Pancreatic beta cells are highly susceptible to oxidative and ER stresses during the development of diabetes

Journal of Proteome Research

Volumn 14, Issue 2, 2015, Pages 688-699

  Gorasia, Dhana G ^a   Dudek, Nadine L ^a,c   Veith, Paul D ^a   Shankar, Renu ^a   Safavi Hemami, Helena ^a,d   Williamson, Nicholas A ^a   Reynolds, Eric C ^a   Hubbard, Michael J ^b   Purcell, Anthony W ^a,c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

2D DIGE; Diabetes; ER stress; inflammation; MALDI TOF MS; oxidative stress

Indexed keywords

PROTEOME;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CELL COMPOSITION; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL HETEROGENEITY; CELL POPULATION; DISEASE COURSE; ENDOPLASMIC RETICULUM STRESS; INSULIN DEPENDENT DIABETES MELLITUS; ISOELECTRIC FOCUSING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; T LYMPHOCYTE; WESTERN BLOTTING; ANIMAL; ENDOPLASMIC RETICULUM; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PATHOLOGY; VALIDATION STUDY;

MURINAE; MUS;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; ENDOPLASMIC RETICULUM; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; OXIDATIVE STRESS;

EID: 84922680373     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500643h     Document Type: Article

References (57)

1. Kagi, D.; Odermatt, B.; Ohashi, P. S.; Zinkernagel, R. M.; Hengartner, H. Development of insulitis without diabetes in transgenic mice lacking perforin-dependent cytotoxicity J. Exp. Med. 1996, 183, 2143-52
2. Kagi, D.; Odermatt, B.; Seiler, P.; Zinkernagel, R. M.; Mak, T. W.; Hengartner, H. Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice J. Exp. Med. 1997, 186, 989-97
3. + T lymphocytes in transgenic nonobese diabetic mice J. Clin. Invest. 1999, 103, 1201-9
4. Savinov, A. Y.; Tcherepanov, A.; Green, E. A.; Flavell, R. A.; Chervonsky, A. V. Contribution of Fas to diabetes development Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 628-32
5. Allison, J.; Thomas, H. E.; Catterall, T.; Kay, T. W.; 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
6. + T lymphocytes Immunol. Cell Biol. 2009, 87, 178-85
7. Mandrup-Poulsen, T. The role of interleukin-1 in the pathogenesis of IDDM Diabetologia 1996, 39, 1005-29
8. Hoorens, A.; Pipeleers, D. Nicotinamide protects human beta cells against chemically-induced necrosis, but not against cytokine-induced apoptosis Diabetologia 1999, 42, 55-9
9. Pavlovic, D.; Chen, M. C.; Gysemans, C. A.; Mathieu, C.; Eizirik, D. L. The role of interferon regulatory factor-1 in cytokine-induced mRNA expression and cell death in murine pancreatic beta-cells Eur. Cytokine Network 1999, 10, 403-12
10. Nerup, J.; Mandrup-Poulsen, T.; Helqvist, S.; Andersen, H. U.; Pociot, F.; Reimers, J. I.; Cuartero, B. G.; Karlsen, A. E.; Bjerre, U.; Lorenzen, T. On the pathogenesis of IDDM Diabetologia 1994, 37, S82-9
11. Rabinovitch, A. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus Diabetes/Metab. Rev. 1998, 14, 129-51
12. Eizirik, D. L.; Pavlovic, D. Is there a role for nitric oxide in beta-cell dysfunction and damage in IDDM? Diabetes/Metab. Rev. 1997, 13, 293-307
13. Delaney, C. A.; Pavlovic, D.; Hoorens, A.; Pipeleers, D. G.; Eizirik, D. L. Cytokines induce deoxyribonucleic acid strand breaks and apoptosis in human pancreatic islet cells Endocrinology 1997, 138, 2610-4
14. Cardozo, A. K.; Heimberg, H.; Heremans, Y.; Leeman, R.; Kutlu, B.; Kruhoffer, M.; Orntoft, T.; Eizirik, D. L. A comprehensive analysis of cytokine-induced and nuclear factor-kappa B-dependent genes in primary rat pancreatic beta-cells J. Biol. Chem. 2001, 276, 48879-86
15. Papaccio, G.; Graziano, A.; D'Aquino, R.; Valiante, S.; Naro, F. A biphasic role of nuclear transcription factor (NF)-kappaB in the islet beta-cell apoptosis induced by interleukin (IL)-1beta J. Cell. Physiol. 2005, 204, 124-30
16. Gysemans, C. A.; Ladriere, L.; Callewaert, H.; Rasschaert, J.; Flamez, D.; Levy, D. E.; Matthys, P.; Eizirik, D. L.; Mathieu, C. Disruption of the gamma-interferon signaling pathway at the level of signal transducer and activator of transcription-1 prevents immune destruction of beta-cells Diabetes 2005, 54, 2396-403
17. Sparre, T.; Christensen, U. B.; Gotfredsen, C. F.; Larsen, P. M.; Fey, S. J.; Hjerno, K.; Roepstorff, P.; Pociot, F.; Karlsen, A. E.; Nerup, J. Changes in expression of IL-1 beta influenced proteins in transplanted islets during development of diabetes in diabetes-prone BB rats Diabetologia 2004, 47, 892-908
18. Sparre, T.; Christensen, U. B.; Mose Larsen, P.; Fey, S. J.; Wrzesinski, K.; Roepstorff, P.; Mandrup-Poulsen, T.; Pociot, F.; Karlsen, A. E.; Nerup, J. IL-1beta induced protein changes in diabetes prone BB rat islets of Langerhans identified by proteome analysis Diabetologia 2002, 45, 1550-61
19. Sparre, T.; Larsen, M. R.; Heding, P. E.; Karlsen, A. E.; Jensen, O. N.; Pociot, F. Unraveling the pathogenesis of type 1 diabetes with proteomics: present and future directions Mol. Cell. Proteomics 2005, 4, 441-57
20. D'Hertog, W.; Overbergh, L.; Lage, K.; Ferreira, G. B.; Maris, M.; Gysemans, C.; Flamez, D.; Cardozo, A. K.; Van den Bergh, G.; Schoofs, L.; Arckens, L.; Moreau, Y.; Hansen, D. A.; Eizirik, D. L.; Waelkens, E.; Mathieu, C. Proteomics analysis of cytokine-induced dysfunction and death in insulin-producing INS-1E cells: new insights into the pathways involved Mol. Cell. Proteomics 2007, 6, 2180-99
21. Hamaguchi, K.; Gaskins, H. R.; Leiter, E. H. NIT-1, a pancreatic beta-cell line established from a transgenic NOD/Lt mouse Diabetes 1991, 40, 842-9
22. Powers, A. C.; Efrat, S.; Mojsov, S.; Spector, D.; Habener, J. F.; Hanahan, D. Proglucagon processing similar to normal islets in pancreatic alpha-like cell line derived from transgenic mouse tumor Diabetes 1990, 39, 406-14
23. Veith, P. D.; O'Brien-Simpson, N. M.; Tan, Y.; Djatmiko, D. C.; Dashper, S. G.; Reynolds, E. C. Outer membrane proteome and antigens of Tannerella forsythia J. Proteome Res. 2009, 8, 4279-92
24. Ashburner, M.; Ball, C. A.; Blake, J. A.; Botstein, D.; Butler, H.; Cherry, J. M.; Davis, A. P.; Dolinski, K.; Dwight, S. S.; Eppig, J. T.; Harris, M. A.; Hill, D. P.; Issel-Tarver, L.; Kasarskis, A.; Lewis, S.; Matese, J. C.; Richardson, J. E.; Ringwald, M.; Rubin, G. M.; Sherlock, G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nat. Genet. 2000, 25, 25-9
25. Bhatia, V. N.; Perlman, D. H.; Costello, C. E.; McComb, M. E. Software tool for researching annotations of proteins: open-source protein annotation software with data visualization Anal. Chem. 2009, 81, 9819-23
26. Eizirik, D. L.; Mandrup-Poulsen, T. A choice of death-the signal-transduction of immune-mediated beta-cell apoptosis Diabetologia 2001, 44, 2115-33
27. Eizirik, D. L.; Pipeleers, D. G.; Ling, Z.; Welsh, N.; Hellerstrom, C.; Andersson, A. Major species differences between humans and rodents in the susceptibility to pancreatic beta-cell injury Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 9253-6
28. Grankvist, K.; Marklund, S. L.; Taljedal, I. B. CuZn-superoxide dismutase, Mn-superoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse Biochem. J. 1981, 199, 393-8
29. Lenzen, S.; Drinkgern, J.; Tiedge, M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues Free Radical Biol. Med. 1996, 20, 463-6
30. Tiedge, M.; Lortz, S.; Drinkgern, J.; Lenzen, S. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells Diabetes 1997, 46, 1733-42
31. Welsh, N.; Margulis, B.; Borg, L. A.; Wiklund, H. J.; Saldeen, J.; Flodstrom, M.; Mello, M. A.; Andersson, A.; Pipeleers, D. G.; Hellerstrom, C. Differences in the expression of heat-shock proteins and antioxidant enzymes between human and rodent pancreatic islets: implications for the pathogenesis of insulin-dependent diabetes mellitus Mol. Med. 1995, 1, 806-20
32. Dudek, N. L.; Tan, C. T.; Gorasia, D. G.; Croft, N. P.; Illing, P. T.; Purcell, A. W. Constitutive and inflammatory immunopeptidome of pancreatic beta-cells Diabetes 2012, 61, 3018-25
33. Pham, H.; Doerrbecker, J.; Ramp, A. A.; D'Souza, C. S.; Gorasia, D. G.; Purcell, A. W.; Ayers, M. M.; Orian, J. M. Experimental autoimmune encephalomyelitis (EAE) IN C57Bl/6 mice is not associated with astrogliosis J. Neuroimmunol. 2011, 232, 51-62
34. Shnyder, S. D.; Mangum, J. E.; Hubbard, M. J. Triplex profiling of functionally distinct chaperones (ERp29/PDI/BiP) reveals marked heterogeneity of the endoplasmic reticulum proteome in cancer J. Proteome Res. 2008, 7, 3364-72
35. Hostens, K.; Pavlovic, D.; Zambre, Y.; Ling, Z.; Van Schravendijk, C.; Eizirik, D. L.; Pipeleers, D. G. Exposure of human islets to cytokines can result in disproportionately elevated proinsulin release J. Clin. Invest. 1999, 104, 67-72
36. Borjesson, A.; Carlsson, C. Altered proinsulin conversion in rat pancreatic islets exposed long-term to various glucose concentrations or interleukin-1beta J. Endocrinol. 2007, 192, 381-7
37. Hansen, B. S.; Nielsen, J. H.; Linde, S.; Spinas, G. A.; Welinder, B. S.; Mandrup-Poulsen, T.; Nerup, J. Effect of interleukin-1 on the biosynthesis of proinsulin and insulin in isolated rat pancreatic islets Biomed. Biochim. Acta 1988, 47, 305-9
38. Thiede, B.; Siejak, F.; Dimmler, C.; Rudel, T. Prediction of translocation and cleavage of heterogeneous ribonuclear proteins and Rho guanine nucleotide dissociation inhibitor 2 during apoptosis by subcellular proteome analysis Proteomics 2002, 2, 996-1006
39. Lee, H. S.; Jeong, J.; Lee, K. J. Characterization of vesicles secreted from insulinoma NIT-1 cells J. Proteome Res. 2009, 8, 2851-62
40. Sanchez, J. C.; Chiappe, D.; Converset, V.; Hoogland, C.; Binz, P. A.; Paesano, S.; Appel, R. D.; Wang, S.; Sennitt, M.; Nolan, A.; Cawthorne, M. A.; Hochstrasser, D. F. The mouse SWISS-2D PAGE database: a tool for proteomics study of diabetes and obesity Proteomics 2001, 1, 136-63
41. Nicolls, M. R.; D'Antonio, J. M.; Hutton, J. C.; Gill, R. G.; Czwornog, J. L.; Duncan, M. W. Proteomics as a tool for discovery: proteins implicated in Alzheimer's disease are highly expressed in normal pancreatic islets J. Proteome Res. 2003, 2, 199-205
42. Ahmed, M.; Bergsten, P. Glucose-induced changes of multiple mouse islet proteins analysed by two-dimensional gel electrophoresis and mass spectrometry Diabetologia 2005, 48, 477-85
43. Waanders, L. F.; Chwalek, K.; Monetti, M.; Kumar, C.; Lammert, E.; Mann, M. Quantitative proteomic analysis of single pancreatic islets Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 18902-7
44. John, N. E.; Andersen, H. U.; Fey, S. J.; Larsen, P. M.; Roepstorff, P.; Larsen, M. R.; Pociot, F.; Karlsen, A. E.; Nerup, J.; Green, I. C.; Mandrup-Poulsen, T. Cytokine- or chemically derived nitric oxide alters the expression of proteins detected by two-dimensional gel electrophoresis in neonatal rat islets of Langerhans Diabetes 2000, 49, 1819-29
45. Larsen, P. M.; Fey, S. J.; Larsen, M. R.; Nawrocki, A.; Andersen, H. U.; Kahler, H.; Heilmann, C.; Voss, M. C.; Roepstorff, P.; Pociot, F.; Karlsen, A. E.; Nerup, J. Proteome analysis of interleukin-1beta-induced changes in protein expression in rat islets of Langerhans Diabetes 2001, 50, 1056-63
46. Ortis, F.; Naamane, N.; Flamez, D.; Ladriere, L.; Moore, F.; Cunha, D. A.; Colli, M. L.; Thykjaer, T.; Thorsen, K.; Orntoft, T. F.; Eizirik, D. L. Cytokines interleukin-1beta and tumor necrosis factor-alpha regulate different transcriptional and alternative splicing networks in primary beta-cells Diabetes 2010, 59, 358-74
47. Maritim, A. C.; Sanders, R. A.; Watkins, J. B., III Diabetes, oxidative stress, and antioxidants: a review J. Biochem. Mol. Toxicol. 2003, 17, 24-38
48. Jiang, Z. Y.; Woollard, A. C.; Wolff, S. P. Hydrogen peroxide production during experimental protein glycation FEBS Lett. 1990, 268, 69-71
49. Wolff, S. P.; Dean, R. T. Glucose autoxidation and protein modification. The potential role of 'autoxidative glycosylation' in diabetes Biochem. J. 1987, 245, 243-50
50. Azevedo-Martins, A. K.; Lortz, S.; Lenzen, S.; Curi, R.; Eizirik, D. L.; Tiedge, M. Improvement of the mitochondrial antioxidant defense status prevents cytokine-induced nuclear factor-kappaB activation in insulin-producing cells Diabetes 2003, 52, 93-101
51. Wolf, G.; Aumann, N.; Michalska, M.; Bast, A.; Sonnemann, J.; Beck, J. F.; Lendeckel, U.; Newsholme, P.; Walther, R. Peroxiredoxin III protects pancreatic ss cells from apoptosis J. Endocrinol. 2010, 207, 163-75
52. Chen, H.; Li, X.; Epstein, P. N. MnSOD and catalase transgenes demonstrate that protection of islets from oxidative stress does not alter cytokine toxicity Diabetes 2005, 54, 1437-46
53. Gurgul, E.; Lortz, S.; Tiedge, M.; Jorns, A.; Lenzen, S. Mitochondrial catalase overexpression protects insulin-producing cells against toxicity of reactive oxygen species and proinflammatory cytokines Diabetes 2004, 53, 2271-80
54. Cnop, M.; Welsh, N.; Jonas, J. C.; Jorns, A.; Lenzen, S.; Eizirik, D. L. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities Diabetes 2005, 54, S97-107
55. Eizirik, D. L.; Cardozo, A. K.; Cnop, M. The role for endoplasmic reticulum stress in diabetes mellitus Endocr. Rev. 2008, 29, 42-61
56. 2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells Diabetes 2005, 54, 452-61
57. Wang, M.; Zhao, X. R.; Wang, P.; Li, L.; Dai, Y.; Huang, H.; Lei, P.; Zhu, H. F.; Shen, G. X. Glucose regulated proteins 78 protects insulinoma cells (NIT-1) from death induced by streptozotocin, cytokines or cytotoxic T lymphocytes Int. J. Biochem. Cell Biol. 2007, 39, 2076-82