TGF-β/Smad3 signaling regulates brown adipocyte induction in white adipose tissue

Frontiers in Endocrinology

Volumn 3, Issue MAR, 2012, Pages

  Yadav, Hariom ^a   Rane, Sushil G ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Brown fat; Obesity; Smad3; TGF beta; White fat

Indexed keywords

EID: 84873501756     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2012.00035     Document Type: Article

References (63)

1. Ahmadian, M., Abbott, M. J., Tang, T., Hudak, C. S., Kim, Y., Bruss, M., Hellerstein, M. K., Lee, H. Y., Samuel, V. T., Shulman, G. I., Wang, Y., Duncan, R. E., Kang, C., and Sul, H. S. (2011). Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 13, 739-748.
2. Atit, R., Sgaier, S. K., Mohamed, O. A., Taketo, M. M., Dufort, D., Joyner, A. L., Niswander, L., and Conlon, R. A. (2006). Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev. Biol. 296,164-176.
3. Barbatelli, G., Murano, I., Madsen, L., Hao, Q., Jimenez, M., Kristiansen, K., Giacobino, J. P., de Matteis, R., and Cinti, S. (2010). The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am. J. Physiol. Endocrinol. Metab. 298, E1244-E1253.
4. Bloom, J. D., Dutia, M. D., Johnson, B. D., Wissner, A., Burns, M. G., Largis, E. E., Dolan, J. A., and Claus, T. H. (1992). Disodium (R,R)-5-[2-[[2-(3-chlorophenyl)-2-hydroxyethyl]-amino] propyl]-1,3-benzodioxole-2,2-dicarboxylate (CL 316,243). A potent beta-adrenergic agonist virtually specific for beta 3 receptors. A promising antidiabetic and antiobesity agent.J. Med. Chem. 35,3081-3084.
5. Bostrom, P., Wu, J., Jedrychowski, M. P., Korde, A., Ye, L., Lo, J. C., Ras-bach, K. A., Bostrom, E. A., Choi, J. H., Long, J. Z., Kajimura, S., Zin-garetti, M. C., Vind, B. F., Tu, H., Cinti, S., Hojlund, K., Gygi, S. P., and Spiegelman, B. M. (2012). A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481,463-468.
6. Cao, L., Choi, E. Y., Liu, X., Martin, A., Wang, C., Xu, X., and During, M. J. (2011). White to brown fat phenotypic switch induced by genetic and environmental activation of a hypothalamic-adipocyte axis. Cell Metab. 14, 324-338.
7. Cederberg, A., Gronning, L. M., Ahren, B., Tasken, K., Carlsson, P., and Ener-back, S. (2001). FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance. Cell 106, 563-573.
8. Chao, P. T., Yang, L., Aja, S., Moran, T. H., and Bi, S. (2011). Knockdown of NPY expression in the promotes development of brown adipocytes and prevents diet-induced obesity. Cell Metab. 13,573-583.
9. Cinti, S. (2011). Between brown and white: novel aspects of adipocyte differentiation. Ann. Med. 43, 104-115.
10. Collins, S., Daniel, K. W., Petro, A. E., and Surwit, R. S. (1997). Strain-specific response to beta 3-adrenergic receptor agonist treatment of diet-induced obesity in mice. Endocrinology 138,405-413.
11. Cousin, B., Cinti, S., Morroni, M., Raimbault, S., Ricquier, D., Peni-caud, L., and Casteilla, L. (1992). Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J. Cell. Sci. 103(Pt 4), 931-942.
12. Crunkhorn, S. (2011). Metabolic disease: turning 'bad' fat into 'good.' Nat. Rev. Drug Discov. 10, 659.
13. Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, E 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.
14. Derynck, R., and Zhang, Y. E. (2003). Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577-584.
15. Enerback, S. (2010). Human brown adipose tissue. CellMetab. 11,248-252.
16. Frontini, A., and Cinti, S. (2010). Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 11,253-256.
17. Gesta, S., Tseng, Y. H., and Kahn, C. R. (2007). Developmental origin of fat: tracking obesity to its source. Cell 131,242-256.
18. Ghorbani, M., Claus, T. H., and Himms-Hagen, J. (1997). Hypertrophy of brown adipocytes in brown and white adipose tissues and reversal of diet-induced obesity in rats treated with a beta3-adrenoceptor agonist. Biochem. Pharmacol. 54,121-131.
19. Ghorbani, M., and Himms-Hagen, J. (1997). Appearance of brown adipocytes in white adipose tissue during CL 316,243-induced reversal of obesity and diabetes in Zucker fa/fa rats. Int. J. Obes. Relat. Metab. Disord. 21, 465-475.
20. Grujic, D., Susulic, V. S., Harper, M. E., Himms-Hagen, J., Cunningham, B. A., Corkey, B. E., and Lowell, B. B. (1997). Beta3-adrenergic receptors on white and brown adipocytes mediate beta3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake. A study using trans-genic and gene knockout mice. J. Biol. Chem. 272, 17686-17693.
21. 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.
22. 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). Tran-scriptional control of preadipocyte determination by Zfp423. Nature 464, 619-623.
23. Hansen, J. B., Jorgensen, C., Petersen, R. K., Hallenborg, P., de Matteis, R., Boye, H. A., Petrovic, N., Enerback, S., Nedergaard, J., Cinti, S., te Riele,H.,andKristiansen,K. (2004). Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 101,4112-4117.
24. Himms-Hagen, J., Cui, J., Danforth, E. Jr., Taatjes, D. J., Lang, S. S., Waters, B. L., and Claus, T. H. (1994). Effect of CL-316,243, a thermogenic beta 3-agonist, on energy balance and brown and white adipose tissues in rats. Am. J. Physiol. 266, R1371-R1382.
25. Himms-Hagen, J., Melnyk, A., Zin-garetti, M. C., Ceresi, E., Barbatelli, G., and Cinti, S. (2000). Multilocu-lar fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am. J. Physiol. Cell Physiol. 279, C670-C681.
26. Hondares, E., Rosell, M., Diaz-Delfin, J., Olmos, Y., Monsalve, M., Igle-sias, R., Villarroya, F., and Giralt, M. (2011). PPARalpha induces PGC-1alpha gene expression and contributes to the thermogenic activation of brown fat; involvement of PRDM16. J. Biol. Chem. 296, 43112-43122.
27. Jimenez, M., Barbatelli, G., Allevi, R., Cinti, S., Seydoux, J., Giacobino, J. P., Muzzin, P., and Preitner, E (2003). Beta 3-adrenoceptor knockout in C57BL/6J mice depresses the occurrence of brown adipocytes in white fat. Eur. J. Biochem. 270, 699-705.
28. Kang, S., Bajnok, L., Longo, K. A., Petersen, R. K., Hansen, J. B., Kristiansen, K., and Macdougald, O. A. (2005). Effects of Wnt signaling on brown adipocyte differentiation and metabolism mediated by PGC-1alpha. Mol. Cell. Biol. 25, 1272-1282.
29. Langin, D. (2009). 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.
30. Lefterova,M. I.,andLazar,M. A. (2009). New developments in adipogene-sis. Trends Endocrinol. Metab. 20, 107-114.
31. Ling, H., Li, X., Jha, S., Wang, W., Karetskaya, L., Pratt, B., and Ledbet-ter, S. (2003). Therapeutic role of TGF-beta-neutralizing antibody in mouse cyclosporine A nephropathy: morphologic improvement associated with functional preservation. J. Am. Soc. Nephrol. 14, 377-388.
32. Loncar, D. (1991). Convertible adipose tissue in mice. Cell Tissue Res. 266, 149-161.
33. Madsen, L., Pedersen, L. M., Lillefosse, H. H., Fjaere, E., Bronstad, I., Hao, Q., Petersen, R. K., Hallenborg, P., Ma, T., de Matteis, R., Araujo, P., Mercader, J., Bonet, M. L., Hansen, J. B., Cannon, B., Nedergaard, J., Wang, J., Cinti, S., Voshol, P., Doskeland, S. O., and Kristiansen, K. (2010). UCP1 induction during recruitment of brown adipocytes in white adipose tissue is dependent on cyclooxyge-nase activity. PLoS ONE 5, e11391. doi:10.1371/journal.pone.0011391
34. Massague, J. (2008). TGFbeta in cancer. Cell 134,215-230.
35. Massague, J., Blain, S. W., and Lo, R. S. (2000). TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309.
36. Mercader, J., Ribot, J., Murano, I., Felipe, E, Cinti, S., Bonet, M. L., and Palou, A. (2006). Remodeling of white adipose tissue after retinoic acid administration in mice. Endocrinology 147, 5325-5332.
37. Mullen, A. C., Orlando, D. A., Newman, J. J., Loven, J., Kumar, R. M., Bilodeau, S., Reddy, J., Guenther, M. G., Dekoter, R. P., and Young, R. A. (2011). Master transcription factors determine cell-type-specific responses to TGF-beta signaling. Cell 147, 565-576.
38. Nam, J. S., Terabe, M., Mamura, M., Kang, M. J., Chae, H., Stuelten, C., Kohn, E., Tang, B., Sabze-vari, H., Anver, M. R., Lawrence, S., Danielpour, D., Lonning, S., Berzofsky, J. A., and Wakefield, L. M. (2008). An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res. 68, 3835-3843.
39. Nedergaard, J., Bengtsson, T., and Cannon, B. (2007). Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452.
40. Nedergaard, J., and Cannon, B. (2010). The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab. 11, 268-272.
41. Park, K. W., Halperin, D. S., and Tontonoz, P. (2008). Before they were fat: adipocyte progenitors. Cell Metab. 8, 454-457.
42. Petrovic, N., Walden, T. B., Shabalina, I. G., Timmons, J. A., Cannon, B., and Nedergaard, J. (2010). Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP 1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem. 285,7153-7164.
43. Rane, S. G., Lee, J. H., and Lin, H. M. (2006). Transforming growth factor-beta pathway: role in pancreas development and pancreatic disease. Cytokine Growth Factor Rev. 17,107-119.
44. Roberts, A. B., and Sporn, M. B. (1985). Transforming growth factors. Cancer Surv. 4, 683-705.
45. Schulz, T. J., Huang, T. L., Tran, T. T., Zhang, H., Townsend, K. L., Shadrach, J. L., Cerletti, M., Mcdougall, L. E., Giorgadze, N., Tchkonia, T., Schrier, D., Falb, D., Kirkland, J. L., Wagers, A. J., and Tseng, Y.H. (2011). Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc. Natl. Acad. Sci. U.S.A. 108, 143-148.
46. Scime, A., Grenier, G., Huh, M. S., Gille-spie, M. A., Bevilacqua, L., Harper, M. E., and Rudnicki, M. A. (2005). Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. CellMetab. 2,283-295.
47. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scime, 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.
48. 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.
49. Soloveva, V., Graves, R. A., Rasenick, M. M., Spiegelman, B. M., and Ross, S. R. (1997). Transgenic mice overex-pressing the beta 1-adrenergic receptor in adipose tissue are resistant to obesity. Mol. Endocrinol. 11, 27-38.
50. Timmons, J. A., Wennmalm, K., Lars-son, O., Walden, T. B., Lassmann, T., Petrovic, N., Hamilton, D. L., Gimeno, R. E., Wahlestedt, C., Baar, K., Nedergaard, J., and Cannon, B. (2007). Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc. Natl. Acad. Sci. U.S.A. 104,4401-4406.
51. Tiraby, C., and Langin, D. (2003). Conversion from white to brown adipocytes: a strategy for the control of fat mass? Trends Endocrinol. Metab. 14,439-441.
52. Tiraby, C., Tavernier, G., Lefort, C., Lar-rouy, 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.
53. Tseng, Y. H., Cypess, A. M., and Kahn, C. R. (2010). Cellular bioenergetics as a target for obesity therapy. Nat. Rev. DrugDiscov. 9, 465-482.
54. Tseng, Y. H., Kokkotou, E., Schulz, T. J., Huang, T. L., Winnay, J. N., Taniguchi, C. M., Tran, T. T., Suzuki, R., Espinoza, D. O., Yamamoto, Y., Ahrens, M. J., Dudley, A. T., Norris, A. W., Kulka-rni, R. N., and Kahn, C. R. (2008). New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 1000-1004.
55. van Marken Lichtenbelt, W. D., Van-hommerig, 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.
56. Vegiopoulos, A., Muller-Decker, K., Str-zoda, D., Schmitt, I., Chichelnit-skiy, E., Ostertag, A., Berriel Diaz, M., Rozman, J., Hrabe de Ange-lis, M., Nusing, R. M., Meyer, C. W., Wahli, W., Klingenspor, M., and Herzig, S. (2010). Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science 328, 1158-1161.
57. Vernochet, C., Peres, S. B., Davis, K. E., Mcdonald, M. E., Qiang, L., Wang, H., Scherer, P. E., and Farmer, S. R. (2009). C/EBPalpha and the corepressors CtBP1 and CtBP2 regulate repression of select visceral white adipose genes during induction of the brown pheno-type in white adipocytes by peroxi-some proliferator-activated receptor gamma agonists. Mol. Cell. Biol. 29, 4714-4728.
58. Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N. J., Enerback, S., and Nuutila, P. (2009). Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360,1518-1525.
59. Walden, T. B., Hansen, I. R., Tim-mons, J. A., Cannon, B., and Ned-ergaard, J. (2011). Recruited versus non-recruited molecular signatures of brown, brite and white adipose tissues. Am. J. Physiol. Endocrinol. Metab. 302,E19-E31.
60. 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.
61. Yadav, H., Quijano, C., Kamaraju, A. K., Gavrilova, O., Malek, R., Chen, W., Zerfas, P., Zhigang, D., Wright, E. C., Stuelten, C., Sun, P., Lonning, S., Skarulis, M., Sumner, A. E., Finkel, T.,andRane,S. G. (2011).Protection from obesity and diabetes by blockade of TGF-beta/Smad3 signaling. Cell Metab. 14, 67-79.
62. Yingling, J. M., Blanchard, K. L., and Sawyer, J. S. (2004). Development of TGF-beta signalling inhibitors for cancer therapy. Nat. Rev. Drug Dis-cov.3, 1011-1022.
63. Yoshida, T., Sakane, N., Umekawa, T., Kogure, A., Kondo, M., Kumamoto, K., Kawada, T., Nagase, I., and Saito, M. (1999). Nicotine induces uncoupling protein 1 in white adipose tissue of obese mice. Int. I Obes. Relat. Metab. Disord. 23, 570-575.