Bone morphogenic proteins signaling in adipogenesis and energy homeostasis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 5, 2013, Pages 915-923

  Modica, Salvatore ^a   Wolfrum, Christian ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Adipogenesis; Bone morphogenic proteins; Brown adipocyte; Energy homeostasis; Mesenchymal stem cells; White adipocyte

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 10; BONE MORPHOGENETIC PROTEIN 11; BONE MORPHOGENETIC PROTEIN 12; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 8A; BONE MORPHOGENETIC PROTEIN 8B; BONE MORPHOGENETIC PROTEIN 9; GROWTH DIFFERENTIATION FACTOR 10; GROWTH DIFFERENTIATION FACTOR 6; OSTEOGENIC PROTEIN 1; OSTEOGENIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; ENERGY; HOMEOSTASIS; HUMAN; MESENCHYMAL STEM CELL; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROADIPOCYTE; REVIEW; SIGNAL TRANSDUCTION;

ADIPOGENESIS; ANIMALS; BONE MORPHOGENETIC PROTEINS; ENERGY METABOLISM; HOMEOSTASIS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84875867013     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.01.010     Document Type: Review

References (99)

1. A.I. Caplan, and S.P. Bruder Mesenchymal stem cells: building blocks for molecular medicine in the 21st century Trends Mol. Med. 7 2001 259 264
2. N. Billon, and C. Dani Developmental origins of the adipocyte lineage: new insights from genetics and genomics studies Stem Cell Rev. 8 2012 55 66
3. S. Enerback The origins of brown adipose tissue N. Engl. J. Med. 360 2009 2021 2023
4. S. Gesta, Y.H. Tseng, and C.R. Kahn Developmental origin of fat: tracking obesity to its source Cell 131 2007 242 256
5. S. Cinti The adipose organ: morphological perspectives of adipose tissues Proc. Nutr. Soc. 60 2001 319 328
6. S. Cinti The adipose organ Prostaglandins Leukot. Essent. Fatty Acids 73 2005 9 15
7. S. Cinti Between brown and white: novel aspects of adipocyte differentiation Ann. Med. 43 2011 104 115
8. A.M. Cypess, S. Lehman, G. Williams, I. Tal, D. Rodman, A.B. Goldfine, F.C. Kuo, E.L. Palmer, Y.H. Tseng, A. Doria, G.M. Kolodny, and C.R. Kahn Identification and importance of brown adipose tissue in adult humans N. Engl. J. Med. 360 2009 1509 1517
9. M. Saito, Y. Okamatsu-Ogura, M. Matsushita, K. Watanabe, T. Yoneshiro, J. Nio-Kobayashi, T. Iwanaga, M. Miyagawa, T. Kameya, K. Nakada, Y. Kawai, and M. Tsujisaki High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity Diabetes 58 2009 1526 1531
10. W.D. van Marken Lichtenbelt, J.W. Vanhommerig, N.M. Smulders, J.M. Drossaerts, G.J. Kemerink, N.D. Bouvy, P. Schrauwen, and G.J. Teule Cold-activated brown adipose tissue in healthy men N. Engl. J. Med. 360 2009 1500 1508
11. K.A. Virtanen, M.E. Lidell, J. Orava, M. Heglind, R. Westergren, T. Niemi, M. Taittonen, J. Laine, N.J. Savisto, S. Enerback, and P. Nuutila Functional brown adipose tissue in healthy adults N. Engl. J. Med. 360 2009 1518 1525
12. A. Koppen, and E. Kalkhoven Brown vs white adipocytes: the PPARgamma coregulator story FEBS Lett. 584 2010 3250 3259
13. H. Aquila, T.A. Link, and M. Klingenberg The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane EMBO J. 4 1985 2369 2376
14. B.B. Lowell, S.S. V, A. Hamann, J.A. Lawitts, J. Himms-Hagen, B.B. Boyer, L.P. Kozak, and J.S. Flier Development of obesity in transgenic mice after genetic ablation of brown adipose tissue Nature 366 1993 740 742
15. J. Kopecky, G. Clarke, S. Enerback, B. Spiegelman, and L.P. Kozak Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity J. Clin. Invest. 96 1995 2914 2923
16. K.W. Park, D.S. Halperin, and P. Tontonoz Before they were fat: adipocyte progenitors Cell Metab. 8 2008 454 457
17. P. Seale, B. Bjork, W. Yang, S. Kajimura, S. Chin, S. Kuang, A. Scime, S. Devarakonda, H.M. Conroe, H. Erdjument-Bromage, P. Tempst, M.A. Rudnicki, D.R. Beier, and B.M. Spiegelman PRDM16 controls a brown fat/skeletal muscle switch Nature 454 2008 961 967
18. K. Gessner, Tigurine Historiae Animalium Lib. I de Quadripedibus uiuiparis, 1551.
19. R. Atit, S.K. Sgaier, O.A. Mohamed, M.M. Taketo, D. Dufort, A.L. Joyner, L. Niswander, and R.A. Conlon Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse Dev. Biol. 296 2006 164 176
20. J.A. Timmons, K. Wennmalm, O. Larsson, T.B. Walden, T. Lassmann, N. Petrovic, D.L. Hamilton, R.E. Gimeno, C. Wahlestedt, K. Baar, J. Nedergaard, and B. Cannon Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages Proc. Natl. Acad. Sci. U. S. A. 104 2007 4401 4406
21. J. Sanchez-Gurmaches, C.M. Hung, C.A. Sparks, Y. Tang, H. Li, and D.A. Guertin PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors Cell Metab. 16 2012 348 362
22. P. Hasty, A. Bradley, J.H. Morris, D.G. Edmondson, J.M. Venuti, E.N. Olson, and W.H. Klein Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene Nature 364 1993 501 506
23. Y.H. Tseng, E. Kokkotou, T.J. Schulz, T.L. Huang, J.N. Winnay, C.M. Taniguchi, T.T. Tran, R. Suzuki, D.O. Espinoza, Y. Yamamoto, M.J. Ahrens, A.T. Dudley, A.W. Norris, R.N. Kulkarni, and C.R. Kahn New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure Nature 454 2008 1000 1004
24. S. Kajimura, P. Seale, T. Tomaru, H. Erdjument-Bromage, M.P. Cooper, J.L. Ruas, S. Chin, P. Tempst, M.A. Lazar, and B.M. Spiegelman Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex Genes Dev. 22 2008 1397 1409
25. L. Sun, H. Xie, M.A. Mori, R. Alexander, B. Yuan, S.M. Hattangadi, Q. Liu, C.R. Kahn, and H.F. Lodish Mir193b-365 is essential for brown fat differentiation Nat. Cell Biol. 13 2011 958 965
26. J. Wu, P. Bostrom, L.M. Sparks, L. Ye, J.H. Choi, A.H. Giang, M. Khandekar, K.A. Virtanen, P. Nuutila, G. Schaart, K. Huang, H. Tu, W.D. van Marken Lichtenbelt, J. Hoeks, S. Enerback, P. Schrauwen, and B.M. Spiegelman Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human Cell 150 2012 366 376
27. B. Cousin, S. Cinti, M. Morroni, S. Raimbault, D. Ricquier, L. Penicaud, and L. Casteilla Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization J. Cell Sci. 103 Pt 4 1992 931 942
28. A. Vegiopoulos, K. Muller-Decker, D. Strzoda, I. Schmitt, E. Chichelnitskiy, A. Ostertag, M. Berriel Diaz, J. Rozman, M. Hrabe de Angelis, R.M. Nusing, C.W. Meyer, W. Wahli, M. Klingenspor, and S. Herzig Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes Science (New York, N.Y.) 328 2010 1158 1161
29. P. Young, J.R. Arch, and M. Ashwell Brown adipose tissue in the parametrial fat pad of the mouse FEBS Lett. 167 1984 10 14
30. N. Petrovic, T.B. Walden, I.G. Shabalina, J.A. Timmons, B. Cannon, and J. Nedergaard 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 2010 7153 7164
31. A. Vitali, I. Murano, M.C. Zingaretti, A. Frontini, D. Ricquier, and S. Cinti The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes J. Lipid Res. 53 2012 619 629
32. B. Xue, J.S. Rim, J.C. Hogan, A.A. Coulter, R.A. Koza, and L.P. Kozak Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat J. Lipid Res. 48 2007 41 51
33. T.J. Schulz, T.L. Huang, T.T. Tran, H. Zhang, K.L. Townsend, J.L. Shadrach, M. Cerletti, L.E. McDougall, N. Giorgadze, T. Tchkonia, D. Schrier, D. Falb, J.L. Kirkland, A.J. Wagers, and Y.H. Tseng Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat Proc. Natl. Acad. Sci. U. S. A. 108 2011 143 148
34. K. Almind, M. Manieri, W.I. Sivitz, S. Cinti, and C.R. Kahn Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice Proc. Natl. Acad. Sci. U. S. A. 104 2007 2366 2371
35. P. Seale, S. Kajimura, W. Yang, S. Chin, L.M. Rohas, M. Uldry, G. Tavernier, D. Langin, and B.M. Spiegelman Transcriptional control of brown fat determination by PRDM16 Cell Metab. 6 2007 38 54
36. W. Jin, T. Takagi, S.N. Kanesashi, T. Kurahashi, T. Nomura, J. Harada, and S. Ishii Schnurri-2 controls BMP-dependent adipogenesis via interaction with Smad proteins Dev. Cell 10 2006 461 471
37. M.C. Ramel, and C.S. Hill Spatial regulation of BMP activity FEBS Lett. 586 2012 1929 1941
38. B.L. Hogan Bone morphogenetic proteins: multifunctional regulators of vertebrate development Genes Dev. 10 1996 1580 1594
39. M.R. Urist Bone: formation by autoinduction Science 150 1965 893 899
40. F.P. Luyten, N.S. Cunningham, S. Ma, N. Muthukumaran, R.G. Hammonds, W.B. Nevins, W.I. Woods, and A.H. Reddi Purification and partial amino acid sequence of osteogenin, a protein initiating bone differentiation J. Biol. Chem. 264 1989 13377 13380
41. J.M. Wozney The bone morphogenetic protein family and osteogenesis Mol. Reprod. Dev. 32 1992 160 167
42. D. Chen, M. Zhao, and G.R. Mundy Bone morphogenetic proteins Growth Factors 22 2004 233 241
43. Q. Kang, W.X. Song, Q. Luo, N. Tang, J. Luo, X. Luo, J. Chen, Y. Bi, B.C. He, J.K. Park, W. Jiang, Y. Tang, J. Huang, Y. Su, G.H. Zhu, Y. He, H. Yin, Z. Hu, Y. Wang, L. Chen, G.W. Zuo, X. Pan, J. Shen, T. Vokes, R.R. Reid, R.C. Haydon, H.H. Luu, and T.C. He A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells Stem Cells Dev. 18 2009 545 559
44. D.B. Constam, and E.J. Robertson Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases J. Cell Biol. 144 1999 139 149
45. R. Nishimura, K. Hata, F. Ikeda, T. Matsubara, K. Yamashita, F. Ichida, and T. Yoneda The role of Smads in BMP signaling Front. Biosci. 8 2003 s275 s284
46. K. Miyazono, Y. Kamiya, and M. Morikawa Bone morphogenetic protein receptors and signal transduction J. Biochem. 147 2010 35 51
47. P.B. Yu, H. Beppu, N. Kawai, E. Li, and K.D. Bloch Bone morphogenetic protein (BMP) type II receptor deletion reveals BMP ligand-specific gain of signaling in pulmonary artery smooth muscle cells J. Biol. Chem. 280 2005 24443 24450
48. C.H. Heldin, K. Miyazono, and P. ten Dijke TGF-beta signalling from cell membrane to nucleus through SMAD proteins Nature 390 1997 465 471
49. M. Murakami, H. Kawachi, K. Ogawa, Y. Nishino, and M. Funaba Receptor expression modulates the specificity of transforming growth factor-beta signaling pathways Genes Cells 14 2009 469 482
50. S. Zhang, T. Fei, L. Zhang, R. Zhang, F. Chen, Y. Ning, Y. Han, X.H. Feng, A. Meng, and Y.G. Chen Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation Mol. Cell. Biol. 27 2007 4488 4499
51. K. Goto, Y. Kamiya, T. Imamura, K. Miyazono, and K. Miyazawa Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors J. Biol. Chem. 282 2007 20603 20611
52. W. Ishida, T. Hamamoto, K. Kusanagi, K. Yagi, M. Kawabata, K. Takehara, T.K. Sampath, M. Kato, and K. Miyazono Smad6 is a Smad1/5-induced smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter J. Biol. Chem. 275 2000 6075 6079
53. Y.W. Zhang, N. Yasui, K. Ito, G. Huang, M. Fujii, J. Hanai, H. Nogami, T. Ochi, K. Miyazono, and Y. Ito A RUNX2/PEBP2alpha A/CBFA1 mutation displaying impaired transactivation and Smad interaction in cleidocranial dysplasia Proc. Natl. Acad. Sci. U. S. A. 97 2000 10549 10554
54. D.L. Jones, and A.J. Wagers No place like home: anatomy and function of the stem cell niche Nat. Rev. Mol. Cell Biol. 9 2008 11 21
55. S.E. Ross, N. Hemati, K.A. Longo, C.N. Bennett, P.C. Lucas, R.L. Erickson, and O.A. MacDougald Inhibition of adipogenesis by Wnt signaling Science 289 2000 950 953
56. J.B. Hansen, C. Jorgensen, R.K. Petersen, P. Hallenborg, R. De Matteis, H.A. Boye, N. Petrovic, S. Enerback, J. Nedergaard, S. Cinti, H. te Riele, and K. Kristiansen Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation Proc. Natl. Acad. Sci. U. S. A. 101 2004 4112 4117
57. A. Scime, G. Grenier, M.S. Huh, M.A. Gillespie, L. Bevilacqua, M.E. Harper, and M.A. Rudnicki Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha Cell Metab. 2 2005 283 295
58. C.M. Smas, and H.S. Sul Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation Cell 73 1993 725 734
59. Y.H. Tseng, A.J. Butte, E. Kokkotou, V.K. Yechoor, C.M. Taniguchi, K.M. Kriauciunas, A.M. Cypess, M. Niinobe, K. Yoshikawa, M.E. Patti, and C.R. Kahn Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin Nat. Cell Biol. 7 2005 601 611
60. F. Picard, M. Gehin, J. Annicotte, S. Rocchi, M.F. Champy, B.W. O'Malley, P. Chambon, and J. Auwerx SRC-1 and TIF2 control energy balance between white and brown adipose tissues Cell 111 2002 931 941
61. J.H. Steel, R. White, and M.G. Parker Role of the RIP140 corepressor in ovulation and adipose biology J. Endocrinol. 185 2005 1 9
62. Z. Wang, C. Qi, A. Krones, P. Woodring, X. Zhu, J.K. Reddy, R.M. Evans, M.G. Rosenfeld, and T. Hunter Critical roles of the p160 transcriptional coactivators p/CIP and SRC-1 in energy balance Cell Metab. 3 2006 111 122
63. R.R. Bowers, J.W. Kim, T.C. Otto, and M.D. Lane Stable stem cell commitment to the adipocyte lineage by inhibition of DNA methylation: role of the BMP-4 gene Proc. Natl. Acad. Sci. U. S. A. 103 2006 13022 13027
64. H. Huang, T.J. Song, X. Li, L. Hu, Q. He, M. Liu, M.D. Lane, and Q.Q. Tang BMP signaling pathway is required for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage Proc. Natl. Acad. Sci. U. S. A. 106 2009 12670 12675
65. Q.Q. Tang, T.C. Otto, and M.D. Lane Commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage Proc. Natl. Acad. Sci. U. S. A. 101 2004 9607 9611
66. O. Khalsa, J.W. Yoon, S. Torres-Schumann, and K.A. Wharton TGF-beta/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing Development 125 1998 2723 2734
67. S. Gesta, M. Bluher, Y. Yamamoto, A.W. Norris, J. Berndt, S. Kralisch, J. Boucher, C. Lewis, and C.R. Kahn Evidence for a role of developmental genes in the origin of obesity and body fat distribution Proc. Natl. Acad. Sci. U. S. A. 103 2006 6676 6681
68. T.L. Chen, W.J. Shen, and F.B. Kraemer Human BMP-7/OP-1 induces the growth and differentiation of adipocytes and osteoblasts in bone marrow stromal cell cultures J. Cell. Biochem. 82 2001 187 199
69. J.M. Gimble, C. Morgan, K. Kelly, X. Wu, V. Dandapani, C.S. Wang, and V. Rosen Bone morphogenetic proteins inhibit adipocyte differentiation by bone marrow stromal cells J. Cell. Biochem. 58 1995 393 402
70. R.C. Pereira, A.M. Delany, and E. Canalis Effects of cortisol and bone morphogenetic protein-2 on stromal cell differentiation: correlation with CCAAT-enhancer binding protein expression Bone 30 2002 685 691
71. M.F. Taha, M.R. Valojerdi, and S.J. Mowla Effect of bone morphogenetic protein-4 (BMP-4) on adipocyte differentiation from mouse embryonic stem cells Anat. Histol. Embryol. 35 2006 271 278
72. C.A. Reznikoff, D.W. Brankow, and C. Heidelberger Establishment and characterization of a cloned line of C3H mouse embryo cells sensitive to postconfluence inhibition of division Cancer Res. 33 1973 3231 3238
73. I. Asahina, T.K. Sampath, and P.V. Hauschka Human osteogenic protein-1 induces chondroblastic, osteoblastic, and/or adipocytic differentiation of clonal murine target cells Exp. Cell Res. 222 1996 38 47
74. E.A. Wang, D.I. Israel, S. Kelly, and D.P. Luxenberg Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells Growth Factors 9 1993 57 71
75. O.P. Lazarenko, S.O. Rzonca, L.J. Suva, and B. Lecka-Czernik Netoglitazone is a PPAR-gamma ligand with selective effects on bone and fat Bone 38 2006 74 84
76. B. Lecka-Czernik, E.J. Moerman, D.F. Grant, J.M. Lehmann, S.C. Manolagas, and R.L. Jilka Divergent effects of selective peroxisome proliferator-activated receptor-gamma 2 ligands on adipocyte versus osteoblast differentiation Endocrinology 143 2002 2376 2384
77. A. Grey Skeletal consequences of thiazolidinedione therapy Osteoporos. Int. 19 2008 129 137
78. T. Akune, S. Ohba, S. Kamekura, M. Yamaguchi, U.I. Chung, N. Kubota, Y. Terauchi, Y. Harada, Y. Azuma, K. Nakamura, T. Kadowaki, and H. Kawaguchi PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors J. Clin. Invest. 113 2004 846 855
79. E.J. Moerman, K. Teng, D.A. Lipschitz, and B. Lecka-Czernik Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways Aging Cell 3 2004 379 389
80. H. Cheng, W. Jiang, F.M. Phillips, R.C. Haydon, Y. Peng, L. Zhou, H.H. Luu, N. An, B. Breyer, P. Vanichakarn, J.P. Szatkowski, J.Y. Park, and T.C. He Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs) J. Bone Joint Surg. Am. 85-A 2003 1544 1552
81. M. Suzawa, Y. Takeuchi, S. Fukumoto, S. Kato, N. Ueno, K. Miyazono, T. Matsumoto, and T. Fujita Extracellular matrix-associated bone morphogenetic proteins are essential for differentiation of murine osteoblastic cells in vitro Endocrinology 140 1999 2125 2133
82. D. Chen, X. Ji, M.A. Harris, J.Q. Feng, G. Karsenty, A.J. Celeste, V. Rosen, G.R. Mundy, and S.E. Harris Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages J. Cell Biol. 142 1998 295 305
83. K. Hata, R. Nishimura, F. Ikeda, K. Yamashita, T. Matsubara, T. Nokubi, and T. Yoneda Differential roles of Smad1 and p38 kinase in regulation of peroxisome proliferator-activating receptor gamma during bone morphogenetic protein 2-induced adipogenesis Mol. Biol. Cell 14 2003 545 555
84. A.J. Whittle, S. Carobbio, L. Martins, M. Slawik, E. Hondares, M.J. Vazquez, D. Morgan, R.I. Csikasz, R. Gallego, S. Rodriguez-Cuenca, M. Dale, S. Virtue, F. Villarroya, B. Cannon, K. Rahmouni, M. Lopez, and A. Vidal-Puig BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions Cell 149 2012 871 885
85. K. Ohyama, R. Das, and M. Placzek Temporal progression of hypothalamic patterning by a dual action of BMP Development 135 2008 3325 3331
86. K.L. Townsend, R. Suzuki, T.L. Huang, E. Jing, T.J. Schulz, K. Lee, C.M. Taniguchi, D.O. Espinoza, L.E. McDougall, H. Zhang, T.C. He, E. Kokkotou, and Y.H. Tseng Bone morphogenetic protein 7 (BMP7) reverses obesity and regulates appetite through a central mTOR pathway FASEB J. 26 2012 2187 2196
87. W. Sebald, J. Nickel, J.L. Zhang, and T.D. Mueller Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction Biol. Chem. 385 2004 697 710
88. Y. Bottcher, H. Unbehauen, N. Kloting, K. Ruschke, A. Korner, D. Schleinitz, A. Tonjes, B. Enigk, S. Wolf, K. Dietrich, M. Koriath, G.H. Scholz, Y.H. Tseng, A. Dietrich, M.R. Schon, W. Kiess, M. Stumvoll, M. Bluher, and P. Kovacs Adipose tissue expression and genetic variants of the bone morphogenetic protein receptor 1A gene (BMPR1A) are associated with human obesity Diabetes 58 2009 2119 2128
89. J.W. Son, M.K. Kim, Y.M. Park, K.H. Baek, S.J. Yoo, K.H. Song, H.S. Son, K.H. Yoon, W.C. Lee, B.Y. Cha, H.Y. Son, and H.S. Kwon Association of serum bone morphogenetic protein 4 levels with obesity and metabolic syndrome in non-diabetic individuals Endocr. J. 58 2011 39 46
90. T. Schulz, T. Huang, Y. Mishina, and Y. Tseng Adipocyte-specific inactivation of type 1A bone morphogenetic protein receptor impacts systemic energy metabolism and fat physiology Diabetes 2009 [Supplement 1]
91. N.J. Rothwell, and M.J. Stock Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour Clin. Sci. (Lond.) 1983 19 23
92. E. Christiansen, L. Garby, and T.I. Sorensen Quantitative analysis of the energy requirements for development of obesity J. Theor. Biol. 234 2005 99 106
93. J.C. Clapham, and J.R. Arch Thermogenic and metabolic antiobesity drugs: rationale and opportunities Diabetes Obes. Metab. 9 2007 259 275
94. L. Bukowiecki, A.J. Collet, N. Follea, G. Guay, and L. Jahjah Brown adipose tissue hyperplasia: a fundamental mechanism of adaptation to cold and hyperphagia Am. J. Physiol. 242 1982 E353 E359
95. G. Zhou, R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M.F. Hirshman, L.J. Goodyear, and D.E. Moller Role of AMP-activated protein kinase in mechanism of metformin action J. Clin. Invest. 108 2001 1167 1174
96. M. Nishio, T. Yoneshiro, M. Nakahara, S. Suzuki, K. Saeki, M. Hasegawa, Y. Kawai, H. Akutsu, A. Umezawa, K. Yasuda, K. Tobe, A. Yuo, K. Kubota, and M. Saito Production of functional classical brown adipocytes from human pluripotent stem cells using specific hemopoietin cocktail without gene transfer Cell Metab. 16 2012 394 406
97. C. Huggins, and B.H. Blocksom Changes in outlying bone marrow accompanying a local increase of temperature within physiological limits J. Exp. Med. 64 1936 253 274
98. C. Huggins, S. Wiseman, and A.H. Reddi Transformation of fibroblasts by allogeneic and xenogeneic transplants of demineralized tooth and bone J. Exp. Med. 132 1970 1250 1258
99. A. Krings, S. Rahman, S. Huang, Y. Lu, P.J. Czernik, and B. Lecka-Czernik Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes Bone 50 2012 546 552