Differentiation of human adipose-derived stem cells into "brite" (brown-in-white) adipocytes

Frontiers in Endocrinology

Volumn 2, Issue NOV, 2011, Pages

  Pisani, Didier F ^a,b   Djedaini, Mansour ^a,b   Beranger, Guillaume E ^a,b   Elabd, Christian ^a,b,c   Scheideler, Marcel ^d   Ailhaud, Gérard ^a,b   Amri, Ez Zoubir ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CENTRE DE BIOCHIMIE   (France)

^c University of California at Berkeley   (United States)

^d GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Adipocyte; Bat,wat; Brite adipocyte; Differentiation; Rosiglitazone; Stem cells; Ucp1

Indexed keywords

EID: 84874369273     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2011.00087     Document Type: Article

References (43)

1. Ailhaud, G., Grimaldi, P., and Negrel, R. (1992). Cellular and molecular aspects of adipose tissue development. Annu. Rev. Nutr. 12,207-233.
2. 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 transdifferentia-tion. Am. J. Physiol. Endocrinol. Metab. 298, E1244-E1253.
3. Bezy, O., Elabd, C., Cochet, O., Petersen, R. K., Kristiansen, K., Dani, C., Ailhaud, G., and Amri, E. Z. (2005). Delta-interacting protein A, a new inhibitory partner of CCAAT/enhancer-binding protein beta, implicated in adipocyte differentiation. J. Biol. Chem. 280, 11432-11438.
4. Cinti, S. (2009a). Reversible physiological transdifferentiation in the adipose organ. Proc. Nutr. Soc. 68, 340-349.
5. Cinti, S. (2009b). Transdifferentiation properties of adipocytes in the adipose organ. Am. J. Physiol. Endocrinol Metab. 297, E977-E986.
6. Cousin, B., Cinti, S., Morroni, M., Raim-bault, S., Ricquier, D., Penicaud, 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.
7. Crisan, M., Casteilla, L., Lehr, L., Carmona, M., Paoloni-Giacobino, A., Yap, S., Sun, B., Leger, B., Logar, A., Penicaud, L., Schrauwen, P., Cameron-Smith, D., Russell, A. P., Peault, B., and Giacobino, J. P. (2008). A reservoir of brown adipocyte progenitors in human skeletal muscle. Stem Cells 26, 2425-2433.
8. 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.
9. Elabd, C., Chiellini, C., Carmona, M., Galitzky, J., Cochet, O., Petersen, R., Penicaud, L., Kristiansen, K., Bouloumie, A., Casteilla, L., Dani, C., Ailhaud, G., and Amri, E. Z. (2009). Human multipotent adipose-derived stem cells differentiate into functional brown adipocytes. Stem Cells 27,2753-2760.
10. Elabd, C., Chiellini, C., Massoudi, A., Cochet, O., Zaragosi, L. E., Trojani, C., Michiels, J. F., Weiss, P., Carle, G., Rochet, N., Dechesne, C. A., Ailhaud, G., Dani, C., and Amri, E. Z. (2007). Human adipose tissue-derived multipotent stem cells differentiate in vitro and in vivo into osteocyte-like cells. Biochem. Bio-phys. Res. Commun. 361,342-348.
11. 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.
12. Fontaine, C., Cousin, W., Plaisant, M., Dani, C., and Peraldi, P. (2008). Hedgehog signaling alters adipocyte maturation of human mesenchymal stem cells. Stem Cells 26,1037-1046.
13. Fruhbeck, G., Becerril, S., Sainz, N., Garrastachu, P., and Garcia-Velloso, M. J. (2009). BAT: a new target for human obesity? Trends Pharmacol. Sci. 30, 387-396.
14. Golozoubova, V., Cannon, B., and Nedergaard, J. (2006). UCP1 is essential for adaptive adrenergic nonshiver-ing thermogenesis. Am. J. Physiol. Endocrinol. Metab. 291,E350-E357.
15. 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.
16. Hooper, J. E., and Scott, M. P. (2005). Communicating with Hedgehogs. Nat. Rev. Mol. Cell Biol. 6, 306-317.
17. Hossain, P., Kawar, B., and El Nahas, M. (2007). Obesity and diabetes in the developing world - a growing challenge. N Engl. J. Med. 356, 213-215.
18. Lee, S. Y., Nakagawa, T., and Reddi, A. H. (2008). Induction of chondroge-nesis and expression of superficial zone protein (SZP)/lubricin by mesenchymal progenitors in the infra-patellar fat pad of the knee joint treated with TGF-beta1 and BMP-7. Biochem. Biophys. Res. Commun. 376, 148-153.
19. 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.
20. Negrel, R., Grimaldi, P., and Ailhaud, G. (1978). Establishment of preadipocyte clonal line from epi-didymalfat pad of ob/ob mouse that responds to insulin and to lipoly-tic hormones. Proc. Natl. Acad. Sci. U.S.A. 75, 6054-6058.
21. 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, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem. 285,7153-7164.
22. Pisani, D. F., Dechesne, C. A., Sac-coni, S., Delplace, S., Belmonte, N., Cochet, O., Clement, N., Wdziekon-ski, B., Villageois, A. P., Butori, C., Bagnis, C., Di Santo, J. P., Kurzenne, J. Y., Desnuelle, C., and Dani, C. (2010). Isolation of a highly myogenic CD34-negative subset of human skeletal muscle cells free of adipogenic potential. Stem Cells 28, 753-764.
23. Pospisilik, J. A., Schramek, D., Schnidar, H., Cronin, S. J., Nehme, N. T., Zhang, X., Knauf, C., Cani, P. D., Aumayr, K., Todoric, J., Bayer, M., Haschemi, A., Puviindran, V., Tar, K., Orthofer, M., Neely, G. G., Dietzl, G., Manoukian, A., Funovics, M., Prager, G., Wagner, O., Ferran-don, D., Aberger, F., Hui, C. C., Esterbauer, H., and Penninger, J. M. (2010). Drosophilagenome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 140, 148-160.
24. Rodriguez, A. M., Elabd, C., Amri, E. Z., Ailhaud, G., and Dani, C. (2005a). The human adipose tissue is a source of multipotent stem cells. Biochimie 87, 125-128.
25. Rodriguez, A. M., Pisani, D., Dechesne, C. A., Turc-Carel, C., Kurzenne, J. Y., Wdziekonski, B., Villageois, A., Bagnis, C., Breittmayer, J. P., Groux, H., Ailhaud, G., and Dani, C. (2005b). Transplantation of a multi-potent cell population from human adipose tissue induces dystrophin expression in the immunocompe-tent mdx mouse. J. Exp. Med. 201, 1397-1405.
26. Rodriguez, A. M., Elabd, C., Delteil, F., Astier, J., Vernochet, C., Saint-Marc, P., Guesnet, J., Guezennec, A., Amri, E. Z., Dani, C., and Ailhaud, G. (2004). Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem. Biophys. Res. Commun. 315, 255-263.
27. Rosen, E. D., and Spiegelman, B. M. (2006). Adipocytes as regulators of energy balance and glucose home-ostasis. Nature 444, 847-853.
28. Saito, M., Okamatsu-Ogura, Y., Matsushita, M., Watanabe, K., Yoneshiro, T., Nio-Kobayashi, J., Iwanaga, T., Miyagawa, M., Kameya, T., Nakada, K., Kawai, Y., and Tsu-jisaki, M. (2009). High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58,1526-1531.
29. 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.
30. 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.
31. Svensson, P. A., Jernas, M., Sjoholm, K., Hoffmann, J. M., Nilsson, B. E., Hansson, M., and Carlsson, L. M. (2011). Gene expression in human brown adipose tissue. Int. J. Mol. Med. 27,227-232.
32. 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.
33. 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.
34. 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., Kulkarni, R. N., and Kahn, C. R. (2008). New role of bone mor-phogenetic protein 7 in brown adi-pogenesis and energy expenditure. Nature 454, 1000-1004.
35. 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.
36. 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.
37. Virtanen, K. A., Li dell, 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.
38. Whittle, A. J., Lopez, M., and Vidal-Puig, A. (2011). Using brown adipose tissue to treat obesity - the central issue. Trends Mol. Med. 17,405-411.
39. 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.
40. Xue, Y., Petrovic, N., Cao, R., Larsson, O., Lim, S., Chen, S., Feldmann, H. M., Liang, Z., Zhu, Z., Nedergaard, J., Cannon, B., and Cao, Y. (2009). Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. CellMetab. 9,99-109.
41. Zaragosi, L. E.,Ailhaud, G.,andDani, C. (2006). Autocrine fibroblast growth factor 2 signaling is critical for self-renewal of human multipotent adipose-derived stem cells. Stem Cells 24, 2412-2419.
42. Zaragosi, L. E., Wdziekonski, B., Vil-lageois, P., Keophiphath, M., Mau-mus, M., Tchkonia, T., Bourlier, V., Mohsen-Kanson, T., Ladoux, A., Elabd, C., Scheideler, M., Trajanoski, Z., Takashima, Y., Amri, E. Z., Lacasa, D., Sengenes, C., Ailhaud, G., Clement, K., Bouloumie, A., Kirk-land, J. L., and Dani, C. (2010). Activin a plays a critical role in proliferation and differentiation of human adipose progenitors. Diabetes 59,2513-2521
43. Zingaretti, M. C., Crosta, F., Vitali, A., Guerrieri, M., Frontini, A., Cannon, B., Nedergaard, J., and Cinti, S. (2009). The presence of UCP1 demonstrates that metabol-ically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 23,3113-3120