BACH2, a candidate risk gene for type 1 diabetes, regulates apoptosis in pancreatic β-cells via JNK1 modulation and crosstalk with the candidate gene PTPN2

Diabetes

Volumn 63, Issue 7, 2014, Pages 2516-2527

  Marroquí, Laura ^a   Santin, Izortze ^a,b   Dos Santos, Reinaldo Sousa ^a   Marselli, Lorella ^c   Marchetti, Piero ^c   Eizirik, Decio L ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b BIOCRUCES BIZKAIA HEALTH RESEARCH INSTITUTE   (Spain)

^c UNIVERSITY OF PISA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR 2; BIM PROTEIN; CYTOKINE; JNK1 PROTEIN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 2; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MODULATION; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; APOPTOSIS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, TYPE 1; EPISTASIS, GENETIC; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATION MEDIATORS; INSULIN-SECRETING CELLS; MALE; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE 8; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 2; RATS; RATS, WISTAR; RISK;

EID: 84903136445     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1443     Document Type: Article

References (50)

1. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and β-cell loss in type 1 diabetes. Nat Rev Endocrinol 2009;5:219-226
2. Todd JA. Etiology of type 1 diabetes. Immunity 2010;32:457-467
3. Polychronakos C, Li Q. Understanding type 1 diabetes through genetics: advances and prospects. Nat Rev Genet 2011;12:781-792
4. Barrett JC, Clayton DG, Concannon P, et al.; Type 1 Diabetes Genetics Consortium. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat Genet 2009;41:703-707
5. Bergholdt R, Brorsson C, Palleja A, et al. Identification of novel type 1 diabetes candidate genes by integrating genome-wide association data, proteinprotein interactions, and human pancreatic islet gene expression. Diabetes 2012;61:954-962
6. Steck AK, Rewers MJ. Genetics of type 1 diabetes. Clin Chem 2011;57:176-185
7. Eizirik DL, Sammeth M, Bouckenooghe T, et al. The human pancreatic islet transcriptome: expression of candidate genes for type 1 diabetes and the impact of pro-inflammatory cytokines. PLoS Genet 2012;8:e1002552
8. Colli ML, Moore F, Gurzov EN, Ortis F, Eizirik DL. MDA5 and PTPN2, two candidate genes for type 1 diabetes, modify pancreatic beta-cell responses to the viral by-product double-stranded RNA. Hum Mol Genet 2010;19:135-146
9. Moore F, Colli ML, Cnop M, et al. PTPN2, a candidate gene for type 1 diabetes, modulates interferon-γ-induced pancreatic β-cell apoptosis. Diabetes 2009;58:1283-1291
10. Nogueira TC, Paula FM, Villate O, et al. GLIS3, a susceptibility gene for type 1 and type 2 diabetes, modulates pancreatic β cell apoptosis via regulation of a splice variant of the BH3-only protein Bim. PLoS Genet 2013;9:e1003532
11. Santin I, Moore F, Colli ML, et al. PTPN2, a candidate gene for type 1 diabetes, modulates pancreatic β-cell apoptosis via regulation of the BH3-only protein Bim. Diabetes 2011;60:3279-3288
12. Santin I, Eizirik DL. Candidate genes for type 1 diabetes modulate pancreatic islet inflammation and β-cell apoptosis. Diabetes Obes Metab 2013;15(Suppl. 3):71-81
13. Cooper JD, Smyth DJ, Smiles AM, et al. Meta-analysis of genome-wide association study data identifies additional type 1 diabetes risk loci. Nat Genet 2008;40:1399-1401
14. Grant SF, Qu HQ, Bradfield JP, et al.; DCCT/EDIC Research Group. Follow-up analysis of genome-wide association data identifies novel loci for type 1 diabetes. Diabetes 2009;58:290-295
15. Franke A, McGovern DP, Barrett JC, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010;42:1118-1125
16. Dubois PC, Trynka G, Franke L, et al. Multiple common variants for celiac disease influencing immune gene expression. Nat Genet 2010;42:295-302
17. Jin Y, Birlea SA, Fain PR, et al. Genome-wide association analyses identify 13 new susceptibility loci for generalized vitiligo. Nat Genet 2012;44:676-680
18. Kometani K, Nakagawa R, Shinnakasu R, et al. Repression of the transcription factor Bach2 contributes to predisposition of IgG1 memory B cells toward plasma cell differentiation. Immunity 2013;39:136-147
19. Swaminathan S, Huang C, Geng H, et al. BACH2 mediates negative selection and p53-dependent tumor suppression at the pre-B cell receptor checkpoint. Nat Med 2013;19:1014-1022
20. Muto A, Tashiro S, Nakajima O, et al. The transcriptional programme of antibody class switching involves the repressor Bach2. Nature 2004;429:566-571 (Pubitemid 38737661)
21. Roychoudhuri R, Hirahara K, Mousavi K, et al. BACH2 represses effector programs to stabilize T(reg)-mediated immune homeostasis. Nature 2013;498:506-510
22. Tsukumo S, Unno M, Muto A, et al. Bach2 maintains T cells in a naive state by suppressing effector memory-related genes. Proc Natl Acad Sci U S A 2013;110:10735-10740
23. Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene 2002;294:1-12 (Pubitemid 35291008)
24. Hong SW, Kim S, Lee DK. The role of Bach2 in nucleic acid-triggered antiviral innate immune responses. Biochem Biophys Res Commun 2008;365:426-432 (Pubitemid 350181673)
25. Rasschaert J, Ladrière L, Urbain M, et al. Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA+ interferon-γ-induced apoptosis in primary pancreatic beta-cells. J Biol Chem 2005;280:33984-33991 (Pubitemid 41443119)
26. Lupi R, Dotta F, Marselli L, et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: evidence that β-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 2002;51:1437-1442 (Pubitemid 34826609)
27. Ravassard P, Hazhouz Y, Pechberty S, et al. A genetically engineered human pancreatic β cell line exhibiting glucose-inducible insulin secretion. J Clin Invest 2011;121:3589-3597
28. Ortis F, Cardozo AK, Crispim D, Störling J, Mandrup-Poulsen T, Eizirik DL. Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-kappaB activation. Mol Endocrinol 2006;20:1867-1879 (Pubitemid 44148090)
29. Moore F, Cunha DA, Mulder H, Eizirik DL. Use of RNA interference to investigate cytokine signal transduction in pancreatic β cells. Methods Mol Biol 2012;820:179-194
30. Moore F, Naamane N, Colli ML, et al. STAT1 is a master regulator of pancreatic β-cell apoptosis and islet inflammation. J Biol Chem 2011;286:929-941
31. Heimberg H, Heremans Y, Jobin C, et al. Inhibition of cytokine-induced NF-kappaB activation by adenovirus-mediated expression of a NF-kappaB super-repressor prevents β-cell apoptosis. Diabetes 2001;50:2219-2224 (Pubitemid 33641904)
32. Kutlu B, Cardozo AK, Darville MI, et al. Discovery of gene networks regulating cytokine-induced dysfunction and apoptosis in insulin-producing INS-1 cells. Diabetes 2003;52:2701-2719 (Pubitemid 37339700)
33. Eizirik DL, Mandrup-Poulsen T. A choice of death - the signal-transduction of immune-mediated β-cell apoptosis. Diabetologia 2001;44:2115-2133 (Pubitemid 34015464)
34. Chen MC, Proost P, Gysemans C, Mathieu C, Eizirik DL. Monocyte chemoattractant protein-1 is expressed in pancreatic islets from prediabetic NOD mice and in interleukin-1 β-exposed human and rat islet cells. Diabetologia 2001;44:325-332 (Pubitemid 32234459)
35. Overbergh L, Valckx D, Waer M, Mathieu C. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine 1999;11:305-312 (Pubitemid 29213178)
36. Cardozo AK, Kruhøffer M, Leeman R, Orntoft T, Eizirik DL. Identification of novel cytokine-induced genes in pancreatic β-cells by high-density oligonucleotide arrays. Diabetes 2001;50:909-920 (Pubitemid 32374519)
37. Gurzov EN, Eizirik DL. Bcl-2 proteins in diabetes: mitochondrial pathways of β-cell death and dysfunction. Trends Cell Biol 2011;21:424-431
38. Gurzov EN, Germano CM, Cunha DA, et al. p53 up-regulated modulator of apoptosis (PUMA) activation contributes to pancreatic β-cell apoptosis induced by proinflammatory cytokines and endoplasmic reticulum stress. J Biol Chem 2010;285:19910-19920
39. Gurzov EN, Ortis F, Cunha DA, et al. Signaling by IL-1β+IFN-γ and ER stress converge on DP5/Hrk activation: a novel mechanism for pancreatic β-cell apoptosis. Cell Death Differ 2009;16:1539-1550
40. Barthson J, Germano CM, Moore F, et al. Cytokines tumor necrosis factor-α and interferon-γ induce pancreatic β-cell apoptosis through STAT1-mediated Bim protein activation. J Biol Chem 2011;286:39632-39643
41. Hübner A, Barrett T, Flavell RA, Davis RJ. Multisite phosphorylation regulates Bim stability and apoptotic activity. Mol Cell 2008;30:415-425 (Pubitemid 351672377)
42. Lee SI, Boyle DL, Berdeja A, Firestein GS. Regulation of inflammatory arthritis by the upstream kinase mitogen activated protein kinase kinase 7 in the c-Jun N-terminal kinase pathway. Arthritis Res Ther 2012;14:R38
43. Svensson CI, Inoue T, Hammaker D, et al. Gadd45β deficiency in rheumatoid arthritis: enhanced synovitis through JNK signaling. Arthritis Rheum 2009;60:3229-3240
44. Salerno DM, Tront JS, Hoffman B, Liebermann DA. Gadd45a and Gadd45b modulate innate immune functions of granulocytes and macrophages by differential regulation of p38 and JNK signaling. J Cell Physiol 2012;227:3613-3620
45. Chen Z, Pittman EF, Romaguera J, et al. Nuclear translocation of B-cell-specific transcription factor, BACH2, modulates ROS mediated cytotoxic responses in mantle cell lymphoma. PLoS ONE 2013;8:e69126
46. Muto A, Tashiro S, Tsuchiya H, et al. Activation of Maf/AP-1 repressor Bach2 by oxidative stress promotes apoptosis and its interaction with promyelocytic leukemia nuclear bodies. J Biol Chem 2002;277:20724-20733 (Pubitemid 34967377)
47. Ortis F, Miani M, Colli ML, et al. Differential usage of NF-κB activating signals by IL-1β and TNF-α in pancreatic beta cells. FEBS Lett 2012;586:984-989
48. Green M, Gandhi MK, Camilleri E, Marlton P, Lea R, Griffiths L. High levels of BACH2 associated with lower levels of BCL2 transcript abundance in t(14;18) (q21;q34) translocation positive non-Hodgkin's lymphoma. Leuk Res 2009;33:731-734
49. Kim EH, Gasper DJ, Lee SH, Plisch EH, Svaren J, Suresh M. Bach2 regulates homeostasis of Foxp3+ regulatory T cells and protects against fatal lung disease in mice. J Immunol 2014;192:985-995
50. Strasser A. The role of BH3-only proteins in the immune system. Nat Rev Immunol 2005;5:189-200 (Pubitemid 40364821)