Insulin resistance and white adipose tissue inflammation are uncoupled in energetically challenged Fsp27-deficient mice

Nature Communications

Volumn 6, Issue , 2015, Pages

  Zhou, Linkang ^a   Park, Shi Young ^b   Xu, Li ^c   Xia, Xiayu ^a   Ye, Jing ^d   Su, Lu ^a   Jeong, Kyeong Hoon ^b   Hur, Jang Ho ^b   Oh, Hyunhee ^b   Tamori, Yoshikazu ^e,f   Zingaretti, Cristina M ^g   Cinti, Saverio ^g   Argente, Jesús ^h,i,j,k   Yu, Miao ^a   Wu, Lizhen ^a   Ju, Shenghong ^l   Guan, Feifei ^m   Yang, Hongyuan ⁿ   Choi, Cheol Soo ^b   Savage, David B ^o   Li, Peng ^a   more..

^a Tsinghua University   (China)

^b Gachon University College of Medicine   (South Korea)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^e KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f Chibune General Hospital   (Japan)

^g UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^h HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

ⁱ Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas   (Spain)

^j UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^k Instituto de Salud Carlos III   (Spain)

^l SOUTHEAST UNIVERSITY   (China)

^m BEIJING HOSPITAL   (China)

ⁿ UNIVERSITY OF NEW SOUTH WALES   (Australia)

^o UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; DIET; FEEDING BEHAVIOR; HORMONE; LIPID; METABOLISM; PHENOTYPE; RODENT;

MUS;

FAT-SPECIFIC PROTEIN 27, MOUSE; INFLAMMASOME; LEPTIN; PROTEIN;

ANIMAL; CROSS BREEDING; ENERGY METABOLISM; GENETICS; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIPID DIET; METABOLISM; MICROARRAY ANALYSIS; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; WESTERN BLOTTING; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; BLOTTING, WESTERN; CROSSES, GENETIC; DIET, HIGH-FAT; ENERGY METABOLISM; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TOLERANCE TEST; INFLAMMASOMES; INFLAMMATION; INSULIN RESISTANCE; LEPTIN; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; PROTEINS;

EID: 84931289926     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6949     Document Type: Article

References (48)

1. Guilherme, A., and Virbasius., J. V., Puri, V. & Czech, M. P. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 9, 367-377 (2008).
2. Puri, V. et al. Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc. Natl Acad. Sci. USA 105, 7833-7838 (2008).
3. Gong, J., Sun, Z. & Li, P. CIDE proteins and metabolic disorders. Curr. Opin. Lipidol. 20, 121-126 (2009).
4. Nordstrom, E. A. et al. A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-alpha)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes 54, 1726-1734 (2005).
5. Matsusue, K. et al. Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab. 7, 302-311 (2008).
6. Zhou, L. et al. Cidea promotes hepatic steatosis by sensing dietary fatty acids. Hepatology 56, 95-107 (2012).
7. Puri, V. et al. Fat-specific protein 27, a novel lipid droplet protein that enhances triglyceride storage. J. Biol. Chem. 282, 34213-34218 (2007).
8. Keller, P. et al. Fat-specific protein 27 regulates storage of triacylglycerol. J. Biol. Chem. 283, 14355-14365 (2008).
9. Gong, J. et al. Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J. Cell Biol. 195, 953-963 (2011).
10. Wu, L. et al. Cidea controls lipid droplet fusion and lipid storage in brown and white adipose tissue. Sci. China Life Sci. 57, 107-116 (2014).
11. Sun, Z. et al. Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat. Commun. 4, 1594 (2013).
12. Toh, S. Y. et al. Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of fsp27 deficient mice. PLoS One 3, e2890 (2008).
13. Nishino, N. et al. FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J. Clin. Invest. 118, 2808-2821 (2008).
14. Rubio-Cabezas, O. et al. Partial lipodystrophy and insulin resistant diabetes in a patient with a homozygous nonsense mutation in CIDEC. EMBO Mol. Med. 1, 280-287 (2009).
15. Rosen, E. D. & Spiegelman, B. M. What we talk about when we talk about fat. Cell 156, 20-44 (2014).
16. Rosen, E. D. & Spiegelman, B. M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847-853 (2006).
17. Frayn, K. N. Adipose tissue as a buffer for daily lipid flux. Diabetologia 45, 1201-1210 (2002).
18. Garg, A. Clinical review: Lipodystrophies: genetic and acquired body fat disorders. J. Clin. Endocrinol. Metab. 96, 3313-3325 (2011).
19. Savage, D. B. Mouse models of inherited lipodystrophy. Dis. Model Mech. 2, 554-562 (2009).
20. Vigouroux, C., Caron-Debarle, M., Le Dour, C., Magre, J. & Capeau, J. Molecular mechanisms of human lipodystrophies: from adipocyte lipid droplet to oxidative stress and lipotoxicity. Int. J. Biochem. Cell Biol. 43, 862-876 (2011).
21. Pendse, A. A., and Johnson., L. A., Tsai, Y. S. & Maeda, N. Pparg-P465L mutation worsens hyperglycemia in Ins2-Akita female mice via adipose-specific insulin resistance and storage dysfunction. Diabetes 59, 2890-2897 (2010).
22. Reue, K. & Phan, J. Metabolic consequences of lipodystrophy in mouse models. Curr. Opin. Clin. Nutr. Metab. Care 9, 436-441 (2006).
23. Lowell, B. B. et al. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature 366, 740-742 (1993).
24. Cinti, S. et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J. Lipid Res. 46, 2347-2355 (2005).
25. Murano, I. et al. Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J. Lipid Res. 49, 1562-1568 (2008).
26. Giordano, A. et al. Obese adipocytes show ultrastructural features of stressed cells and die of pyroptosis. J. Lipid Res. 54, 2423-2436 (2013).
27. Vandanmagsar, B. et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179-188 (2011).
28. Hamann, A., Flier, J. S. & Lowell, B. B. Obesity after genetic ablation of brown adipose tissue. Z. Ernahrungswiss 37 (Suppl 1), 1-7 (1998).
29. Perry, R. J., and Samuel., V. T., Petersen, K. F. & Shulman, G. I. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature 510, 84-91 (2014).
30. Sun, Z. & Lazar, M. A. Dissociating fatty liver and diabetes. Trends Endocrinol. Metab. 24, 4-12 (2013).
31. Reitman, M. L. Metabolic lessons from genetically lean mice. Annu. Rev. Nutr. 22, 459-482 (2002).
32. Asterholm, I. W., Halberg, N. & Scherer, P. E. Mouse models of lipodystrophy key reagents for the understanding of the metabolic syndrome. Drug Discov. Today Dis. Models 4, 17-24 (2007).
33. Gray, S. L. et al. Leptin deficiency unmasks the deleterious effects of impaired peroxisome proliferator-activated receptor gamma function (P465L PPARgamma) in mice. Diabetes 55, 2669-2677 (2006).
34. Hotamisligil, G. S., Shargill, N. S. & Spiegelman, B. M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259, 87-91 (1993).
35. Glass, C. K. & Olefsky, J. M. Inflammation and lipid signaling in the etiology of insulin resistance. Cell Metab. 15, 635-645 (2012).
36. McNelis, J. C. & Olefsky, J. M. Macrophages, immunity, and metabolic disease. Immunity 41, 36-48 (2014).
37. Ferrante, Jr. A. W. Macrophages, fat, and the emergence of immunometabolism. J. Clin. Invest. 123, 4992-4993 (2013).
38. Peng, X. G. et al. Comparison of brown and white adipose tissue fat fractions in ob, seipin, and Fsp27 gene knockout mice by chemical shift-selective imaging and (1)H-MR spectroscopy. Am. J. Physiol. Endocrinol. Metab. 304, E160-E167 (2013).
39. Choi, C. S. et al. Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Proc. Natl Acad. Sci. USA 104, 16480-16485 (2007).
40. Kim, K. H. et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat. Med. 19, 83-92 (2013).
41. Li, D. et al. Regulation of gene expression by FSP27 in white and brown adipose tissue. BMC Genomics 11, 446 (2010).
42. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
43. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
44. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3 (2004).
45. van Iersel, M. P. et al. Presenting and exploring biological pathways with PathVisio. BMC Bioinformatics 9, 399 (2008).
46. Kelder, T. et al. WikiPathways: building research communities on biological pathways. Nucleic Acids Res. 40, D1301-D1307 (2012).
47. Li, H. et al. Cell death-inducing DFF45-like effector b (Cideb) is present in pancreatic beta-cells and involved in palmitate induced beta-cell apoptosis. Diabetes Metab. Res. Rev. 28, 145-155 (2012).
48. Tschop, M. H. et al. A guide to analysis of mouse energy metabolism. Nat. Methods 9, 57-63 (2012).