The nuclear orphan receptor Nur77 is a lipotoxicity sensor regulating glucose-induced insulin secretion in pancreatic β-cells

Molecular Endocrinology

Volumn 26, Issue 3, 2012, Pages 399-413

  Briand, Olivier ^a,b,c   Helleboid Chapman, Audrey ^a,b,c   Ploton, Maheul ^a,b,c   Hennuyer, Nathalie ^a,b,c   Carpentier, Rodolphe ^a,b,c   Pattou, François ^b   Van de walle, Brigitte ^b   Moerman, Ericka ^b   Gmyr, Valery ^b   Kerr Conte, Julie ^b   Eeckhoute, Jérôme ^a,b,c   Staels, Bart ^a,b,c   Lefebvre, Philippe ^a,b,c  

^a INSTITUT PASTEUR DE LILLE   (France)

^b INSERM   (France)

^c UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; NUCLEAR RECEPTOR NUR77; NUCLEAR RECEPTOR RELATED FACTOR 1; ORPHAN NUCLEAR RECEPTOR; ORPHAN NUCLEAR RECEPTOR NOR1; PALMITIC ACID; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; ZINC;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; GLUCOSE INDUCED INSULIN SECRETION; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN RELEASE; INSULIN SYNTHESIS; INSULINOMA; LIPOTOXICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CELL LINE; CHROMOGRANIN A; FATTY ACIDS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MAF TRANSCRIPTION FACTORS, LARGE; MICE; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; PANCREAS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; STRESS, PHYSIOLOGICAL;

MURINAE;

EID: 84857486560     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1317     Document Type: Article

References (50)

1. Cabrera O, Berman DM, Kenyon NS, Ricordi C, Berggren PO, Caicedo A 2006 The unique cytoarchitecture of human pancreatic islets has implications for islet cell function. Proc Natl Acad Sci USA 103:2334-2339.
2. Prentki M, Nolan CJ 2006 Islet β cell failure in type 2 diabetes. J Clin Invest 116:1802-1812.
3. Aramata S, Han SI, Kataoka K 2007 Roles and regulation of transcription factor MafA in islet β-cells. Endocr J 54:659-666
4. Remedi MS, Nichols CG 2009 Hyperinsulinism and diabetes: genetic dissection of βcell metabolism-excitation coupling in mice. Cell Metab 10:442-453.
5. Muoio DM, Newgard CB 2006 Obesity-related derangements in metabolic regulation. Annu Rev Biochem 75:367-401.
6. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M 2003 Free fatty acids regulate insulin secretion from pancreatic βcells through GPR40. Nature 422:173-176.
7. Colditz GA, Willett WC, Rotnitzky A, Manson JE 1995 Weight gain as a risk factor for clinical diabetes mellitus in women. Ann Intern Med 122:481-486.
8. Donath MY, Størling J, Maedler K, Mandrup-Poulsen T 2003 Inflammatory mediators and islet β-cell failure: a link between type 1 and type 2 diabetes. J Mol Med 81:455-470.
9. Eizirik DL, Sandler S, Welsh N, Cetkovic-Cvrlje M, Nieman A, Geller DA, Pipeleers DG, Bendtzen K, Hellerström C 1994 Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 93:1968-1974.
10. Tulachan SS, Doi R, Kawaguchi Y, Tsuji S, Nakajima S, Masui T, Koizumi M, Toyoda E, Mori T, Ito D, Kami K, Fujimoto K, ImamuraM2003 All-trans retinoic acid induces differentiation of ducts and endocrine cells by mesenchymal/epithelial interactions in embryonic pancreas. Diabetes 52:76-84.
11. Micallef SJ, Janes ME, Knezevic K, Davis RP, Elefanty AG, Stanley EG 2005 Retinoic acid induces Pdx1-positive endoderm in differentiating mouse embryonic stem cells. Diabetes 54:301-305.
12. Sugden MC, Holness MJ 2008 Role of nuclear receptors in the modulation of insulin secretion in lipid-induced insulin resistance. Biochem Soc Trans 36:891-900.
13. Popescu IR, Helleboid-Chapman A, Lucas A, Vandewalle B, Dumont J, Bouchaert E, Derudas B, Kerr-Conte J, Caron S, Pattou F, Staels B 2010 The nuclear receptor FXR is expressed in pancreatic β-cells and protects human islets from lipotoxicity. FEBS Lett 584: 2845-2851.
14. Pei L, Castrillo A, Chen M, Hoffmann A, Tontonoz P 2005 Induction of NR4Aorphan nuclear receptor expression in macrophages in response to inflammatory stimuli. J Biol Chem 280:29256-29262.
15. Arkenbout EK, de Waard V, van Bragt M, van Achterberg TA, Grimbergen JM, Pichon B, Pannekoek H, de Vries CJ 2002 Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation 106:1530-1535.
16. Busch AK, Cordery D, Denyer GS, Biden TJ 2002 Expression profiling of palmitate- and oleate-regulated genes provides novel in- sights into the effects of chronic lipid exposure on pancreatic β-cell function. Diabetes 51:977-987.
17. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ 2007 Endoplasmic reticulum stress contributes to βcell apoptosis in type 2 diabetes. Diabetologia 50:752-763.
18. Zhang XK 2007 Targeting Nur77 translocation. Expert Opin Ther Targets 11:69-79.
19. Pei L, Waki H, Vaitheesvaran B, Wilpitz DC, Kurland IJ, Tontonoz P 2006 NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat Med 12:1048-1055.
20. Evans-Molina C, Garmey JC, Ketchum R, Brayman KL, Deng S, Mirmira RG 2007 Glucose regulation of insulin gene transcription and pre-mRNA processing in human islets. Diabetes 56:827-835.
21. Docherty HM, Hay CW, Ferguson LA, Barrow J, Durward E, Docherty K 2005 Relative contribution of PDX-1, MafA and E47/ β2 to the regulation of the human insulin promoter. Biochem J 389: 813-820.
22. Hirota K, Daitoku H, Matsuzaki H, Araya N, Yamagata K, Asada S, Sugaya T, Fukamizu A 2003 Hepatocyte nuclear factor-4 is a novel downstream target of insulin via FKHR as a signal-regulated transcriptional inhibitor. J Biol Chem 278:13056-13060.
23. Dowell P, Otto TC, Adi S, Lane MD 2003 Convergence of peroxisome proliferator-activated receptor γ and Foxo1 signaling pathways. J Biol Chem 278:45485-45491.
24. Zhao Y, Bruemmer D 2010 NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler Thromb Vasc Biol 30:1535-1541.
25. Susini S, Roche E, Prentki M, Schlegel W 1998 Glucose and glucoincretin peptides synergize to induce c-fos, c-jun, junB, zif-268, and nur-77 gene expression in pancreatic β(INS-1) cells. FASEB J 12: 1173-1182.
26. Roche E, Buteau J, Aniento I, Reig JA, Soria B, Prentki M 1999 Palmitate and oleate induce the immediate-early response genes c-fos and nur-77 in the pancreatic β-cell line INS-1. Diabetes 48: 2007-2014.
27. Giacca A, Xiao C, Oprescu AI, Carpentier AC, Lewis GF 2011 Lipid-induced pancreatic β-cell dysfunction: focus on in vivo studies. Am J Physiol Endocrinol Metab 300:E255-E262
28. Poitout V, Amyot J, Semache M, Zarrouki B, Hagman D, Fontés G 2010 Glucolipotoxicity of the pancreatic βcell. Biochim Biophys Acta 1801:289-298.
29. Brunham LR, Kruit JK, Hayden MR, Verchere CB 2010 Cholesterol in β-cell dysfunction: the emerging connection between HDL cholesterol and type 2 diabetes. Curr Diab Rep 10:55-60.
30. Wang H, Brun T, Kataoka K, Sharma AJ, Wollheim CB 2007 MAFA controls genes implicated in insulin biosynthesis and secretion. Diabetologia 50:348-358.
31. Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W, Accili D 2005 FoxO1 protects against pancreatic βcell failure through NeuroD and MafA induction. Cell Metab 2:153-163.
32. Haeusler RA, Kaestner KH, Accili D 2010 FoxOs function synergistically to promote glucose production. J Biol Chem 285:35245-35248
33. Choi JW, Park SC, Kang GH, Liu JO, Youn HD 2004 Nur77 activated by hypoxia-inducible factor-1α overproduces proopiomelanocortin in von Hippel-Lindau-mutated renal cell carcinoma. Cancer Res 64:35-39.
34. Lam BY, Zhang W, Ng DC, Maruthappu M, Roderick HL, Chawla S 2010 CREB-dependent Nur77 induction following depolarization in PC12 cells and neurons is modulated by MEF2 transcription factors. J Neurochem 112:1065-1073.
35. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK 2009 A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammationinduced death. Cell 137:47-59.
36. Pei L, Castrillo A, Tontonoz P 2006 Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol Endocrinol 20:786-794.
37. Bonta PI, van Tiel CM, Vos M, Pols TW, van Thienen JV, Ferreira V, Arkenbout EK, Seppen J, Spek CA, van der Poll T, Pannekoek H, de Vries CJ 2006 Nuclear receptors Nur77, Nurr1, and NOR-1 expressed in atherosclerotic lesion macrophages reduce lipid loading and inflammatory responses. Arterioscler Thromb Vasc Biol 26:2288-2294.
38. Igoillo-Esteve M, Marselli L, Cunha DA, Ladriére L, Ortis F, Grieco FA, Dotta F, Weir GC, Marchetti P, Eizirik DL, Cnop M 2010 Palmitate induces a pro-inflammatory response in human pancreatic islets that mimics CCL2 expression by βcells in type 2 diabetes. Diabetologia 53:1395-1405.
39. Fu Y, Luo L, Luo N, Zhu X, Garvey WT 2007 NR4A orphan nuclear receptors modulate insulin action and the glucose transport system: potential role in insulin resistance. J Biol Chem 282:31525-31533
40. Kanzleiter T, Preston E, Wilks D, Ho B, Benrick A, Reznick J, Heilbronn LK, Turner N, Cooney GJ 2010 Overexpression of the orphan receptor Nur77 alters glucose metabolism in rat muscle cells and rat muscle in vivo. Diabetologia 53:1174-1183.
41. Lefebvre B, Benomar Y, Guédin A, Langlois A, Hennuyer N, Dumont J, Bouchaert E, Dacquet C, Pénicaud L, Casteilla L, Pattou F, Ktorza A, Staels B, Lefebvre P 2010 Proteasomal degradation of retinoid X receptor α reprograms transcriptional activity of PPARγ in obese mice and humans. J Clin Invest 120:1454-1468.
42. Huang da W, Sherman BT, Lempicki RA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57.
43. Raum JC, Gerrish K, Artner I, Henderson E, Guo M, Sussel L, Schisler JC, Newgard CB, Stein R 2006 FoxA2, Nkx2.2, and PDX-1 regulate islet β-cell-specific mafA expression through conserved sequences located between base pairs-8118 and-7750 upstream from the transcription start site. Mol Cell Biol 26:5735-5743.
44. German MS, Wang J, Chadwick RB, Rutter WJ 1992 Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex. Genes Dev 6:2165-2176.
45. Pols TW, Ottenhoff R, Vos M, Levels JH, Quax PH, Meijers JC, Pannekoek H, Groen AK, de Vries CJ 2008 Nur77 modulates hepatic lipid metabolism through suppression of SREBP1c activity. Biochem Biophys Res Commun 366:910-916.
46. Pirih FQ, Tang A, Ozkurt IC, Nervina JM, Tetradis S 2004 Nuclear orphan receptor Nurr1 directly transactivates the osteocalcin gene in osteoblasts. J Biol Chem 279:53167-53174.
47. Lalloyer F, Vandewalle B, Percevault F, Torpier G, Kerr-Conte J, Oosterveer M, Paumelle R, Fruchart JC, Kuipers F, Pattou F, Fiévet C, Staels B 2006 Peroxisome proliferator-activated receptor α improves pancreatic adaptation to insulin resistance in obese mice and reduces lipotoxicity in human islets. Diabetes 55:1605-1613.
48. Sérandour AA, Avner S, Percevault F, Demay F, Bizot M, Lucchetti- Miganeh C, Barloy-Hubler F, Brown M, Lupien M, Métivier R, Salbert G, Eeckhoute J 2011 Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res 21:555-565.
49. Au WS, Payne VA, O'Rahilly S, Rochford JJ 2008 The NR4A family of orphan nuclear receptors are not required for adipogenesis. Int J Obes (Lond) 32:388-392.
50. Wang X, Li H, De Leo D, Guo W, Koshkin V, Fantus IG, Giacca A, Chan CB, Der S, Wheeler MB 2004 Gene and protein kinase expression profiling of reactive oxygen species-associated lipotoxicity in the pancreatic β-cell line MIN6. Diabetes 53:129-140