A Natural Genetic Variant of Granzyme B Confers Lethality to a Common Viral Infection

PLoS Pathogens

Volumn 10, Issue 12, 2014, Pages

  Andoniou, Christopher E ^a,b   Sutton, Vivien R ^c,d   Wikstrom, Matthew E ^a,b   Fleming, Peter ^a,b   Thia, Kevin Y T ^c,d   Matthews, Antony Y ^e   Kaiserman, Dion ^e   Schuster, Iona S ^a,b   Coudert, Jerome D ^a,b   Eldi, Preethi ^f   Chaudhri, Geeta ^f   Karupiah, Gunasegaran ^f   Bird, Phillip I ^e   Trapani, Joseph A ^c,d   Degli Esposti, Mariapia A ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LIONS EYE INSTITUTE   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; GAMMA INTERFERON; GRANZYME A; GRANZYME B; PROCASPASE 3; PROCASPASE 7; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; GRANZYME;

ALLELE; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIVIRAL SUSCEPTIBILITY; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GRANULOCYTE; HUMAN; HUMAN CELL; LEUKOCYTE; LIVER INJURY; MITOCHONDRIAL MEMBRANE POTENTIAL; MONOCYTE; MOUSE; NONHUMAN; SURVIVAL RATE; VIRUS INFECTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; METABOLISM; MOLECULAR GENETICS; MORTALITY; MUROMEGALOVIRUS; PATHOLOGY; VIROLOGY;

MAIZE CHLOROTIC MOTTLE VIRUS; MURID HERPESVIRUS 1; MUS;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CASPASES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; GENETIC VARIATION; GRANZYMES; HERPESVIRIDAE INFECTIONS; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUROMEGALOVIRUS; VIRUS DISEASES;

EID: 84919623105     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004526     Document Type: Article

References (51)

1. Russell JH, Ley TJ, (2002) Lymphocyte-mediated cytotoxicity. Ann Rev Immunol 20: 323–370.
2. Mullbacher A, Waring P, Tha Hla R, 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: 13950–13995.
3. 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. European journal of immunology 30: 1350–1355.
4. van Dommelen SL, Sumaria N, Schreiber RD, Scalzo AA, Smyth MJ, et al. (2006) Perforin and granzymes have distinct roles in defensive immunity and immunopathology. Immunity 25: 835–848.
5. Voskoboinik I, Smyth MJ, Trapani JA, (2006) Perforin-mediated target-cell death and immune homeostasis. Nature reviews Immunology 6: 940–952.
6. Beresford PJ, Xia Z, Greenberg AH, J L, (1999) Granzyme A loading induces rapid cytolysis and a novel form of DNA damage independently of caspase activation. Immunity 10: 585–594.
7. Martinvalet D, Zhu P, Lieberman J, (2005) Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis. Immunity 22: 355–370.
8. Susanto O, Stewart SE, Voskoboinik I, Brasacchio D, Hagn M, et al. (2013) Mouse granzyme A induces a novel death with writhing morphology that is mechanistically distinct from granzyme B-induced apoptosis. Cell death and differentiation 20: 1183–1193.
9. Cullen SP, Adrain C, Luthi AU, Duriez PJ, Martin SJ, (2007) Human and murine granzyme B exhibit divergent substrate preferences. The Journal of cell biology 176: 435–444.
10. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, et al. (2006) The major human and mouse granzymes are structurally and functionally divergent. The Journal of cell biology 175: 619–630.
11. Casciola-Rosen L, Garcia-Calvo M, Bull HG, Becker JW, Hines T, et al. (2007) Mouse and human granzyme B have distinct tetrapeptide specificities and abilities to recruit the bid pathway. The Journal of biological chemistry 282: 4545–4552.
12. Sutton VR, Davis JE, Cancilla M, Johnstone RW, Ruefli AA, et al. (2000) Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. The Journal of experimental medicine 192: 1403–1414.
13. Sutton VR, Wowk ME, Cancilla M, Trapani JA, (2003) Caspase activation by granzyme B is indirect, and caspase autoprocessing requires the release of proapoptotic mitochondrial factors. Immunity 18: 319–329.
14. Waterhouse NJ, Sedelies KA, Browne KA, Wowk ME, Newbold A, et al. (2005) A central role for Bid in granzyme B-induced apoptosis. The Journal of biological chemistry 280: 4476–4482.
15. Waterhouse NJ, Sedelies KA, Sutton VR, Pinkoski MJ, Thia KY, et al. (2006) Functional dissociation of DeltaPsim and cytochrome c release defines the contribution of mitochondria upstream of caspase activation during granzyme B-induced apoptosis. Cell death and differentiation 13: 607–618.
16. Knickelbein JE, Khanna KM, Yee MB, Baty CJ, Kinchington PR, et al. (2008) Noncytotoxic lytic granule-mediated CD8+ T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322: 268–271.
17. Andrade F, Fellows E, Jenne DE, Rosen A, Young CS, (2007) Granzyme H destroys the function of critical adenoviral proteins required for viral DNA replication and granzyme B inhibition. EMBO J 26: 2148–2157.
18. McIlroy D, Cartron P-F, Tuffery P, Dudoit Y, Samri A, et al. (2003) A triple-mutated allele of granzyme B incapable of inducing apoptosis. Proceedings of the National Academy of Sciences of the United States of America 100: 2562–2567.
19. Sun J, Bird CH, Thia KY, Matthews AY, Trapani JA, et al. (2004) Granzyme B encoded by the commonly occurring human RAH allele retains pro-apoptotic activity. The Journal of biological chemistry 279: 16907–16911.
20. Thia KYT, Trapani JA, (2007) The granzyme B gene is highly polymorphic in wild mice but essentially invariant in common inbred laboratory strains. Tissue antigens 70: 198–204.
21. Sun J, Bird CH, Buzza MS, McKee KE, Whisstock JC, et al. (1999) Expression and purification of recombinant human granzyme B from Pichia pastoris. Biochemical and biophysical research communications 261: 251–255.
22. Sun J, Bird CH, Sutton V, McDonald L, Coughlin PB, et al. (1996) A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. The Journal of biological chemistry 271: 27802–27809.
23. Sun J, Ooms L, Bird CH, Sutton VR, Trapani JA, et al. (1997) A new family of 10 murine ovalbumin serpins includes two homologs of proteinase inhibitor 8 and two homologs of the granzyme B inhibitor (proteinase inhibitor 9). The Journal of biological chemistry 272: 15434–15441.
24. Bird CH, Sutton VR, Sun JR, Hirst CE, Novak A, et al. (1998) 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 18: 6387–6398.
25. Anthony DA, Andrews DM, Watt SV, Trapani JA, Smyth MJ, (2010) Functional dissection of the granzyme family: cell death and inflammation. Immunological Reviews 235: 73–92.
26. Edwards KM, Kam CM, Powers JC, Trapani JA, (1999) The human cytotoxic T cell granule serine protease granzyme H has chymotrypsin-like (chymase) activity and is taken up into cytoplasmic vesicles reminiscent of granzyme B-containing endosomes. Journal of Biological Chemistry 274: 30468–30473.
27. Voigt V, Forbes CA, Tonkin JN, Degli-Esposti MA, Smith HR, et al. (2003) Murine cytomegalovirus m157 mutation and variation leads to immune evasion of natural killer cells. Proc Natl Acad Sci U S A 100: 13483–13488.
28. Scalzo AA, Manzur M, Forbes CA, Brown MG, Shellam GR, (2005) NK gene complex haplotype variability and host resistance alleles to murine cytomegalovirus in wild mouse populations. Immunology & Cell Biology 83: 144–149.
29. Kees U, Blanden RV, (1976) A single genetic element in H-2K affects mouse T-cell antiviral function in poxvirus infection. Journal of Experimental Medicine 143: 450–455.
30. Loh J, Chu DT, O'Guin AK, Yokoyama WM, Virgin HWt, (2005) Natural killer cells utilize both perforin and gamma interferon to regulate murine cytomegalovirus infection in the spleen and liver. J Virol 79: 661–667.
31. Zhang M, Park S-M, Wang Y, Shah R, Liu N, et al. (2006) Serine protease inhibitor 6 protects cytotoxic T cells from self-inflicted injury by ensuring the integrity of cytotoxic granules. Immunity 24: 451–461.
32. Gold MC, Munks MW, Wagner M, Koszinowski UH, Hill AB, et al. (2002) The murine cytomegalovirus immunomodulatory gene m152 prevents recognition of infected cells by M45-specific CTL but does not alter the immunodominance of the M45-specific CD8 T cell response in vivo. Journal of Immunology 169: 359–365.
33. 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.
34. Anthony DA, Andrews DM, Chow M, Watt SV, House C, et al. (2010) A role for granzyme M in TLR4-driven inflammation and endotoxicosis. Journal of immunology (Baltimore, Md: 1950) 185: 1794–1803.
35. Baschuk N, Wang N, Watt SV, Halse H, House C, et al. (2014) NK cell intrinsic regulation of MIP-1alpha by granzyme M. Cell death & disease. 5: e1115.
36. Sedelies KA, Ciccone A, Clarke CJP, Oliaro J, Sutton VR, et al. (2008) Blocking granule-mediated death by primary human NK cells requires both protection of mitochondria and inhibition of caspase activity. Cell death and differentiation 15: 708–717.
37. Pinkoski MJ, Waterhouse NJ, Heibein JA, Wolf BB, Kuwana T, et al. (2001) Granzyme B-mediated apoptosis proceeds predominantly through a Bcl-2-inhibitable mitochondrial pathway. The Journal of biological chemistry 276: 12060–12067.
38. Jurak I, Schumacher U, Simic H, Voigt S, Brune W, (2008) Murine cytomegalovirus m38.5 protein inhibits Bax-mediated cell death. J Virol 82: 4812–4822.
39. Manzur M, Fleming P, Huang DC, Degli-Esposti MA, Andoniou CE, (2009) Virally mediated inhibition of Bax in leukocytes promotes dissemination of murine cytomegalovirus. Cell Death Differ 16: 312–320.
40. Cam M, Handke W, Picard-Maureau M, Brune W, (2010) Cytomegaloviruses inhibit Bak- and Bax-mediated apoptosis with two separate viral proteins. Cell Death Differ 17: 655–665.
41. Fleming P, Kvansakul M, Voigt V, Kile BT, Kluck RM, et al. (2013) MCMV-mediated inhibition of the pro-apoptotic Bak protein is required for optimal in vivo replication. PLoS Pathogens 9: e1003192.
42. Sun J, Coughlin P, Salem HH, Bird P, (1995) Production and characterization of recombinant human proteinase inhibitor 6 expressed in Pichia pastoris. Biochimica et biophysica acta 1252: 28–34.
43. Song J, Matthews AY, Reboul CF, Kaiserman D, Pike RN, et al. (2011) Predicting serpin/protease interactions. Methods in enzymology 501: 237–273.
44. Rizzitelli A, Meuter S, Vega Ramos J, Bird CH, Mintern JD, et al. (2012) Serpinb9 (Spi6)-deficient mice are impaired in dendritic cell-mediated antigen cross-presentation. Immunology and cell biology 90: 841–851.
45. Lopez JA, Jenkins MR, Rudd-Schmidt JA, Brennan AJ, Danne JC, et al. (2013) Rapid and unidirectional perforin pore delivery at the cytotoxic immune synapse. Journal of immunology (Baltimore, Md: 1950) 191: 2328–2334.
46. Konjar S, Sutton VR, Hoves S, Repnik U, Yagita H, et al. (2010) Human and mouse perforin are processed in part through cleavage by the lysosomal cysteine proteinase cathepsin L. Immunology. 131: 257–267.
47. Sutton VR, Waterhouse NJ, Browne KA, Sedelies K, Ciccone A, et al. (2007) Residual active granzyme B in cathepsin C-null lymphocytes is sufficient for perforin-dependent target cell apoptosis. The Journal of cell biology 176: 425–433.
48. Corbett AJ, Coudert JD, Forbes CA, Scalzo AA, (2011) Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation. J Immunol 186: 1713–1722.
49. Ong ML, Wikstrom ME, Fleming P, Estcourt MJ, Hertzog PJ, et al. (2013) CpG pretreatment enhances antiviral T-cell immunity against cytomegalovirus. Blood 122: 55–60.
50. Tahiliani V, Chaudhri G, Eldi P, Karupiah G, (2013) The orchestrated functions of innate leukocytes and T cell subsets contribute to humoral immunity, virus control, and recovery from secondary poxvirus challenge. Journal of Virology 87: 3852–3861.
51. Sutton VR, Vaux DL, Trapani JA, (1997) bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J Immunol 158: 5783–5790.