SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation

Journal of Clinical Investigation

Volumn 123, Issue 1, 2013, Pages 362-379

  Toubal, Amine ^a,b,c,d   Clément, Karine ^a,b,c,d   Fan, Rongrong ^e   Ancel, Patricia ^a,b,c,d   Pelloux, Veronique ^a,b,c,d   Rouault, Christine ^a,b,c,d   Veyrie, Nicolas ^a,b,c,d   Hartemann, Agnes ^a,b,d   Treuter, Eckardt ^e   Venteclef, Nicolas ^a,b,c,d  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c INSERM   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COREPRESSOR PROTEIN; G PROTEIN PATHWAY SUPPRESSOR 2; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; REGULATOR PROTEIN; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; TWIST1 PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ARTICLE; CHRONIC INFLAMMATION; CLINICAL ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; MALE; MORBID OBESITY; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; RNA INTERFERENCE; STOMACH BYPASS; TRANSCRIPTION REGULATION; WEIGHT REDUCTION;

ADIPOCYTES; CELLS, CULTURED; CHEMOKINE CCL2; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NUCLEAR PROTEINS; NUCLEAR RECEPTOR CO-REPRESSOR 2; OBESITY, MORBID; PPAR GAMMA; TRANSCRIPTION, GENETIC; TWIST TRANSCRIPTION FACTOR;

EID: 84873846887     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64052     Document Type: Article

References (59)

1. Calder PC, et al. Inflammatory disease processes and interactions with nutrition. Br J Nutr. 2009; 101(suppl 1):S1-S45.
2. Hotamisligil GS. Inflammation and metabolic disorders. Nature. 2006;444(7121): 860-867.
3. Kolb H, Mandrup-Poulsen T. The global diabetes epidemic as a consequence of lifestyle-induced lowgrade inflammation. Diabetologia. 2010;53(1): 10-20.
4. Fernandez-Real JM, Pickup JC. Innate immunity, insulin resistance and type 2 diabetes. Trends Endocrinol Metab. 2008;19(1): 10-16.
5. Glass CK, Olefsky JM. Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab. 2012;15(5): 635-645.
6. Michaud A, Drolet R, Noël S, Paris G, Tchernof A. Visceral fat accumulation is an indicator of adipose tissue macrophage infiltration in women. Metabolism. 2012;61(5): 689-698.
7. Cancello R, et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes. 2005;54(8): 2277-2286.
8. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6(10): 772-783.
9. Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr. 2004;92(3): 347-355.
10. Wellen KE, Hotamisligil GS. Obesity-induced inflammatory changes in adipose tissue. J Clin Invest. 2003;112(12): 1785-1788.
11. Dalmas E, et al. Variations in circulating inflammatory factors are related to changes in calorie and carbohydrate intakes early in the course of surgeryinduced weight reduction. Am J Clin Nutr. 2011; 94(2): 450-458.
12. Skurk T, Alberti-Huber C, Herder C, Hauner H. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab. 2007;92(3): 1023-1033.
13. Tordjman J, Guerre-Millo M, Clement K. Adipose tissue inflammation and liver pathology in human obesity. Diabetes Metab. 2008;34(6 pt 2): 658-663.
14. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nature reviews. Immunology. 2011;11(2): 98-107.
15. Arner P, et al. Dynamics of human adipose lipid turnover in health and metabolic disease. Nature. 2011; 478(7367): 110-113.
16. Dalmas E, Clement K, Guerre-Millo M. Defining macrophage phenotype and function in adipose tissue. Trends Immunol. 2011;32(7): 307-314.
17. Kumar A, Takada Y, Boriek AM, Aggarwal BB. Nuclear factor-kappaB: its role in health and disease. J Mol Med (Berl). 2004;82(7): 434-448.
18. Sigal LH. Basic science for the clinician 39: NFkappaB- function, activation, control, and consequences. J Clin Rheumatol. 2006;12(4): 207-211.
19. Suganami T, et al. Role of the Toll-like receptor 4/NF-kappaB pathway in saturated fatty acidinduced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol. 2007;27(1): 84-91.
20. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med. 2012;18(3): 363-374.
21. Rosenfeld MG, Lunyak VV, Glass CK. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 2006;20(11): 1405-1428.
22. Medzhitov R, Horng T. Transcriptional control of the inflammatory response. Nat Rev Immunol. 2009; 9(10): 692-703.
23. Rosell M, Jones MC, Parker MG. Role of nuclear receptor corepressor RIP140 in metabolic syndrome. Biochim Biophys Acta. 2011;1812(8): 919-928.
24. Villanueva CJ, et al. TLE3 is a dual-function transcriptional coregulator of adipogenesis. Cell Metab. 2011;13(4): 413-427.
25. Siersbæk R, Mandrup S. Transcriptional networks controlling adipocyte differentiation. Cold Spring Harb Symp Quant Biol. 2011;76: 247-255.
26. Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol. 2011; 11(11): 775-787.
27. Venteclef N, Jakobsson T, Steffensen KR, Treuter E. Metabolic nuclear receptor signaling and the inflammatory acute phase response. Trends Endocrinol Metab. 2011;22: 333-343.
28. Huang W, et al. Coronin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature. 2011;470(7334): 414-418.
29. Venteclef N, et al. GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev. 2010;24(4): 381-395.
30. Nofsinger RR, et al. SMRT repression of nuclear receptors controls the adipogenic set point and metabolic homeostasis. Proc Natl Acad Sci U S A. 2008; 105(50): 20021-20026.
31. Li P, et al. Adipocyte NCoR knockout decreases PPARgamma phosphorylation and enhances PPARgamma activity and insulin sensitivity. Cell. 2011; 147(4): 815-826.
32. Henegar C, et al. Adipose tissue transcriptomic signature highlights the pathological relevance of extracellular matrix in human obesity. Genome Biol. 2008;9(1):R14.
33. Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol. 2010;314(1): 1-16.
34. Ghisletti S, et al. Cooperative NCoR/SMRT interactions establish a corepressor-based strategy for integration of inflammatory and anti-inflammatory signaling pathways. Genes Dev. 2009;23(6): 681-693.
35. Chen FH, Crist SA, Zhang GJ, Iwamoto Y, See WA. Interleukin-6 production by human bladder tumor cell lines is upregulated by bacillus Calmette- Guerin through nuclear factor-kappaB and Ap-1 via an immediate early pathway. J Urol. 2002; 168(2): 786-797.
36. Dandrea M, Donadelli M, Costanzo C, Scarpa A, Palmieri M. MeCP2/H3meK9 are involved in IL-6 gene silencing in pancreatic adenocarcinoma cell lines. Nucleic Acids Res. 2009;37(20): 6681-6690.
37. Pettersson AT, et al. A possible inflammatory role of twist1 in human white adipocytes. Diabetes. 2010;59(3): 564-571.
38. Pettersson AT, et al. Twist1 in human white adipose tissue and obesity. J Clin Endocrinol Metab. 2011; 96(1): 133-141.
39. Clement K, et al. Weight loss regulates inflammation- related genes in white adipose tissue of obese subjects. FASEB J. 2004;18(14): 1657-1669.
40. Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell. 1994; 79(7): 1147-1156.
41. Willson TM, Lambert MH, Kliewer SA. Peroxisome proliferator-activated receptor gamma and metabolic disease. Annu Rev Biochem. 2001;70: 341-367.
42. Pan D, Fujimoto M, Lopes A, Wang YX. Twist-1 is a PPARdelta-inducible, negative-feedback regulator of PGC-1alpha in brown fat metabolism. Cell. 2009; 137(1): 73-86.
43. Hartemann-Heurtier A, et al. Effects of bed-time insulin versus pioglitazone on abdominal fat accumulation, inflammation and gene expression in adipose tissue in patients with type 2 diabetes. Diabetes Res Clin Pract. 2009;86(1): 37-43.
44. Kanda H, et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest. 2006; 116(6): 1494-1505.
45. Tsou CL, et al. Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest. 2007;117(4): 902-909.
46. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest. 2007;117(1): 175-184.
47. Arner E, et al. Adipose tissue microRNAs as regulators of CCL2 production in human obesity. Diabetes. 2012;61(8): 1986-1993.
48. Fang S, et al. Corepressor SMRT promotes oxidative phosphorylation in adipose tissue and protects against diet-induced obesity and insulin resistance. Proc Natl Acad Sci U S A. 2011;108(8): 3412-3417.
49. Oberoi J, et al. Structural basis for the assembly of the SMRT/NCoR core transcriptional repression machinery. Nat Struct Mol Biol. 2011;18(2): 177-184.
50. Cardamone MD, et al. A protective strategy against hyperinflammatory responses requiring the nontranscriptional actions of GPS2. Mol Cell. 2012;46(1): 1-14.
51. Franco HL, Casasnovas J, Rodríguez-Medina JR, Cadilla CL. Redundant or separate entities? Roles of Twist1 and Twist2 as molecular switches during gene transcription. Nucleic Acids Res. 2011; 39(4): 1177-1186.
52. He W, et al. Adipose-specific peroxisome proliferator- activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci U S A. 2003;100(26): 15712-15717.
53. Imai T, et al. Peroxisome proliferator-activated receptor gamma is required in mature white and brown adipocytes for their survival in the mouse. Proc Natl Acad Sci U S A. 2004;101(13): 4543-4547.
54. Odegaard JI, et al. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature. 2007;447(7148): 1116-1120.
55. Hevener AL, et al. Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest. 2007;117(6): 1658-1669.
56. Pascual G, et al. Anti-inflammatory and antidiabetic roles of PPARgamma. Novartis Found Symp. 2007; 286: 183-196.
57. Choi JH, et al. Antidiabetic actions of a non-agonist PPARgamma ligand blocking Cdk5-mediated phosphorylation. Nature. 2011;477(7365): 477-481.
58. Keophiphath M, Rouault C, Divoux A, Clement K, Lacasa D. CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol. 2010;30(1): 39-45.
59. Prifti E, Zucker JD, Clement K, Henegar C. FunNet: an integrative tool for exploring transcriptional interactions. Bioinformatics. 2008; 24(22): 2636-2638.