The histone demethylase UTX promotes brown adipocyte thermogenic program via coordinated regulation of H3K27 demethylation and acetylation

Journal of Biological Chemistry

Volumn 290, Issue 41, 2015, Pages 25151-25163

  Zha, Lin ^a,b   Li, Fenfen ^b   Wu, Rui ^b   Artinian, Liana ^b   Rehder, Vincent ^b   Yu, Liqing ^c   Liang, Houjie ^a   Xue, Bingzhong ^b   Shi, Hang ^c  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b GEORGIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; AMINO ACIDS; CHEMICAL ACTIVATION; GENE EXPRESSION; GENES; MOLECULAR WEIGHT; TISSUE;

ADIPOCYTE DIFFERENTIATION; CO-ORDINATED CONTROL; EPIGENETIC MECHANISMS; GENETIC MECHANISM; HISTONE ACETYLTRANSFERASES; MOLECULAR MECHANISM; TETRATRICOPEPTIDE REPEATS; WHITE ADIPOSE TISSUES;

GENE EXPRESSION REGULATION;

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HISTONE DEMETHYLASE; HISTONE DEMETHYLASE UTX; HISTONE H3; HISTONE H3 LYSINE 27; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SUZ12 PROTEIN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1; EZH2 PROTEIN, MOUSE; HISTONE; ION CHANNEL; LYSINE; MITOCHONDRIAL PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PPARGC1A PROTEIN, MOUSE; SUZ12 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; UCP1 PROTEIN, MOUSE; UTX PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; COLD EXPOSURE; CONTROLLED STUDY; DOWN REGULATION; ENHANCER REGION; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; HISTONE DEMETHYLATION; LIPID METABOLISM; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; THERMOGENESIS; TRANSCRIPTION INITIATION; WHITE ADIPOSE TISSUE; ACETYLATION; ANIMAL; CELL LINE; CHEMISTRY; COLD; CYTOLOGY; GENETICS; METABOLISM; METHYLATION;

ACETYLATION; ADIPOCYTES, BROWN; ANIMALS; CELL DIFFERENTIATION; CELL LINE; COLD TEMPERATURE; CREB-BINDING PROTEIN; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTONE DEMETHYLASES; HISTONES; ION CHANNELS; LIPID METABOLISM; LYSINE; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; METHYLATION; MICE; MITOCHONDRIAL PROTEINS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; THERMOGENESIS; TRANSCRIPTION FACTORS; UNCOUPLING PROTEIN 1;

EID: 84943778234     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.662650     Document Type: Article

References (61)

1. Hill, J. O., Wyatt, H. R., and Peters, J. C. (2012) Energy balance and obesity. Circulation 126, 126-132
2. Lowell, B. B., and Spiegelman, B. M. (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652-660
3. Cohen, P., Levy, J. D., Zhang, Y., Frontini, A., Kolodin, D. P., Svensson, K. J., Lo, J. C., Zeng, X., Ye, L., Khandekar, M. J., Wu, J., Gunawardana, S. C., Banks, A. S., Camporez, J. P., Jurczak, M. J., Kajimura, S., Piston, D. W., Mathis, D., Cinti, S., Shulman, G. I., Seale, P., and Spiegelman, B. M. (2014) Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch. Cell 156, 304-316
4. Feldmann, H. M., Golozoubova, V., Cannon, B., and Nedergaard, J. (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9, 203-209
5. Seale, P., Conroe, H. M., Estall, J., Kajimura, S., Frontini, A., Ishibashi, J., Cohen, P., Cinti, S., and Spiegelman, B. M. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121, 96-105
6. Cannon, B., and Nedergaard, J. (1985) The biochemistry of an inefficient tissue: brown adipose tissue. Essays in Biochemistry 20, 110-164
7. Nicholls, D. G., and Locke, R. M. (1984) Thermogenic mechanisms in brown fat. Physiological Reviews 64, 1-64
8. Kopecky, J., Clarke, G., Enerbäck, S., Spiegelman, B., and Kozak, L. P. (1995) Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J. Clin. Invest. 96, 2914-2923
9. Kopecký, J., Hodný, Z., Rossmeisl, M., Syrový, I., and Kozak, L. P. (1996) Reduction of dietary obesity in aP2-Ucp transgenic mice: physiology and adipose tissue distribution. Am. J. Physiol. 270, E768-E775
10. Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y. H., Doria, A., Kolodny, G. M., and Kahn, C. R. (2009) Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517
11. Van Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M., Kemerink, G. J., Bouvy, N. D., Schrauwen, P., and Teule, G. J. (2009) Cold-activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508
12. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N. J., Enerbäck, S., and Nuutila, P. (2009) Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525
13. Maunakea, A. K., Chepelev, I., and Zhao, K. (2010) Epigenome mapping in normal and disease states. Circ. Res. 107, 327-339
14. Bäckdahl, L., Bushell, A., and Beck, S. (2009) Inflammatory signalling as mediator of epigenetic modulation in tissue-specific chronic inflammation. IntJBiochem. Cell Biol. 41, 176-184
15. Dambacher, S., Hahn, M., and Schotta, G. (2010) Epigenetic regulation of development by histone lysine methylation. Heredity 105, 24-37
16. Edwards, T. M., and Myers, J. P. (2007) Environmental exposures and gene regulation in disease etiology. Environ. Health Perspect. 115, 1264-1270
17. Skinner, M. K., Manikkam, M., and Guerrero-Bosagna, C. (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab. 21, 214-222
18. Campión, J., Milagro, F. I., and Martínez, J. A. (2009) Individuality and epigenetics in obesity. Obes. Rev. 10, 383-392
19. Holness, M. J., and Sugden, M. C. (2006) Epigenetic regulation of metabolism in children born small for gestational age. Curr. Opin. Clin. Nutr. Metab. Care 9, 482-488
20. Ling, C., and Groop, L. (2009) Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58, 2718-2725
21. Maier, S., and Olek, A. (2002) Diabetes: a candidate disease for efficient DNA methylation profiling. J. Nutr. 132, 2440S-2443S
22. Szarc Vel Szic, K., Ndlovu, M. N., Haegeman, G., and Vanden Berghe, W. (2010) Nature or nurture: let food be your epigenetic medicine in chronic inflammatory disorders. Biochem. Pharmacol. 80, 1816-1832
23. Uldry, M., Yang, W., St-Pierre, J., Lin, J., Seale, P., and Spiegelman, B. M. (2006) Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 3, 333-341
24. Seale, P., Kajimura, S., Yang, W., Chin, S., Rohas, L. M., Uldry, M., Tavernier, G., Langin, D., and Spiegelman, B. M. (2007) Transcriptional control of brown fat determination by PRDM16. Cell Metab. 6, 38-54
25. Ge, K. (2012) Epigenetic regulation of adipogenesis by histone methylation. Biochim. Biophys. Acta 1819, 727-732
26. Hong, S., Cho, Y. W., Yu, L. R., Yu, H., Veenstra, T. D., and Ge, K. (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. U. S. A. 104, 18439-18444
27. Wang, L., Jin, Q., Lee, J. E., Su, I. H., and Ge, K. (2010) Histone H3K27 methyltransferase Ezh2 represses Wnt genes to facilitate adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 107, 7317-7322
28. Iida, A., Iwagawa, T., Kuribayashi, H., Satoh, S., Mochizuki, Y., Baba, Y., Nakauchi, H., Furukawa, T., Koseki, H., Murakami, A., and Watanabe, S. (2014) Histone demethylase Jmjd3 is required for the development of subsets of retinal bipolar cells. Proc. Natl. Acad. Sci. U. S. A. 111, 3751-3756
29. Lewis, P. W., Müller, M. M., Koletsky, M. S., Cordero, F., Lin, S., Banaszynski, L. A., Garcia, B. A., Muir, T. W., Becher, O. J., and Allis, C. D. (2013) Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340, 857-861
30. Ntziachristos, P., Tsirigos, A., Welstead, G. G., Trimarchi, T., Bakogianni, S., Xu, L., Loizou, E., Holmfeldt, L., Strikoudis, A., King, B., Mullenders, J., Becksfort, J., Nedjic, J., Paietta, E., Tallman, M. S., Rowe, J. M., Tonon, G., Satoh, T., Kruidenier, L., Prinjha, R., Akira, S., Van Vlierberghe, P., Ferrando, A. A., Jaenisch, R., Mullighan, C G., and Aifantis, I. (2014) Contrasting roles of histone 3 lysine 27 demethylases in acute lymphoblastic leukaemia. Nature 514, 513-517
31. Xue, B., Rim, J. S., Hogan, J. C., Coulter, A. A., Koza, R. A., and Kozak, L. P. (2007) Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J. Lipid Res. 48, 41-51
32. Rajakumari, S., Wu, J., Ishibashi, J., Lim, H. W., Giang, A. H., Won, K. J., Reed, R. R., and Seale, P. (2013) EBF2 determines and maintains brown adipocyte identity. Cell Metab. 17, 562-574
33. Cao, Q., Wang, X., Jia, L., Mondal, A. K., Diallo, A., Hawkins, G. A., Das, S. K., Parks, J. S., Yu, L., Shi, H., Shi, H., and Xue, B. (2014) Inhibiting DNA Methylation by 5-Aza-2'-deoxycytidine ameliorates atherosclerosis through suppressing macrophage inflammation. Endocrinology 155, 4925-4938
34. Shi, H., Moustaid-Moussa, N., Wilkison, W. O., and Zemel, M. B. (1999) Role of the sulfonylurea receptor in regulating human adipocyte metabolism. FASEBJ. 13, 1833-1838
35. Zhao, X., Sternsdorf, T., Bolger, T. A., Evans, R. M., and Yao, T. P. (2005) Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylasemediated lysine modifications. Mol. Cell. Biol. 25, 8456-8464
36. Yang, X., Wang, X., Liu, D., Yu, L., Xue, B., and Shi, H. (2014) Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b. Mol. Endocrinol. 28, 565-574
37. Shi, H., Kokoeva, M. V., Inouye, K., Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025
38. Shi, H., Tzameli, I., Bjørbaek, C., and Flier, J. S. (2004) Suppressor of cytokine signaling 3 is a physiological regulator of adipocyte insulin signaling. J. Biol. Chem. 279, 34733-34740
39. Xue, B., Coulter, A., Rim, J. S., Koza, R. A., and Kozak, L. P. (2005) Transcriptional synergy and the regulation of Ucp1 during brown adipocyte induction in white fat depots. Mol. Cell. Biol. 25, 8311-8322
40. Gaydos, L. J., Wang, W., and Strome, S. (2014) Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 345, 1515-1518
41. Kozak, U. C., Kopecky, J., Teisinger, J., Enerbäck, S., Boyer, B., and Kozak, L. P. (1994) An upstream enhancer regulating brown-fat-specific expression of the mitochondrial uncoupling protein gene. Mol. Cell. Biol. 14, 59-67
42. Grégoire, S., Xiao, L., Nie, J., Zhang, X., Xu, M., Li, J., Wong, J., Seto, E., and Yang, X. J. (2007) Histone deacetylase 3 interacts with and deacetylates myocyte enhancer factor 2. Mol. Cell. Biol. 27, 1280-1295
43. Handschin, C., Rhee, J., Lin, J., Tarr, P. T., and Spiegelman, B. M. (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc. Natl. Acad. Sci. U. S. A. 100, 7111-7116
44. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S., and Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043
45. Jin, Q., Yu, L. R., Wang, L., Zhang, Z., Kasper, L. H., Lee, J. E., Wang, C., Brindle, P. K., Dent, S. Y., and Ge, K. (2011) Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBOJ. 30, 249-262
46. Shore, A., Karamitri, A., Kemp, P., Speakman, J. R., and Lomax, M. A. (2010) Role of Ucp1 enhancer methylation and chromatin remodelling in the control of Ucp1 expression in murine adipose tissue. Diabetologia 53, 1164-1173
47. Tateishi, K., Okada, Y., Kallin, E. M., and Zhang, Y. (2009) Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 458, 757-761
48. Wang, L., Xu, S., Lee, J. E., Baldridge, A., Grullon, S., Peng, W., and Ge, K. (2013) Histone H3K9 methyltransferase G9a represses PPAR7 expression and adipogenesis. EMBOJ. 32, 45-59
49. Ishibashi, J., and Seale, P. (2010) Medicine. Beige can be slimming. Science 328, 1113-1114
50. 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) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967
51. Wu, J., Boström, P., Sparks, L. M., Ye, L., Choi, J. H., Giang, A. H., Khandekar, M., Virtanen, K. A., Nuutila, P., Schaart, G., Huang, K., Tu, H., Van Marken Lichtenbelt, W. D., Hoeks, J., Enerbäck, S., Schrauwen, P., and Spiegelman, B. M. (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376
52. Guerra, C., Koza, R. A., Yamashita, H., Walsh, K., and Kozak, L. P. (1998) Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J. Clin. Invest. 102, 412-420
53. Brito, N. A., Brito, M. N., and Bartness, T. J. (2008) Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1445-R1452
54. Vaughan, C H., Zarebidaki, E., Ehlen, J. C., and Bartness, T. J. (2014) Analysis and measurement of the sympathetic and sensory innervation of white and brown adipose tissue. Methods Enzymol. 537, 199-225
55. Long, J. Z., Svensson, K. J., Tsai, L., Zeng, X., Roh, H. C., Kong, X., Rao, R. R., Lou, J., Lokurkar, I., Baur, W., Castellot, J. J., Jr., Rosen, E. D., and Spiegelman, B. M. (2014) A smooth muscle-like origin for beige adipocytes. Cell Metab. 19, 810-820
56. Shinoda, K., Luijten, I. H., Hasegawa, Y., Hong, H., Sonne, S. B., Kim, M., Xue, R., Chondronikola, M., Cypess, A. M., Tseng, Y. H., Nedergaard, J., Sidossis, L. S., and Kajimura, S. (2015) Genetic and functional characterization of clonally derived adult human brown adipocytes. Nat. Med. 21, 389-394
57. Finck, B. N., and Kelly, D. P. (2006) PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116, 615-622
58. Lin, J., Handschin, C., and Spiegelman, B. M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370
59. Rim, J. S., and Kozak, L. P. (2002) Regulatory motifs for CREB-binding protein and Nfe2l2 transcription factors in the upstream enhancer of the mitochondrial uncoupling protein 1 gene. J. Biol. Chem. 277, 34589-34600
60. Cao, W., Daniel, K. W., Robidoux, J., Puigserver, P., Medvedev, A. V., Bai, X., Floering, L. M., Spiegelman, B. M., and Collins, S. (2004) p38 mitogenactivated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24, 3057-3067
61. Herzig, S., Long, F., Jhala, U. S., Hedrick, S., Quinn, R., Bauer, A., Rudolph, D., Schutz, G., Yoon, C., Puigserver, P., Spiegelman, B., and Montminy, M. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413, 179-183