Independent stem cell lineages regulate adipose organogenesis and adipose homeostasis

Cell Reports

Volumn 9, Issue 3, 2014, Pages 1007-1022

  Jiang, Yuwei ^a   Berry, Daniel C ^a   Tang, Wei ^a   Graff, Jonathan M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMOOTH MUSCLE ACTIN;

ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; ADULT; ADULT ADIPOSE PROGENITOR; ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LABELING; CELL LINE; CELL LINEAGE; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL ADIPOSE PROGENITOR; EMBRYO; FUNCTIONAL ANATOMY; GENE INACTIVATION; HOMEOSTASIS; LIPID STORAGE; MOLECULAR BIOLOGY; MOUSE; MURAL CELL FATE MAPPING; MUTANT; NONHUMAN; ORGANOGENESIS; PERICYTE; AGING; ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; STAINING; STEM CELL; TIME;

ADIPOSE TISSUE; AGING; ANIMALS; CELL LINEAGE; HOMEOSTASIS; MICE; ORGANOGENESIS; PPAR GAMMA; STAINING AND LABELING; STEM CELLS; TIME FACTORS;

EID: 84919727190     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.09.049     Document Type: Article

References (56)

1. Ahmadian, M., Suh, J.M., Hah, N., Liddle, C., Atkins, A.R., Downes, M., and Evans, R.M. (2013). PPARg signaling and metabolism: the good, the bad and the future. Nat. Med. 19, 557-566.
2. Ailhaud, G., Grimaldi, P., and Négrel, R. (1992). Cellular and molecular aspects of adipose tissue development. Annu. Rev. Nutr. 12, 207-233.
3. Armulik, A., Genové, G., and Betsholtz, C. (2011). Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215.
4. Berry, R., and Rodeheffer, M.S. (2013). Characterization of the adipocyte cellular lineage in vivo. Nat. Cell Biol. 15, 302-308.
5. Berry, D.C., Stenesen, D., Zeve, D., and Graff, J.M. (2013). The developmental origins of adipose tissue. Development 140, 3939-3949.
6. Birsoy, K., Berry, R., Wang, T., Ceyhan, O., Tavazoie, S., Friedman, J.M., and Rodeheffer, M.S. (2011). Analysis of gene networks in white adipose tissue development reveals a role for ETS2 in adipogenesis. Development 138, 4709-4719.
7. Cai, X., Lin, Y., Hauschka, P.V., and Grottkau, B.E. (2011). Adipose stem cells originate from perivascular cells. Biol. Cell 103, 435-447.
8. Chawla, A., Schwarz, E.J., Dimaculangan, D.D., and Lazar, M.A. (1994). Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 135, 798-800.
9. Chen, H.C. (2005). Boyden chamber assay. Methods Mol. Biol. 294, 15-22.
10. Copley, M.R., and Eaves, C.J. (2013). Developmental changes in hematopoietic stem cell properties. Exp. Mol. Med. 45, e55.
11. Crossno, J.T., Jr., Majka, S.M., Grazia, T., Gill, R.G., and Klemm, D.J. (2006). Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J. Clin. Invest. 116, 3220-3228.
12. Cunningham, S.A., Kramer, M.R., and Narayan, K.M. (2014). Incidence of childhood obesity in the United States. N. Engl. J. Med. 370, 403-411.
13. Dani, C., Smith, A.G., Dessolin, S., Leroy, P., Staccini, L., Villageois, P., Darimont, C., and Ailhaud, G. (1997). Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 110, 1279-1285.
14. Daniels, J. (2006). Obesity: America's epidemic. Am. J. Nurs. 106, 40-49, quiz 49-50.
15. Dietz, W.H. (1997). Periods of risk in childhood for the development of adult obesity-what do we need to learn? J. Nutr. 127, 1884S-1886S.
16. Duan, S.Z., Ivashchenko, C.Y., Whitesall, S.E., D'Alecy, L.G., Duquaine, D.C., Brosius, F.C., 3rd, Gonzalez, F.J., Vinson, C., Pierre, M.A., Milstone, D.S., and Mortensen, R.M. (2007). Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J. Clin. Invest. 117, 812-822.
17. Faust, I.M., Johnson, P.R., Stern, J.S., and Hirsch, J. (1978). Diet-induced adipocyte number increase in adult rats: a new model of obesity. Am. J. Physiol. 235, E279-E286.
18. Fordham, R.P., Yui, S., Hannan, N.R., Soendergaard, C., Madgwick, A., Schweiger, P.J., Nielsen, O.H., Vallier, L., Pedersen, R.A., Nakamura, T., et al. (2013). Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell 13, 734-744.
19. Gealekman, O., Burkart, A., Chouinard, M., Nicoloro, S.M., Straubhaar, J., and Corvera, S. (2008). Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am. J. Physiol. Endocrinol. Metab. 295, E1056-E1064.
20. Gesta, S., Tseng, Y.H., and Kahn, C.R. (2007). Developmental origin of fat: tracking obesity to its source. Cell 131, 242-256.
21. 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). Transcriptional control of preadipocyte determination by Zfp423. Nature 464, 619-623.
22. Gupta, R.K., Mepani, R.J., Kleiner, S., Lo, J.C., Khandekar, M.J., Cohen, P., Frontini, A., Bhowmick, D.C., Ye, L., Cinti, S., and Spiegelman, B.M. (2012). Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab. 15, 230-239.
23. Han, J., Lee, J.E., Jin, J., Lim, J.S., Oh, N., Kim, K., Chang, S.I., Shibuya, M., Kim, H., and Koh, G.Y. (2011). The spatiotemporal development of adipose tissue. Development 138, 5027-5037.
24. 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.
25. Hudak, C.S., Gulyaeva, O., Wang, Y., Park, S.M., Lee, L., Kang, C., and Sul, H.S. (2014). Pref-1 marks very early mesenchymal precursors required for adipose tissue development and expansion. Cell Reports 8, 678-687.
26. Johnson, P.R., and Hirsch, J. (1972). Cellularity of adipose depots in six strains of genetically obese mice. J. Lipid Res. 13, 2-11.
27. Kanda, T., Sullivan, K.F., and Wahl, G.M. (1998). Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385.
28. Knapp, D.J., and Eaves, C.J. (2014). Control of the hematopoietic stem cell state. Cell Res. 24, 3-4.
29. Koh, Y.J., Kang, S., Lee, H.J., Choi, T.S., Lee, H.S., Cho, C.H., and Koh, G.Y. (2007). Bone marrow-derived circulating progenitor cells fail to transdifferentiate into adipocytes in adult adipose tissues in mice. J. Clin. Invest. 117, 3684-3695.
30. Kopelman, P.G. (2000). Obesity as a medical problem. Nature 404, 635-643.
31. Lee, Y.H., Petkova, A.P., Mottillo, E.P., and Granneman, J.G. (2012). In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab. 15, 480-491.
32. Li, L., and Clevers, H. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327, 542-545.
33. Li, G., Fang, L., Fernández, G., and Pleasure, S.J. (2013). The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron 78, 658-672.
34. López-Otín, C., Blasco, M.A., Partridge, L., Serrano, M., and Kroemer, G. (2013). The hallmarks of aging. Cell 153, 1194-1217.
35. Morrison, S.J., and Scadden, D.T. (2014). The bone marrow niche for haematopoietic stem cells. Nature 505, 327-334.
36. Nehls, V., and Drenckhahn, D. (1993). The versatility of microvascular pericytes: from mesenchyme to smooth muscle? Histochemistry 99, 1-12.
37. Pietras, E.M., and Passegué, E. (2013). Linking HSCs to their youth. Nat. Cell Biol. 15, 885-887.
38. Prins, J.B., and O'Rahilly, S. (1997). Regulation of adipose cell number in man. Clin. Sci. 92, 3-11.
39. Rigamonti, A., Brennand, K., Lau, F., and Cowan, C.A. (2011). Rapid cellular turnover in adipose tissue. PLoS ONE 6, e17637.
40. Rodeheffer, M.S., Birsoy, K., and Friedman, J.M. (2008). Identification of white adipocyte progenitor cells in vivo. Cell 135, 240-249.
41. Rosen, E.D., and Spiegelman, B.M. (2006). Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847-853.
42. Rosen, E.D., Sarraf, P., Troy, A.E., Bradwin, G., Moore, K., Milstone, D.S., Spiegelman, B.M., and Mortensen, R.M. (1999). PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 4, 611-617.
43. Rousseau, K., Atcha, Z., and Loudon, A.S. (2003). Leptin and seasonal mammals. J. Neuroendocrinol. 15, 409-414.
44. Sanchez-Gurmaches, J., Hung, C.M., Sparks, C.A., Tang, Y., Li, H., and Guertin, D.A. (2012). PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab. 16, 348-362.
45. Schwimmer, H., and Haim, A. (2009). Physiological adaptations of small mammals to desert ecosystems. Integr. Zool. 4, 357-366.
46. Spalding, K.L., Arner, E., Westermark, P.O., Bernard, S., Buchholz, B.A., Bergmann, O., Blomqvist, L., Hoffstedt, J., Näslund, E., Britton, T., et al. (2008). Dynamics of fat cell turnover in humans. Nature 453, 783-787.
47. Spiegelman, B.M., and Flier, J.S. (2001). Obesity and the regulation of energy balance. Cell 104, 531-543.
48. Tang, W., Zeve, D., Suh, J.M., Bosnakovski, D., Kyba, M., Hammer, R.E., Tallquist, M.D., and Graff, J.M. (2008). White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586.
49. Tang, W., Zeve, D., Seo, J., Jo, A.Y., and Graff, J.M. (2011). Thiazolidinediones regulate adipose lineage dynamics. Cell Metab. 14, 116-122.
50. Tontonoz, P., and Spiegelman, B.M. (2008). Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 77, 289-312.
51. Tontonoz, P., Hu, E., and Spiegelman, B.M. (1994). Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79, 1147-1156.
52. Tran, K.V., Gealekman, O., Frontini, A., Zingaretti, M.C., Morroni, M., Giordano, A., Smorlesi, A., Perugini, J., De Matteis, R., Sbarbati, A., et al. (2012). The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 15, 222-229.
53. Weissman, I.L. (2000). Stem cells: units of development, units of regeneration, and units in evolution. Cell 100, 157-168.
54. Wendling, O., Bornert, J.M., Chambon, P., and Metzger, D. (2009). Efficient temporally-controlled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis 47, 14-18.
55. Whitaker, R.C., Wright, J.A., Pepe, M.S., Seidel, K.D., and Dietz, W.H. (1997). Predicting obesity in young adulthood from childhood and parental obesity. N. Engl. J. Med. 337, 869-873.
56. Zeve, D., Seo, J., Suh, J.M., Stenesen, D., Tang, W., Berglund, E.D., Wan, Y., Williams, L.J., Lim, A., Martinez, M.J., et al. (2012). Wnt signaling activation in adipose progenitors promotes insulin-independent muscle glucose uptake. Cell Metab. 15, 492-504.