DJ-1 protects pancreatic beta cells from cytokine- and streptozotocin-mediated cell death

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Jain, Deepak ^a,b   Weber, Gesine ^a   Eberhard, Daniel ^a   Mehana, Amir E ^c,d   Eglinger, Jan ^a,b   Welters, Alena ^a,b,e   Bartosinska, Barbara ^a   Jeruschke, Kay ^a   Weiss, Jürgen ^a   Päth, Günter ^c   Ariga, Hiroyoshi ^f   Seufert, Jochen ^c   Lammert, Eckhard ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d Suez Canal University   (Egypt)

^e UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^f HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DJ 1 PROTEIN; INTERLEUKIN 1BETA; STREPTOZOCIN; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; INSULIN; ONCOPROTEIN; PARK7 PROTEIN, MOUSE; PEROXIREDOXIN; PROTEIN DEGLYCASE DJ-1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROTECTION; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE MICROSCOPY; GENE; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; IMMUNOFLUORESCENCE TEST; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; LASER MICROSCOPY; MALE; MITOCHONDRION; MORPHOLOGY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PARK7 GENE; PROTEIN ANALYSIS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SECRETORY VESICLE;

ANIMALS; CELL DEATH; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; ONCOGENE PROTEINS; PEROXIREDOXINS; PROTEIN DEGLYCASE DJ-1; SECRETORY VESICLES;

EID: 84947776217     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138535     Document Type: Article

References (41)

1. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and beta-cell loss in type 1 diabetes Nature reviews Endocrinology. 2009; 5(4):219-26. Epub 2009/04/09. DOI: 10.1038/nrendo.2009.21 PMID: 19352320.
2. Cnop M, Vidal J, Hull RL, Utzschneider KM, Carr DB, Schraw T, et al. Progressive loss of beta-cell function leads to worsening glucose tolerance in first-degree relatives of subjects with type 2 diabetes. Diabetes care. 2007; 30(3):677-82. Epub 2007/03/01. DOI: 10.2337/dc06-1834 PMID: 17327340.
3. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003; 52(1):102-10. Epub 2002/12/28. PMID: 12502499.
4. Lundh M, Scully SS, Mandrup-Poulsen T, Wagner BK. Small-molecule inhibition of inflammatory betacell death. Diabetes, obesity & metabolism. 2013; 15 Suppl 3:176-84. Epub 2013/09/18. DOI: 10.1111/ dom.12158 PMID: 24003935; PubMed Central PMCID: PMC3777666.
5. Jorns A, Arndt T, Meyer zu Vilsendorf A, Klempnauer J, Wedekind D, Hedrich HJ, et al. Islet infiltration, cytokine expression and beta cell death in the NOD mouse, BB rat, Komeda rat, LEW.1AR1-iddm rat and humans with type 1 diabetes. Diabetologia. 2014; 57(3):512-21. Epub 2013/12/07. DOI: 10.1007/ s00125-013-3125-4 PMID: 24310561.
6. Bensellam M, Laybutt DR, Jonas JC. The molecular mechanisms of pancreatic beta-cell glucotoxicity: recent findings and future research directions. Molecular and cellular endocrinology. 2012; 364(1-2):1-27. Epub 2012/08/14. DOI: 10.1016/j.mce.2012.08.003 PMID: 22885162.
7. Abdulreda MH, Berggren PO. Islet inflammation in plain sight. Diabetes, obesity & metabolism. 2013; 15 Suppl 3:105-16. Epub 2013/09/18. DOI: 10.1111/dom.12160 PMID: 24003927; PubMed Central PMCID: PMC3777660.
8. Donath MY, Schumann DM, Faulenbach M, Ellingsgaard H, Perren A, Ehses JA. Islet inflammation in type 2 diabetes: from metabolic stress to therapy. Diabetes care. 2008; 31 Suppl 2:S161-4. Epub 2008/02/15. DOI: 10.2337/dc08-s243 PMID: 18227479.
9. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nature reviews Immunology. 2011; 11(2):98-107. Epub 2011/01/15. DOI: 10.1038/nri2925 PMID: 21233852.
10. Jain D, Jain R, Eberhard D, Eglinger J, Bugliani M, Piemonti L, et al. Age- and diet-dependent requirement of DJ-1 for glucose homeostasis in mice with implications for human type 2 diabetes. Journal of molecular cell biology. 2012; 4(4):221-30. Epub 2012/05/23. DOI: 10.1093/jmcb/mjs025 PMID: 22611253.
11. Waanders LF, Chwalek K, Monetti M, Kumar C, Lammert E, Mann M. Quantitative proteomic analysis of single pancreatic islets. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(45):18902-7. Epub 2009/10/23. DOI: 10.1073/pnas.0908351106 PMID: 19846766; PubMed Central PMCID: PMC2765458.
12. Inberg A, Linial M. Protection of pancreatic beta-cells from various stress conditions is mediated by DJ-1. The Journal of biological chemistry. 2010; 285(33):25686-98. Epub 2010/06/03. DOI: 10.1074/jbc. M110.109751 PMID: 20516060; PubMed Central PMCID: PMC2919132.
13. Junn E, Taniguchi H, Jeong BS, Zhao X, Ichijo H, Mouradian MM. Interaction of DJ-1 with Daxx inhibits apoptosis signal-regulating kinase 1 activity and cell death. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(27):9691-6. Epub 2005/06/29. DOI: 10.1073/pnas. 0409635102 PMID: 15983381; PubMed Central PMCID: PMC1172235.
14. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, et al. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature. 2010; 468(7324):696-700. Epub 2010/11/12. DOI: 10.1038/nature09536 PMID: 21068725.
15. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free radical biology & medicine. 1996; 20(3):463-6. Epub 1996/01/01. PMID: 8720919.
16. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochemical Society transactions. 2008; 36(Pt 3):343-7. Epub 2008/05/17. DOI: 10.1042/BST0360343 PMID: 18481954.
17. Martinat C, Shendelman S, Jonason A, Leete T, Beal MF, Yang L, et al. Sensitivity to oxidative stress in DJ-1-deficient dopamine neurons: an ES- derived cell model of primary Parkinsonism. PLoS biology. 2004; 2(11):e327. Epub 2004/10/27. DOI: 10.1371/journal.pbio.0020327 PMID: 15502868; PubMed Central PMCID: PMC521171.
18. Hwang S, Song S, Hong YK, Choi G, Suh YS, Han SY, et al. Drosophila DJ-1 decreases neural sensitivity to stress by negatively regulating Daxx-like protein through dFOXO. PLoS genetics. 2013; 9(4): e1003412. Epub 2013/04/18. DOI: 10.1371/journal.pgen.1003412 PMID: 23593018; PubMed Central PMCID: PMC3616925.
19. Mabley JG, Rabinovitch A, Suarez-Pinzon W, Hasko G, Pacher P, Power R, et al. Inosine protects against the development of diabetes in multiple-low-dose streptozotocin and nonobese diabetic mouse models of type 1 diabetes. Mol Med. 2003; 9(3-4):96-104. Epub 2003/07/17. PMID: 12865945; PubMed Central PMCID: PMC1430728.
20. Emre Y, Hurtaud C, Karaca M, Nubel T, Zavala F, Ricquier D. Role of uncoupling protein UCP2 in cellmediated immunity: how macrophage-mediated insulitis is accelerated in a model of autoimmune diabetes. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104 (48):19085-90. Epub 2007/11/17. DOI: 10.1073/pnas.0709557104 PMID: 18006654; PubMed Central PMCID: PMC2141912.
21. Goldberg MS, Pisani A, Haburcak M, Vortherms TA, Kitada T, Costa C, et al. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron. 2005; 45(4):489-96. Epub 2005/02/22. DOI: 10.1016/j.neuron.2005.01.041 PMID: 15721235.
22. Konstantinova I, Nikolova G, Ohara-Imaizumi M, Meda P, Kucera T, Zarbalis K, et al. EphA-Ephrin-Amediated beta cell communication regulates insulin secretion from pancreatic islets. Cell. 2007; 129 (2):359-70. Epub 2007/04/24. DOI: 10.1016/j.cell.2007.02.044 PMID: 17448994.
23. Yamaguchi S, Yamane T, Takahashi-Niki K, Kato I, Niki T, Goldberg MS, et al. Transcriptional activation of low-density lipoprotein receptor gene by DJ-1 and effect of DJ-1 on cholesterol homeostasis. PLoS One. 2012; 7(5):e38144. DOI: 10.1371/journal.pone.0038144 PMID: 22666465; PubMed Central PMCID: PMCPMC3364227.
24. Spurr AR. A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of ultrastructure research. 1969; 26(1):31-43. Epub 1969/01/01. PMID: 4887011.
25. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nature methods. 2012; 9(7):676-82. Epub 2012/06/30. DOI: 10. 1038/nmeth.2019 PMID: 22743772; PubMed Central PMCID: PMC3855844.
26. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3(6):1101-8. PMID: 18546601.
27. Soltani N, Qiu H, Aleksic M, Glinka Y, Zhao F, Liu R, et al. GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(28):11692-7. Epub 2011/06/29. DOI: 10.1073/pnas. 1102715108 PMID: 21709230; PubMed Central PMCID: PMC3136292.
28. Hansen JB, Tonnesen MF, Madsen AN, Hagedorn PH, Friberg J, Grunnet LG, et al. Divalent metal transporter 1 regulates iron-mediated ROS and pancreatic beta cell fate in response to cytokines. Cell metabolism. 2012; 16(4):449-61. Epub 2012/09/25. DOI: 10.1016/j.cmet.2012.09.001 PMID: 23000401.
29. Xiang FL, Lu X, Strutt B, Hill DJ, Feng Q. NOX2 deficiency protects against streptozotocin-induced beta-cell destruction and development of diabetes in mice. Diabetes. 2010; 59(10):2603-11. Epub 2010/07/16. DOI: 10.2337/db09-1562 PMID: 20627937; PubMed Central PMCID: PMC3279537.
30. Kim JM, Jang HJ, Choi SY, Park SA, Kim IS, Yang YR, et al. DJ-1 contributes to adipogenesis and obesity-induced inflammation. Scientific reports. 2014; 4:4805. Epub 2014/06/14. DOI: 10.1038/srep04805 PMID: 24925581; PubMed Central PMCID: PMC4055892.
31. Seyfarth K, Poschmann G, Rozman J, Fromme T, Rink N, Hofmann A, et al. The development of dietinduced obesity and associated metabolic impairments in Dj-1 deficient mice. J Nutr Biochem. 2015; 26 (1):75-81. DOI: 10.1016/j.jnutbio.2014.09.002 PMID: 25448609.
32. Chen H, Li X, Epstein PN. MnSOD and catalase transgenes demonstrate that protection of islets from oxidative stress does not alter cytokine toxicity. Diabetes. 2005; 54(5):1437-46. Epub 2005/04/28. PMID: 15855331.
33. Ren H, Fu K, Wang D, Mu C, Wang G. Oxidized DJ-1 interacts with the mitochondrial protein BCL-XL. The Journal of biological chemistry. 2011; 286(40):35308-17. Epub 2011/08/20. DOI: 10.1074/jbc. M110.207134 PMID: 21852238; PubMed Central PMCID: PMC3186373.
34. Mitsumoto A, Nakagawa Y. DJ-1 is an indicator for endogenous reactive oxygen species elicited by endotoxin. Free Radic Res. 2001; 35(6):885-93. PMID: 11811539.
35. Clements CM, McNally RS, Conti BJ, Mak TW, Ting JP. DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(41):15091-6. DOI: 10.1073/ pnas.0607260103 PMID: 17015834; PubMed Central PMCID: PMC1586179.
36. Wang X, Petrie TG, Liu Y, Liu J, Fujioka H, Zhu X. Parkinson's disease-associated DJ-1 mutations impair mitochondrial dynamics and cause mitochondrial dysfunction. J Neurochem. 2012; 121(5):830-9. DOI: 10.1111/j.1471-4159.2012.07734.x PMID: 22428580; PubMed Central PMCID: PMC3740560.
37. Kim YC, Kitaura H, Taira T, Iguchi-Ariga SM, Ariga H. Oxidation of DJ-1-dependent cell transformation through direct binding of DJ-1 to PTEN. Int J Oncol. 2009; 35(6):1331-41. PMID: 19885556.
38. Evans-Molina C, Hatanaka M, Mirmira RG. Lost in translation: endoplasmic reticulum stress and the decline of beta-cell health in diabetes mellitus. Diabetes, obesity & metabolism. 2013; 15 Suppl 3:159-69. DOI: 10.1111/dom.12163 PMID: 24003933; PubMed Central PMCID: PMCPMC3777692.
39. Fonseca SG, Gromada J, Urano F. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol Metab. 2011; 22(7):266-74. DOI: 10.1016/j.tem.2011.02.008 PMID: 21458293; PubMed Central PMCID: PMCPMC3130122.
40. Zhou W, Bercury K, Cummiskey J, Luong N, Lebin J, Freed CR. Phenylbutyrate up-regulates the DJ-1 protein and protects neurons in cell culture and in animal models of Parkinson disease. The Journal of biological chemistry. 2011; 286(17):14941-51. Epub 2011/03/05. DOI: 10.1074/jbc.M110.211029 PMID: 21372141; PubMed Central PMCID: PMC3083206.
41. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006; 313(5790):1137-40. Epub 2006/08/26. DOI: 10.1126/science.1128294 PMID: 16931765.