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Research Article

Between brown and white: Novel aspects of adipocyte differentiation

Pages 104-115 | Received 04 Aug 2010, Accepted 21 Oct 2010, Published online: 24 Jan 2011

References

  • Friedman JM. Leptin at 14 y of age: an ongoing story. Am J Clin Nutr. 2009;89:973S–9S.
  • Matsuzawa Y. Adiponectin: a key player in obesity related disorders. Curr Pharm Des. 2010;16:1896–901.
  • Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, . Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med. 1995;1:1155–61.
  • Greenberg AS, Egan JJ, Wek SA, Garty NB, Blanchette-Mackie EJ, Londos C. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J Biol Chem. 1991; 266:11341–6.
  • Cinti S, Cigolini M, Bosello O, Bjorntorp P. A morphological study of the adipocyte precursor. J Submicrosc Cytol. 1984;16:243–51.
  • Cinti S, Cigolini M, Gazzanelli G, Bosello O. An ultrastructural study of adipocyte precursors from epididymal fat pads of adult rats in culture. J Submicrosc Cytol. 1985;17:631–6.
  • Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, . White fat progenitor cells reside in the adipose vasculature. Science. 2008;322:583–6.
  • Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135:240–9.
  • Cinti S, Cigolini M, Morroni M, Zingaretti MC. S-100 protein in white preadipocytes: an immunoelectronmicroscopic study. Anat Rec. 1989;224:466–72.
  • Cinti S. The adipose organ. Milan: Kurtis; 1999.
  • Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, . Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr. 2009;90:1579–85.
  • Kushlan JA. The evolution of hairlessness in man. The American Naturalist. 1980;116:727–9.
  • Lean J, James P. Brown adipose tissue in man. Trayhurn P, Nicholls DG, Brown adipose tissue. Edward Arnold; London. 1986. 339–65.
  • Ricquier D. Molecular biology of brown adipose tissue. Proc Nutr Soc. 1989;48:183–7.
  • Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277–359.
  • Cinti S, Zancanaro C, Sbarbati A, Cicolini M, Vogel P, Ricquier D, . Immunoelectron microscopical identification of the uncoupling protein in brown adipose tissue mitochondria. Biol Cell. 1989;67:359–62.
  • Rial E, Gonzalez-Barroso MM. Physiological regulation of the transport activity in the uncoupling proteins UCP1 and UCP2. Biochim Biophys Acta. 2001;1504:70–81.
  • Casteilla L, Muzzin P, Revelli JP, Ricquier D, Giacobino JP. Expression of beta 1- and beta 3-adrenergic-receptor messages and adenylate cyclase beta-adrenergic response in bovine perirenal adipose tissue during its transformation from brown into white fat. Biochem J. 1994;297 (Pt 1):93–7.
  • Collins S, Surwit RS. The beta-adrenergic receptors and the control of adipose tissue metabolism and thermogenesis. Recent Prog Horm Res. 2001;56:309–28.
  • Cinti S, Cancello R, Zingaretti MC, Ceresi E, De Matteis R, Giordano A, . CL316,243 and cold stress induce heterogeneous expression of UCP1 mRNA and protein in rodent brown adipocytes. J Histochem Cytochem. 2002; 50:21–31.
  • Barbatelli G, Morroni M, Vinesi P, Cinti S, Michetti F. S-100 protein in rat brown adipose tissue under different functional conditions: a morphological, immunocytochemical, and immunochemical study. Exp Cell Res. 1993;208:226–31.
  • Cinti S, Frederich RC, Zingaretti MC, De Matteis R, Flier JS, Lowell BB. Immunohistochemical localization of leptin and uncoupling protein in white and brown adipose tissue. Endocrinology. 1997;138:797–804.
  • Cancello R, Zingaretti MC, Sarzani R, Ricquier D, Cinti S. Leptin and UCP1 genes are reciprocally regulated in brown adipose tissue. Endocrinology. 1998;139:4747–50.
  • Bachman ES, Dhillon H, Zhang CY, Cinti S, Bianco AC, Kobilka BK, . betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science. 2002;297: 843–5.
  • Timmons JA, Wennmalm K, Larsson O, Walden TB, Lassmann T, Petrovic N, . Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc Natl Acad Sci U S A. 2007; 104:4401–6.
  • Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, . PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008;454:961–7.
  • Cinti S, Morroni M. Brown adipocyte precursor cells: a morphological study. Ital J Anat Embryol. 1995;100 Suppl 1:75–81.
  • Cinti S. The adipose organ. Prostaglandins Leukot Essent Fatty Acids. 2005;73:9–15.
  • Giordano A, Frontini A, Cinti S. Adipose organ nerves revealed by immunohistochemistry. Methods Mol Biol. 2008;456:83–95.
  • Giordano A, Frontini A, Murano I, Tonello C, Marino MA, Carruba MO, . Regional-dependent increase of sympathetic innervation in rat white adipose tissue during prolonged fasting. J Histochem Cytochem. 2005;53:679–87.
  • Bartness TJ. Dual innervation of white adipose tissue: some evidence for parasympathetic nervous system involvement. J Clin Invest. 2002;110:1235–7.
  • Bartness TJ, Bamshad M. Innervation of mammalian white adipose tissue: implications for the regulation of total body fat. Am J Physiol. 1998;275(5 Pt 2):R1399–411.
  • Bartness TJ, Song CK. Thematic review series: adipocyte biology. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res. 2007;48:1655–72.
  • Demas GE, Bartness TJ. Direct innervation of white fat and adrenal medullary catecholamines mediate photoperiodic changes in body fat. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1499–505.
  • Murano I, Barbatelli G, Giordano A, Cinti S. Noradrenergic parenchymal nerve fiber branching after cold acclimatisation correlates with brown adipocyte density in mouse adipose organ. J Anat. 2009;214:171–8.
  • Murano I, Zingaretti CM, Cinti S. The adipose organ of Sv129 mice contains a prevalence of brown adipocytes and shows plasticity after cold exposure. Adipocytes. 2005;1: 121–30.
  • 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.
  • Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, . Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360: 1509–17.
  • van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, . Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500–8.
  • Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, . Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–25.
  • Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, . 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.
  • Manieri M, Murano I, Fianchini A, Brunelli A, Cinti S. Morphological and immunohistochemical features of brown adipocytes and preadipocytes in a case of human hibernoma. Nutr Metab Cardiovasc Dis. 2010;20:567–74.
  • Boiani R, Cinti S, Savage DB, Vidal-Puig A, O'Rahilly S. Abdominal subcutaneous adipose tissue morphology in a patient with a dominant-negative mutation (P467L) in the nuclear receptor peroxisome proliferator-activated receptor-gamma (PPARG) gene. Nutr Metab Cardiovasc Dis. 2010;20:e11–2.
  • Kuji I, Imabayashi E, Minagawa A, Matsuda H, Miyauchi T. Brown adipose tissue demonstrating intense FDG uptake in a patient with mediastinal pheochromocytoma. Ann Nucl Med. 2008;22:231–5.
  • Ricquier D, Mory G, Nechad M, Combes-George M, Thibault J. Development and activation of brown fat in rats with pheochromocytoma PC 12 tumors. Am J Physiol. 1983;245:C172–7.
  • Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, . High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526–31.
  • Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281:31–5.
  • Lowell BB, S-Susulic V, Hamann A, Lawitts JA, Himms-Hagen J, Boyer BB, . Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature. 1993;366:740–2.
  • Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203–9.
  • Guerra C, Navarro P, Valverde AM, Arribas M, Bruning J, Kozak LP, . Brown adipose tissue-specific insulin receptor knockout shows diabetic phenotype without insulin resistance. J Clin Invest. 2001;108:1205–13.
  • Guerra C, Koza RA, Yamashita H, Walsh K, Kozak LP. Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J Clin Invest. 1998;102:412–20.
  • Almind K, Manieri M, Sivitz WI, Cinti S, Kahn CR. 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. 2007;104:2366–71.
  • Kopecky J, Clarke G, Enerback S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest. 1995;96:2914–23.
  • Tosh D, Slack JM. How cells change their phenotype. Nat Rev Mol Cell Biol. 2002;3:187–94.
  • Cinti S. The adipose organ: morphological perspectives of adipose tissues. Proc Nutr Soc. 2001;60:319–28.
  • Cinti S. Adipocyte differentiation and transdifferentiation: plasticity of the adipose organ. J Endocrinol Invest. 2002;25:823–35.
  • Granneman JG, Li P, Zhu Z, Lu Y. Metabolic and cellular plasticity in white adipose tissue I: effects of beta3-adrenergic receptor activation. Am J Physiol Endocrinol Metab. 2005;289:E608–16.
  • Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol. 2000;279:C670–81.
  • Cypess AM, Kahn CR. Brown fat as a therapy for obesity and diabetes. Curr Opin Endocrinol Diabetes Obes. 2010;17:143–9.
  • Enerback S. Human brown adipose tissue. Cell Metab. 2010;11:248–52.
  • Morroni M, Giordano A, Zingaretti MC, Boiani R, De Matteis R, Kahn BB, . Reversible transdifferentiation of secretory epithelial cells into adipocytes in the mammary gland. Proc Natl Acad Sci U S A. 2004;101:16801–6.
  • De Matteis R, Zingaretti MC, Murano I, Vitali A, Frontini A, Giannulis I, . In vivo physiological transdifferentiation of adult adipose cells. Stem Cells. 2009;27:2761–8.
  • Barbatelli G, Murano I, Madsen L, Hao Q, Jimenez M, Kristiansen K, . 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.
  • 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. 2009;285:7153–64.
  • Seale P, Kajimura S, Spiegelman BM. Transcriptional control of brown adipocyte development and physiological function—of mice and men. Genes Dev. 2009;23:788–97.
  • Atit R, Sgaier SK, Mohamed OA, Taketo MM, Dufort D, Joyner AL, . Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev Biol. 2006;296:164–76.
  • Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112: 1796–808.
  • Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, . Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest. 2003;112:1821–30.
  • Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, . Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res. 2005;46:2347–55.
  • Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, . Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.
  • Arner P, Spalding KL. Fat cell turnover in humans. Biochem Biophys Res Commun. 2010;396:101–4.
  • Hoffstedt J, Arner E, Wahrenberg H, Andersson DP, Qvisth V, Lofgren P, . Regional impact of adipose tissue morphology on the metabolic profile in morbid obesity. Diabetologia. 2010;53(12):2496–503.
  • Bjorntorp P. Metabolic abnormalities in visceral obesity. Ann Med. 1992;24:3–5.
  • Murano I, Barbatelli G, Parisani V, Latini C, Muzzonigro G, Castellucci M, . Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J Lipid Res. 2008;49:1562–8.
  • Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW 2nd, Defuria J, Jick Z, . Adipocyte death, adipose tissue remodeling and obesity complications. Diabetes. 2007;56: 2910–8.
  • Cancello R, Tordjman J, Poitou C, Guilhem G, Bouillot JL, Hugol D, . Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes. 2006;55: 1554–61.
  • Johnson PR, Hirsch J. Cellularity of adipose depots in six strains of genetically obese mice. J Lipid Res. 1972;13: 2–11.
  • Sacks HS, Fain JN, Holman B, Cheema P, Chary A, Parks F, . Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat. J Clin Endocrinol Metab. 2009;94:3611–5.
  • Rubino F, Marescaux J. Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg. 2004;239:1–11.
  • Rubino F, R'Bibo SL, del Genio F, Mazumdar M, McGraw TE. Metabolic surgery: the role of the gastrointestinal tract in diabetes mellitus. Nat Rev Endocrinol. 2010;6:102–9.
  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444: 1027–31.
  • Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, . Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut. 2009; 58:1091–103.
  • Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, . Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature. 2010;463:540–4.
  • Rangel-Moreno J, Moyron-Quiroz JE, Carragher DM, Kusser K, Hartson L, Moquin A, . Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity. 2009;30:731–43.
  • Shimotsuma M, Shields JW, Simpson-Morgan MW, Sakuyama A, Shirasu M, Hagiwara A, . Morpho-physiological function and role of omental milky spots as omentum-associated lymphoid tissue (OALT) in the peritoneal cavity. Lymphology. 1993;26:90–101.
  • Virtue S, Vidal-Puig A. Adipose tissue expandability, lipotoxicity and the metabolic syndrome—an allostatic perspective. Biochim Biophys Acta. 2010;1801:338–49.
  • Marchesini G, Marzocchi R, Agostini F, Bugianesi E. Nonalcoholic fatty liver disease and the metabolic syndrome. Curr Opin Lipidol. 2005;16:421–7.
  • Trayhurn P, Wang B, Wood IS. Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity? Br J Nutr. 2008;100:227–35.
  • Seale P, Kajimura S, Yang W, Chin S, Rohas LM, Uldry M, . Transcriptional control of brown fat determination by PRDM16. Cell Metab. 2007;6:38–54.
  • Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM, . New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature. 2008;454:1000–4.
  • Mercader J, Ribot J, Murano I, Feddersen S, Cinti S, Madsen L, . Haploinsufficiency of the retinoblastoma protein gene reduces diet-induced obesity, insulin resistance, and hepatosteatosis in mice. Am J Physiol Endocrinol Metab. 2009;297:E184–93.
  • Madsen L, Pedersen LM, Lillefosse HH, Fjaere E, Bronstad I, Hao Q, . UCP1 induction during recruitment of brown adipocytes in white adipose tissue is dependent on cyclooxygenase activity. PLoS One. 2010;5:e11391.
  • Vegiopoulos A, Muller-Decker K, Strzoda D, Schmitt I, Chichelnitskiy E, Ostertag A, . Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328:1158–61.

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