Reducing or increasing β-cell apoptosis without inflammation does not affect diabetes initiation in neonatal NOD mice

European Journal of Immunology

Volumn 41, Issue 8, 2011, Pages 2238-2247

  Carrington, Emma M ^a,b   Kos, Cameron ^c   Zhan, Yifan ^b   Krishnamurthy, Balasubramanian ^c   Allison, Janette ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

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

Author keywords

Apoptosis; Autoimmunity; Diabetes; Transgenic knockout mice

Indexed keywords

ANTIGEN; INSULIN; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL INFILTRATION; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPH NODE; MALE; MOUSE; NEWBORN; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PANCREATIC LYMPH NODE; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENIC ANIMAL;

ADOPTIVE TRANSFER; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; DIABETES MELLITUS, TYPE 1; IN SITU NICK-END LABELING; INFLAMMATION; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TIME FACTORS;

EID: 79960724246     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141476     Document Type: Article

References (45)

1. Kurts, C., Heath, W. R., Carbone, F. R., Allison, J., Miller, J. F. and Kosaka, H., Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 1996. 184: 923-930.
2. Mathis, D., Vence, L. and Benoist, C., Beta-Cell death during progression to diabetes. Nature 2001. 414: 792-798.
3. Gagnerault, M. C., Luan, J. J., Lotton, C. and Lepault, F., Pancreatic lymph nodes are required for priming of beta cell reactive T cells in NOD mice. J. Exp. Med. 2002. 196: 369-377.
4. Hoglund, P., Mintern, J., Waltzinger, C., Heath, W., Benoist, C. and Mathis, D., Initiation of autoimmune diabetes by developmentally regulated presentation of islet cell antigens in the pancreatic lymph nodes. J. Exp. Med. 1999. 189: 331-339.
5. Turley, S., Poirot, L., Hattori, M., Benoist, C. and Mathis, D., Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 2003. 198: 1527-1537.
6. Zhang, Y., O'Brien, B., Trudeau, J., Tan, R., Santamaria, P. and Dutz, J. P., In situ beta cell death promotes priming of diabetogenic CD8+T lymphocytes. J. Immunol. 2002. 168: 1466-1472.
7. Forster, I. and Lieberam, I., Peripheral tolerance of CD4+T cells following local activation in adolescent mice. Eur. J. Immunol. 1996. 26: 3194-3202.
8. Morgan, D. J., Kurts, C., Kreuwel, H. T., Holst, K. L., Heath, W. R. and Sherman, L. A., Ontogeny of T cell tolerance to peripherally expressed antigens. Proc. Natl. Acad. Sci. USA 1999. 96: 3854-3858.
9. Mintern, J. D., Sutherland, R. M., Lew, A. M., Shortman, K., Carbone, F. R. and Heath, W. R., Constitutive, but not inflammatory, cross-presentation is disabled in the pancreas of young mice. Eur. J. Immunol. 2002. 32: 1044-1051.
10. Katz, J. D., Wang, B., Haskins, K., Benoist, C. and Mathis, D., Following a diabetogenic T cell from genesis through pathogenesis. Cell 1993. 74: 1089-1100.
11. Verdaguer, J., Schmidt, D., Amrani, A., Anderson, B., Averill, N. and Santamaria, P., Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice. J. Exp. Med. 1997. 186: 1663-1676.
12. Finegood, D. T., Scaglia, L. and Bonner-Weir, S., Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 1995. 44: 249-256.
13. Trudeau, J. D., Dutz, J. P., Arany, E., Hill, D. J., Fieldus, W. E. and Finegood, D. T., Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 2000. 49: 1-7.
14. Kassem, S. A., Ariel, I., Thornton, P. S., Scheimberg, I. and Glaser, B., Beta-cell proliferation and apoptosis in the developing normal human pancreas and in hyperinsulinism of infancy. Diabetes 2000. 49: 1325-1333.
15. Coles, H. S., Burne, J. F. and Raff, M. C., Large-scale normal cell death in the developing rat kidney and its reduction by epidermal growth factor. Development 1993. 118: 777-784.
16. Barres, B. A., Hart, I. K., Coles, H. S., Burne, J. F., Voyvodic, J. T., Richardson, W. D. and Raff, M. C., Cell death in the oligodendrocyte lineage. J. Neurobiol. 1992. 23: 1221-1230.
17. Jacobson, M. D., Burne, J. F. and Raff, M. C., Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J. 1994. 13: 1899-1910.
18. Scaglia, L., Cahill, C. J., Finegood, D. T. and Bonner-Weir, S., Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology 1997. 138: 1736-1741.
19. O'Brien, B. A., Fieldus, W. E., Field, C. J. and Finegood, D. T., Clearance of apoptotic beta-cells is reduced in neonatal autoimmune diabetes-prone rats. Cell Death Differ. 2002. 9: 457-464.
20. O'Brien, B. A., Huang, Y., Geng, X., Dutz, J. P. and Finegood, D. T., Phagocytosis of apoptotic cells by macrophages from NOD mice is reduced. Diabetes 2002. 51: 2481-2488.
21. Petrik, J., Arany, E., McDonald, T. J. and Hill, D. J., Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor II that may act as a survival factor. Endocrinology 1998. 139: 2994-3004.
22. Petrik, J., Reusens, B., Arany, E., Remacle, C., Coelho, C., Hoet, J. J. and Hill, D. J., A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 1999. 140: 4861-4873.
23. Hill, D. J., Strutt, B., Arany, E., Zaina, S., Coukell, S. and Graham, C. F., Increased and persistent circulating insulin-like growth factor II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic islets. Endocrinology 2000. 141: 1151-1157.
24. Hettiarachchi, K. D., Zimmet, P. Z., Danial, N. N. and Myers, M. A., Transplacental exposure to the vacuolar-ATPase inhibitor bafilomycin disrupts survival signaling in beta cells and delays neonatal remodeling of the endocrine pancreas. Exp. Toxicol. Pathol. 2008. 60: 295-306.
25. Maree, A. F., Kublik, R., Finegood, D. T. and Edelstein-Keshet, L., Modelling the onset of Type 1 diabetes: can impaired macrophage phagocytosis make the difference between health and disease? Philos. Transact. A Math. Phys. Eng. Sci. 2006. 364: 1267-1282.
26. Allison, J., Campbell, I. L., Morahan, G., Mandel, T. E., Harrison, L. C. and Miller, J. F., Diabetes in transgenic mice resulting from over-expression of class I histocompatibility molecules in pancreatic beta cells. Nature 1988. 333: 529-533.
27. Naik, P., Karrim, J. and Hanahan, D., The rise and fall of apoptosis during multistage tumorigenesis: down-modulation contributes to tumor progression from angiogenic progenitors. Genes Dev. 1996. 10: 2105-2116.
28. Hager, J. H. and Hanahan, D., Tumor cells utilize multiple pathways to down-modulate apoptosis. Lessons from a mouse model of islet cell carcinogenesis. Ann. N. Y. Acad. Sci. 1999. 887: 150-163.
29. Surh, C. D. and Sprent, J., T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994. 372: 100-103.
30. Allison, J., Georgiou, H. M., Strasser, A. and Vaux, D. L., Transgenic expression of CD95 ligand on islet beta cells induces a granulocytic infiltration but does not confer immune privilege upon islet allografts. Proc. Natl. Acad. Sci. USA 1997. 94: 3943-3947.
31. Stadinski, B. D., Delong, T., Reisdorph, N., Reisdorph, R., Powell, R. L., Armstrong, M., Piganelli, J. D. et al., Chromogranin A is an autoantigen in type 1 diabetes. Nat. Immunol. 2010. 11: 225-231.
32. McIntire, C. R., Yeretssian, G. and Saleh, M., Inflammasomes in infection and inflammation. Apoptosis 2009. 14: 522-535.
33. Jager, R., Herzer, U., Schenkel, J. and Weiher, H., Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 1997. 15: 1787-1795.
34. Calderon, B., Suri, A., Miller, M. J. and Unanue, E. R., Dendritic cells in islets of Langerhans constitutively present beta cell-derived peptides bound to their class II MHC molecules. Proc. Natl. Acad. Sci. USA 2008. 105: 6121-6126.
35. Mohan, J. F., Levisetti, M. G., Calderon, B., Herzog, J. W., Petzold, S. J. and Unanue, E. R., Unique autoreactive T cells recognize insulin peptides generated within the islets of Langerhans in autoimmune diabetes. Nat. Immunol. 2010. 11: 350-354.
36. Melli, K., Friedman, R. S., Martin, A. E., Finger, E. B., Miao, G., Szot, G. L., Krummel, M. F. and Tang, Q., Amplification of autoimmune response through induction of dendritic cell maturation in inflamed tissues. J. Immunol. 2009. 182: 2590-2600.
37. Heath, W. R. and Carbone, F. R., Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 2001. 19: 47-64.
38. Garvy, B. A. and Qureshi, M. H., Delayed inflammatory response to Pneumocystis carinii infection in neonatal mice is due to an inadequate lung environment. J. Immunol. 2000. 165: 6480-6486.
39. Qureshi, M. H., Empey, K. M. and Garvy, B. A., Modulation of proinflammatory responses to Pneumocystis carinii f. sp. muris in neonatal mice by granulocyte-macrophage colony-stimulating factor and IL-4: role of APCs. J. Immunol. 2005. 174: 441-448.
40. Nelson, D. J., McMenamin, C., McWilliam, A. S., Brenan, M. and Holt, P. G., Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J. Exp. Med. 1994. 179: 203-212.
41. Allison, J., Thomas, H., Beck, D., Brady, J. L., Lew, A. M., Elefanty, A., Kosaka, H. et al., Transgenic overexpression of human Bcl-2 in islet beta cells inhibits apoptosis but does not prevent autoimmune destruction. Int. Immunol. 2000. 12: 9-17.
42. Strasser, A., Harris, A. W. and Cory, S., bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 1991. 67: 889-899.
43. Serreze, D. V., Chapman, H. D., Varnum, D. S., Gerling, I., Leiter, E. H. and Shultz, L. D., Initiation of autoimmune diabetes in NOD/Lt mice is MHC class I-dependent. J. Immunol. 1997. 158: 3978-3986.
44. Allison, J., Thomas, H. E., Catterall, T., Kay, T. W. and Strasser, A., Transgenic expression of dominant-negative Fas-associated death domain protein in beta cells protects against Fas ligand-induced apoptosis and reduces spontaneous diabetes in nonobese diabetic mice. J. Immunol. 2005. 175: 293-301.
45. Augstein, P., Stephens, L. A., Allison, J., Elefanty, A. G., Ekberg, M., Kay, T. W. and Harrison, L. C., Beta-cell apoptosis in an accelerated model of autoimmune diabetes. Mol. Med. 1998. 4: 495-501.