Transcriptional regulation of adipocyte differentiation: A central role for CCAAT/ enhancer-binding protein (C/EBP) β

Journal of Biological Chemistry

Volumn 290, Issue 2, 2015, Pages 755-761

  Guo, Liang ^a   Li, Xi ^a   Tang, Qi Qun ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DISEASE CONTROL; MOLECULAR WEIGHT; PROCESS CONTROL; PROTEINS; TRANSCRIPTION;

ADIPOCYTE DIFFERENTIATION; CCAAT/ENHANCER-BINDING PROTEINS; ENHANCER BINDING PROTEINS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; POST-TRANSLATIONAL MODIFICATIONS; TRANSCRIPTIONAL FACTORS; TRANSCRIPTIONAL REGULATION; UNFOLDED PROTEIN RESPONSE;

C (PROGRAMMING LANGUAGE);

CCAAT ENHANCER BINDING PROTEIN BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SUMO PROTEIN; X BOX BINDING PROTEIN 1;

ADIPOCYTE; ADIPOGENESIS; BINDING AFFINITY; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; DIMERIZATION; ENDOPLASMIC RETICULUM; EPIGENETICS; GLYCOSYLATION; IMMUNE RESPONSE; MOLECULAR DYNAMICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; AUTOPHAGY; GENETICS; HUMAN; METABOLISM;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; AUTOPHAGY; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CELL PROLIFERATION; EPIGENOMICS; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; UNFOLDED PROTEIN RESPONSE;

EID: 84920887709     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R114.619957     Document Type: Review

References (70)

1. Rosen, E. D., and Spiegelman, B. M. (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847-853
2. Haslam, D. W., and James, W. P. (2005) Obesity. Lancet 366, 1197-1209
3. Shepherd, P. R., Gnudi, L., Tozzo, E., Yang, H., Leach, F., and Kahn, B. B. (1993) Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J. Biol. Chem. 268, 22243-22246
4. Green, H., and Kehinde, O. (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5, 19-27
5. Tang, Q. Q., Otto, T. C., and Lane, M. D. (2003) Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 44-49
6. Farmer, S. R. (2006) Transcriptional control of adipocyte formation. Cell Metab. 4, 263-273
7. Zhang, Y. Y., Li, X., Qian, S. W., Guo, L., Huang, H. Y., He, Q., Liu, Y., Ma, C. G., and Tang, Q. Q. (2011) Transcriptional activation of histone H4 by C/EBPβ during the mitotic clonal expansion of 3T3-L1 adipocyte differentiation. Mol. Biol. Cell 22, 2165-2174
8. Guo, L., Li, X., Huang, J. X., Huang, H. Y., Zhang, Y. Y., Qian, S. W., Zhu, H., Zhang, Y. D., Liu, Y., Liu, Y., Wang, K. K., and Tang, Q. Q. (2012) Histone demethylase Kdm4b functions as a co-factor of C/EBPβ to promote mitotic clonal expansion during differentiation of 3T3-L1 preadipocytes. Cell Death Differ. 19, 1917-1927
9. Yeh, W. C., Cao, Z., Classon, M., and McKnight, S. L. (1995) Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev. 9, 168-181
10. Tanaka, T., Yoshida, N., Kishimoto, T., and Akira, S. (1997) Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBP∂ gene. EMBO J. 16, 7432-7443
11. Tang, Q. Q., and Lane, M. D. (1999) Activation and centromeric localization of CCAAT/enhancer-binding proteins during the mitotic clonal expansion of adipocyte differentiation. Genes Dev. 13, 2231-2241
12. Qiu, Z., Wei, Y., Chen, N., Jiang, M.,Wu,J., and Liao, K. (2001)DNAsynthesis and mitotic clonal expansion is not a required step for 3T3-L1 preadipocyte differentiation into adipocytes. J. Biol. Chem. 276, 11988-11995
13. Li, X., Kim, J. W., Grønborg, M., Urlaub, H., Lane, M. D., and Tang, Q. Q. (2007) Role of cdk2 in the sequential phosphorylation/activation of C/EBPβ during adipocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 104, 11597-11602
14. Reichert, M., and Eick, D. (1999) Analysis of cell cycle arrest in adipocyte differentiation. Oncogene 18, 459-466
15. Yeh, W. C., Bierer, B. E., and McKnight, S. L. (1995) Rapamycin inhibits clonal expansion and adipogenic differentiation of 3T3-L1 cells. Proc. Natl. Acad. Sci. U.S.A. 92, 11086-11090
16. Johmura, Y., Osada, S., Nishizuka, M., and Imagawa, M. (2008) FAD24 acts in concert with histone acetyltransferase HBO1 to promote adipogenesis by controlling DNA replication. J. Biol. Chem. 283, 2265-2274
17. Cornelius, P., MacDougald, O. A., and Lane, M. D. (1994) Regulation of adipocyte development. Annu. Rev. Nutr. 14, 99-129
18. Greenwel, P., Tanaka, S., Penkov, D., Zhang, W., Olive, M., Moll, J., Vinson, C., Di Liberto, M., and Ramirez, F. (2000) Tumor necrosis factor αinhibits type I collagen synthesis through repressive CCAAT/enhancerbinding proteins. Mol. Cell Biol. 20, 912-918
19. Zhang, J. W., Tang, Q. Q., Vinson, C., and Lane, M. D. (2004) Dominantnegative C/EBP disrupts mitotic clonal expansion and differentiation of 3T3-L1 preadipocytes. Proc. Natl. Acad. Sci. U.S.A. 101, 43-47
20. Seagroves, T. N., Krnacik, S., Raught, B., Gay, J., Burgess-Beusse, B., Darlington, G. J., and Rosen, J. M. (1998) C/EBPβ, but not C/EBPα, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev. 12, 1917-1928
21. Iyer, V. V., Kadakia, T. B., McCabe, L. R., and Schwartz, R. C. (2004) CCAAT/enhancer-binding protein-β has a role in osteoblast proliferation and differentiation. Exp. Cell Res. 295, 128-137
22. Zhu, S., Yoon, K., Sterneck, E., Johnson, P. F., and Smart, R. C. (2002) CCAAT/enhancer binding protein-β is a mediator of keratinocyte survival and skin tumorigenesis involving oncogenic Ras signaling. Proc. Natl. Acad. Sci. U.S.A. 99, 207-212
23. Aparicio, T., Ibarra, A., and Méndez, J. (2006) Cdc45-MCM-GINS, a new power player for DNA replication. Cell Div. 1, 18
24. Turowski, P., Franckhauser, C., Morris, M. C., Vaglio, P., Fernandez, A., and Lamb, N. J. (2003) Functional cdc25C dual-specificity phosphatase is required for S-phase entry in human cells. Mol. Biol. Cell 14, 2984-2998
25. Wakabayashi, K., Okamura, M., Tsutsumi, S., Nishikawa, N. S., Tanaka, T., Sakakibara, I., Kitakami, J., Ihara, S., Hashimoto, Y., Hamakubo, T., Kodama, T., Aburatani, H., and Sakai, J. (2009) The peroxisome prolifera-tor-activated receptor γ/retinoid X receptor αheterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop. Mol. Cell Biol. 29, 3544-3555
26. 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
27. Wang, L., Xu, S., Lee, J. E., Baldridge, A., Grullon, S., Peng, W., and Ge, K. (2013) Histone H3K9 methyltransferase G9a represses PPARγ expression and adipogenesis. EMBO J. 32, 45-59
28. Fodor, B. D., Kubicek, S., Yonezawa, M., O'Sullivan, R. J., Sengupta, R., Perez-Burgos, L., Opravil, S., Mechtler, K., Schotta, G., and Jenuwein, T. (2006) Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 20, 1557-1562
29. Kawazu, M., Saso, K., Tong, K. I., McQuire, T., Goto, K., Son, D. O., Wakeham, A., Miyagishi, M., Mak, T. W., and Okada, H. (2011) Histone demethylase JMJD2B functions as a co-factor of estrogen receptor in breast cancer proliferation and mammary gland development. PLoS One 6, e17830
30. Tachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., Fukuda, M., Takeda, N., Niida, H., Kato, H., and Shinkai, Y. (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779-1791
31. Shinkai, Y., and Tachibana, M. (2011) H3K9 methyltransferase G9a and the related molecule GLP. Genes Dev. 25, 781-788
32. Li, S. F., Guo, L., Qian, S. W., Liu, Y., Zhang, Y. Y., Zhang, Z. C., Zhao, Y., Shou, J. Y., Tang, Q. Q., and Li, X. (2013) G9a is transactivated by C/EBPβ to facilitate mitotic clonal expansion during 3T3-L1 preadipocyte differentiation. Am. J. Physiol. Endocrinol. Metab. 304, E990-E998
33. Luo, W., and Semenza, G. L. (2012) Emerging roles of PKM2 in cell metabolism and cancer progression. Trends Endocrinol. Metab. 23, 560-566
34. Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., Fleming, M. D., Schreiber, S. L., and Cantley, L. C. (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233
35. Yang, W., Xia, Y., Ji, H., Zheng, Y., Liang, J., Huang, W., Gao, X., Aldape, K., and Lu, Z. (2011) Nuclear PKM2 regulates β-catenin transactivation upon EGFR activation. Nature 480, 118-122
36. Yang, W., Xia, Y., Hawke, D., Li, X., Liang, J., Xing, D., Aldape, K., Hunter, T., Alfred Yung, W. K., and Lu, Z. (2012) PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 150, 685-696
37. Jiang, Y., Guo, L., Xie, L. Q., Zhang, Y. Y., Liu, X. H., Zhang, Y., Zhu, H., Yang, P. Y., Lu, H. J., and Tang, Q. Q. (2014) Proteome profiling of mitotic clonal expansion during 3T3-L1 adipocyte differentiation using iTRAQ-2DLC-MS/MS. J. Proteome Res. 13, 1307-1314
38. Tang, Q. Q., and Lane, M. D. (2012) Adipogenesis: from stem cell to adipocyte. Annu. Rev. Biochem. 81, 715-736
39. Lee, J., and Ozcan, U. (2014) Unfolded protein response signaling and metabolic diseases. J. Biol. Chem. 289, 1203-1211
40. Park, S. W., and Ozcan, U. (2013) Potential for therapeutic manipulation of the UPR in disease. Semin. Immunopathol. 35, 351-373
41. Gregor, M. F., and Hotamisligil, G. S. (2007) Thematic review series: Adipocyte Biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J. Lipid Res. 48, 1905-1914
42. Sha, H., He, Y., Chen, H., Wang, C., Zenno, A., Shi, H., Yang, X., Zhang, X., and Qi, L. (2009) The IRE1α-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab. 9, 556-564
43. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873
44. Cecconi, F., and Levine, B. (2008) The role of autophagy in mammalian development: cell makeover rather than cell death. Dev. Cell 15, 344-357
45. Singh, R., Xiang, Y., Wang, Y., Baikati, K., Cuervo, A. M., Luu, Y. K., Tang, Y., Pessin, J. E., Schwartz, G. J., and Czaja, M. J. (2009) Autophagy regulates adipose mass and differentiation in mice. J. Clin. Invest. 119, 3329-3339
46. Baerga, R., Zhang, Y., Chen, P. H., Goldman, S., and Jin, S. (2009) Targeted deletion of autophagy-related 5 (atg5) impairs adipogenesis in a cellular model and in mice. Autophagy 5, 1118-1130
47. Guo, L., Huang, J. X., Liu, Y., Li, X., Zhou, S. R., Qian, S. W., Liu, Y., Zhu, H., Huang, H. Y., Dang, Y. J., and Tang, Q. Q. (2013) Transactivation of Atg4b by C/EBPβ promotes autophagy to facilitate adipogenesis. Mol. Cell Biol. 33, 3180-3190
48. Ma, D., Panda, S., and Lin, J. D. (2011) Temporal orchestration of circadian autophagy rhythm by C/EBPβ. EMBO J. 30, 4642-4651
49. Oishi, Y., Manabe, I., Tobe, K., Tsushima, K., Shindo, T., Fujiu, K., Nishimura, G., Maemura, K., Yamauchi, T., Kubota, N., Suzuki, R., Kitamura, T., Akira, S., Kadowaki, T., and Nagai, R. (2005) Kruppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab. 1, 27-39
50. Payne, V. A., Au, W. S., Lowe, C. E., Rahman, S. M., Friedman, J. E., O'Rahilly, S., and Rochford, J. J. (2010) C/EBP transcription factors regulate SREBP1c gene expression during adipogenesis. Biochem. J. 425, 215-223
51. 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
52. Chung, S. S., Lee, J. S., Kim, M., Ahn, B. Y., Jung, H. S., Lee, H. M., Kim, J. W., and Park, K. S. (2012) Regulation of Wnt/β-catenin signaling by CCAAT/enhancer binding protein β during adipogenesis. Obesity (Silver Spring) 20, 482-487
53. Tang, Q. Q., Grønborg, M., Huang, H., Kim, J. W., Otto, T. C., Pandey, A., and Lane, M. D. (2005) Sequential phosphorylation of CCAAT enhancerbinding protein β by MAPK and glycogen synthase kinase 3β is required for adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 9766-9771
54. Kim, J. W., Tang, Q. Q., Li, X., and Lane, M. D. (2007) Effect of phosphorylation and S-S bond-induced dimerization on DNA binding and transcriptional activation by C/EBPβ. Proc. Natl. Acad. Sci. U.S.A. 104, 1800-1804
55. Zhang, Y. Y., Li, S. F., Qian, S. W., Zhang, Y. Y., Liu, Y., Tang, Q. Q., and Li, X. (2012) Phosphorylation prevents C/EBPβ from the calpain-dependent degradation. Biochem. Biophys. Res. Commun. 419, 550-555
56. Li, X., Molina, H., Huang, H., Zhang, Y. Y., Liu, M., Qian, S. W., Slawson, C., Dias, W. B., Pandey, A., Hart, G. W., Lane, M. D., and Tang, Q. Q. (2009) O-Linked N-acetylglucosamine modification on CCAAT enhanc-er-binding protein β: role during adipocyte differentiation. J. Biol. Chem. 284, 19248-19254
57. Ceseña, T. I., Cardinaux, J. R., Kwok, R., and Schwartz, J. (2007) CCAAT/ enhancer-binding protein (C/EBP) β is acetylated at multiple lysines: acetylation of C/EBPβ at lysine 39 modulates its ability to activate transcription. J. Biol. Chem. 282, 956-967
58. Ceseña, T. I., Cui, T. X., Subramanian, L., Fulton, C. T., Iñiguez-Lluhí, J. A., Kwok, R. P., and Schwartz, J. (2008) Acetylation and deacetylation regulate CCAAT/enhancer binding protein β at K39 in mediating gene transcription. Mol. Cell Endocrinol. 289, 94-101
59. Wiper-Bergeron, N., Salem, H. A., Tomlinson, J. J., Wu, D., and Haché, R. J. (2007) Glucocorticoid-stimulated preadipocyte differentiation is mediated through acetylation of C/EBPβ by GCN5. Proc. Natl. Acad. Sci. U.S.A. 104, 2703-2708
60. Xu, M., Nie, L., Kim, S. H., and Sun, X. H. (2003) STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPβ. EMBO J. 22, 893-904
61. Pless, O., Kowenz-Leutz, E., Knoblich, M., Lausen, J., Beyermann, M., Walsh, M. J., and Leutz, A. (2008) G9a-mediated lysine methylation alters the function of CCAAT/enhancer-binding protein-β. J. Biol. Chem. 283, 26357-26363
62. Kowenz-Leutz, E., Pless, O., Dittmar, G., Knoblich, M., and Leutz, A. (2010) Crosstalk between C/EBPβ phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. EMBO J. 29, 1105-1115
63. Hattori, T., Ohoka, N., Inoue, Y., Hayashi, H., and Onozaki, K. (2003) C/EBP family transcription factors are degraded by the proteasome but stabilized by forming dimer. Oncogene 22, 1273-1280
64. Yeh, E. T. (2009) SUMOylation and De-SUMOylation: wrestling with life's processes. J. Biol. Chem. 284, 8223-8227
65. Kim, J., Cantwell, C. A., Johnson, P. F., Pfarr, C. M., and Williams, S. C. (2002) Transcriptional activity of CCAAT/enhancer-binding proteins is controlled by a conserved inhibitory domain that is a target for sumoylation. J. Biol. Chem. 277, 38037-38044
66. Eaton, E. M., and Sealy, L. (2003) Modification of CCAAT/enhancerbinding protein-β by the small ubiquitin-like modifier (SUMO) family members, SUMO-2 and SUMO-3. J. Biol. Chem. 278, 33416-33421
67. Subramanian, L., Benson, M. D., and Iñiguez-Lluhí, J. A. (2003) A synergy control motif within the attenuator domain of CCAAT/enhancer-binding protein βinhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J. Biol. Chem. 278, 9134-9141
68. Berberich-Siebelt, F., Berberich, I., Andrulis, M., Santner-Nanan, B., Jha, M. K., Klein-Hessling, S., Schimpl, A., and Serfling, E. (2006) SUMOylation interferes with CCAAT/enhancer-binding protein β-mediated c-myc repression, but not IL-4 activation in T cells. J. Immunol. 176, 4843-4851
69. Liu, Y., Zhang, Y. D., Guo, L., Huang, H. Y., Zhu, H., Huang, J. X., Liu, Y., Zhou, S. R., Dang, Y. J., Li, X., and Tang, Q. Q. (2013) Protein inhibitor of activated STAT 1 (PIAS1) is identified as the SUMO E3 ligase of CCAAT/ enhancer-binding protein β (C/EBPβ) during adipogenesis. Mol. Cell Biol. 33, 4606-4617
70. Chung, S. S., Ahn, B. Y., Kim, M., Choi, H. H., Park, H. S., Kang, S., Park, S. G., Kim, Y. B., Cho, Y. M., Lee, H. K., Chung, C. H., and Park, K. S. (2010) Control of adipogenesis by the SUMO-specific protease SENP2. Mol. Cell Biol. 30, 2135-2146