Granzyme B is dispensable in the development of diabetes in non-obese diabetic mice

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Mollah, Zia U ^a   Graham, Kate L ^a   Krishnamurthy, Balasubramanian ^a   Trivedi, Prerak ^a,b   Brodnicki, Thomas C ^a,b   Trapani, Joseph A ^c   Kay, Thomas W ^a,b   Thomas, Helen E ^a,b  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL KILLING; CELL MATURATION; DISEASE COURSE; ENZYME ACTIVITY; FEMALE; IN VITRO STUDY; INCIDENCE; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; MALE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; THYMUS; WILD TYPE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELL PROLIFERATION; DIABETES MELLITUS, TYPE 1; FEMALE; GRANZYMES; ISLETS OF LANGERHANS; LYMPH NODES; LYMPHOCYTE COUNT; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, INBRED NOD; PANCREAS; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC; THYMUS GLAND;

MUS;

EID: 84863617427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040357     Document Type: Article

References (38)

1. Walter U, Santamaria P, (2005) CD8+ T cells in autoimmunity. Curr Opin Immunol 17: 624-631.
2. Katz J, Benoist C, Mathis D, (1993) Major histocompatibility complex class I molecules are required for the development of insulitis in non-obese diabetic mice. Eur J Immunol 23: 3358-3360.
3. Serreze DV, Leiter EH, Christianson GJ, Greiner D, Roopenian DC, (1994) Major histocompatibility complex class I-deficient NOD-B2mnull mice are diabetes and insulitis resistant. Diabetes 43: 505-509.
4. Sumida T, Furukawa M, Sakamoto A, Namekawa T, Maeda T, et al. (1994) Prevention of insulitis and diabetes in beta 2-microglobulin-deficient non-obese diabetic mice. Int Immunol 6: 1445-1449.
5. Wicker LS, Leiter EH, Todd JA, Renjilian RJ, Peterson E, et al. (1994) Beta 2-microglobulin-deficient NOD mice do not develop insulitis or diabetes. Diabetes 43: 500-504.
6. Skowera A, Ellis RJ, Varela-Calvino R, Arif S, Huang GC, et al. (2008) CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J Clin Invest 118: 3390-3402.
7. Graser RT, DiLorenzo TP, Wang F, Christianson GJ, Chapman HD, et al. (2000) Identification of a CD8 T cell that can independently mediate autoimmune diabetes development in the complete absence of CD4 T cell helper functions. J Immunol 164: 3913-3918.
8. Verdaguer J, Schmidt D, Amrani A, Anderson B, Averill N, et al. (1997) Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J Exp Med 186: 1663-1676.
9. Wong FS, Visintin I, Wen L, Flavell RA, Janeway CA Jr, (1996) CD8 T cell clones from young nonobese diabetic (NOD) islets can transfer rapid onset of diabetes in NOD mice in the absence of CD4 cells. J Exp Med 183: 67-76.
10. Coppieters KT, Dotta F, Amirian N, Campbell PD, Kay TW, et al. (2012) Demonstration of islet-autoreactive CD8 T cells in insulitic lesions from recent onset and long-term type 1 diabetes patients. J Exp Med 209: 51-60.
11. Toso C, Isse K, Demetris AJ, Dinyari P, Koh A, et al. (2009) Histologic graft assessment after clinical islet transplantation. Transplantation 88: 1286-1293.
12. Anthony DA, Andrews DM, Watt SV, Trapani JA, Smyth MJ, (2010) Functional dissection of the granzyme family: cell death and inflammation. Immunol Rev 235: 73-92.
13. Afonina IS, Cullen SP, Martin SJ, (2010) Cytotoxic and non-cytotoxic roles of the CTL/NK protease granzyme B. Immunol Rev 235: 105-116.
14. Alimonti JB, Shi L, Baijal PK, Greenberg AH, (2001) Granzyme B induces BID-mediated cytochrome c release and mitochondrial permeability transition. J Biol Chem 276: 6974-6982.
15. Heibein JA, Goping IS, Barry M, Pinkoski MJ, Shore GC, et al. (2000) Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members bid and Bax. J Exp Med 192: 1391-1402.
16. 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. J Exp Med 192: 1403-1414.
17. Waterhouse NJ, Sedelies KA, Browne KA, Wowk ME, Newbold A, et al. (2005) A central role for Bid in granzyme B-induced apoptosis. J Biol Chem 280: 4476-4482.
18. 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.
19. 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.
20. Estella E, McKenzie MD, Catterall T, Sutton VR, Bird PI, et al. (2006) Granzyme B-mediated death of pancreatic beta-cells requires the proapoptotic BH3-only molecule bid. Diabetes 55: 2212-2219.
21. Amrani A, Verdaguer J, Anderson B, Utsugi T, Bou S, et al. (1999) Perforin-independent β-cell destruction by diabetogenic CD8(+) T lymphocytes in transgenic nonobese diabetic mice. J Clin Invest 103: 1201-1209.
22. Kagi D, Odermatt B, Seiler P, Zinkernagel RM, Mak TW, et al. (1997) Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice. J Exp Med 186: 989-997.
23. Sutton VR, Estella E, Li C, Chen M, Thomas HE, et al. (2006) A critical role for granzyme B, in addition to perforin and TNFalpha, in alloreactive CTL-induced mouse pancreatic beta cell death. Transplantation 81: 146-154.
24. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ, (1994) Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76: 977-987.
25. Leiter EH, Reifsnyder PC, Wallace R, Li R, King B, et al. (2009) NOD×129.H2(g7) backcross delineates 129S1/SvImJ-derived genomic regions modulating type 1 diabetes development in mice. Diabetes 58: 1700-1703.
26. Driver JP, Serreze DV, Chen YG, (2011) Mouse models for the study of autoimmune type 1 diabetes: a NOD to similarities and differences to human disease. Semin Immunopathol 33: 67-87.
27. Graham KL, Krishnamurthy B, Fynch S, Mollah ZU, Slattery R, et al. (2011) Autoreactive cytotoxic T lymphocytes acquire higher expression of cytotoxic effector markers in the islets of NOD mice after priming in pancreatic lymph nodes. Am J Pathol 178: 2716-2725.
28. Ebnet K, Hausmann M, Lehmann-Grube F, Mullbacher A, Kopf M, et al. (1995) Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J 14: 4230-4239.
29. Zajac AJ, Dye JM, Quinn DG, (2003) Control of lymphocytic choriomeningitis virus infection in granzyme B deficient mice. Virology 305: 1-9.
30. 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.
31. Kelly JM, Waterhouse NJ, Cretney E, Browne KA, Ellis S, et al. (2004) Granzyme M mediates a novel form of perforin-dependent cell death. J Biol Chem 279: 22236-22242.
32. 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.
33. Joeckel LT, Wallich R, Martin P, Sanchez-Martinez D, Weber FC, et al. (2011) Mouse granzyme K has pro-inflammatory potential. Cell Death Differ 18: 1112-1119.
34. Angstetra E, Graham KL, Emmett S, Dudek NL, Darwiche R, et al. (2009) In vivo effects of cytokines on pancreatic beta-cells in models of type I diabetes dependent on CD4(+) T lymphocytes. Immunol Cell Biol 87: 178-185.
35. Nakayama M, Beilke JN, Jasinski JM, Kobayashi M, Miao D, et al. (2007) Priming and effector dependence on insulin B:9-23 peptide in NOD islet autoimmunity. J Clin Invest 117: 1835-1843.
36. McKenzie MD, Carrington EM, Kaufmann T, Strasser A, Huang DC, et al. (2008) Proapoptotic BH3-only protein Bid is essential for death receptor-induced apoptosis of pancreatic beta-cells. Diabetes 57: 1284-1292.
37. Darwiche R, Chong MM, Santamaria P, Thomas HE, Kay TW, (2003) Fas is detectable on beta cells in accelerated, but not spontaneous, diabetes in nonobese diabetic mice. J Immunol 170: 6292-6297.
38. Dudek NL, Thomas HE, Mariana L, Sutherland RM, Allison J, et al. (2006) Cytotoxic T-cells from T-cell receptor transgenic NOD8.3 mice destroy beta-cells via the perforin and Fas pathways. Diabetes 55: 2412-2418.