Early B-cell factor-1 (EBF1) is a key regulator of metabolic and inflammatory signaling pathways in mature adipocytes

Journal of Biological Chemistry

Volumn 288, Issue 50, 2013, Pages 35925-35939

  Griffin, Michael J ^a,b   Zhou, Yiming ^a   Kang, Sona ^a   Zhang, Xiaolan ^c   Mikkelsen, Tarjei S ^c   Rosen, Evan D ^a,b,c  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLAMMATORY CYTOKINES; INFLAMMATORY SIGNALING; INSULIN-STIMULATED GLUCOSE; LOCATION ANALYSIS; SIGNALING EVENTS; SIGNALING PATHWAYS; TRANSCRIPTIONAL MECHANISMS; TRANSCRIPTIONAL PROFILING;

BIOSYNTHESIS; GENE EXPRESSION; METABOLISM; SIGNAL TRANSDUCTION;

CELL SIGNALING;

CYTOKINE; EARLY B CELL FACTOR 1 PROTEIN; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REGULATOR PROTEIN; STAT1 PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL METABOLISM; CELL TYPE; CONTROLLED STUDY; CYTOKINE RELEASE; ENHANCER REGION; ENZYME REGULATION; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GLUCOSE TRANSPORT; HORMONE ACTION; INFLAMMATION; INTRACELLULAR SIGNALING; LIPOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SEQUENCE ANALYSIS;

ADIPOCYTE; B LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION (CHIP); EBF1; INFLAMMATION; INSULIN SIGNALING; SIGNAL TRANSDUCTION; TRANSCRIPTION/DEVELOPMENTAL FACTORS;

3T3-L1 CELLS; ADIPOCYTES; ADIPOKINES; ANIMALS; GENE KNOCKDOWN TECHNIQUES; GENOMICS; INFLAMMATION; INSULIN; MICE; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTORS; TRANS-ACTIVATORS;

EID: 84890387700     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491936     Document Type: Article

References (47)

1. Skurk, T., Mack, I., Kempf, K., Kolb, H., Hauner, H., and Herder, C. (2009) Expression and secretion of RANTES (CCL5) in human adipocytes in response to immunological stimuli and hypoxia. Horm. Metab. Res. 41, 183-189
2. Lee, H. S., Park, J. H., Kang, J. H., Kawada, T., Yu, R., and Han, I. S. (2009) Chemokine and chemokine receptor gene expression in the mesenteric adipose tissue of KKAy mice. Cytokine 46, 160-165
3. Gregor, M. F., and Hotamisligil, G. S. (2011) Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 29, 415-445
4. Gisler, R., Jacobsen, S. E., and Sigvardsson, M. (2000) Cloning of human early B-cell factor and identification of target genes suggest a conserved role in B-cell development in man and mouse. Blood 96, 1457-1464
5. Hagman, J., Belanger, C., Travis, A., Turck, C. W., and Grosschedl, R. (1993) Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev. 7, 760-773
6. Lin, H., and Grosschedl, R. (1995) Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263-267
7. Lukin, K., Fields, S., Hartley, J., and Hagman, J. (2008) Early B cell factor. Regulator of B lineage specification and commitment. Semin. Immunol. 20, 221-227
8. Milatovich, A., Qiu, R. G., Grosschedl, R., and Francke, U. (1994) Gene for a tissue-specific transcriptional activator (EBF or Olf-1), expressed in early B lymphocytes, adipocytes, and olfactory neurons, is located on human chromosome 5, band q34, and proximal mouse chromosome 11. Mamm. Genome 5, 211-215
9. Wang, M. M., and Reed, R. R. (1993) Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 364, 121-126
10. Jimenez, M. A., Akerblad, P., Sigvardsson, M., and Rosen, E. D. (2007) Critical role for Ebf1 and Ebf2 in the adipogenic transcriptional cascade. Mol. Cell. Biol. 27, 743-757
11. Fretz, J. A., Nelson, T., Xi, Y., Adams, D. J., Rosen, C. J., and Horowitz, M. C. (2010) Altered metabolism and lipodystrophy in the early B-cell factor 1-deficient mouse. Endocrinology 151, 1611-1621
12. Hesslein, D. G., Fretz, J. A., Xi, Y., Nelson, T., Zhou, S., Lorenzo, J. A., Schatz, D. G., and Horowitz, M. C. (2009) Ebf1-dependent control of the osteoblast and adipocyte lineages. Bone 44, 537-546
13. Festa, E., Fretz, J., Berry, R., Schmidt, B., Rodeheffer, M., Horowitz, M., and Horsley, V. (2011) Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771
14. 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
15. Nutt, S. L., and Kee, B. L. (2007) The transcriptional regulation of B cell lineage commitment. Immunity 26, 715-725
16. Mandel, E. M., and Grosschedl, R. (2010) Transcription control of early B cell differentiation. Curr. Opin. Immunol. 22, 161-167
17. Pongubala, J. M., Northrup, D. L., Lancki, D. W., Medina, K. L., Treiber, T., Bertolino, E., Thomas, M., Grosschedl, R., Allman, D., and Singh, H. (2008) Transcription factor EBF restricts alternative lineage options and promotes B cell fate commitment independently of Pax5. Nat. Immunol. 9, 203-215
18. Lukin, K., Fields, S., Guerrettaz, L., Straign, D., Rodriguez, V., Zandi, S., Månsson, R., Cambier, J. C., Sigvardsson, M., and Hagman, J. (2011) A dose-dependent role for EBF1 in repressing non-B-cell-specific genes. Eur. J. Immunol. 41, 1787-1793
19. Zandi, S., Mansson, R., Tsapogas, P., Zetterblad, J., Bryder, D., and Sigvardsson, M. (2008) EBF1 is essential for B-lineage priming and establishment of a transcription factor network in common lymphoid progenitors. J. Immunol. 181, 3364-3372
20. Sigvardsson, M., Clark, D. R., Fitzsimmons, D., Doyle, M., Akerblad, P., Breslin, T., Bilke, S., Li, R., Yeamans, C., Zhang, G., and Hagman, J. (2002) Early B-cell factor, E2A, and Pax-5 cooperate to activate the early B cells-pecific mb-1 promoter. Mol. Cell. Biol. 22, 8539-8551
21. O'Riordan, M., and Grosschedl, R. (1999) Coordinate regulation of B cell differentiation by the transcription factors EBF and E2A. Immunity 11, 21-31
22. Treiber, T., Mandel, E. M., Pott, S., Györy, I., Firner, S., Liu, E. T., and Grosschedl, R. (2010) Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription-independent poising of chromatin. Immunity 32, 714-725
23. Lin, Y. C., Jhunjhunwala, S., Benner, C., Heinz, S., Welinder, E., Mansson, R., Sigvardsson, M., Hagman, J., Espinoza, C. A., Dutkowski, J., Ideker, T., Glass, C. K., and Murre, C. (2010) A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 11, 635-643
24. Györy, I., Boller, S., Nechanitzky, R., Mandel, E., Pott, S., Liu, E., and Grosschedl, R. (2012) Transcription factor Ebf1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev. 26, 668-682
25. Maier, H., Ostraat, R., Gao, H., Fields, S., Shinton, S. A., Medina, K. L., Ikawa, T., Murre, C., Singh, H., Hardy, R. R., and Hagman, J. (2004) Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat. Immunol. 5, 1069-1077
26. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
27. Tusher, V. G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98, 5116-5121
28. MAQC Consortium, Shi, L., Reid, L. H., Jones, W. D., Shippy, R., Warrington, J. A., Baker, S. C., Collins, P. J., de Longueville, F., Kawasaki, E. S., Lee, K. Y., Luo, Y., Sun, Y. A., Willey, J. C., Setterquist, R. A., Fischer, G. M., Tong, W., Dragan, Y. P., Dix, D. J., Frueh, F. W., Goodsaid, F. M., Herman, D., Jensen, R. V., Johnson, C. D., Lobenhofer, E. K., Puri, R. K., Schrf, U., Thierry-Mieg, J., Wang, C., Wilson, M., Wolber, P. K., Zhang, L., Amur, S., Bao, W., Barbacioru, C. C., Lucas, A. B., Bertholet, V., Boysen, C., Bromley, B., Brown, D., Brunner, A., Canales, R., Cao, X. M., Cebula, T. A., Chen, J. J., Cheng, J., Chu, T. M., Chudin, E., Corson, J., Corton, J. C., Croner, L. J., Davies, C., Davison, T. S., Delenstarr, G., Deng, X., Dorris, D., Eklund, A. C., Fan, X. H., Fang, H., Fulmer-Smentek, S., Fuscoe, J. C., Gallagher, K., Ge, W., Guo, L., Guo, X., Hager, J., Haje, P. K., Han, J., Han, T., Harbottle, H. C., Harris, S. C., Hatchwell, E., Hauser, C. A., Hester, S., Hong, H., Hurban, P., Jackson, S. A., Ji, H., Knight, C. R., Kuo, W. P., LeClerc, J. E., Levy, S., Li, Q. Z., Liu, C., Liu, Y., Lombardi, M. J., Ma, Y., Magnuson, S. R., Maqsodi, B., McDaniel, T., Mei, N., Myklebost, O., Ning, B., Novoradovskaya, N., Orr, M. S., Osborn, T. W., Papallo, A., Patterson, T. A., Perkins, R. G., Peters, E. H., Peterson, R., Philips, K. L., Pine, P. S., Pusztai, L., Qian, F., Ren, H., Rosen, M., Rosenzweig, B. A., Samaha, R. R., Schena, M., Schroth, G. P., Shchegrova, S., Smith, D. D., Staedtler, F., Su, Z., Sun, H., Szallasi, Z., Tezak, Z., Thierry-Mieg, D., Thompson, K. L., Tikhonova, I., Turpaz, Y., Vallanat, B., Van, C., Walker, S. J., Wang, S. J., Wang, Y., Wolfinger, R., Wong, A., Wu, J., Xiao, C., Xie, Q., Xu, J., Yang, W., Zhang, L., Zhong, S., Zong, Y., and Slikker, W., Jr. (2006) The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat. Biotechnol. 24, 1151-1161
29. Hartigan, J. A., and Wong, M. A. (1979) A K-means clustering algorithm. J. R. Stat. Soc. Ser. C 28, 100-108
30. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis. A knowledgebased approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550
31. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P., Lee, W., Mendenhall, E., O'Donovan, A., Presser, A., Russ, C., Xie, X., Meissner, A., Wernig, M., Jaenisch, R., Nusbaum, C., Lander, E. S., and Bernstein, B. E. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560
32. Li, H., Ruan, J., and Durbin, R. (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18, 1851-1858
33. Mikkelsen, T. S., Xu, Z., Zhang, X., Wang, L., Gimble, J. M., Lander, E. S., and Rosen, E. D. (2010) Comparative epigenomic analysis of murine and human adipogenesis. Cell 143, 156-169
34. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate. A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300
35. Quinlan, A. R., and Hall, I. M. (2010) BEDTools. A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842
36. Grant, C. E., Bailey, T. L., and Noble, W. S. (2011) FIMO. Scanning for occurrences of a given motif. Bioinformatics 27, 1017-1018
37. Siersbæk, R., Nielsen, R., John, S., Sung, M. H., Baek, S., Loft, A., Hager, G. L., and Mandrup, S. (2011) Extensive chromatin remodelling and establishment of transcription factor "hotspots" during early adipogenesis. EMBO J. 30, 1459-1472
38. Tsai, R. Y., and Reed, R. R. (1998) Identification of DNA recognition sequences and protein interaction domains of the multiple-Zn-finger protein Roaz. Mol. Cell. Biol. 18, 6447-6456
39. Tsai, R. Y., and Reed, R. R. (1997) Cloning and functional characterization of Roaz, a zinc finger protein that interacts with O/E-1 to regulate gene expression. Implications for olfactory neuronal development. J. Neurosci. 17, 4159-4169
40. Kang, S., Akerblad, P., Kiviranta, R., Gupta, R. K., Kajimura, S., Griffin, M. J., Min, J., Baron, R., and Rosen, E. D. (2012) Regulation of early adipose commitment by Zfp521. PLoS Biol. 10, e1001433
41. Gupta, R. K., Arany, Z., Seale, P., Mepani, R. J., Ye, L., Conroe, H. M., Roby, Y. A., Kulaga, H., Reed, R. R., and Spiegelman, B. M. (2010) Transcriptional control of preadipocyte determination by Zfp423. Nature 464, 619-623
42. Smith, E. M., Gisler, R., and Sigvardsson, M. (2002) Cloning and characterization of a promoter flanking the early B cell factor (EBF) gene indicates roles for E-proteins and autoregulation in the control of EBF expression. J. Immunol. 169, 261-270
43. Loots, G. G., and Ovcharenko, I. (2007) Mulan. Multiple-sequence alignment to predict functional elements in genomic sequences. Methods Mol. Biol. 395, 237-254
44. Balhoff, J. P., and Stephens, J. M. (1998) Highly specific and quantitative activation of STATs in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 247, 894-900
45. Dowell, P., and Cooke, D. W. (2002) Olf-1/early B cell factor is a regulator of glut4 gene expression in 3T3-L1 adipocytes. J. Biol. Chem. 277, 1712-1718
46. Travis, A., Hagman, J., Hwang, L., and Grosschedl, R. (1993) Purification of early-B-cell factor and characterization of its DNA-binding specificity. Mol. Cell. Biol. 13, 3392-3400
47. Karczewski, K. J., Tatonetti, N. P., Landt, S. G., Yang, X., Slifer, T., Altman, R. B., and Snyder, M. (2011) Cooperative transcription factor associations discovered using regulatory variation. Proc. Natl. Acad. Sci. U.S.A. 108, 13353-13358