Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance

Nature Communications

Volumn 6, Issue , 2015, Pages

  Kim, A Young ^a   Park, Yoon Jeong ^a   Pan, Xuebo ^b   Shin, Kyung Cheul ^a   Kwak, Soo Heon ^c   Bassas, Abdulelah F ^d   Sallam, Reem M ^d   Park, Kyong Soo ^c,e   Alfadda, Assim A ^d,f   Xu, Aimin ^b,g   Kim, Jae Bum ^a  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c Seoul National University College of Medicine   (South Korea)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e Seoul National University   (South Korea)

^f KING SAUD UNIVERSITY   (Saudi Arabia)

^g UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; INTERLEUKIN 1BETA; MESSENGER RNA; N PHTHALOYLTRYPTOPHAN; TUMOR NECROSIS FACTOR ALPHA; ADIPOQ PROTEIN, HUMAN; ADIPOQ PROTEIN, MOUSE; CYTOKINE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; LEPTIN RECEPTOR; LEPTIN RECEPTOR, MOUSE;

DISEASE TREATMENT; DNA; ENZYME ACTIVITY; GENE EXPRESSION; GLUCOSE; HOMEOSTASIS; HORMONE; LIPID; METABOLISM; METHYLATION; OBESITY; PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; EPIGENETICS; GENE EXPRESSION; GLUCOSE INTOLERANCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; MALE; MOUSE; NONHUMAN; OBESITY; PROMOTER REGION; PROTEIN EXPRESSION; 3T3 CELL LINE; ADIPOSE TISSUE; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; GENETICS; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

3T3-L1 CELLS; ADIPONECTIN; ADIPOSE TISSUE; ANIMALS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; CYTOKINES; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; HUMANS; INFLAMMATION; INSULIN RESISTANCE; MICE; OBESITY; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LEPTIN; RNA, MESSENGER;

EID: 84936802727     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8585     Document Type: Article

References (51)

1. Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 (Suppl) 245-254 (2003).
2. Carone, B. R. et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096 (2010).
3. Park, J. H., Stoffers, D. A., Nicholls, R. D. & Simmons, R. A. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J. Clin. Invest. 118, 2316-2324 (2008).
4. Sandovici, I. et al. Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets. Proc. Natl Acad. Sci. USA 108, 5449-5454 (2011).
5. Barres, R. et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab. 10, 189-198 (2009).
6. Ng, S. F. et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963-966 (2010).
7. Dunn, G. A. & Bale, T. L. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150, 4999-5009 (2009).
8. Scherer, P. E., Williams, S., Fogliano, M., Baldini, G. & Lodish, H. F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270, 26746-26749 (1995).
9. Yamauchi, T. et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288-1295 (2002).
10. Yamauchi, T. et al. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332-339 (2007).
11. Lim, S. et al. Association of adiponectin and resistin with cardiovascular events in Korean patients with type 2 diabetes: the Korean atherosclerosis study (KAS): a 42-month prospective study. Atherosclerosis 196, 398-404 (2008).
12. Maeda, N. et al. Diet-induced insulin resistance in mice lacking adiponectin/ ACRP30. Nat. Med. 8, 731-737 (2002).
13. Yamauchi, T. et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 7, 941-946 (2001).
14. Okada-Iwabu, M. et al. A small-molecule AdipoR agonist for type 2 diabetes and short life in obesity. Nature 503, 493-499 (2013).
15. Kadowaki, T. et al. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J. Clin. Invest. 116, 1784-1792 (2006).
16. Furukawa, S. et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752-1761 (2004).
17. Liu, M. et al. A disulfide-bond A oxidoreductase-like protein (DsbA-L) regulates adiponectin multimerization. Proc. Natl Acad. Sci. USA 105, 18302-18307 (2008).
18. Hu, E., Liang, P. & Spiegelman, B. M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem. 271, 10697-10703 (1996).
19. Kern, P. A., Di Gregorio, G. B., Lu, T., Rassouli, N. & Ranganathan, G. Adiponectin expression from human adipose tissue: relation to obesity, insulin resistance, and tumor necrosis factor-alpha expression. Diabetes 52, 1779-1785 (2003).
20. Rottach, A., Leonhardt, H. & Spada, F. DNA methylation-mediated epigenetic control. J. Cell. Biochem. 108, 43-51 (2009).
21. Cedar, H. & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304 (2009).
22. Degawa-Yamauchi, M. et al. Regulation of adiponectin expression in human adipocytes: effects of adiposity, glucocorticoids, and tumor necrosis factor alpha. Obes. Res. 13, 662-669 (2005).
23. Ye, J., Gao, Z., Yin, J. & He, Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 293, E1118-E1128 (2007).
24. Zhou, L. et al. DsbA-L alleviates endoplasmic reticulum stress-induced adiponectin downregulation. Diabetes 59, 2809-2816 (2010).
25. Kim, J. Y. et al. Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J. Clin. Invest. 117, 2621-2637 (2007).
26. Folco, E. J., Rocha, V. Z., Lopez-Ilasaca, M. & Libby, P. Adiponectin inhibits pro-inflammatory signaling in human macrophages independent of interleukin-10. J. Biol. Chem. 284, 25569-25575 (2009).
27. Ohashi, K. et al. Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J. Biol. Chem. 285, 6153-6160 (2010).
28. Zhou, M. et al. Mitochondrial dysfunction contributes to the increased vulnerabilities of adiponectin knockout mice to liver injury. Hepatology 48, 1087-1096 (2008).
29. Kirchner, H., Osler, M. E., Krook, A. & Zierath, J. R. Epigenetic flexibility in metabolic regulation: disease cause and prevention? Trends Cell Biol. 23, 203-209 (2013).
30. Bannister, A. J. & Kouzarides, T. Regulation of chromatin by histone modifications. Cell Res. 21, 381-395 (2011).
31. Hotamisligil, G. S. Inflammation and metabolic disorders. Nature 444, 860-867 (2006).
32. Sun, K., Kusminski, C. M. & Scherer, P. E. Adipose tissue remodeling and obesity. J. Clin. Invest. 121, 2094-2101 (2011).
33. Mathur, M., Tucker, P. W. & Samuels, H. H. PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell. Biol. 21, 2298-2311 (2001).
34. Yan, Q. et al. BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol. Cell 36, 110-120 (2009).
35. Esteve, P. O., Chin, H. G. & Pradhan, S. Human maintenance DNA (cytosine-5)-methyltransferase and p53 modulate expression of p53-repressed promoters. Proc. Natl Acad. Sci. USA 102, 1000-1005 (2005).
36. Robertson, K. D. et al. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25, 338-342 (2000).
37. Hervouet, E., Vallette, F. M. & Cartron, P. F. Dnmt1/transcription factor interactions: an alternative mechanism of DNA methylation inheritance. Genes Cancer 1, 434-443 (2010).
38. Hara, K. et al. Genetic variation in the gene encoding adiponectin is associated with an increased risk of type 2 diabetes in the Japanese population. Diabetes 51, 536-540 (2002).
39. Stumvoll, M. et al. Association of the T-G polymorphism in adiponectin (exon 2) with obesity and insulin sensitivity: interaction with family history of type 2 diabetes. Diabetes 51, 37-41 (2002).
40. Vasseur, F. et al. Single-nucleotide polymorphism haplotypes in the both proximal promoter and exon 3 of the APM1 gene modulate adipocyte-secreted adiponectin hormone levels and contribute to the genetic risk for type 2 diabetes in French Caucasians. Hum. Mol. Genet. 11, 2607-2614 (2002).
41. Takahashi, M. et al. Genomic structure and mutations in adipose-specific gene, adiponectin. Int. J. Obes. Relat. Metab. Disord. 24, 861-868 (2000).
42. Kondo, H. et al. Association of adiponectin mutation with type 2 diabetes: a candidate gene for the insulin resistance syndrome. Diabetes 51, 2325-2328 (2002).
43. Heid, I. M. et al. Genetic architecture of the APM1 gene and its influence on adiponectin plasma levels and parameters of the metabolic syndrome in 1, 727 healthy Caucasians. Diabetes 55, 375-384 (2006).
44. Bouatia-Naji, N. et al. ACDC/adiponectin polymorphisms are associated with severe childhood and adult obesity. Diabetes 55, 545-550 (2006).
45. Vasseur, F. et al. Hypoadiponectinaemia and high risk of type 2 diabetes are associated with adiponectin-encoding (ACDC) gene promoter variants in morbid obesity: evidence for a role of ACDC in diabesity. Diabetologia 48, 892-899 (2005).
46. Petrone, A. et al. The promoter region of the adiponectin gene is a determinant in modulating insulin sensitivity in childhood obesity. Obesity 14, 1498-1504 (2006).
47. Xu, A. et al. Testosterone selectively reduces the high molecular weight form of adiponectin by inhibiting its secretion from adipocytes. J. Biol. Chem. 280, 18073-18080 (2005).
48. Lee, Y. S. et al. Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance. Diabetes 60, 2474-2483 (2011).
49. Kim, A. Y. et al. Adiponectin represses colon cancer cell proliferation via AdipoR1-and-R2-mediated AMPK activation. Mol. Endocrinol. 24, 1441-1452 (2010).
50. Lee, Y. S. et al. Chromatin remodeling complex interacts with ADD1/SREBP1c to mediate insulin-dependent regulation of gene expression. Mol. Cell. Biol. 27, 438-452 (2007).
51. Fukuyama, H. et al. On-bead tryptic proteolysis: an attractive procedure for LC-MS/MS analysis of the Drosophila caspase 8 protein complex during immune response against bacteria. J. Proteomics 75, 4610-4619 (2012).