High glucose induces dysfunction in insulin secretory cells by different pathways: A proteomic approach

Journal of Proteome Research

Volumn 9, Issue 12, 2010, Pages 6274-6287

  Maris, Michael ^a   Ferreira, Gabriela B ^a   D'Hertog, Wannes ^a   Cnop, Miriam ^b,c   Waelkens, Etienne ^d,e   Overbergh, Lut ^a   Mathieu, Chantal ^a  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c ERASME HOSPITAL   (Belgium)

^d LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLUCOSE; INSULIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HYPERGLYCEMIA; INSULIN RELEASE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; PROTEOMICS; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; INSULINOMA; MODELS, BIOLOGICAL; PROTEINS; PROTEOMICS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 78649826295     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr100557w     Document Type: Article

References (78)

1. Unger, R. H.; Grundy, S. Hyperglycaemia as an inducer as well as a consequence of impaired islet cell function and insulin resistance: implications for the management of diabetes Diabetologia 1985, 28, 119-121
2. Ahren, B. Insulin secretion and insulin sensitivity in relation to fasting glucose in healthy subjects Diabetes Care 2007, 30, 644-648
3. Poitout, V.; Hagman, D.; Stein, R. Regulation of the insulin gene by glucose and fatty acids J. Nutr. 2006, 136, 873-876
4. Hagman, D. K.; Latour, M. G.; Chakrabarti, S. K. Cyclical and alternating infusions of glucose and intralipid in rats inhibit insulin gene expression and Pdx-1 binding in islets Diabetes 2008, 57, 424-431
5. Olofsson, C. S.; Collins, S.; Bengtsson, M. Long-term exposure to glucose and lipids inhibits glucose-induced insulin secretion downstream of granule fusion with plasma membrane Diabetes 2007, 56, 1888-1897
6. Carlsson, C.; Borg, L. A.; Welsh, N. Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro Endocrinology 1999, 140, 3422-3428
7. Ihara, Y.; Toyokuni, S.; Uchida, K. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes Diabetes 1999, 48, 927-932
8. Maestre, I.; Jordan, J.; Calvo, S. Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS- 1 Endocrinology 2003, 144, 335-345
9. Lenzen, S.; Drinkgern, J.; Tiedge, M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues Free Radic. Biol. Med. 1996, 20, 463-466
10. Rutkowski, D. T.; Kaufman, R. J. A trip to the ER: coping with stress Trends Cell Biol. 2004, 14, 20-28
11. Boyce, M.; Yuan, J. Cellular response to endoplasmic reticulum stress: a matter of life or death Cell Death Differ. 2006, 13, 363-373
12. Schroder, M. The unfolded protein response Mol. Biotechnol. 2006, 34, 279-290
13. Nyblom, H. K.; Thorn, K.; Ahmed, M. Mitochondrial protein patterns correlating with impaired insulin secretion from INS-1E cells exposed to elevated glucose concentrations Proteomics 2006, 6, 5193-5198
14. Coute, Y.; Brunner, Y.; Schvartz, D. Early activation of the fatty acid metabolism pathway by chronic high glucose exposure in rat insulin secretory beta-cells Proteomics 2010, 10, 59-71
15. Alberti, A.; Karamessinis, P.; Peroulis, M. ERp46 is reduced by high glucose and regulates insulin content in pancreatic beta-cells Am J Physiol Endocrinol Metab 2009, 297 E812-E821
16. Dowling, P.; O'Driscoll, L.; O'Sullivan, F. Proteomic screening of glucose-responsive and glucose non-responsive MIN-6 beta cells reveals differential expression of proteins involved in protein folding, secretion and oxidative stress Proteomics 2006, 6, 6578-6587
17. Waanders, L. F.; Chwalek, K.; Monetti, M. Quantitative proteomic analysis of single pancreatic islets Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 18902-18907
18. Merglen, A.; Theander, S.; Rubi, B. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E. insulinoma cells Endocrinology 2004, 145, 667-678
19. Olson, L. K.; Redmon, J. B.; Towle, H. C. Chronic exposure of HIT cells to high glucose concentrations paradoxically decreases insulin gene transcription and alters binding of insulin gene regulatory protein J. Clin. Invest. 1993, 92, 514-519
20. Poitout, V.; Olson, L. K.; Robertson, R. P. Chronic exposure of betaTC-6 cells to supraphysiologic concentrations of glucose decreases binding of the RIPE3b1 insulin gene transcription activator J. Clin. Invest. 1996, 97, 1041-1046
21. Ishihara, H.; Asano, T.; Tsukuda, K. Pancreatic beta cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets Diabetologia 1993, 36, 1139-1145
22. Asfari, M.; Janjic, D.; Meda, P. Establishment of 2 mercaptoethanol- dependent differentiated insulin-secreting cell lines Endocrinology 1992, 130, 167-178
23. Bensellam, M.; Van, L. L.; Overbergh, L. Cluster analysis of rat pancreatic islet gene mRNA levels after culture in low-, intermediate- and high-glucose concentrations Diabetologia 2009, 52, 463-476
24. Elouil, H.; Bensellam, M.; Guiot, Y. Acute nutrient regulation of the unfolded protein response and integrated stress response in cultured rat pancreatic islets Diabetologia 2007, 50, 1442-1452
25. Efanova, I. B.; Zaitsev, S. V.; Zhivotovsky, B. Glucose and tolbutamide induce apoptosis in pancreatic beta-cells. A process dependent on intracellular Ca2+ concentration J. Biol. Chem. 1998, 273, 33501-33507
26. Van de Casteele, M.; Kefas, B. A.; Cai, Y. Prolonged culture in low glucose induces apoptosis of rat pancreatic beta-cells through induction of c-myc Biochem. Biophys. Res. Commun. 2003, 312, 937-944
27. Robertson, R. P.; Harmon, J.; Tran, P. O. Glucose toxicity in beta-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection Diabetes 2003, 52, 581-587
28. Callewaert, H. I.; Gysemans, C. A.; Ladriere, L. Deletion of STAT-1 pancreatic islets protects against streptozotocin-induced diabetes and early graft failure but not against late rejection Diabetes 2007, 56, 2169-2173
29. Gysemans, C. A.; Ladriere, L.; Callewaert, H. 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, 2396-2403
30. Gysemans, C. A.; Cardozo, A. K.; Callewaert, H. 1,25 Dihydroxyvitamin D3 modulates expression of chemokines and cytokines in pancreatic islets: implications for prevention of diabetes in nonobese diabetic mice Endocrinology 2005, 146, 1956-1964
31. Cunha, D. A.; Hekerman, P.; Ladriere, L. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells J. Cell Sci. 2008, 121, 2308-2318
32. Hopcroft, D. W.; Mason, D. R.; Scott, R. S. Standardization of insulin secretion from pancreatic islets: validation of a DNA assay Horm.Metab Res. 1985, 17, 559-561
33. D'Hertog, W.; Overbergh, L.; Lage, K.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, 2180-2199
34. Moore, F.; Colli, M. L.; Cnop, M. PTPN2, a candidate gene for type 1 diabetes, modulates interferon-gamma-induced pancreatic beta-cell apoptosis Diabetes 2009, 58, 1283-1291
35. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 2001, 29, e45
36. Randle, P. J. Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years Diabetes Metab. Rev. 1998, 14, 263-283
37. Roche, E.; ssimacopoulos-Jeannet, F.; Witters, L. A. Induction by glucose of genes coding for glycolytic enzymes in a pancreatic beta-cell line (INS-1) J. Biol. Chem. 1997, 272, 3091-3098
38. Sol, E. R.; Hovsepyan, M.; Bergsten, P. Proteins altered by elevated levels of palmitate or glucose implicated in impaired glucose-stimulated insulin secretion Proteome Sci. 2009, 7, 24
39. Kajimoto, Y.; Kaneto, H. Role of oxidative stress in pancreatic beta-cell dysfunction Ann. N.Y. Acad. Sci. 2004, 1011, 168-176
40. Robertson, R. P. Oxidative stress and impaired insulin secretion in type 2 diabetes Curr. Opin. Pharmacol. 2006, 6, 615-619
41. Maechler, P.; Jornot, L.; Wollheim, C. B. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells J. Biol. Chem. 1999, 274, 27905-27913
42. Eizirik, D. L.; Cardozo, A. K.; Cnop, M. The role for endoplasmic reticulum stress in diabetes mellitus Endocr. Rev. 2008, 29, 42-61
43. Scheuner, D.; Kaufman, R. J. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes Endocr. Rev. 2008, 29, 317-333
44. Laybutt, D. R.; Preston, A. M.; Akerfeldt, M. C. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes Diabetologia 2007, 50, 752-763
45. Nakatani, Y.; Kaneto, H.; Kawamori, D. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes J. Biol. Chem. 2005, 280, 847-851 (Pubitemid 40165054)
46. Kobayashi, T.; Ogawa, S.; Yura, T. Abundant expression of 150 kDa oxygen-regulated protein in mouse pancreatic beta cells is correlated with insulin secretion Biochem. Biophys. Res. Commun. 2000, 267, 831-837
47. Holcik, M.; Sonenberg, N. Translational control in stress and apoptosis Nat. Rev. Mol. Cell. Biol. 2005, 6, 318-327
48. Richter-Cook, N. J.; Dever, T. E.; Hensold, J. O. Purification and characterization of a new eukaryotic protein translation factor. Eukaryotic initiation factor 4H J. Biol. Chem. 1998, 273, 7579-7587
49. Richter, N. J.; Rogers, G. W., Jr.; Hensold, J. O. Further biochemical and kinetic characterization of human eukaryotic initiation factor 4H J. Biol. Chem. 1999, 274, 35415-35424
50. Rogers, G. W., Jr.; Richter, N. J.; Lima, W. F. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F J. Biol. Chem. 2001, 276, 30914-30922
51. Browne, G. J.; Proud, C. G. Regulation of peptide-chain elongation in mammalian cells Eur. J. Biochem. 2002, 269, 5360-5368
52. Venema, R. C.; Peters, H. I.; Traugh JA Phosphorylation of elongation factor 1 (EF-1) and valyl-tRNA synthetase by protein kinase C and stimulation of EF-1 activity J. Biol. Chem. 1991, 266, 12574-12580
53. Venema, R. C.; Peters, H. I.; Traugh JA Phosphorylation of valyl-tRNA synthetase and elongation factor 1 in response to phorbol esters is associated with stimulation of both activities J. Biol. Chem. 1991, 266, 11993-11998
54. Yan, L.; Nairn, A. C.; Palfrey, H. C. Glucose regulates EF-2 phosphorylation and protein translation by a protein phosphatase-2A-dependent mechanism in INS-1-derived 832/13 cells J. Biol. Chem. 2003, 278, 18177-18183
55. Harding, H. P.; Novoa, I.; Zhang, Y. Regulated translation initiation controls stress-induced gene expression in mammalian cells Mol. Cell 2000, 6, 1099-1108
56. Terai, K.; Hiramoto, Y.; Masaki, M. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress Mol. Cell. Biol. 2005, 25, 9554-9575
57. Boyce, M.; Py, B. F.; Ryazanov, A. G. A pharmacoproteomic approach implicates eukaryotic elongation factor 2 kinase in ER stress-induced cell death Cell Death Differ. 2008, 15, 589-599
58. Hu, B. R.; Janelidze, S.; Ginsberg, M. D. Protein aggregation after focal brain ischemia and reperfusion J. Cereb. Blood Flow Metab. 2001, 21, 865-875
59. Bence, N. F.; Sampat, R. M.; Kopito, R. R. Impairment of the ubiquitin-proteasome system by protein aggregation Science 2001, 292, 1552-1555
60. Demand, J.; Alberti, S.; Patterson, C. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling Curr. Biol. 2001, 11, 1569-1577
61. Ballinger, C. A.; Connell, P.; Wu, Y. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions Mol. Cell. Biol. 1999, 19, 4535-4545
62. Wojcik, C.; Di, N. M. Ubiquitin-proteasome system and proteasome inhibition: new strategies in stroke therapy Stroke 2004, 35, 1506-1518
63. Kitiphongspattana, K.; Mathews, C. E.; Leiter, E. H. Proteasome inhibition alters glucose-stimulated (pro)insulin secretion and turnover in pancreatic {beta}-cells J. Biol. Chem. 2005, 280, 15727-15734
64. Kawaguchi, M.; Minami, K.; Nagashima, K. Essential role of ubiquitin-proteasome system in normal regulation of insulin secretion J. Biol. Chem. 2006, 281, 13015-13020
65. Casas, S.; Gomis, R.; Gribble, F. M. Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic beta-cell apoptosis Diabetes 2007, 56, 2284-2294
66. Hayashi, T.; Juliet, P. A.; Miyazaki, A. High glucose downregulates the number of caveolae in monocytes through oxidative stress from NADPH oxidase: implications for atherosclerosis Biochim. Biophys. Acta 2007, 1772, 364-372
67. King, S. J.; Schroer, T. A. Dynactin increases the processivity of the cytoplasmic dynein motor Nat. Cell Biol. 2000, 2, 20-24
68. Deacon, S. W.; Serpinskaya, A. S.; Vaughan, P. S. Dynactin is required for bidirectional organelle transport J. Cell Biol. 2003, 160, 297-301
69. Heald, R.; Nogales, E. Microtubule dynamics J. Cell Sci. 2002, 115, 3-4
70. Smith, R.; Bacos, K.; Fedele, V. Mutant huntingtin interacts with {beta}-tubulin and disrupts vesicular transport and insulin secretion Hum. Mol. Genet. 2009, 18, 3942-3954
71. Friden, B.; Wallin, M. Dependency of microtubule-associated proteins (MAPs) for tubulin stability and assembly; use of estramustine phosphate in the study of microtubules Mol. Cell. Biochem. 1991, 105, 149-158
72. Lu, H.; Yang, Y.; Allister, E. M. The identification of potential factors associated with the development of type 2 diabetes: a quantitative proteomics approach Mol. Cell. Proteomics 2008, 7, 1434-1451
73. Dubois, M.; Vacher, P.; Roger, B. Glucotoxicity inhibits late steps of insulin exocytosis Endocrinology 2007, 148, 1605-1614
74. Marouga, R.; David, S.; Hawkins, E. The development of the DIGE system: 2D fluorescence difference gel analysis technology Anal. Bioanal. Chem. 2005, 382, 669-678
75. Gorg, A.; Weiss, W.; Dunn, M. J. Current two-dimensional electrophoresis technology for proteomics Proteomics 2004, 4, 3665-3685
76. Alban, A.; David, S. O.; Bjorkesten, L. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard Proteomics 2003, 3, 36-44
77. Friedman, D. B.; Hill, S.; Keller, J. W. Proteome analysis of human colon cancer by two-dimensional difference gel electro-phoresis and mass spectrometry Proteomics 2004, 4, 793-811
78. Knowles, M. R.; Cervino, S.; Skynner, H. A. Multiplex proteomic analysis by two-dimensional differential in-gel electrophoresis Proteomics 2003, 3, 1162-1171