Up-regulation of the sirtuin 1 (Sirt1) and peroxisome proliferator-activated receptor γ Coactivator-1α (PGC-1α) genes in white adipose tissue of id1 protein-deficient mice: Implications in the protection against diet and age-induced glucose intolerance

Journal of Biological Chemistry

Volumn 289, Issue 42, 2014, Pages 29112-29122

  Zhao, Ying ^a   Ling, Flora ^a,b   Griffin, Timothy M ^a,b   He, Ting ^a   Towner, Rheal ^a   Ruan, Hong ^c   Sun, Xiao Hong ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COACTIVATORS; GLUCOSE INTOLERANCE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; SIRTUIN; UP-REGULATION; WHITE ADIPOSE TISSUES;

CYTOCHROME C; FAT DROPLET; INHIBITOR OF DIFFERENTIATION 1; INSULIN; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; MEMBRANE PROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN ET2; SIRTUIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; FATTY ACID; GLUCOSE; IDB1 PROTEIN, MOUSE; OXYGEN; PPARGC1A PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ADIPOCYTE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AP3 GENE; ARTICLE; BIOGENESIS; BODY FAT; BROWN ADIPOSE TISSUE; COMPARATIVE STUDY; CONTROLLED STUDY; CYT C GENE; DISEASE RESISTANCE; ENERGY EXPENDITURE; ENERGY METABOLISM; FATTY ACID OXIDATION; FATTY LIVER; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HISTOPATHOLOGY; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN SENSITIVITY; KNOCKOUT MOUSE; LIPID DIET; LIPID METABOLISM; LIPID OXIDATION; MALE; MCAD GENE; METABOLIC PARAMETERS; METABOLIC REGULATION; MITOCHONDRIAL BIOGENESIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OBESITY; OXIDATIVE PHOSPHORYLATION; PGC 1 ALPHA GENE; PHENOTYPE; PROTEIN DEFICIENCY; PROTEIN FUNCTION; RESPIRATORY EXCHANGE RATIO; SIRT1 GENE; TNF ALPHA GENE; UPREGULATION; WEIGHT REDUCTION; WHITE ADIPOSE TISSUE; ANIMAL; BLOOD; C57BL MOUSE; CALORIMETRY; GENETICS; GENOTYPE; GLUCOSE TOLERANCE TEST; METABOLISM;

ADIPOSE TISSUE, WHITE; ANIMALS; CALORIMETRY; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOTYPE; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INSULIN; MALE; MICE; MICE, INBRED C57BL; OBESITY; OXYGEN; SIRTUIN 1; TRANSCRIPTION FACTORS;

EID: 84908112251     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.571679     Document Type: Article

References (47)

1. Finucane, M. M., Stevens, G. A., Cowan, M. J., Danaei, G., Lin, J. K., Paciorek, C. J., Singh, G. M., Gutierrez, H. R., Lu, Y., Bahalim, A. N., Farzadfar, F., Riley, L. M., and Ezzati, M. (2011) National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet 377, 557-567.
2. Malik, V. S., Willett, W. C., and Hu, F. B. (2013) Global obesity: Trends, risk factors, and policy implications. Nat. Rev. Endocrinol. 9, 13-27.
3. Gesta, S., Tseng, Y. H., and Kahn, C. R. (2007) Developmental origin of fat: Tracking obesity to its source. Cell 131, 242-256.
4. Seale, P., Kajimura, S., and Spiegelman, B. M. (2009) Transcriptional control of brown adipocyte development and physiological function: of mice and men. Genes Dev. 23, 788-797.
5. Biddinger, S. B., and Kahn, C. R. (2006) From mice to men: insights into the insulin resistance syndromes. Annu. Rev. Physiol. 68, 123-158.
6. Spiegelman, B. M. (2013) Banting Lecture 2012: Regulation of adipogenesis: Toward new therapeutics for metabolic disease. Diabetes 62, 1774-1782.
7. Harms, M., and Seale, P. (2013) Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263.
8. Langin, D. (2010) Recruitment of brown fat and conversion of white into brown adipocytes: strategies to fight the metabolic complications of obesity? Biochim. Biophys. Acta 1801, 372-376.
9. Rosen, E. D., Sarraf, P., Troy, A. E., Bradwin, G., Moore, K., Milstone, D. S., Spiegelman, B. M., and Mortensen, R. M. (1999) PPARγ is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 4, 611-617.
10. Barak, Y., Nelson, M. C., Ong, E. S., Jones, Y. Z., Ruiz-Lozano, P., Chien, K. R., Koder, A., and Evans, R. M. (1999) PPARγ is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585-595.
11. Spiegelman, B. M., Puigserver, P., and Wu, Z. (2000) Regulation of adipogenesis and energy balance by PPARγ and PGC-1. Int. J. Obes. Relat. Metab. Disord. 24, S8-S10.
12. Puigserver, P., and Spiegelman, B. M. (2003) Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1 α): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90.
13. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegelman, B. M. (1998)Acold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839.
14. Tiraby, C., Tavernier, G., Lefort, C., Larrouy, D., Bouillaud, F., Ricquier, D., and Langin, D. (2003) Acquirement of brown fat cell features by human white adipocytes. J. Biol. Chem. 278, 33370-33376.
15. Kleiner, S., Mepani, R. J., Laznik, D., Ye, L., Jurczak, M. J., Jornayvaz, F. R., Estall, J. L., Chatterjee Bhowmick, D., Shulman, G. I., and Spiegelman, B. M. (2012) Development of insulin resistance in mice lacking PGC-1 α in adipose tissues. Proc. Natl. Acad. Sci. U.S.A. 109, 9635-9640.
16. Rodgers, J. T., Lerin, C., Haas, W., Gygi, S. P., Spiegelman, B. M., and Puigserver, P. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1 α and SIRT1. Nature 434, 113-118.
17. Yang, T., Fu, M., Pestell, R., and Sauve, A. A. (2006) SIRT1 and endocrine signaling. Trends Endocrinol. Metab. 17, 186-191.
18. Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012) Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13, 225-238.
19. Handschin, C., Rhee, J., Lin, J., Tarr, P. T., and Spiegelman, B. M. (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor γ coactivator 1α expression in muscle. Proc. Natl. Acad. Sci. U.S.A. 100, 7111-7116.
20. Sun, X. H. (2004) Multitasking of helix-loop-helix proteins in lymphopoiesis. Adv. Immunol. 84, 43-77.
21. Kee, B. L. (2009) E and ID proteins branch out. Nat. Rev. Immunol. 9, 175-184.
22. Satyanarayana, A., Klarmann, K. D., Gavrilova, O., and Keller, J. R. (2012) Ablation of the transcriptional regulator Id1 enhances energy expenditure, increases insulin sensitivity, and protects against age- And diet-induced insulin resistance, and hepatosteatosis. FASEB J. 26, 309-323.
23. Park, K. W., Waki, H., Villanueva, C. J., Monticelli, L. A., Hong, C., Kang, S., MacDougald, O. A., Goldrath, A. W., and Tontonoz, P. (2008) Inhibitor of DNA binding 2 is a small molecule-inducible modulator of peroxisome proliferator-activated receptor-γ expression and adipocyte differentiation. Mol. Endocrinol. 22, 2038-2048.
24. Moldes, M., Lasnier, F., Fève, B., Pairault, J., and Djian, P. (1997) Id3 prevents differentiation of preadipose cells. Mol. Cell Biol. 17, 1796-1804.
25. Murad, J. M., Place, C. S., Ran, C., Hekmatyar, S. K., Watson, N. P., Kauppinen, R. A., and Israel, M. A. (2010) Inhibitor of DNA binding 4 (ID4) regulation of adipocyte differentiation and adipose tissue formation in mice. J. Biol. Chem. 285, 24164-24173.
26. Doran, A. C., Meller, N., Cutchins, A., Deliri, H., Slayton, R. P., Oldham, S. N., Kim, J. B., Keller, S. R., and McNamara, C. A. (2008) The helix-loophelix factors Id3 and E47 are novel regulators of adiponectin. Circ. Res. 103, 624-634.
27. Cutchins, A., Harmon, D. B., Kirby, J. L., Doran, A. C., Oldham, S. N., Skaflen, M., Klibanov, A. L., Meller, N., Keller, S. R., Garmey, J., and Mc-Namara, C. A. (2012) Inhibitor of differentiation-3 mediates high fat dietinduced visceral fat expansion. Arterioscler. Thromb. Vasc. Biol. 32, 317-324.
28. Akerfeldt, M. C., and Laybutt, D. R. (2011) Inhibition of Id1 augments insulin secretion and protects against high-fat diet-induced glucose intolerance. Diabetes 60, 2506-2514.
29. Cochrane, S. W., Zhao, Y., Welner, R. S., and Sun, X. H. (2009) Balance between Id and E proteins regulates myeloid versus lymphoid lineage decisions. Blood 113, 1016-1026.
30. Perry, S. S., Zhao, Y., Nie, L., Cochrane, S. W., Huang, Z., and Sun, X. H. (2007) Id1, but not Id3, directs long-term repopulating hematopoietic stem-cell maintenance. Blood 110, 2351-2360.
31. He, W., Barak, Y., Hevener, A., Olson, P., Liao, D., Le, J., Nelson, M., Ong, E., Olefsky, J. M., and Evans, R. M. (2003) Adipose-specific peroxisome proliferator-activated receptor γ knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. U.S.A. 100, 15712-15717.
32. Fasshauer, M., Klein, J., Ueki, K., Kriauciunas, K. M., Benito, M., White, M. F., and Kahn, C. R. (2000) Essential role of insulin receptor substrate-2 in insulin stimulation of Glut4 translocation and glucose uptake in brown adipocytes. J. Biol. Chem. 275, 25494-25501.
33. Fasshauer, M., Klein, J., Kriauciunas, K. M., Ueki, K., Benito, M., and Kahn, C. R. (2001) Essential role of insulin receptor substrate 1 in differentiation of brown adipocytes. Mol. Cell Biol. 21, 319-329.
34. Tschöp, M., Smiley, D. L., and Heiman, M. L. (2000) Ghrelin induces adiposity in rodents. Nature 407, 908-913.
35. Garteiser, P., Doblas, S., Towner, R. A., and Griffin, T. M. (2013) Calibration of a semi-automated segmenting method for quantification of adipose tissue compartments from magnetic resonance images of mice. Metabolism 62, 1686-1695.
36. Nieto-Vazquez, I., Fernández-Veledo, S., Krämer, D. K., Vila-Bedmar, R., Garcia-Guerra, L., and Lorenzo, M. (2008) Insulin resistance associated to obesity: The link TNF-α. Arch. Physiol. Biochem. 114, 183-194.
37. Ruzinova, M. B., and Benezra, R. (2003) Id proteins in development, cell cycle, and cancer. Trends Cell Biol. 13, 410-418.
38. Zhang, X., Ling, M. T., Wang, Q., Lau, C. K., Leung, S. C., Lee, T. K., Cheung, A. L., Wong, Y. C., and Wang, X. (2007) Identification of a novel inhibitor of differentiation-1 (ID-1) binding partner, caveolin-1, and its role in epithelial-mesenchymal transition and resistance to apoptosis in prostate cancer cells. J. Biol. Chem. 282, 33284-33294.
39. Peng, X., Wang, Y., Kolli, S., Deng, J., Li, L., Wang, Z., Raj, J. U., and Gou, D. (2012) Physical and functional interaction between the ID1 and p65 for activation of NF-κB. Am. J. Physiol. Cell Physiol. 303, C267-C277.
40. Li, X. (2013) SIRT1 and energy metabolism. Acta Biochim. Biophys. Sin. 45, 51-60.
41. Chalkiadaki, A., and Guarente, L. (2012) High fat diet triggers inflammation- induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab. 16, 180-188.
42. Picard, F., Kurtev, M., Chung, N., Topark-Ngarm, A., Senawong, T., Machado De Oliveira, R., Leid, M., McBurney, M. W., and Guarente, L. (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-γ. Nature 429, 771-776.
43. Yang, Y., Liou, H. C., and Sun, X. H. (2006) Id1 potentiates NF-κB activation upon T cell receptor signaling. J. Biol. Chem. 281, 34989-34996.
44. Zhao, Y., Ling, F., Wang, H. C., and Sun, X. H. (2013) Chronic TLR signaling impairs the long-term repopulating potential of hematopoietic stem cells of wild type but not Id1 deficient mice. PLoS. ONE 8, e55552.
45. Pan, D., Fujimoto, M., Lopes, A., Wang, Y. X. (2009) Twist-1 is a PPARδ- inducible, negative-feedback regulator of PGC-1α in brown fat metabolism. Cell 137, 73-86.
46. Wang, X., and Seed, B. (2003) A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res. 31, e154.
47. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H., Tempst, P., Rudnicki, M. A., Beier, D. R., and Spiegelman, B. M. (2008) PRDM1 controls a brown fat/skeletal muscle switch. Nature 454, 961-967.