PPARγ Activation Attenuates Glycated-Serum Induced Pancreatic Beta-Cell Dysfunction through Enhancing Pdx1 and Mafa Protein Stability

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Zhu, Yunxia ^a   Ma, Ai ^a   Zhang, Hongxiu ^c   Li, Chaojun ^a,b  

^a NANJING NORMAL UNIVERSITY   (China)

^b MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLATED PROTEIN; INSULIN; NEUROGENIC DIFFERENTIATION FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR PDX 1; TROGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEDIFFERENTIATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; GENE; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORT; INSULIN GENE; INSULIN RELEASE; INSULIN SYNTHESIS; MALE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PDX1 GENE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STABILITY; RAT;

ANIMALS; CELL LINE, TUMOR; CHROMANS; DRUG SYNERGISM; GENE EXPRESSION REGULATION; GLYCOSYLATION; HOMEODOMAIN PROTEINS; INSULIN; INSULIN-SECRETING CELLS; LECTINS, C-TYPE; MALE; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; POTASSIUM; PPAR GAMMA; PROTEIN STABILITY; RATS; RATS, SPRAGUE-DAWLEY; SERUM; THIAZOLIDINEDIONES; TRANS-ACTIVATORS; UBIQUITIN;

EID: 84873711913     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056386     Document Type: Article

References (58)

1. Ramasamy R, Vannucci SJ, Yan SS, Herold K, Yan SF, et al. (2005) Advanced glycation end products and RAGE: a common thread in aging, diabetes, neurodegeneration, and inflammation. Glycobiology 15: 16R-28R.
2. Grillo MA, Colombatto S, (2008) Advanced glycation end-products (AGEs): involvement in aging and in neurodegenerative diseases. Amino Acids 35: 29-36.
3. Vlassara H, Palace MR, (2002) Diabetes and advanced glycation endproducts. J Intern Med 251: 87-101.
4. Fukami K, Yamagishi S, Ueda S, Okuda S, (2008) Role of AGEs in diabetic nephropathy. Curr Pharm Des 14: 946-952.
5. Toth C, Rong LL, Yang C, Martinez J, Song F, et al. (2008) Receptor for advanced glycation end products (RAGEs) and experimental diabetic neuropathy. Diabetes 57: 1002-1017.
6. Soro-Paavonen A, Watson AM, Li J, Paavonen K, Koitka A, et al. (2008) Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 57: 2461-2469.
7. Dhar A, Dhar I, Jiang B, Desai KM, Wu L, (2011) Chronic methylglyoxal infusion by minipump causes pancreatic beta-cell dysfunction and induces type 2 diabetes in Sprague-Dawley rats. Diabetes 60: 899-908.
8. Zhao Z, Zhao C, Zhang XH, Zheng F, Cai W, et al. (2009) Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome c oxidase and adenosine triphosphate synthesis. Endocrinology 150: 2569-2576.
9. Shu T, Zhu Y, Wang H, Lin Y, Ma Z, et al. (2011) AGEs decrease insulin synthesis in pancreatic beta-cell by repressing Pdx-1 protein expression at the post-translational level. PLoS One 6: e18782.
10. Puddu A, Storace D, Odetti P, Viviani GL, (2010) Advanced glycation end-products affect transcription factors regulating insulin gene expression. Biochem Biophys Res Commun 395: 122-125.
11. Zhu Y, Shu T, Lin Y, Wang H, Yang J, et al. (2011) Inhibition of the receptor for advanced glycation endproducts (RAGE) protects pancreatic beta-cells. Biochem Biophys Res Commun 404: 159-165.
12. Leibowitz G, Yuli M, Donath MY, Nesher R, Melloul D, et al. (2001) beta-cell glucotoxicity in the Psammomys obesus model of type 2 diabetes. Diabetes 50 (Suppl 1):: S113-117.
13. Li J, Liu X, Ran X, Chen J, Li X, et al. (2010) Sterol regulatory element-binding protein-1c knockdown protected INS-1E cells from lipotoxicity. Diabetes Obes Metab 12: 35-46.
14. Andersson AK, Borjesson A, Sandgren J, Sandler S, (2005) Cytokines affect PDX-1 expression, insulin and proinsulin secretion from iNOS deficient murine islets. Mol Cell Endocrinol 240: 50-57.
15. You YH, Ham DS, Park HS, Rhee M, Kim JW, et al. (2011) Adenoviruses Expressing PDX-1, BETA2/NeuroD and MafA Induces the Transdifferentiation of Porcine Neonatal Pancreas Cell Clusters and Adult Pig Pancreatic Cells into Beta-Cells. Diabetes Metab J 35: 119-129.
16. Kaneto H, Matsuoka TA, Katakami N, Matsuhisa M, (2009) Combination of MafA, PDX-1 and NeuroD is a useful tool to efficiently induce insulin-producing surrogate beta-cells. Curr Med Chem 16: 3144-3151.
17. Chandra V, Huang P, Hamuro Y, Raghuram S, Wang Y, et al. (2008) Structure of the intact PPAR-gamma-RXR- nuclear receptor complex on DNA. Nature 456: 350-356.
18. Rosen ED, Spiegelman BM, (2001) PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276: 37731-37734.
19. Yki-Jarvinen H, (2004) Thiazolidinediones. N Engl J Med 351: 1106-1118.
20. Vivas Y, Martinez-Garcia C, Izquierdo A, Garcia-Garcia F, Callejas S, et al. (2011) Early Peroxisome proliferator-activated receptor gamma regulated genes involved in expansion of pancreatic beta cell mass. BMC Med Genomics 4: 86.
21. Dubois M, Pattou F, Kerr-Conte J, Gmyr V, Vandewalle B, et al. (2000) Expression of peroxisome proliferator-activated receptor gamma (PPARgamma) in normal human pancreatic islet cells. Diabetologia 43: 1165-1169.
22. Brown KK, Henke BR, Blanchard SG, Cobb JE, Mook R, et al. (1999) A novel N-aryl tyrosine activator of peroxisome proliferator-activated receptor-gamma reverses the diabetic phenotype of the Zucker diabetic fatty rat. Diabetes 48: 1415-1424.
23. Higa M, Zhou YT, Ravazzola M, Baetens D, Orci L, et al. (1999) Troglitazone prevents mitochondrial alterations, beta cell destruction, and diabetes in obese prediabetic rats. Proc Natl Acad Sci U S A 96: 11513-11518.
24. Kim HI, Kim JW, Kim SH, Cha JY, Kim KS, et al. (2000) Identification and functional characterization of the peroxisomal proliferator response element in rat GLUT2 promoter. Diabetes 49: 1517-1524.
25. Kim HI, Cha JY, Kim SY, Kim JW, Roh KJ, et al. (2002) Peroxisomal proliferator-activated receptor-gamma upregulates glucokinase gene expression in beta-cells. Diabetes 51: 676-685.
26. Gupta D, Jetton TL, Mortensen RM, Duan SZ, Peshavaria M, et al. (2008) In vivo and in vitro studies of a functional peroxisome proliferator-activated receptor gamma response element in the mouse pdx-1 promoter. J Biol Chem 283: 32462-32470.
27. Moibi JA, Gupta D, Jetton TL, Peshavaria M, Desai R, et al. (2007) Peroxisome proliferator-activated receptor-gamma regulates expression of PDX-1 and NKX6.1 in INS-1 cells. Diabetes 56: 88-95.
28. Han X, Sun Y, Scott S, Bleich D, (2001) Tissue inhibitor of metalloproteinase-1 prevents cytokine-mediated dysfunction and cytotoxicity in pancreatic islets and beta-cells. Diabetes 50: 1047-1055.
29. Xu ZK, Chen NG, Ma CY, Meng ZX, Sun YJ, et al. (2006) Role of peroxisome proliferator-activated receptor gamma in glucose-induced insulin secretion. Acta Biochim Biophys Sin (Shanghai) 38: 1-7.
30. Chang-Chen KJ, Mullur R, Bernal-Mizrachi E, (2008) Beta-cell failure as a complication of diabetes. Rev Endocr Metab Disord 9: 329-343.
31. Stadtman ER, (1992) Protein oxidation and aging. Science 257: 1220-1224.
32. Okada K, Wangpoengtrakul C, Osawa T, Toyokuni S, Tanaka K, et al. (1999) 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J Biol Chem 274: 23787-23793.
33. Kaniuk NA, Kiraly M, Bates H, Vranic M, Volchuk A, et al. (2007) Ubiquitinated-protein aggregates form in pancreatic beta-cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 56: 930-939.
34. Kaneto H, Kajimoto Y, Miyagawa J, Matsuoka T, Fujitani Y, et al. (1999) Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 48: 2398-2406.
35. Dubois M, Vantyghem MC, Schoonjans K, Pattou F, (2002) [Thiazolidinediones in type 2 diabetes. Role of peroxisome proliferator-activated receptor gamma (PPARgamma)]. Ann Endocrinol (Paris) 63: 511-523.
36. Rosen ED, Kulkarni RN, Sarraf P, Ozcan U, Okada T, et al. (2003) Targeted elimination of peroxisome proliferator-activated receptor gamma in beta cells leads to abnormalities in islet mass without compromising glucose homeostasis. Mol Cell Biol 23: 7222-7229.
37. Kono T, Ahn G, Moss DR, Gann L, Zarain-Herzberg A, et al. (2012) PPAR-gamma activation restores pancreatic islet SERCA2 levels and prevents beta-cell dysfunction under conditions of hyperglycemic and cytokine stress. Mol Endocrinol 26: 257-271.
38. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, et al. (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13: 21-29.
39. Alavian KN, Li H, Collis L, Bonanni L, Zeng L, et al. (2011) Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat Cell Biol 13: 1224-1233.
40. Tornero D, Posadas I, Cena V, (2011) Bcl-x(L) blocks a mitochondrial inner membrane channel and prevents Ca2+ overload-mediated cell death. PLoS One 6: e20423.
41. Satoh T, Enokido Y, Aoshima H, Uchiyama Y, Hatanaka H, (1997) Changes in mitochondrial membrane potential during oxidative stress-induced apoptosis in PC12 cells. J Neurosci Res 50: 413-420.
42. Lee JW, Kim WH, Lim JH, Song EH, Song J, et al. (2009) Mitochondrial dysfunction: glucokinase downregulation lowers interaction of glucokinase with mitochondria, resulting in apoptosis of pancreatic beta-cells. Cell Signal 21: 69-78.
43. Evans-Molina C, Robbins RD, Kono T, Tersey SA, Vestermark GL, et al. (2009) Peroxisome proliferator-activated receptor gamma activation restores islet function in diabetic mice through reduction of endoplasmic reticulum stress and maintenance of euchromatin structure. Mol Cell Biol 29: 2053-2067.
44. Fong WH, Tsai HD, Chen YC, Wu JS, Lin TN, (2010) Anti-apoptotic actions of PPAR-gamma against ischemic stroke. Mol Neurobiol 41: 180-186.
45. Wu JS, Lin TN, Wu KK, (2009) Rosiglitazone and PPAR-gamma overexpression protect mitochondrial membrane potential and prevent apoptosis by upregulating anti-apoptotic Bcl-2 family proteins. J Cell Physiol 220: 58-71.
46. Kanjanabuch T, Ma LJ, Chen J, Pozzi A, Guan Y, et al. (2007) PPAR-gamma agonist protects podocytes from injury. Kidney Int 71: 1232-1239.
47. Ren Y, Sun C, Sun Y, Tan H, Wu Y, et al. (2009) PPAR gamma protects cardiomyocytes against oxidative stress and apoptosis via Bcl-2 upregulation. Vascul Pharmacol 51: 169-174.
48. Fuenzalida K, Quintanilla R, Ramos P, Piderit D, Fuentealba RA, et al. (2007) Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J Biol Chem 282: 37006-37015.
49. Miglio G, Rosa AC, Rattazzi L, Collino M, Lombardi G, et al. (2009) PPARgamma stimulation promotes mitochondrial biogenesis and prevents glucose deprivation-induced neuronal cell loss. Neurochem Int 55: 496-504.
50. Strum JC, Shehee R, Virley D, Richardson J, Mattie M, et al. (2007) Rosiglitazone induces mitochondrial biogenesis in mouse brain. J Alzheimers Dis 11: 45-51.
51. Kitamura T, Nakae J, Kitamura Y, Kido Y, Biggs WH 3rd, et al. (2002) The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J Clin Invest 110: 1839-1847.
52. Zhang X, Yong W, Lv J, Zhu Y, Zhang J, et al. (2009) Inhibition of forkhead box O1 protects pancreatic beta-cells against dexamethasone-induced dysfunction. Endocrinology 150: 4065-4073.
53. Meng Z, Lv J, Luo Y, Lin Y, Zhu Y, et al. (2009) Forkhead box O1/pancreatic and duodenal homeobox 1 intracellular translocation is regulated by c-Jun N-terminal kinase and involved in prostaglandin E2-induced pancreatic beta-cell dysfunction. Endocrinology 150: 5284-5293.
54. Humphrey RK, Yu SM, Flores LE, Jhala US, (2010) Glucose regulates steady-state levels of PDX1 via the reciprocal actions of GSK3 and AKT kinases. J Biol Chem 285: 3406-3416.
55. Kim HI, Ahn YH, (2004) Role of peroxisome proliferator-activated receptor-gamma in the glucose-sensing apparatus of liver and beta-cells. Diabetes 53 (Suppl 1):: S60-65.
56. Kim SK, Selleri L, Lee JS, Zhang AY, Gu X, et al. (2002) Pbx1 inactivation disrupts pancreas development and in Ipf1-deficient mice promotes diabetes mellitus. Nat Genet 30: 430-435.
57. Wang H, Brun T, Kataoka K, Sharma AJ, Wollheim CB, (2007) MAFA controls genes implicated in insulin biosynthesis and secretion. Diabetologia 50: 348-358.
58. Zhang C, Moriguchi T, Kajihara M, Esaki R, Harada A, et al. (2005) MafA is a key regulator of glucose-stimulated insulin secretion. Mol Cell Biol 25: 4969-4976.