Chaperones ameliorate beta cell dysfunction associated with human islet amyloid polypeptide overexpression

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Cadavez, Lisa ^a,b   Montane, Joel ^a,b   Alcarraz Vizán, Gema ^a,b   Visa, Montse ^a,b   Vidal Fàbrega, Laia ^a   Servitja, Joan Marc ^a,b   Novials, Anna ^a,b  

^a HOSPITAL CLÍNIC   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; ADENOVIRUS VECTOR; AMYLIN; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; INSULIN; PALMITIC ACID; PROTEIN DISULFIDE ISOMERASE; TAUROURSODEOXYCHOLIC ACID; THAPSIGARGIN; CHAPERONE; DDIT3 PROTEIN, RAT; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL DYSFUNCTION; PANCREAS ISLET DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; VIRAL GENE DELIVERY SYSTEM; ANIMAL; APOPTOSIS; CELL LINE; CYTOLOGY; DEFICIENCY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION; GENE SILENCING; GENETICS; HUMAN; METABOLISM; MOUSE; PANCREAS ISLET BETA CELL; SECRETION (PROCESS);

ANIMALS; APOPTOSIS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; MICE; MOLECULAR CHAPERONES; PALMITIC ACID; RATS; THAPSIGARGIN; TRANSCRIPTION FACTOR CHOP;

EID: 84904248428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101797     Document Type: Article

References (53)

1. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, et al. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110. (Pubitemid 36042113)
2. Montane J, Klimek-Abercrombie A, Potter KJ, Westwell-Roper C, Bruce Verchere C (2012) Metabolic stress, IAPP and islet amyloid. Diabetes Obes Metab 14 Suppl 3: 68-77.
3. Costes S, Langen R, Gurlo T, Matveyenko AV, Butler PC (2013) beta-Cell failure in type 2 diabetes: a case of asking too much of too few? Diabetes 62: 327-335.
4. Marzban L, Trigo-Gonzalez G, Verchere CB (2005) Processing of pro-islet amyloid polypeptide in the constitutive and regulated secretory pathways of beta cells. Mol Endocrinol 19: 2154-2163. (Pubitemid 41124209)
5. Zraika S, Hull RL, Verchere CB, Clark A, Potter KJ, et al. (2010) Toxic oligomers and islet beta cell death: guilty by association or convicted by circumstantial evidence? Diabetologia 53: 1046-1056.
6. Marchetti P, Bugliani M, Lupi R, Marselli L, Masini M, et al. (2007) The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients. Diabetologia 50: 2486-2494. (Pubitemid 350060637)
7. Hotamisligil GS (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917.
8. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880-885. (Pubitemid 44523966)
9. Montane J, Cadavez L, Novials A (2014) Stress and the inflammatory process: a major cause of pancreatic cell death in type 2 diabetes Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy 2014: 24-35.
10. Eizirik DL, Miani M, Cardozo AK (2013) Signalling danger: endoplasmic reticulum stress and the unfolded protein response in pancreatic islet inflammation. Diabetologia 56: 234-241.
11. Ellis RJ (2006) Molecular chaperones: assisting assembly in addition to folding. Trends Biochem Sci 31: 395-401.
12. Teodoro-Morrison T, Schuiki I, Zhang L, Belsham DD, Volchuk A (2013) GRP78 overproduction in pancreatic beta cells protects against high-fat-diet-induced diabetes in mice. Diabetologia 56: 1057-1067.
13. Sun A, Jiang Y, Wang X, Liu Q, Zhong F, et al. (2010) Liverbase: a comprehensive view of human liver biology. J Proteome Res 9: 50-58.
14. Zhang L, Lai E, Teodoro T, Volchuk A (2009) GRP78, but Not Proteindisulfide Isomerase, Partially Reverses Hyperglycemia-induced Inhibition of Insulin Synthesis and Secretion in Pancreatic {beta}-Cells. J Biol Chem 284: 5289-5298.
15. Papp E, Szaraz P, Korcsmaros T, Csermely P (2006) Changes of endoplasmic reticulum chaperone complexes, redox state, and impaired protein disulfide reductase activity in misfolding alpha1-antitrypsin transgenic mice. FASEB J 20: 1018-1020.
16. Sitia R, Molteni SN (2004) Stress, protein (mis)folding, and signaling: the redox connection. Sci STKE 2004: pe27.
17. Gillece P, Luz JM, Lennarz WJ, de La Cruz FJ, Romisch K (1999) Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J Cell Biol 147: 1443-1456. (Pubitemid 30027400)
18. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, et al. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140. (Pubitemid 44300242)
19. Basseri S, Lhotak S, Sharma AM, Austin RC (2009) The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res 50: 2486-2501.
20. Schneeberger M, Dietrich MO, Sebastian D, Imbernon M, Castano C, et al. (2013) Mitofusin 2 in POMC neurons connects ER stress with leptin resistance and energy imbalance. Cell 155: 172-187.
21. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6: 11-22. (Pubitemid 40052135)
22. Yang Y, Song W (2013) Molecular links between Alzheimer's disease and diabetes mellitus. Neuroscience 250: 140-150.
23. Chien V, Aitken JF, Zhang S, Buchanan CM, Hickey A, et al. (2010) The chaperone proteins HSP70, HSP40/DnaJ and GRP78/BiP suppress misfolding and formation of beta-sheet-containing aggregates by human amylin: a potential role for defective chaperone biology in Type 2 diabetes. Biochem J 432: 113-121.
24. Casas S, Gomis R, Gribble FM, Altirriba J, Knuutila S, et al. (2007) 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 56: 2284-2294. (Pubitemid 47358235)
25. Haataja L, Gurlo T, Huang CJ, Butler PC (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr Rev 29: 303-316. (Pubitemid 351679701)
26. Soty M, Visa M, Soriano S, Carmona Mdel C, Nadal A, et al. (2011) Involvement of ATP-sensitive potassium (K(ATP)) channels in the loss of beta-cell function induced by human islet amyloid polypeptide. J Biol Chem 286: 40857-40866.
27. Penas C, Font-Nieves M, Fores J, Petegnief V, Planas A, et al. (2011) Autophagy, and BiP level decrease are early key events in retrograde degeneration of motoneurons. Cell Death Differ 18: 1617-1627.
28. Hull RL, Zraika S, Udayasankar J, Aston-Mourney K, Subramanian SL, et al. (2009) Amyloid formation in human IAPP transgenic mouse islets and pancreas, and human pancreas, is not associated with endoplasmic reticulum stress. Diabetologia 52: 1102-1111.
29. Huang CJ, Haataja L, Gurlo T, Butler AE, Wu X, et al. (2007) Induction of endoplasmic reticulum stress-induced beta-cell apoptosis and accumulation of polyubiquitinated proteins by human islet amyloid polypeptide. Am J Physiol Endocrinol Metab 293: E1656-1662. (Pubitemid 350255116)
30. Hong J, Jeppesen PB, Hermansen K (2009) Effects of elevated fatty acid and glucose concentrations on pancreatic islet function in vitro. Diabetes Obes Metab 11: 397-404.
31. Cnop M, Ladriere L, Igoillo-Esteve M, Moura RF, Cunha DA (2010) Causes and cures for endoplasmic reticulum stress in lipotoxic beta-cell dysfunction. Diabetes Obes Metab 12 Suppl 2: 76-82.
32. Poitout V, Robertson RP (2002) Minireview: Secondary beta-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 143: 339-342. (Pubitemid 34107184)
33. Ohtsubo K, Chen MZ, Olefsky JM, Marth JD (2011) Pathway to diabetes through attenuation of pancreatic beta cell glycosylation and glucose transport. Nat Med 17: 1067-1075.
34. McGarry JD, Dobbins RL (1999) Fatty acids, lipotoxicity and insulin secretion. Diabetologia 42: 128-138. (Pubitemid 29064233)
35. Jacqueminet S, Briaud I, Rouault C, Reach G, Poitout V (2000) Inhibition of insulin gene expression by long-term exposure of pancreatic beta cells to palmitate is dependent on the presence of a stimulatory glucose concentration. Metabolism 49: 532-536. (Pubitemid 30196583)
36. Milburn JL Jr, Hirose H, Lee YH, Nagasawa Y, Ogawa A, et al. (1995) Pancreatic beta-cells in obesity. Evidence for induction of functional, morphologic, and metabolic abnormalities by increased long chain fatty acids. J Biol Chem 270: 1295-1299.
37. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, et al. (2010) Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 11: 897-904.
38. Lin CY, Gurlo T, Kayed R, Butler AE, Haataja L, et al. (2007) Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced beta-cell apoptosis in h-IAPP transgenic mice. Diabetes 56: 1324-1332. (Pubitemid 46715613)
39. Srivastava S, Chan C (2007) Hydrogen peroxide and hydroxyl radicals mediate palmitate-induced cytotoxicity to hepatoma cells: relation to mitochondrial permeability transition. Free Radic Res 41: 38-49. (Pubitemid 44896873)
40. Maestre I, Jordan J, Calvo S, Reig JA, Cena V, et al. (2003) Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS-1. Endocrinology 144: 335-345. (Pubitemid 36076123)
41. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ (2008) Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 118: 3378-3389.
42. Potter KJ, Westwell-Roper CY, Klimek-Abercrombie AM, Warnock GL, Verchere CB (2014) Death and Dysfunction of Transplanted beta-Cells: Lessons Learned From Type 2 Diabetes? Diabetes 63: 12-19.
43. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389. (Pubitemid 38489416)
44. Tokuyama T, Yagui K, Yamaguchi T, Huang CI, Kuramoto N, et al. (1997) Expression of human islet amyloid polypeptide/amylin impairs insulin secretion in mouse pancreatic beta cells. Metabolism 46: 1044-1051. (Pubitemid 27371822)
45. Xiuju Wu LH, Butler PC (2011) Chaperone Proteins Hsp70 and BiP Fold and Traffic Islet Amyloid Polypeptide in Humans, Candidates for Increased b-Cell Apoptosis in Type 2 Diabetes. 71st Scientific Sessions of American Diabetes Association. San Diego.
46. Rajpal G, Schuiki I, Liu M, Volchuk A, Arvan P (2012) Action of protein disulfide isomerase on proinsulin exit from endoplasmic reticulum of pancreatic beta-cells. J Biol Chem 287: 43-47.
47. Poitout V, Robertson RP (2008) Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 29: 351-366. (Pubitemid 351679704)
48. Flower TR, Chesnokova LS, Froelich CA, Dixon C, Witt SN (2005) Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson's disease. J Mol Biol 351: 1081-1100. (Pubitemid 41133454)
49. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, et al. (2009) GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 119: 1201-1215.
50. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, et al. (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 9: 35-51.
51. Tang C, Koulajian K, Schuiki I, Zhang L, Desai T, et al. (2012) Glucoseinduced beta cell dysfunction in vivo in rats: link between oxidative stress and endoplasmic reticulum stress. Diabetologia 55: 1366-1379.
52. Kars M, Yang L, Gregor MF, Mohammed BS, Pietka TA, et al. (2010) Tauroursodeoxycholic Acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes 59: 1899-1905.
53. Xiao C, Giacca A, Lewis GF (2011) Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and beta-cell dysfunction in humans. Diabetes 60: 918-924.