl-2) family protein. Protein Sci 16: 118-124.
36. Fenner F (1949) Mouse-pox; infectious ectromelia of mice; a review. J Immunol 63: 341-373.
37. Mullbacher A, Wallich R, Moyer RW, Simon MM (1999) Poxvirus-encoded serpins do not prevent cytolytic T cell-mediated recovery from primary infections. J Immunol 162: 7315-7321.
38. Wallich R, Simon MM, Mullbacher A (2001) Virulence of mousepox virus is independent of serpin-mediated control of cellular cytotoxicity. Viral Immunol 14: 71-81.
39. Turner SJ, Silke J, Kenshole B, Ruby J (2000) Characterization of the ectromelia virus serpin, SPI-2. J Gen Virol 81: 2425-2430.
40. Brick DJ, Burke RD, Minkley AA, Upton C (2000) Ectromelia virus virulence factor p28 acts upstream of caspase-3 in response to UV light-induced apoptosis. J Gen Virol 81: 1087-1097.
41. Chen N, Danila MI, Feng Z, Buller RM, Wang C, et al. (2003) The genomic sequence of ectromelia virus, the causative agent of mousepox. Virology 317: 165-186.
42. Pardo J, Balkow S, Anel A, Simon MM (2002) The differential contribution of granzyme A and granzyme B in cytotoxic T lymphocyte-mediated apoptosis is determined by the quality of target cells. Eur J Immunol 32: 1980-1985.
43. Pardo J, Bosque A, Brehm R, Wallich R, Naval J, et al. (2004) Apoptotic pathways are selectively activated by granzyme A and/or granzyme B in CTL-mediated target cell lysis. J Cell Biol 167: 457-468.
44. Pardo J, Wallich R, Martin P, Urban C, Rongvaux A, et al. (2008) Granzyme B-induced cell death exerted by ex vivo CTL: discriminating requirements for cell death and some of its signs. Cell Death Differ 15: 567-579.
45. Simon MM, Hausmann M, Tran T, Ebnet K, Tschopp J, et al. (1997) In vitro-and ex vivo-derived cytolytic leukocytes from granzyme A x B double knockout mice are defective in granule-mediated apoptosis but not lysis of target cells. J Exp Med 186: 1781-1786.
46. Pham CT, MacIvor DM, Hug BA, Heusel JW, Ley TJ (1996) Long-range disruption of gene expression by a selectable marker cassette. Proc Natl Acad Sci U S A 93: 13090-13095.
47. Krzyzowska M, Schollenberger A, Skierski J, Niemialtowski M (2002) Apoptosis during ectromelia orthopoxvirus infection is DEVDase dependent: in vitro and in vivo studies. Microbes Infect 4: 599-611.
48. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, et al. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334.
49. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, et al. (2007) Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13: 54-61.
50. Tewari M, Telford WG, Miller RA, Dixit VM (1995) CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J Biol Chem 270: 22705-22708.
51. Blanden RV (1974) T cell response to viral and bacterial infection. Transplant Rev 19: 56-88.
52. Mullbacher A, Blanden RV (2004) T-cell-mediated control of poxvirus infection in mice. Prog Mol Subcell Biol 36: 39-55.
53. Mullbacher A, Ebnet K, Blanden RV, Hla RT, Stehle T, et al. (1996) Granzyme A is critical for recovery of mice from infection with the natural cytopathic viral pathogen, ectromelia. Proc Natl Acad Sci U S A 93: 5783-5787.
54. Regner M, Pavlinovic L, Koskinen A, Young N, Trapani JA, et al. (2009) Cutting edge: Rapid and efficient in vivo cytotoxicity by cytotoxic T cells is independent of granzymes A and B. J Immunol 183: 37-40.
55. Metkar SS, Menaa C, Pardo J, Wang B, Wallich R, et al. (2008) Human and mouse granzyme A induce a proinflammatory cytokine response. Immunity 29: 720-733.
56. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
57. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, et al. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730.
58. Lakhani SA, Masud A, Kuida K, Porter GA, Jr., Booth CJ, et al. (2006) Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 311: 847-851.
59. Tscharke DC, Karupiah G, Zhou J, Palmore T, Irvine KR, et al. (2005) Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J Exp Med 201: 95-104.
60. Martin P, Wallich R, Pardo J, Mullbacher A, Munder M, et al. (2005) Quiescent and activated mouse granulocytes do not express granzyme A and B or perforin: similarities or differences with human polymorphonuclear leukocytes? Blood 106: 2871-2878.
61. Pardo J, Wallich R, Ebnet K, Iden S, Zentgraf H, et al. (2007) Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin. Cell Death Differ 14: 1768-1779.