The pro-apoptotic BH3-only protein Bid is dispensable for development of insulitis and diabetes in the non-obese diabetic mouse

Apoptosis

Volumn 16, Issue 8, 2011, Pages 822-830

  Mollah, Zia U A ^a   Wali, Jibran ^a,b   McKenzie, Mark D ^a,d   Krishnamurthy, Balasubramanian ^a   Graham, Kate L ^a   Fynch, Stacey ^a   Szanyi, Joshua ^a   Santamaria, Pere ^c   Brodnicki, Thomas ^a,b   Allison, Janette ^a   Strasser, Andreas ^b,d   Kay, Thomas W H ^a,b   Thomas, Helen E ^a,b  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF CALGARY   (Canada)

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

Author keywords

Beta cell apoptosis; BH3 interacting domain death agonist; NOD mouse; Type 1 diabetes

Indexed keywords

FAS LIGAND; PROTEIN BID;

ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; GENE OVEREXPRESSION; GENOTYPE; HOMOLOGOUS RECOMBINATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD95; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DNA FRAGMENTATION; FAS LIGAND PROTEIN; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE SYSTEM; IMMUNOPHENOTYPING; INSULIN-SECRETING CELLS; INTERFERON-GAMMA; INTERLEUKIN-1BETA; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 80051545963     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-011-0615-z     Document Type: Article

References (37)

1. HE Thomas MD McKenzie E Angstetra PD Campbell TW Kay 2009 Beta cell apoptosis in diabetes Apoptosis 14 1389 1404 19322660 10.1007/s10495-009-0339-5
2. A Amrani J Verdaguer B Anderson T Utsugi S Bou P Santamaria 1999 Perforin-independent beta-cell destruction by diabetogenic CD8(+) T lymphocytes in transgenic nonobese diabetic mice J Clin Invest 103 1201 1209 10207172 10.1172/JCI6266 1:CAS:528:DyaK1MXis1GnsbY%3D (Pubitemid 29207254)
3. NL Dudek HE Thomas L Mariana RM Sutherland J Allison E Estella E Angstetra JA Trapani P Santamaria AM Lew TW Kay 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 16936188 10.2337/db06-0109 1:CAS:528:DC%2BD28XpsVOrtrk%3D (Pubitemid 44871141)
4. HT Kreuwel DJ Morgan T Krahl A Ko N Sarvetnick LA Sherman 1999 Comparing the relative role of perforin/granzyme versus Fas/Fas ligand cytotoxic pathways in CD8+ T cell-mediated insulin-dependent diabetes mellitus J Immunol 163 4335 4341 10510373 1:CAS:528:DyaK1MXmsleltr8%3D (Pubitemid 29474500)
5. MD McKenzie NL Dudek L Mariana MM Chong JA Trapani TW Kay HE Thomas 2006 Perforin and Fas induced by IFNgamma and TNFalpha mediate beta cell death by OT-I CTL Int Immunol 18 837 846 16574667 10.1093/intimm/dxl020 1:CAS:528:DC%2BD28XmsVejtL8%3D (Pubitemid 43983279)
6. HE Thomas R Darwiche JA Corbett TW Kay 1999 Evidence that beta cell death in the nonobese diabetic mouse is Fas independent J Immunol 163 1562 1569 10415060 1:CAS:528:DyaK1MXkslOgsLY%3D (Pubitemid 29352780)
7. M Moriwaki N Itoh J Miyagawa K Yamamoto A Imagawa K Yamagata H Iwahashi H Nakajima M Namba S Nagata T Hanafusa Y Matsuzawa 1999 Fas and Fas ligand expression in inflamed islets in pancreas sections of patients with recent-onset Type I diabetes mellitus Diabetologia 42 1332 1340 10550417 10.1007/s001250051446 1:CAS:528:DyaK1MXmvF2ms7Y%3D (Pubitemid 29500970)
8. R Darwiche MM Chong P Santamaria HE Thomas TW Kay 2003 Fas is detectable on beta cells in accelerated, but not spontaneous, diabetes in nonobese diabetic mice J Immunol 170 6292 6297 12794162 1:CAS:528:DC%2BD3sXktlKrtLk%3D (Pubitemid 36682615)
9. J Allison A Strasser 1998 Mechanisms of beta cell death in diabetes: a minor role for CD95 Proc Natl Acad Sci USA 95 13818 13822 9811884 10.1073/pnas.95.23.13818 1:CAS:528:DyaK1cXnsVGgur4%3D (Pubitemid 28523056)
10. AV Chervonsky Y Wang FS Wong I Visintin RA Flavell CA Janeway Jr LA Matis 1997 The role of Fas in autoimmune diabetes Cell 89 17 24 9094710 10.1016/S0092-8674(00)80178-6 1:CAS:528:DyaK2sXisVygt7k%3D (Pubitemid 27180581)
11. N Itoh A Imagawa T Hanafusa M Waguri K Yamamoto H Iwahashi M Moriwaki H Nakajima J Miyagawa M Namba S Makino S Nagata N Kono Y Matsuzawa 1997 Requirement of Fas for the development of autoimmune diabetes in nonobese diabetic mice J Exp Med 186 613 618 9254659 10.1084/jem.186.4.613 1:CAS:528:DyaK2sXlsFWmur0%3D (Pubitemid 27360805)
12. AS Mohamood ML Guler Z Xiao D Zheng A Hess Y Wang H Yagita JP Schneck AR Hamad 2007 Protection from autoimmune diabetes and T-cell lymphoproliferation induced by FasL mutation are differentially regulated and can be uncoupled pharmacologically Am J Pathol 171 97 106 17591957 10.2353/ajpath.2007.070148 1:CAS:528:DC%2BD2sXosValsrY%3D (Pubitemid 47339230)
13. M Nakayama M Nagata H Yasuda K Arisawa R Kotani K Yamada SA Chowdhury S Chakrabarty ZZ Jin H Yagita K Yokono M Kasuga 2002 Fas/Fas ligand interactions play an essential role in the initiation of murine autoimmune diabetes Diabetes 51 1391 1397 11978635 10.2337/diabetes.51.5.1391 1:CAS:528:DC%2BD38XjtlGmt7s%3D (Pubitemid 34826604)
14. WL Suarez-Pinzon RF Power A Rabinovitch 2000 Fas ligand-mediated mechanisms are involved in autoimmune destruction of islet beta cells in non-obese diabetic mice Diabetologia 43 1149 1156 11043861 10.1007/s001250051506 1:CAS:528:DC%2BD3cXnt1Oltb8%3D
15. L Vence C Benoist D Mathis 2004 Fas deficiency prevents type 1 diabetes by inducing hyporesponsiveness in islet beta-cell-reactive T-cells Diabetes 53 2797 2803 15504959 10.2337/diabetes.53.11.2797 1:CAS:528:DC%2BD2cXpvV2it70%3D (Pubitemid 39425904)
16. J Allison HE Thomas T Catterall TW Kay A Strasser 2005 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 175 293 301 15972661 1:CAS:528:DC%2BD2MXltlynurs%3D (Pubitemid 40884331)
17. S Hugues E Mougneau W Ferlin D Jeske P Hofman D Homann L Beaudoin C Schrike M Von Herrath A Lehuen N Glaichenhaus 2002 Tolerance to islet antigens and prevention from diabetes induced by limited apoptosis of pancreatic beta cells Immunity 16 169 181 11869679 10.1016/S1074-7613(02)00273-X 1:CAS:528:DC%2BD38XitVCju7Y%3D (Pubitemid 34211958)
18. I Millet FS Wong W Gurr L Wen W Zawalich EA Green RA Flavell RS Sherwin 2006 Targeted expression of the anti-apoptotic gene CrmA to NOD pancreatic islets protects from autoimmune diabetes J Autoimmun 26 7 15 16338119 10.1016/j.jaut.2005.10.005 1:CAS:528:DC%2BD28XotVCqtA%3D%3D (Pubitemid 43138887)
19. AY Savinov A Tcherepanov EA Green RA Flavell AV Chervonsky 2003 Contribution of Fas to diabetes development Proc Natl Acad Sci USA 100 628 632 12525697 10.1073/pnas.0237359100 1:CAS:528:DC%2BD3sXnvVKmug%3D%3D (Pubitemid 36126103)
20. I Apostolou Z Hao K Rajewsky H von Boehmer 2003 Effective destruction of Fas-deficient insulin-producing beta cells in type 1 diabetes J Exp Med 198 1103 1106 14530378 10.1084/jem.20030698 1:CAS:528:DC%2BD3sXotVWgs7Y%3D (Pubitemid 37248625)
21. EH Leiter P Reifsnyder J Driver S Kamdar C Choisy-Rossi DV Serreze M Hara A Chervonsky 2007 Unexpected functional consequences of xenogeneic transgene expression in beta-cells of NOD mice Diabetes Obes Metab 9 Suppl 2 14 22 17919174 10.1111/j.1463-1326.2007.00770.x 1:CAS:528:DC%2BD2sXhtlOhsLnI (Pubitemid 47543122)
22. JY Lee M Ristow X Lin MF White MA Magnuson L Hennighausen 2006 RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function J Biol Chem 281 2649 2653 16326700 10.1074/jbc.M512373200 1:CAS:528:DC%2BD28XovVeitA%3D%3D (Pubitemid 43845726)
23. D Pomplun S Florian T Schulz AF Pfeiffer M Ristow 2007 Alterations of pancreatic beta-cell mass and islet number due to Ins2-controlled expression of Cre recombinase: RIP-Cre revisited; part 2 Horm Metab Res 39 336 340 17533574 10.1055/s-2007-976538 1:CAS:528:DC%2BD2sXntlKltLw%3D (Pubitemid 46877848)
24. MD McKenzie EM Carrington T Kaufmann A Strasser DC Huang TW Kay J Allison HE Thomas 2008 Proapoptotic BH3-only protein Bid is essential for death receptor-induced apoptosis of pancreatic beta-cells Diabetes 57 1284 1292 18252892 10.2337/db07-1692 1:CAS:528:DC%2BD1cXlvVKjtLg%3D
25. T Kaufmann L Tai PG Ekert DC Huang F Norris RK Lindemann RW Johnstone VM Dixit A Strasser 2007 The BH3-only protein bid is dispensable for DNA damage- and replicative stress-induced apoptosis or cell-cycle arrest Cell 129 423 433 17448999 10.1016/j.cell.2007.03.017 1:CAS:528:DC%2BD2sXlsVWlsLw%3D (Pubitemid 46574974)
26. J Verdaguer D Schmidt A Amrani B Anderson N Averill P Santamaria 1997 Spontaneous autoimmune diabetes in monoclonal T cell nonobese diabetic mice J Exp Med 186 1663 1676 9362527 10.1084/jem.186.10.1663 1:CAS:528: DyaK2sXnsVeitr4%3D (Pubitemid 27506280)
27. S Ghosh SM Palmer NR Rodrigues HJ Cordell CM Hearne RJ Cornall JB Prins P McShane GM Lathrop LB Peterson, et al. 1993 Polygenic control of autoimmune diabetes in nonobese diabetic mice Nat Genet 4 404 409 8401590 10.1038/ng0893-404 1:CAS:528:DyaK3sXmsVagtbc%3D (Pubitemid 23231491)
28. UC Rogner C Boitard J Morin E Melanitou P Avner 2001 Three loci on mouse chromosome 6 influence onset and final incidence of type I diabetes in NOD.C3H congenic strains Genomics 74 163 171 11386752 10.1006/geno.2001.6508 1:CAS:528:DC%2BD3MXjvFCjsr8%3D (Pubitemid 32550137)
29. B Krishnamurthy NL Dudek MD McKenzie AW Purcell AG Brooks S Gellert PG Colman LC Harrison AM Lew HE Thomas TW Kay 2006 Responses against islet antigens in NOD mice are prevented by tolerance to proinsulin but not IGRP J Clin Invest 116 3258 3265 17143333 10.1172/JCI29602 1:CAS:528:DC%2BD28XhtlWgsbnJ (Pubitemid 44878640)
30. SM Lieberman T Takaki B Han P Santamaria DV Serreze TP DiLorenzo 2004 Individual nonobese diabetic mice exhibit unique patterns of CD8+ T cell reactivity to three islet antigens, including the newly identified widely expressed dystrophia myotonica kinase J Immunol 173 6727 6734 15557165 1:CAS:528:DC%2BD2cXhtVShsb%2FM (Pubitemid 39541058)
31. XM Yin K Wang A Gross Y Zhao S Zinkel B Klocke KA Roth SJ Korsmeyer 1999 Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis Nature 400 886 891 10476969 10.1038/23730 1:CAS:528:DyaK1MXlslGkt7w%3D (Pubitemid 29406726)
32. D Kagi B Odermatt P Seiler RM Zinkernagel TW Mak H Hengartner 1997 Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice J Exp Med 186 989 997 9314549 10.1084/jem.186.7.989 1:CAS:528:DyaK2sXmsFaru7k%3D (Pubitemid 27441144)
33. WL Suarez-Pinzon C Szabo A Rabinovitch 1997 Development of autoimmune diabetes in NOD mice is associated with the formation of peroxynitrite in pancreatic islet beta-cells Diabetes 46 907 911 9133563 10.2337/diabetes.46.5. 907 1:CAS:528:DyaK2sXjtVGnur4%3D (Pubitemid 27188272)
34. P Vandenabeele L Galluzzi T Vanden Berghe G Kroemer 2010 Molecular mechanisms of necroptosis: an ordered cellular explosion Nat Rev Mol Cell Biol 11 700 714 20823910 10.1038/nrm2970 1:CAS:528:DC%2BC3cXhtFajsL7P
35. HS Jung KW Chung J Won Kim J Kim M Komatsu K Tanaka YH Nguyen TM Kang KH Yoon JW Kim YT Jeong MS Han MK Lee KW Kim J Shin MS Lee 2008 Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia Cell Metab 8 318 324 18840362 10.1016/j.cmet.2008.08.013 1:CAS:528: DC%2BD1cXht1Cit77O
36. D Choi A Radziszewska SA Schroer N Liadis Y Liu Y Zhang PP Lam L Sheu Z Hao HY Gaisano M Woo 2009 Deletion of Fas in the pancreatic beta-cells leads to enhanced insulin secretion Am J Physiol Endocrinol Metab 297 E1304 E1312 19755672 10.1152/ajpendo.00217.2009 1:CAS:528:DC%2BD1MXhsFOgsbnP
37. DM Schumann K Maedler I Franklin D Konrad J Storling M Boni-Schnetzler A Gjinovci MO Kurrer BR Gauthier D Bosco A Andres T Berney M Greter B Becher AV Chervonsky PA Halban T Mandrup-Poulsen CB Wollheim MY Donath 2007 The Fas pathway is involved in pancreatic beta cell secretory function Proc Natl Acad Sci USA 104 2861 2866 17299038 10.1073/pnas.0611487104 1:CAS:528: DC%2BD2sXisVSntL4%3D (Pubitemid 46327970)