Pref-1 in brown adipose tissue: Specific involvement in brown adipocyte differentiation and regulatory role of C/EBPδ

Biochemical Journal

Volumn 443, Issue 3, 2012, Pages 799-810

  Armengol, Jordi ^a   Villena, Josep A ^b   Hondares, Elayne ^a   Carmona, María C ^a   Sul, Hei Sook ^c   Iglesias, Roser ^a   Giralt, Marta ^a   Villarroya, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brown adipose tissue; CCAAT enhancer binding protein (C EBP ); Glucocorticoid; Pref 1; Thermogenesis

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN DELTA; DEXAMETHASONE; MEMBRANE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PRE ADIPOCYTE FACTOR 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL CULTURE; CELL DIFFERENTIATION; FEMALE; FETUS; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; RODENT; THERMOGENESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ADIPOSE TISSUE, BROWN; ANIMALS; BASE SEQUENCE; BLOTTING, NORTHERN; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; GENE EXPRESSION REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84860158411     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111714     Document Type: Article

References (33)

1. Cannon, B. and Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (Pubitemid 38054374)
2. 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, 111-112
3. 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
4. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H. et al. (2008) PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967
5. Kajimura, S., Seale, P. and Spiegelman, B. M. (2010) Transcriptional control of brown fat development. Cell Metab. 11, 257-262
6. Kajimura, S., Seale, P., Kubota, K., Lunsford, E., Frangioni, J. V., Gygi, S. P. and Spiegelman, B. M. (2009) Initiation of myoblast to brown fat switch by a PRDM16- C/EBP-β transcriptional complex. Nature 460, 1154-1158
7. Wang, Y. and Sul, H. S. (2006) Ectodomain shedding of preadipocyte factor 1 (Pref-1) by tumor necrosis factor α converting enzyme (TACE) and inhibition of adipocyte differentiation. Mol. Cell. Biol. 26, 5421-5435 (Pubitemid 44036210)
8. Smas, C. M. and Sul, H. S. (1993) Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 73, 725-734 (Pubitemid 23159011)
9. Moon, Y. S., Smas, C. M., Lee, K., Villena, J. A., Kim, K. H., Yun, E. J. and Sul, H. S. (2002) Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22, 5585-5592 (Pubitemid 34755767)
10. Lee, K., Villena, J. A., Moon, Y. S., Kim, K. H., Lee, S., Kang, C. and Sul, H. S. (2003) Inhibition of adipogenesis and development of glucose intolerance by soluble preadipocyte factor-1 (Pref-1). J. Clin. Invest. 111, 453-461 (Pubitemid 36228002)
11. Sul, H. S. (2009) Minireview: Pref-1: role in adipogenesis and mesenchymal cell fate. Mol. Endocrinol. 23, 1717-1725
12. Wang, Y. and Sul, H. S. (2009) Pref-1 regulates mesenchymal cell commitment and differentiation through Sox9. Cell Metab. 9, 287-302
13. Baladrón, V., Ruiz-Hidalgo, M. J., Nueda, M. L., Díaz-Guerra, M. J., García-Ramírez, J. J., Bonvini, E., Gubina, E. and Laborda, J. (2005) dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp. Cell. Res. 303, 343-359 (Pubitemid 40126268)
14. Nueda, M. L., Baladron, V., Sanchez-Solana, B., Ballesteros, M. A. and Laborda, J. (2007) The EGF-like protein dlk1 inhibits notch signaling and potentiates adipogenesis of mesenchymal cells. J. Mol. Biol. 367, 1281-1293 (Pubitemid 46413261)
15. Wang, N. D., Finegold, M. J., Bradley, A., Ou, C. N., Abdelsayed, S. V., Wilde, M. D., Taylor, L. R., Wilson, D. R. and Darlington, G. J. (1995) Impaired energy homeostasis in C/EBPα knockout mice. Science 269, 1108-1112
16. Linhart, H. G., Ishimura-Oka, K., De Mayo, F., Kibe, T., Repka, D., Poindexter, B., Bick, R. J. and Darlington, G. J. (2001) C/EBPα is required for differentiation of white, but not brown, adipose tissue. Proc. Natl. Acad. Sci. U.S.A. 98, 12532-12537 (Pubitemid 33019980)
17. Weibel, E. R. (1979) In Stereological Methods, Academic Press, New York
18. Baddeley, A. J., Gundersen, H. J. and Cruz-Orive, L. M. (1986) Estimation of surface area from vertical sections. J. Microsc. 142, 259-276
19. Villarroya, J., Dorado, B., Vilà, M. R., Garcia-Arumí, E., Domingo, P., Giralt, M., Hirano, M. and Villarroya, F. (2011) Thymidine kinase 2 deficiency-induced mitochondrial DNA depletion causes abnormal development of adipose tissues and adipokine levels in mice. PLoS ONE 6, e29691
20. Alvarez, R., de Andrés, J., Yubero, P., Viñas, O., Mampel, T., Iglesias, R., Giralt, M. and Villarroya, F. (1995) A novel regulatory pathway of brown fat thermogenesis. Retinoic acid is a transcriptional activator of the mitochondrial uncoupling protein gene. J. Biol. Chem. 270, 5666-5673
21. Klaus, S., Choy, L., Champigny, O., Cassard-Doulcier, A. M., Ross, S., Spiegelman, B. and Ricquier, D. J. (1994) Characterization of the novel brown adipocyte cell line HIB 1B. Adrenergic pathways involved in regulation of uncoupling protein gene expression. J. Cell. Sci. 107, 313-319
22. Valmaseda, A., Carmona, M. C., Barbera, M. J., Vinas, O., Mampel, T., Iglesias, R., Villarroya, F. and Giralt, M. (1999) Opposite regulation of PPAR-α and -γ gene expression by both their ligands and retinoic acid in brown adipocytes. Mol. Cell. Endocrinol. 154, 101-109 (Pubitemid 29387335)
23. Takemori, H., Doi, J., Katoh, Y., Halder, S. K., Lin, X. Z., Horike, N., Hatano, O. and Okamoto, M. (2001) Characterization of a proximal element in the rat preadipocyte factor-1 (Pref-1) gene promoter. Eur. J. Biochem. 268, 205-217 (Pubitemid 32862650)
24. Párrizas, M., Boj, S. F., Luco, R. F., Maestro, M. A. and Ferrer, J. (2003) Chromatin immunoprecipitation using isolated islets of Langerhans. Methods Mol. Med. 83, 61-71
25. Giralt, M., Martin, I., Iglesias, R., Viñas, O., Villarroya, F. and Mampel, T. (1990) Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5′-deiodinase activity is necessary for the response to environmental temperature at birth. Eur. J. Biochem. 193, 297-302 (Pubitemid 20331642)
26. Houstek, J., Kopecky, J., Rychter, Z. and Soukup, T. (1988) Uncoupling protein in embryonic brown adipose tissue: existence of nonthermogenic and thermogenic mitochondria. Biochim. Biophys. Acta 935, 19-25
27. Carmona, M. C., Iglesias, R., Obregón, M. J., Darlington, G. J., Villarroya, F. and Giralt, M. (2002) Mitochondrial biogenesis and thyroid status maturation in brown fat require CCAAT/enhancer-binding protein α. J. Biol. Chem. 277, 21489-21498 (Pubitemid 34952292)
28. Cao, Z., Umek, R. M. and Mcknight, S. L. (1991) Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 5, 1538-1552 (Pubitemid 21906060)
29. Shimomura, I., Hammer, R. E., Richardson, J. A., Ikemoto, S., Bashmakov, Y., Goldstein, J. L. and Brown, M. S. (1998) Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes Dev. 12, 3182-3194 (Pubitemid 28496263)
30. Smas, C. M., Kachinskas, D., Liu, C. M., Xie, X., Dircks, L. K. and Sul, H. S. (1998) Transcriptional control of the pref-1 gene in 3T3-L1 adipocyte differentiation. Sequence requirement for differentiation-dependent suppression. J. Biol. Chem. 273, 31751-31758 (Pubitemid 29177106)
31. Smas, C. M., Chen, L., Zhao, L., Latasa, M. J. and Sul, H. S. (1999) Transcriptional repression of pref-1 by glucocorticoids promotes 3T3-L1 adipocyte differentiation. J. Biol. Chem. 274, 12632-12641
32. Soumano, K., Desbiens, S., Rabelo, R., Bakopanos, E., Camirand, A. and Silva, J. E. (2000) Glucocorticoids inhibit the transcriptional response of the uncoupling protein-1 gene to adrenergic stimulation in a brown adipose cell line. Mol. Cell. Endocrinol. 165, 7-15 (Pubitemid 30625178)
33. Casteilla, L., Nouguès, J., Reyne, Y. and Ricquier, D. (1991) Differentiation of ovine brown adipocyte precursor cells in a chemically defined serum-free medium. Importance of glucocorticoids and age of animals. Eur. J. Biochem. 198, 195-199