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Adipose Stem Cells

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Angiogenesis in Adipose Tissue

Abstract

Once considered an inert mass of stored energy, the past 2 decades have seen a surge in interest in the complexity of adipose tissue and its role in disease. In addition to serving as a site for energy storage, adipocytes secrete proteins involved in inflammation, appetite regulation, blood pressure control, and energy balance. Adipocytes are unique in their ability to store large quantities of lipids that can be rapidly released and used for energy by other organs, when necessary; however, excessive adipose tissue, particularly in the visceral adipose tissue depot, is associated with increased risk of insulin resistance, cardiovascular disease, and cancer. As such, adipose tissue is capable of extensive expansion or retraction depending on the energy balance or disease state of the host, a plasticity that is unparalleled in other organs. Expansion of adipose tissue is driven by both hypertrophy and hyperplasia of adipocytes, which can renew frequently to compensate for cell death, suggesting the necessity of adipocyte progenitor cells within the adipose tissue depot, that are capable of differentiating into mature and functional adipocytes.

Epidemiological studies estimate that more than one billion people worldwide are overweight and at least 400 million clinically obese. Therefore, in order to combat the global obesity pandemic, the origin and the molecular mechanisms controlling the development and expansion of adipocytes must be fully understood so that novel approaches to prevention and therapy can be developed.

The authors Carolyn Algire and Dasa Medrikova have equally contributed.

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References

  • Ahmadian M, Abbott MJ, Tang T, Hudak CS, Kim Y, Bruss M, Hellerstein MK, Lee HY, Samuel VT, Shulman GI, Wang Y, Duncan RE, Kang C, Sul HS. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 2011;13:739–48.

    Article  PubMed  CAS  Google Scholar 

  • Amos AF, McCarty DJ, Zimmet P. The rising global burden of diabetes and its complications: estimates and projections to the year 2010. Diabet Med. 1997;14 Suppl 5:S1–85.

    PubMed  Google Scholar 

  • Arch JR. beta(3)-Adrenoceptor agonists: potential, pitfalls and progress. Eur J Pharmacol. 2002;440:99–107.

    Article  PubMed  CAS  Google Scholar 

  • Ashjian PH, Elbarbary AS, Edmonds B, DeUgarte D, Zhu M, Zuk PA, Lorenz HP, Benhaim P, Hedrick MH. In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg. 2003;111:1922–31.

    Article  PubMed  Google Scholar 

  • Astrup A, Bulow J, Madsen J, Christensen NJ. Contribution of BAT and skeletal muscle to thermogenesis induced by ephedrine in man. Am J Physiol. 1985;248:E507–15.

    PubMed  CAS  Google Scholar 

  • Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, Giacobino JP, De Matteis R, Cinti S. 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. 2010;298:E1244–53.

    Article  PubMed  CAS  Google Scholar 

  • Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmuller A, Gordts PL, Rinninger F, Bruegelmann K, Freund B, Nielsen P, Merkel M, Heeren J. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17(2):200–5.

    Article  PubMed  CAS  Google Scholar 

  • Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Hojlund K, Gygi SP, Spiegelman BM. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8.

    Article  PubMed  Google Scholar 

  • Bowers RR, Lane MD. A role for bone morphogenetic protein-4 in adipocyte development. Cell Cycle. 2007;6:385–9.

    Article  PubMed  CAS  Google Scholar 

  • Bray GA, Wilson JF. In the clinic. Obesity. Ann Intern Med. 2008;149:ITC4-1-15; quiz ITC14-16.

    Google Scholar 

  • Bronnikov G, Bengtsson T, Kramarova L, Golozoubova V, Cannon B, Nedergaard J. beta1 to beta3 switch in control of cyclic adenosine monophosphate during brown adipocyte development explains distinct beta-adrenoceptor subtype mediation of proliferation and differentiation. Endocrinology. 1999;140:4185–97.

    Article  PubMed  CAS  Google Scholar 

  • Brzoska M, Geiger H, Gauer S, Baer P. Epithelial differentiation of human adipose tissue-derived adult stem cells. Biochem Biophys Res Commun. 2005;330:142–50.

    Article  PubMed  CAS  Google Scholar 

  • Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004;4:579–91.

    Article  PubMed  CAS  Google Scholar 

  • Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277–359.

    Article  PubMed  CAS  Google Scholar 

  • Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A. Adipogenesis and WNT signalling. Trends Endocrinol Metab. 2009;20:16–24.

    Article  PubMed  CAS  Google Scholar 

  • Cohen DH, Leroith D. Obesity, type 2 diabetes and cancer: the insulin and insulin-like growth factor connection. Endocr Relat Cancer. 2012;19(5):F27–45.

    Article  PubMed  CAS  Google Scholar 

  • Crossno Jr JT, Majka SM, Grazia T, Gill RG, Klemm DJ. Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J Clin Invest. 2006;116:3220–8.

    Article  PubMed  CAS  Google Scholar 

  • Daley GQ, Scadden DT. Prospects for stem cell-based therapy. Cell. 2008;132:544–8.

    Article  PubMed  CAS  Google Scholar 

  • Dorresteijn JA, Visseren FL, Spiering W. Mechanisms linking obesity to hypertension. Obes Rev. 2012;13:17–26.

    Article  PubMed  CAS  Google Scholar 

  • Fajas L, Fruchart JC, Auwerx J. PPARgamma3 mRNA: a distinct PPARgamma mRNA subtype transcribed from an independent promoter. FEBS Lett. 1998;438:55–60.

    Article  PubMed  CAS  Google Scholar 

  • Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, Singh GM, Gutierrez HR, Lu Y, Bahalim AN, Farzadfar F, Riley LM, Ezzati M. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011;377:557–67.

    Article  PubMed  Google Scholar 

  • Fraser JK, Wulur I, Alfonso Z, Hedrick MH. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 2006;24:150–4.

    Article  PubMed  CAS  Google Scholar 

  • Frontini A, Cinti S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 2010;11:253–6.

    Article  PubMed  CAS  Google Scholar 

  • Galani C, Schneider H. Prevention and treatment of obesity with lifestyle interventions: review and meta-analysis. Int J Public Health. 2007;52:348–59.

    Article  PubMed  Google Scholar 

  • Garcia-Olmo D, Garcia-Arranz M, Herreros D, Pascual I, Peiro C, Rodriguez-Montes JA. A phase I clinical trial of the treatment of Crohn’s fistula by adipose mesenchymal stem cell transplantation. Dis Colon Rectum. 2005;48:1416–23.

    Article  PubMed  Google Scholar 

  • Green H, Kehinde O. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell. 1975;5:19–27.

    Article  PubMed  CAS  Google Scholar 

  • Greenway FL, Whitehouse MJ, Guttadauria M, Anderson JW, Atkinson RL, Fujioka K, Gadde KM, Gupta AK, O’Neil P, Schumacher D, Smith D, Dunayevich E, Tollefson GD, Weber E, Cowley MA. Rational design of a combination medication for the treatment of obesity. Obesity (Silver Spring). 2008;17(1):30–9.

    Article  Google Scholar 

  • Halvorsen YD, Franklin D, Bond AL, Hitt DC, Auchter C, Boskey AL, Paschalis EP, Wilkison WO, Gimble JM. Extracellular matrix mineralization and osteoblast gene expression by human adipose tissue-derived stromal cells. Tissue Eng. 2001;7:729–41.

    Article  PubMed  CAS  Google Scholar 

  • Hamm JK, Park BH, Farmer SR. A role for C/EBPbeta in regulating peroxisome proliferator-activated receptor gamma activity during adipogenesis in 3T3-L1 preadipocytes. J Biol Chem. 2001;276:18464–71.

    Article  PubMed  CAS  Google Scholar 

  • Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F. Hepatic FGF21 expression is induced at birth via PPARalpha in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab. 2010;11:206–12.

    Article  PubMed  CAS  Google Scholar 

  • Huang H, Song TJ, Li X, Hu L, He Q, Liu M, Lane MD, Tang QQ. BMP signaling pathway is required for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc Natl Acad Sci U S A. 2009;106:12670–5.

    Article  PubMed  CAS  Google Scholar 

  • Huang HY, Hu LL, Song TJ, Li X, He Q, Sun X, Li YM, Lu HJ, Yang PY, Tang QQ. Involvement of cytoskeleton-associated proteins in the commitment of C3H10T1/2 pluripotent stem cells to adipocyte lineage induced by BMP2/4. Mol Cell Proteomics. 2011;10(M110):002691.

    PubMed  Google Scholar 

  • Hubbell JA. Biomaterials science and high-throughput screening. Nat Biotechnol. 2004;22:828–9.

    Article  PubMed  CAS  Google Scholar 

  • Ioannides-Demos LL, Proietto J, McNeil JJ. Pharmacotherapy for obesity. Drugs. 2005;65:1391–418.

    Article  PubMed  CAS  Google Scholar 

  • Isenmann S, Arthur A, Zannettino AC, Turner JL, Shi S, Glackin CA, Gronthos S. TWIST family of basic helix-loop-helix transcription factors mediate human mesenchymal stem cell growth and commitment. Stem Cells. 2009;27:2457–68.

    Article  PubMed  CAS  Google Scholar 

  • Jia B, Madsen L, Petersen RK, Techer N, Kopperud R, Ma T, Doskeland SO, Ailhaud G, Wang J, Amri EZ, Kristiansen K. Activation of protein kinase A and exchange protein directly activated by cAMP promotes adipocyte differentiation of human mesenchymal stem cells. PLoS One. 2012;7:e34114.

    Article  PubMed  CAS  Google Scholar 

  • Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem. 2007;282:14515–24.

    Article  PubMed  CAS  Google Scholar 

  • Kim JB, Wright HM, Wright M, Spiegelman BM. ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proc Natl Acad Sci U S A. 1998;95:4333–7.

    Article  PubMed  CAS  Google Scholar 

  • Kopelman PG. Obesity as a medical problem. Nature. 2000;404:635–43.

    PubMed  CAS  Google Scholar 

  • Lee YH, Petkova AP, Mottillo EP, Granneman JG. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab. 2012;15:480–91.

    Article  PubMed  CAS  Google Scholar 

  • Leroith D. Pathophysiology of the metabolic syndrome: implications for the cardiometabolic risks associated with type 2 diabetes. Am J Med Sci. 2012;343:13–6.

    Article  PubMed  Google Scholar 

  • Lin G, Garcia M, Ning H, Banie L, Guo YL, Lue TF, Lin CS. Defining stem and progenitor cells within adipose tissue. Stem Cells Dev. 2008;17:1053–63.

    Article  PubMed  CAS  Google Scholar 

  • Lopez M, Varela L, Vazquez MJ, Rodriguez-Cuenca S, Gonzalez CR, Velagapudi VR, Morgan DA, Schoenmakers E, Agassandian K, Lage R, Martinez de Morentin PB, Tovar S, Nogueiras R, Carling D, Lelliott C, Gallego R, Oresic M, Chatterjee K, Saha AK, Rahmouni K, Dieguez C, Vidal-Puig A. Hypothalamic AMPK and fatty acid metabolism mediate thyroid regulation of energy balance. Nat Med. 2010;16:1001–8.

    Article  PubMed  CAS  Google Scholar 

  • Majka SM, Fox KE, Psilas JC, Helm KM, Childs CR, Acosta AS, Janssen RC, Friedman JE, Woessner BT, Shade TR, Varella-Garcia M, Klemm DJ. De novo generation of white adipocytes from the myeloid lineage via mesenchymal intermediates is age, adipose depot, and gender specific. Proc Natl Acad Sci U S A. 2010;107:14781–6.

    Article  PubMed  CAS  Google Scholar 

  • Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293:E444–52.

    Article  PubMed  CAS  Google Scholar 

  • Ning H, Lin G, Lue TF, Lin CS. Neuron-like differentiation of adipose tissue-derived stromal cells and vascular smooth muscle cells. Differentiation. 2006;74:510–8.

    Article  PubMed  CAS  Google Scholar 

  • Nissen SE, Wolski K. Rosiglitazone revisited: an updated meta-analysis of risk for myocardial infarction and cardiovascular mortality. Arch Intern Med. 2010;170:1191–201.

    Article  PubMed  CAS  Google Scholar 

  • Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerback S, Virtanen KA. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14:272–9.

    Article  PubMed  CAS  Google Scholar 

  • Ouellet V, Labbe SM, Blondin DP, Phoenix S, Guerin B, Haman F, Turcotte EE, Richard D, Carpentier AC. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545–52.

    Article  PubMed  Google Scholar 

  • Pantoja C, Huff JT, Yamamoto KR. Glucocorticoid signaling defines a novel commitment state during adipogenesis in vitro. Mol Biol Cell. 2008;19:4032–41.

    Article  PubMed  CAS  Google Scholar 

  • Park DH, Borlongan CV, Eve DJ, Sanberg PR. The emerging field of cell and tissue engineering. Med Sci Monit. 2008;14:RA206–20.

    PubMed  Google Scholar 

  • Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. 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. 2010;285:7153–64.

    Article  PubMed  CAS  Google Scholar 

  • Pfannenberg C, Werner MK, Ripkens S, Stef I, Deckert A, Schmadl M, Reimold M, Haring HU, Claussen CD, Stefan N. Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes. 2010;59:1789–93.

    Article  PubMed  CAS  Google Scholar 

  • Pisani DF, Djedaini M, Beranger GE, Elabd C, Scheideler M, Ailhaud G, Amri EZ. Differentiation of human adipose-derived stem cells into “brite” (brown-in-white) adipocytes. Front Endocrinol (Lausanne). 2011;2:87.

    CAS  Google Scholar 

  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.

    Article  PubMed  CAS  Google Scholar 

  • Poissonnet CM, Burdi AR, Garn SM. The chronology of adipose tissue appearance and distribution in the human fetus. Early Hum Dev. 1984;10:1–11.

    Article  PubMed  CAS  Google Scholar 

  • Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–4.

    Article  PubMed  CAS  Google Scholar 

  • Rehnmark S, Nechad M, Herron D, Cannon B, Nedergaard J. Alpha- and beta-adrenergic induction of the expression of the uncoupling protein thermogenin in brown adipocytes differentiated in culture. J Biol Chem. 1990;265:16464–71.

    PubMed  CAS  Google Scholar 

  • Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature. 2005;434:843–50.

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro MO, Bianco SD, Kaneshige M, Schultz JJ, Cheng SY, Bianco AC, Brent GA. Expression of uncoupling protein 1 in mouse brown adipose tissue is thyroid hormone receptor-beta isoform specific and required for adaptive thermogenesis. Endocrinology. 2010;151:432–40.

    Article  PubMed  CAS  Google Scholar 

  • Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135:240–9.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez AM, Elabd C, Amri EZ, Ailhaud G, Dani C. The human adipose tissue is a source of multipotent stem cells. Biochimie. 2005;87:125–8.

    Article  PubMed  CAS  Google Scholar 

  • Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol. 2006;7:885–96.

    Article  PubMed  CAS  Google Scholar 

  • Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev. 2000;14:1293–307.

    PubMed  CAS  Google Scholar 

  • Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science. 2000;289:950–3.

    Article  PubMed  CAS  Google Scholar 

  • Rothwell NJ, Stock MJ. Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour. Clin Sci (Lond). 1983;64:19–23.

    CAS  Google Scholar 

  • Russell TR, Ho R. Conversion of 3T3 fibroblasts into adipose cells: triggering of differentiation by prostaglandin F2alpha and 1-methyl-3-isobutyl xanthine. Proc Natl Acad Sci U S A. 1976;73:4516–20.

    Article  PubMed  CAS  Google Scholar 

  • Saltiel AR. New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell. 2001;104:517–29.

    Article  PubMed  CAS  Google Scholar 

  • Schaffler A, Buchler C. Concise review: adipose tissue-derived stromal cells–basic and clinical implications for novel cell-based therapies. Stem Cells. 2007;25:818–27.

    Article  PubMed  Google Scholar 

  • Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008;454:961–7.

    Article  PubMed  CAS  Google Scholar 

  • Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, Cohen P, Cinti S, Spiegelman BM. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest. 2011;121:96–105.

    Article  PubMed  CAS  Google Scholar 

  • Sengenes C, Lolmede K, Zakaroff-Girard A, Busse R, Bouloumie A. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J Cell Physiol. 2005;205:114–22.

    Article  PubMed  CAS  Google Scholar 

  • Sera Y, LaRue AC, Moussa O, Mehrotra M, Duncan JD, Williams CR, Nishimoto E, Schulte BA, Watson PM, Watson DK, Ogawa M. Hematopoietic stem cell origin of adipocytes. Exp Hematol. 2009;37:1108–20. 1120 e1101–1104.

    Article  PubMed  CAS  Google Scholar 

  • Skarulis MC, Celi FS, Mueller E, Zemskova M, Malek R, Hugendubler L, Cochran C, Solomon J, Chen C, Gorden P. Thyroid hormone induced brown adipose tissue and amelioration of diabetes in a patient with extreme insulin resistance. J Clin Endocrinol Metab. 2010;95:256–62.

    Article  PubMed  CAS  Google Scholar 

  • Soyka M. Rimonabant and depression. Pharmacopsychiatry. 2008;41:204–5.

    Article  PubMed  CAS  Google Scholar 

  • Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Ryden M, Frisen J, Arner P. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.

    Article  PubMed  CAS  Google Scholar 

  • Sun K, Kusminski CM, Scherer PE. Adipose tissue remodeling and obesity. J Clin Invest. 2011;121:2094–101.

    Article  PubMed  CAS  Google Scholar 

  • Tamori Y, Masugi J, Nishino N, Kasuga M. Role of peroxisome proliferator-activated receptor-gamma in maintenance of the characteristics of mature 3T3-L1 adipocytes. Diabetes. 2002;51:2045–55.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka T, Yoshida N, Kishimoto T, Akira S. Defective adipocyte differentiation in mice lacking the C/EBPbeta and/or C/EBPdelta gene. EMBO J. 1997;16:7432–43.

    Article  PubMed  CAS  Google Scholar 

  • Tang QQ, Gronborg M, Huang H, Kim JW, Otto TC, Pandey A, Lane MD. Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc Natl Acad Sci U S A. 2005;102:9766–71.

    Article  PubMed  CAS  Google Scholar 

  • Tang QQ, Lane MD. Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem. 2012;81:715–36.

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322:583–6.

    Article  PubMed  CAS  Google Scholar 

  • Tran KV, Gealekman O, Frontini A, Zingaretti MC, Morroni M, Giordano A, Smorlesi A, Perugini J, De Matteis R, Sbarbati A, Corvera S, Cinti S. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 2012;15:222–9.

    Article  PubMed  CAS  Google Scholar 

  • Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, Tran TT, Suzuki R, Espinoza DO, Yamamoto Y, Ahrens MJ, Dudley AT, Norris AW, Kulkarni RN, Kahn CR. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature. 2008;454:1000–4.

    Article  PubMed  CAS  Google Scholar 

  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500–8.

    Article  PubMed  Google Scholar 

  • Vegiopoulos A, Muller-Decker K, Strzoda D, Schmitt I, Chichelnitskiy E, Ostertag A, Berriel Diaz M, Rozman J, Hrabe de Angelis M, Nusing RM, Meyer CW, Wahli W, Klingenspor M, Herzig S. Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328:1158–61.

    Article  PubMed  CAS  Google Scholar 

  • Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–25.

    Article  PubMed  CAS  Google Scholar 

  • Walden TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J. Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues. American journal of physiology. Endocrinol Metab. 2012;302:E19–31.

    CAS  Google Scholar 

  • Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. Beige Adipocytes Are a Distinct Type of Thermogenic Fat Cell in Mouse and Human. Cell. 2012;150(2):366–76.

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Zhou YL, Erickson RL, Macdougald OA, Snead ML. Physical dissection of the CCAAT/enhancer-binding protein alpha in regulating the mouse amelogenin gene. Biochem Biophys Res Commun. 2007;354:56–61.

    Article  PubMed  CAS  Google Scholar 

  • Zhang JW, Tang QQ, Vinson C, Lane MD. Dominant-negative C/EBP disrupts mitotic clonal expansion and differentiation of 3T3-L1 preadipocytes. Proc Natl Acad Sci U S A. 2004;101:43–7.

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Qi C, Korenberg JR, Chen XN, Noya D, Rao MS, Reddy JK. Structural organization of mouse peroxisome proliferator-activated receptor gamma (mPPAR gamma) gene: alternative promoter use and different splicing yield two mPPAR gamma isoforms. Proc Natl Acad Sci U S A. 1995;92:7921–5.

    Article  PubMed  CAS  Google Scholar 

  • Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Peault B, Rubin JP, Donnenberg AD. Stromal vascular progenitors in adult human adipose tissue. Cytometry A. 2010;77:22–30.

    PubMed  Google Scholar 

  • Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, Nedergaard J, Cinti S. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009;23:3113–20.

    Article  PubMed  CAS  Google Scholar 

  • Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–28.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We apologize to our colleagues whose contributions could not be cited due to space limitations. We thank members of our lab for critically reading the manuscript and discussions. In particular, we thank Tatiana Golea for administrative and graphical support. Our work is supported by grants from the Deutsche Forschungsgemeinschaft, the European Foundation for the Study of Diabetes, the FP7 DIABAT consortium, the German Cancer Aid, and the Network Aging Research.

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Algire, C., Medrikova, D., Herzig, S. (2013). Adipose Stem Cells. In: Cao, Y. (eds) Angiogenesis in Adipose Tissue. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8069-3_2

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