Role of the saturated nonesterified fatty acid palmitate in beta cell dysfunction

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 347-362

  Maris, Michael ^a   Robert, Sofie ^a   Waelkens, Etienne ^b,c   Derua, Rita ^b   Hernangomez, Miriam H ^d   D'Hertog, Wannes ^a   Cnop, Miriam ^d,e   Mathieu, Chantal ^b,c   Overbergh, Lut ^b,c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^c KU LEUVEN   (Belgium)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e ERASME HOSPITAL   (Belgium)

Author keywords

2D DIGE; Beta cells; Endoplasmic reticulum; Free fatty acids; Glucolipotoxicity; Lipotoxicity; Palmitate; Proteomics; Type 2 diabetes

Indexed keywords

GLUCOSE; INSULIN; LEVO GLUCOSE; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL DAMAGE; CELL DEATH; CELL LYSATE; CELL MATURATION; CELL MIGRATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; LIPOGENESIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEOMICS; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; FATTY ACIDS, NONESTERIFIED; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; PALMITATES; PROTEIN BIOSYNTHESIS; PROTEOMICS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84874047426     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300596g     Document Type: Article

References (64)

1. Kahn, B. B.; Flier, J. S. Obesity and insulin resistance. J. Clin. Invest. 2000, 106 (4), 473-481.
2. Wellen, K. E.; Hotamisligil, G. S. Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 115 (5), 1111-1119.
3. Shimabukuro, M.; Zhou, Y. T.; Levi, M.; Unger, R. H. Fatty acidinduced beta cell apoptosis: a link between obesity and diabetes. Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (5), 2498-2502.
4. Prentki, M.; Joly, E.; El-Assaad, W.; Roduit, R. Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: role in beta-cell adaptation and failure in the etiology of diabetes. Diabetes 2002, 51 (Suppl 3), S405-S413.
5. Poitout, V.; Robertson, R. P. Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr. Rev. 2008, 29 (3), 351-366.
6. Hagman, D. K.; Latour, M. G.; Chakrabarti, S. K.; Fontes, G.; Amyot, J.; Tremblay, C.; Semache, M.; Lausier, J. A.; Roskens, V.; Mirmira, R. G.; Jetton, T. L.; Poitout, V. Cyclical and alternating infusions of glucose and intralipid in rats inhibit insulin gene expression and Pdx-1 binding in islets. Diabetes 2008, 57 (2), 424-431.
7. Eizirik, D. L.; Cardozo, A. K.; Cnop, M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 2008, 29 (1), 42-61.
8. Karaskov, E.; Scott, C.; Zhang, L.; Teodoro, T.; Ravazzola, M.; Volchuk, A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 2006, 147 (7), 3398-3407.
9. Hagman, D. K.; Hays, L. B.; Parazzoli, S. D.; Poitout, V. Palmitate inhibits insulin gene expression by altering PDX-1 nuclear localization and reducing MafA expression in isolated rat islets of Langerhans. J. Biol. Chem. 2005, 280 (37), 32413-32418.
10. Sol, E. R.; Hovsepyan, M.; Bergsten, P. Proteins altered by elevated levels of palmitate or glucose implicated in impaired glucosestimulated insulin secretion. Proteome Sci. 2009, 7, 24.
11. Hovsepyan, M.; Sargsyan, E.; Bergsten, P. Palmitate-induced changes in protein expression of insulin secreting INS-1E cells. J. Proteomics 2010, 73 (6), 1148-1155.
12. Jeffrey, K. D.; Alejandro, E. U.; Luciani, D. S.; Kalynyak, T. B.; Hu, X.; Li, H.; Lin, Y.; Townsend, R. R.; Polonsky, K. S.; Johnson, J. D. Carboxypeptidase E mediates palmitate-induced beta-cell ER stress and apoptosis. Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (24), 8452-8457.
13. Fountoulakis, M.; Juranville, J. F.; Tsangaris, G.; Suter, L. Fractionation of liver proteins by preparative electrophoresis. Amino Acids 2004, 26 (1), 27-36.
14. Stone, S. J.; Vance, J. E. Phosphatidylserine synthase-1 and-2 are localized to mitochondria-associated membranes. J. Biol. Chem. 2000, 275 (44), 34534-34540.
15. Maris, M.; Ferreira, G. B.; D'Hertog, W.; Cnop, M.; Waelkens, E.; Overbergh, L.; Mathieu, C. High glucose induces dysfunction in insulin secretory cells by different pathways: a proteomic approach. J. Proteome Res. 2010, 9 (12), 6274-6287.
16. Maris, M.; Waelkens, E.; Cnop, M.; D'Hertog, W.; Cunha, D. A.; Korf, H.; Koike, T.; Overbergh, L.; Mathieu, C. Oleate-induced beta cell dysfunction and apoptosis: a proteomic approach to glucolipotoxicity by an unsaturated fatty acid. J. Proteome Res. 2011, 10 (8), 3372-3385.
17. Cunha, D. A.; Ladriere, L.; Ortis, F.; Igoillo-Esteve, M.; Gurzov, E. N.; Lupi, R.; Marchetti, P.; Eizirik, D. L.; Cnop, M. Glucagon-like peptide-1 agonists protect pancreatic beta-cells from lipotoxic endoplasmic reticulum stress through upregulation of BiP and JunB. Diabetes 2009, 58 (12), 2851-2862.
18. Cnop, M.; Ladriere, L.; Hekerman, P.; Ortis, F.; Cardozo, A. K.; Dogusan, Z.; Flamez, D.; Boyce, M.; Yuan, J.; Eizirik, D. L. Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J. Biol. Chem. 2007, 282 (6), 3989-3997.
19. Maedler, K.; Oberholzer, J.; Bucher, P.; Spinas, G. A.; Donath, M. Y. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003, 52 (3), 726-733.
20. Johnson, J. D.; Han, Z.; Otani, K.; Ye, H.; Zhang, Y.; Wu, H.; Horikawa, Y.; Misler, S.; Bell, G. I.; Polonsky, K. S. RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J. Biol. Chem. 2004, 279 (23), 24794-24802.
21. Furukawa, H.; Carroll, R. J.; Swift, H. H.; Steiner, D. F. Longterm elevation of free fatty acids leads to delayed processing of proinsulin and prohormone convertases 2 and 3 in the pancreatic betacell line MIN6. Diabetes 1999, 48 (7), 1395-1401.
22. Kashemsant, N. B.; Hassanabad, S.; Harper, Z.; Chan, M. C., Impairment of Proinsulin Processing in Cells Exposed to Saturated Free Fatty Acid Is Dependent on Uncoupling Protein-2 Expression. Can. J. Diabetes 2012, 36 (5), 228-236.
23. Berman, Y.; Mzhavia, N.; Polonskaia, A.; Devi, L. A. Impaired prohormone convertases in Cpe(fat)/Cpe(fat) mice. J. Biol. Chem. 2001, 276 (2), 1466-1473.
24. Bjorklund, A.; Grill, V. Enhancing effects of long-term elevated glucose and palmitate on stored and secreted proinsulin-to-insulin ratios in human pancreatic islets. Diabetes 1999, 48 (7), 1409-1414.
25. Kim, J. Y.; Hickner, R. C.; Cortright, R. L.; Dohm, G. L.; Houmard, J. A. Lipid oxidation is reduced in obese human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2000, 279 (5), E1039-E1044.
26. Prentki, M.; Vischer, S.; Glennon, M. C.; Regazzi, R.; Deeney, J. T.; Corkey, B. E. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J. Biol. Chem. 1992, 267 (9), 5802-5810.
27. Sargsyan, E.; Bergsten, P. Lipotoxicity is glucose-dependent in INS-1E cells but not in human islets and MIN6 cells. Lipids Health Dis. 2011, 10, 115.
28. Prentki, M.; Corkey, B. E. Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 1996, 45 (3), 273-283.
29. Lupi, R.; Dotta, F.; Marselli, L.; Del, G. S.; Masini, M.; Santangelo, C.; Patane, G.; Boggi, U.; Piro, S.; Anello, M.; Bergamini, E.; Mosca, F.; Di, M. U.; Del, P. S.; Marchetti, P. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on humanpancreatic islets: evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 2002, 51 (5), 1437-1442.
30. Summers, S. A. Ceramides in insulin resistance and lipotoxicity. Prog. Lipid Res. 2006, 45 (1), 42-72.
31. Poitout, V.; Hagman, D.; Stein, R.; Artner, I.; Robertson, R. P.; Harmon, J. S. Regulation of the insulin gene by glucose and fatty acids. J. Nutr. 2006, 136 (4), 873-876.
32. Robertson, R. P. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 2004, 279 (41), 42351-42354.
33. Robertson, R. P.; Harmon, J.; Tran, P. O.; Poitout, V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes 2004, 53 (Suppl 1), S119-S124.
34. Maechler, P.; Jornot, L.; Wollheim, C. B. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J. Biol. Chem. 1999, 274 (39), 27905-27913.
35. Kajimoto, Y.; Kaneto, H. Role of oxidative stress in pancreatic beta-cell dysfunction. Ann. N.Y. Acad. Sci. 2004, 1011, 168-176.
36. Chen, L.; Na, R.; Gu, M.; Salmon, A. B.; Liu, Y.; Liang, H.; Qi, W.; Van, R. H.; Richardson, A.; Ran, Q. Reduction of mitochondrial H2O2 by overexpressing peroxiredoxin 3 improves glucose tolerance in mice. Aging Cell 2008, 7 (6), 866-878.
37. Wakil, S. J.; Stoops, J. K.; Joshi, V. C. Fatty acid synthesis and its regulation. Annu. Rev. Biochem. 1983, 52, 537-579.
38. Rorsman, P.; Trube, G. Glucose dependent K+-channels in pancreatic beta-cells are regulated by intracellular ATP. Pflugers Arch. 1985, 405 (4), 305-309.
39. Cunha, D. A.; Hekerman, P.; Ladriere, L.; Bazarra-Castro, A.; Ortis, F.; Wakeham, M. C.; Moore, F.; Rasschaert, J.; Cardozo, A. K.; Bellomo, E.; Overbergh, L.; Mathieu, C.; Lupi, R.; Hai, T.; Herchuelz, A.; Marchetti, P.; Rutter, G. A.; Eizirik, D. L.; Cnop, M. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J. Cell Sci. 2008, 121 (Pt 14), 2308-2318.
40. Lai, E.; Bikopoulos, G.; Wheeler, M. B.; Rozakis-Adcock, M.; Volchuk, A. Differential activation of ER stress and apoptosis in response to chronically elevated free fatty acids in pancreatic beta-cells. Am. J. Physiol. Endocrinol. Metab. 2008, 294 (3), E540-E550.
41. Wada, I.; Imai, S.; Kai, M.; Sakane, F.; Kanoh, H. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J. Biol. Chem. 1995, 270 (35), 20298-20304.
42. Ozawa, M.; Muramatsu, T. Reticulocalbin, a novel endoplasmic reticulum resident Ca(2+)-binding protein with multiple EF-hand motifs and a carboxyl-terminal HDEL sequence. J. Biol. Chem. 1993, 268 (1), 699-705.
43. D'Hertog, W.; Overbergh, L.; Lage, K.; Ferreira, G. B.; Maris, M.; Gysemans, C.; Flamez, D.; Cardozo, A. K.; Van den, B. 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 (12), 2180-2199.
44. Savitz, A. J.; Meyer, D. I. 180-kD ribosome receptor is essential for both ribosome binding and protein translocation. J. Cell Biol. 1993, 120 (4), 853-863.
45. Olofsson, C. S.; Collins, S.; Bengtsson, M.; Eliasson, L.; Salehi, A.; Shimomura, K.; Tarasov, A.; Holm, C.; Ashcroft, F.; Rorsman, P. Long-term exposure to glucose and lipids inhibits glucose-induced insulin secretion downstream of granule fusion with plasma membrane. Diabetes 2007, 56 (7), 1888-1897.
46. Collins, S. C.; Salehi, A.; Eliasson, L.; Olofsson, C. S.; Rorsman, P. Long-term exposure of mouse pancreatic islets to oleate or palmitate results in reduced glucose-induced somatostatin and oversecretion of glucagon. Diabetologia 2008, 51 (9), 1689-1693.
47. Karki, S.; Holzbaur, E. L. Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 1999, 11 (1), 45-53.
48. Hamill, D. R.; Suprenant, K. A. Characterization of the sea urchin major vault protein: a possible role for vault ribonucleoprotein particles in nucleocytoplasmic transport. Dev. Biol. 1997, 190 (1), 117-128.
49. Zhang, L.; Ashendel, C. L.; Becker, G. W.; Morre, D. J. Isolation and characterization of the principal ATPase associated with transitional endoplasmic reticulum of rat liver. J. Cell Biol. 1994, 127 (6 Pt 2), 1871-1883.
50. Westermann, S.; Weber, K. Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 2003, 4 (12), 938-947.
51. Preston, A. M.; Gurisik, E.; Bartley, C.; Laybutt, D. R.; Biden, T. J. Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse beta cells by promoting protein overload. Diabetologia 2009, 52 (11), 2369-2373.
52. McDaniel, M. L.; Bry, C. G.; Homer, R. W.; Fink, C. J.; Ban, D.; Lacy, P. E. Temporal changes in islet polymerized and depolymerized tubulin during biphasic insulin release. Metabolism 1980, 29 (8), 762-766.
53. Pipeleers, D. G.; Pipeleers-Marichal, M. A.; Kipnis, D. M. Regulation of tubulin synthesis in islets of Langerhans. Proc. Natl. Acad. Sci. U.S.A. 1976, 73 (9), 3188-3191.
54. Smith, R.; Bacos, K.; Fedele, V.; Soulet, D.; Walz, H. A.; Obermuller, S.; Lindqvist, A.; Bjorkqvist, M.; Klein, P.; Onnerfjord, P.; Brundin, P.; Mulder, H.; Li, J. Y. Mutant huntingtin interacts with {beta}-tubulin and disrupts vesicular transport and insulin secretion. Hum. Mol. Genet. 2009, 18 (20), 3942-3954.
55. Pan, T. L.; Wang, P. W.; Chen, C. C.; Fang, J. Y.; Sintupisut, N. Functional proteomics reveals hepatotoxicity and the molecular mechanisms of different forms of chromium delivered by skin administration. Proteomics 2012, 12 (3), 477-489.
56. Ryu, S. J.; An, H. J.; Oh, Y. S.; Choi, H. R.; Ha, M. K.; Park, S. C. On the role of major vault protein in the resistance of senescent human diploid fibroblasts to apoptosis. Cell Death Differ. 2008, 15 (11), 1673-1680.
57. Krecic, A. M.; Swanson, M. S. hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 1999, 11 (3), 363-371.
58. Banroques, J.; Abelson, J. N. PRP4: a protein of the yeast U4/U6 small nuclear ribonucleoprotein particle. Mol. Cell. Biol. 1989, 9 (9), 3710-3719.
59. vis-Smyth, T.; Duncan, R. C.; Zheng, T.; Michelotti, G.; Levens, D. The far upstream element-binding proteins comprise an ancient family of single-strand DNA-binding transactivators. J. Biol. Chem. 1996, 271 (49), 31679-31687.
60. Weber, A.; Kristiansen, I.; Johannsen, M.; Oelrich, B.; Scholmann, K.; Gunia, S.; May, M.; Meyer, H. A.; Behnke, S.; Moch, H.; Kristiansen, G. The FUSE binding proteins FBP1 and FBP3 are potential c-myc regulators in renal, but not in prostate and bladder cancer. BMC Cancer 2008, 8, 369.
61. Laybutt, D. R.; Weir, G. C.; Kaneto, H.; Lebet, J.; Palmiter, R. D.; Sharma, A.; Bonner-Weir, S. Overexpression of c-Myc in beta-cells of transgenic mice causes proliferation and apoptosis, downregulation of insulin gene expression, and diabetes. Diabetes 2002, 51 (6), 1793-1804.
62. Gygi, S. P.; Corthals, G. L.; Zhang, Y.; Rochon, Y.; Aebersold, R. Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (17), 9390-9395.
63. Fountoulakis, M.; Juranville, J. F.; Berndt, P.; Langen, H.; Suter, L. Two-dimensional database of mouse liver proteins. An update. Electrophoresis 2001, 22 (9), 1747-1763.
64. Fountoulakis, M.; Suter, L. Proteomic analysis of the rat liver. J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2002, 782 (1-2), 197-218.