Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Hormone Molecular Biology and Clinical Investigation

Editor-in-Chief: Chetrite, Gérard S.

Editorial Board Member: Alexis, Michael N. / Baniahmad, Aria / Beato, Miguel / Bouillon, Roger / Brodie, Angela / Carruba, Giuseppe / Chen, Shiuan / Cidlowski, John A. / Clarke, Robert / Coelingh Bennink, Herjan J.T. / Darbre, Philippa D. / Drouin, Jacques / Dufau, Maria L. / Edwards, Dean P. / Falany, Charles N. / Fernandez-Perez, Leandro / Ferroud, Clotilde / Feve, Bruno / Flores-Morales, Amilcar / Foster, Michelle T. / Garcia-Segura, Luis M. / Gastaldelli, Amalia / Gee, Julia M.W. / Genazzani, Andrea R. / Greene, Geoffrey L. / Groner, Bernd / Hampl, Richard / Hilakivi-Clarke, Leena / Hubalek, Michael / Iwase, Hirotaka / Jordan, V. Craig / Klocker, Helmut / Kloet, Ronald / Labrie, Fernand / Mendelson, Carole R. / Mück, Alfred O. / Nicola, Alejandro F. / O'Malley, Bert W. / Raynaud, Jean-Pierre / Ruan, Xiangyan / Russo, Jose / Saad, Farid / Sanchez, Edwin R. / Schally, Andrew V. / Schillaci, Roxana / Schindler, Adolf E. / Söderqvist, Gunnar / Speirs, Valerie / Stanczyk, Frank Z. / Starka, Luboslav / Sutter, Thomas R. / Tresguerres, Jesús A. / Wahli, Walter / Wildt, Ludwig / Yang, Kaiping / Yu, Qi

4 Issues per year


CiteScore 2016: 2.15

SCImago Journal Rank (SJR) 2015: 0.432
Source Normalized Impact per Paper (SNIP) 2015: 0.334

Online
ISSN
1868-1891
See all formats and pricing
More options …
Volume 31, Issue 2 (Sep 2017)

Issues

Critical review of beige adipocyte thermogenic activation and contribution to whole-body energy expenditure

Érique Castro
  • Department of Physiology and Biophysics, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508000, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Tiago E. Oliveira Silva
  • Department of Physiology and Biophysics, Institute of Biomedical Sciences, University of São Paulo, São Paulo 05508000, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ William T. Festuccia
  • Corresponding author
  • Department of Physiology and Biophysics, Institute of Biomedical Sciences, University of São Paulo, Av. Prof Lineu Prestes 1524, São Paulo 05508000, Brazil, Phone: +55 11 26488238, Fax: +55 11 30917285
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-09-01 | DOI: https://doi.org/10.1515/hmbci-2017-0042

Abstract

Beige (or brite, “brown in white”) adipocytes are uncoupling protein 1 (UCP1)-positive cells residing in white adipose depots that, depending on the conditions, behave either as classic white adipocytes, storing energy as lipids, or as brown adipocytes, dissipating energy from oxidative metabolism as heat through non-shivering thermogenesis. Because of their thermogenic potential and, therefore, possible usage to treat metabolic diseases such as obesity and type 2 diabetes, beige cells have attracted the attention of many scientists worldwide aiming to develop strategies to safely recruit and activate their thermogenic activity. Indeed, in recent years, a large variety of conditions, molecules (including nutrients) and signaling pathways were reported to promote the recruitment of beige adipocytes. Despite of those advances, the true contribution of beige adipocyte thermogenesis to whole-body energy expenditure is still not completely defined. Herein, we discuss some important aspects that should be considered when studying beige adipocyte biology and the contribution to energy balance and whole-body metabolism.

Keywords: beige adipocyte; browning; lipolysis; macrophages; sympathetic innervation; thermogenesis; UCP1

References

  • [1]

    Hall KD, Heymsfield SB, Kemnitz JW, Klein S, Schoeller DA, Speakman JR. Energy balance and its components: implications for body weight regulation. Am J Clin Nutr. 2012;95:989–94.CrossrefGoogle Scholar

  • [2]

    RosenED, SpiegelmanBM. What we talk about when we talk about fat. Cell. 2014;156:20–44.CrossrefGoogle Scholar

  • [3]

    KuryszkoJ, SławutaP, SapikowskiG. Secretory function of adipose tissue. Pol J Vet Sci. 2016;19:441–6.Google Scholar

  • [4]

    IshibashiJ, SealeP. Medicine. Beige can be slimming. Science. 2010;328:1113–4.CrossrefGoogle Scholar

  • [5]

    WuJ, BoströmP, SparksLM, YeL, ChoiJH, GiangAH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150:366–76.CrossrefGoogle Scholar

  • [6]

    PetrovicN, WaldenTB, ShabalinaIG, TimmonsJA, CannonB, NedergaardJ. Chronic peroxisome proliferator-activated receptor γ (PPARγ) 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.CrossrefGoogle Scholar

  • [7]

    WaldénTB, HansenIR, TimmonsJA, CannonB, NedergaardJ. Recruited vs. nonrecruited molecular signatures of brown, “brite,” and white adipose tissues. Am J Physiol Endocrinol Metab. 2012;302:E19–31.CrossrefGoogle Scholar

  • [8]

    LeeY-H, PetkovaAP, MottilloEP, GrannemanJG. In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab. 2012;15:480–91.CrossrefGoogle Scholar

  • [9]

    ShabalinaI, PetrovicN, deJongJA, KalinovichA, CannonB, NedergaardJ. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 2013;5:1196–203.CrossrefGoogle Scholar

  • [10]

    BartesaghiS, HallenS, HuangL, SvenssonP-A, MomoRA, WallinS, et al. Thermogenic activity of UCP1 in human white fat-derived beige adipocytes. Mol Endocrinol. 2015;29:130–9.CrossrefGoogle Scholar

  • [11]

    HemsDA, RathEA, VerrinderTR. Fatty acid synthesis in liver and adipose tissue of normal and genetically obese (ob/ob) mice during the 24-hour cycle. Biochem J. 1975;150:167–73.CrossrefGoogle Scholar

  • [12]

    YoungP, ArchJR, AshwellM. Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett. 1984;167:10–4.CrossrefGoogle Scholar

  • [13]

    JankovicA, GolicI, MarkelicM, StancicA, OtasevicV, BuzadzicB, et al. Two key temporally distinguishable molecular and cellular components of white adipose tissue browning during cold acclimation. J Physiol. 2015;593:3267–80.CrossrefGoogle Scholar

  • [14]

    CintiS. Transdifferentiation properties of adipocytes in the adipose organ. AJP Endocrinol Metab. 2009;297:E977–86.CrossrefGoogle Scholar

  • [15]

    BarbatelliG, MuranoI, MadsenL, HaoQ, JimenezM, KristiansenK, et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. AJP Endocrinol Metab. 2010;298:E1244–53.CrossrefGoogle Scholar

  • [16]

    WangQA, TaoC, GuptaRK, SchererPE. Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat Med. 2013;19:1338–44.CrossrefGoogle Scholar

  • [17]

    LeeP, WernerC, KebebewE, CeliF. Functional thermogenic beige adipogenesis is inducible in human neck fat. Int J Obes. 2013;38:170–6.CrossrefGoogle Scholar

  • [18]

    VitaliA, MuranoI, ZingarettiMC, FrontiniA, RicquierD, CintiS. The adipose organ of obesity-prone C57BL/6J mice is composed of mixed white and brown adipocytes. J Lipid Res. 2012;53:619–29.CrossrefGoogle Scholar

  • [19]

    BoströmP, WuJ, JedrychowskiMP, KordeA, YeL, LoJC, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463–8.CrossrefGoogle Scholar

  • [20]

    PatsourisD, QiP, AbdullahiA, StanojcicM, ChenP, ParousisA, et al. Burn induces browning of the subcutaneous white adipose tissue in mice and humans. Cell Rep. 2015;13:1538–44.CrossrefGoogle Scholar

  • [21]

    SidossisLS, PorterC, SarafMK, BørsheimE, RadhakrishnanRS, ChaoT, et al. Browning of subcutaneous white adipose tissue in humans after severe adrenergic stress. Cell Metab. 2015;22:219–27.CrossrefGoogle Scholar

  • [22]

    PetruzzelliM, SchweigerM, SchreiberR, Campos-OlivasR, TsoliM, AllenJ, et al. A switch from white to brown fat increases energy expenditure in cancer-associated cachexia. Cell Metab. 2014;20:433–47.CrossrefGoogle Scholar

  • [23]

    KirS, WhiteJP, KleinerS, KazakL, CohenP, BaracosVE, et al. Tumour-derived PTH-related protein triggers adipose tissue browning and cancer cachexia. Nature. 2014;513:100–4.CrossrefGoogle Scholar

  • [24]

    VergnesL, DaviesGR, LinJY, YehMW, LivhitsMJ, HarariA, et al. Adipocyte browning and higher mitochondrial function in periadrenal but not SC fat in pheochromocytoma. J Clin Endocrinol Metab. 2016;101:4440–8.CrossrefGoogle Scholar

  • [25]

    GnadT, ScheiblerS, von KügelgenI, ScheeleC, KilićA, GlödeA, et al. Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors. Nature. 2014;516:395–9.CrossrefGoogle Scholar

  • [26]

    HuiX, GuP, ZhangJ, NieT, PanY, WuD, et al. Adiponectin enhances cold-induced browning of subcutaneous adipose tissue via promoting M2 macrophage proliferation. Cell Metab. 2015;22:279–90.CrossrefGoogle Scholar

  • [27]

    BordicchiaM, LiuD, AmriEZ, AilhaudG, Dessì-FulgheriP, ZhangC, et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest. 2012;122:1022–36.CrossrefGoogle Scholar

  • [28]

    BrestoffJR, KimBS, SaenzSA, StineRR, MonticelliLA, SonnenbergGF, et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature. 2014;519:242–6.CrossrefGoogle Scholar

  • [29]

    QiuY, NguyenKD, OdegaardJI, CuiX, TianX, LocksleyRM, et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell. 2014;157:1292–308.CrossrefGoogle Scholar

  • [30]

    CoskunT, BinaHA, SchneiderMA, DunbarJD, HuCC, ChenY, et al. Fibroblast growth factor 21 corrects obesity in mice. Endocrinology. 2008;149:6018–27.CrossrefGoogle Scholar

  • [31]

    FisherFM, KleinerS, DourisN, FoxEC, MepaniRJ, VerdeguerF, et al. FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 2012;26:271–81.CrossrefGoogle Scholar

  • [32]

    LeeP, LindermanJD, SmithS, BrychtaRJ, WangJ, IdelsonC, et al. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab. 2014;19:302–9.CrossrefGoogle Scholar

  • [33]

    NguyenKD, QiuY, CuiX, GohYP, MwangiJ, DavidT, et al. Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature. 2011;480:104–8.CrossrefGoogle Scholar

  • [34]

    LeeMW, OdegaardJI, MukundanL, QiuY, MolofskyAB, NussbaumJC, et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell. 2015;160:74–87.CrossrefGoogle Scholar

  • [35]

    LynchL, HoganAE, DuquetteD, LesterC, BanksA, LeClairK, et al. iNKT cells induce FGF21 for thermogenesis and are required for maximal weight loss in GLP1 therapy. Cell Metab. 2016;24:510–9.CrossrefGoogle Scholar

  • [36]

    Suárez-ZamoranoN, FabbianoS, ChevalierC, StojanovićO, ColinDJ, StevanovićA, et al. Microbiota depletion promotes browning of white adipose tissue and reduces obesity. Nat Med. 2015;21:1497–501.CrossrefGoogle Scholar

  • [37]

    LeeJ-Y, TakahashiN, YasubuchiM, KimY-I, HashizakiH, KimM-J, et al. Triiodothyronine induces UCP-1 expression and mitochondrial biogenesis in human adipocytes. Am J Physiol Cell Physiol. 2012;302:C463–72.CrossrefGoogle Scholar

  • [38]

    Himms-HagenJ, MelnykA, ZingarettiMC, CeresiE, BarbatelliG, CintiS. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol. 2000;279:C670–81.Google Scholar

  • [39]

    RachidTL, Penna-de-CarvalhoA, BringhentiI, AguilaMB, Mandarim-de-LacerdaCA, Souza-MelloV. Fenofibrate (PPARalpha agonist) induces beige cell formation in subcutaneous white adipose tissue from diet-induced male obese mice. Mol Cell Endocrinol. 2015;402:86–94.CrossrefGoogle Scholar

  • [40]

    SellH, BergerJP, SamsonP, CastriotaG, LalondeJ, DeshaiesY, et al. Peroxisome proliferator-activated receptor γ agonism increases the capacity for sympathetically mediated thermogenesis in lean and ob/ob mice. Endocrinology. 2004;145:3925–34.CrossrefGoogle Scholar

  • [41]

    FukuiY, MasuiS, OsadaS, UmesonoK, MotojimaK. A new thiazolidinedione, NC-2100, which is a weak PPAR-gamma activator, exhibits potent antidiabetic effects and induces uncoupling protein 1 in white adipose tissue of KKAy obese mice. Diabetes. 2000;49:759–67.CrossrefGoogle Scholar

  • [42]

    CoelhoMS, de LimaCL, RoyerC, SilvaJB, OliveiraFC, ChristCG, et al. GQ-16, a TZD-derived partial PPARγ agonist, induces the expression of thermogenesis-related genes in brown fat and visceral white fat and decreases visceral adiposity in obese and hyperglycemic mice. PLoS One. 2016;11:e0154310.CrossrefGoogle Scholar

  • [43]

    BaskaranP, KrishnanV, RenJ, ThyagarajanB. Capsaicin induces browning of white adipose tissue and counters obesity by activating TRPV1 channel-dependent mechanisms. Br J Pharmacol. 2016;173:2369–89.CrossrefGoogle Scholar

  • [44]

    OhyamaK, NogusaY, ShinodaK, SuzukiK, BannaiM, KajimuraS. A synergistic antiobesity effect by a combination of capsinoids and cold temperature through promoting beige adipocyte biogenesis. Diabetes. 2016;65:1410–23.CrossrefGoogle Scholar

  • [45]

    ShenW, BaldwinJ, CollinsB, HixsonL, LeeK-T, HerbergT, et al. Low level of trans-10, cis-12 conjugated linoleic acid decreases adiposity and increases browning independent of inflammatory signaling in overweight Sv129 mice. J Nutr Biochem. 2015;26:616–25.CrossrefGoogle Scholar

  • [46]

    KimM, GotoT, YuR, UchidaK, TominagaM, KanoY, et al. Fish oil intake induces UCP1 upregulation in brown and white adipose tissue via the sympathetic nervous system. Sci Rep. 2016;5:18013.CrossrefGoogle Scholar

  • [47]

    LiQ, WangK, MaY, QinC, DongC, JinP, et al. Resveratrol derivative BTM-0512 mitigates obesity by promoting beige remodeling of subcutaneous preadipocytes. Acta Biochim Biophys Sin (Shanghai). 2017;49:318–27.CrossrefGoogle Scholar

  • [48]

    MercaderJ, RibotJ, MuranoI, FelipeF, CintiS, BonetML, et al. Remodeling of white adipose tissue after retinoic acid administration in mice. Endocrinology. 2006;147:5325–32.CrossrefGoogle Scholar

  • [49]

    MercaderJ, PalouA, Luisa BonetM. Induction of uncoupling protein-1 in mouse embryonic fibroblast-derived adipocytes by retinoic acid. Obesity. 2010;18:655–62.CrossrefGoogle Scholar

  • [50]

    ZhaoS, MugaboY, BallentineG, AttaneC, IglesiasJ, PoursharifiP, et al. α/β-Hydrolase domain 6 deletion induces adipose browning and prevents obesity and type 2 diabetes. Cell Rep. 2016;14:2872–88.CrossrefGoogle Scholar

  • [51]

    ShahidM, JavedAA, ChandraD, RamseyHE, ShahD, KhanMF, et al. IEX-1 deficiency induces browning of white adipose tissue and resists diet-induced obesity. Sci Rep. 2016;6:24135.CrossrefGoogle Scholar

  • [52]

    KarbienerM, PisaniDF, FrontiniA, OberreiterLM, LangE, VegiopoulosA, et al. MicroRNA-26 family is required for human adipogenesis and drives characteristics of brown adipocytes. Stem Cells. 2014;32:1578–90.CrossrefGoogle Scholar

  • [53]

    HuF, WangM, XiaoT, YinB, HeL, MengW, et al. MiR-30 promotes thermogenesis and the development of beige fat by targeting RIP140. Diabetes. 2015;64:2056–68.CrossrefGoogle Scholar

  • [54]

    MoriM, NakagamiH, Rodriguez-AraujoG, NimuraK, KanedaY. Essential role for miR-196a in brown adipogenesis of white fat progenitor cells. PLoS Biol. 2012;10:e1001314.CrossrefGoogle Scholar

  • [55]

    MagdalonJ, ChiminP, BelchiorT, NevesRX, Vieira-LaraMA, AndradeML, et al. Constitutive adipocyte mTORC1 activation enhances mitochondrial activity and reduces visceral adiposity in mice. Biochim Biophys Acta. 2016;1861:430–8.CrossrefGoogle Scholar

  • [56]

    LiuD, BordicchiaM, ZhangC, FangH, WeiW, LiJ-L, et al. Activation of mTORC1 is essential for β-adrenergic stimulation of adipose browning. J Clin Invest. 2016;126:1704–16.CrossrefGoogle Scholar

  • [57]

    SealeP, ConroeHM, EstallJ, KajimuraS, FrontiniA, IshibashiJ, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest. 2011;121:96–105.CrossrefGoogle Scholar

  • [58]

    YadavH, QuijanoC, KamarajuAK, GavrilovaO, MalekR, ChenW, et al. Protection from obesity and diabetes by blockade of TGF-β/Smad3 signaling. Cell Metab. 2011;14:67–79.CrossrefGoogle Scholar

  • [59]

    CanoonB, NedergaardJ. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277–359.CrossrefGoogle Scholar

  • [60]

    LassA, ZimmermannR, HaemmerleG, RiedererM, SchoiswohlG, SchweigerM, et al. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in chanarin-dorfman syndrome. Cell Metab. 2006;3:309–19.CrossrefGoogle Scholar

  • [61]

    GrannemanJG, MooreH-P, KrishnamoorthyR, RathodM. Perilipin controls lipolysis by regulating the interactions of AB-hydrolase containing 5 (Abhd5) and adipose triglyceride lipase (Atgl). J Biol Chem. 2009;284:34538–44.CrossrefGoogle Scholar

  • [62]

    FestucciaWT, Guerra-SáR, KawashitaNH, GarófaloMA, EvangelistaEA, RodriguesV, et al. Expression of glycerokinase in brown adipose tissue is stimulated by the sympathetic nervous system. Am J Physiol. 2003;284:R1536–41.Google Scholar

  • [63]

    RialE, PoustieA, NichollsDG. Brown-adipose-tissue mitochondria: the regulation of the 32 000-Mr uncoupling protein by fatty acids and purine nucleotides. Eur J Biochem. 1983;137:197–203.CrossrefGoogle Scholar

  • [64]

    AhmadianM, AbbottMJ, TangT, HudakCS, KimY, BrussM, et al. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 2011;13:739–48.CrossrefGoogle Scholar

  • [65]

    SchoiswohlG, Stefanovic-RacicM, MenkeMN, WillsRC, SurlowBA, BasantaniMK, et al. Impact of reduced ATGL-mediated adipocyte lipolysis on obesity-associated insulin resistance and inflammation in male mice. Endocrinology. 2015;156:3610–24.CrossrefGoogle Scholar

  • [66]

    MiyoshiH, SouzaSC, ZhangH-H, StrisselKJ, ChristoffoleteMA, KovsanJ, et al. Perilipin promotes hormone-sensitive lipase-mediated adipocyte lipolysis via phosphorylation-dependent and -independent mechanisms. J Biol Chem. 2006;281:15837–44.CrossrefGoogle Scholar

  • [67]

    MouraMA, FestucciaWT, KawashitaNH, GarófaloMA, BritoSR, KettelhutIC, et al. Brown adipose tissue glyceroneogenesis is activated in rats exposed to cold. Pflugers Arch Eur J Physiol. 2005;449:463–9.CrossrefGoogle Scholar

  • [68]

    ChavesVE, FrassonD, GarófaloMA, NavegantesLC, MiglioriniRH, KettelhutIC. Increased glyceride–glycerol synthesis in liver and brown adipose tissue of rat: in-vivo contribution of glycolysis and glyceroneogenesis. Lipids. 2012;47:773–80.CrossrefGoogle Scholar

  • [69]

    BarteltA, WeigeltC, CherradiML, NiemeierA, TödterK, HeerenJ, et al. Effects of adipocyte lipoprotein lipase on de novo lipogenesis and white adipose tissue browning. Biochim Biophys Acta. 2013;1831:934–42.CrossrefGoogle Scholar

  • [70]

    FestucciaWT, BlanchardP-G, DeshaiesY. Control of brown adipose tissue glucose and lipid metabolism by PPAR?. Front Endocrinol (Lausanne). 2011;2:1–6.Google Scholar

  • [71]

    MatthiasA, OhlsonKB, FredrikssonJM, JacobssonA, NedergaardJ, CannonB. Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. J Biol Chem. 2000;275:25073–81.CrossrefGoogle Scholar

  • [72]

    JiaR, LuoX-Q, WangG, LinC-X, QiaoH, WangN, et al. Characterization of cold-induced remodelling reveals depot-specific differences across and within brown and white adipose tissues in mice. Acta Physiol. 2016;217:311–24.CrossrefGoogle Scholar

  • [73]

    FerranniniG, NamwanjeM, FangB, DamleM, LiD, LiuQ, et al. Genetic backgrounds determine brown remodeling of white fat in rodents. Mol Metab. 2016;5:948–58.CrossrefGoogle Scholar

  • [74]

    HausmanDB, DiGirolamoM, BartnessTJ, HausmanGJ, MartinRJ. The biology of white adipocyte proliferation. Obes Rev. 2001;2:239–54.CrossrefGoogle Scholar

  • [75]

    BritoNA, BritoMN, BartnessTJ. Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. AJP Regul Integr Comp Physiol. 2008;294:R1445–52.CrossrefGoogle Scholar

  • [76]

    GarofaloMA, KettelhutIC, RoselinoJE, MiglioriniRH. Effect of acute cold exposure on norepinephrine turnover rates in rat white adipose tissue. J Auton Nerv Syst. 1996;60:206–8.CrossrefGoogle Scholar

  • [77]

    FestucciaWT, BlanchardP-G, RichardD, DeshaiesY. Basal adrenergic tone is required for maximal stimulation of rat brown adipose tissue UCP1 expression by chronic PPAR-gamma activation. Am J Physiol Regul Integr Comp Physiol. 2010;299:R159–67.CrossrefGoogle Scholar

  • [78]

    DenjeanF, LachuerJ, GéloënA, Cohen-AdadF, MoulinC, BarréH, et al. Differential regulation of uncoupling protein-1, -2 and -3 gene expression by sympathetic innervation in brown adipose tissue of thermoneutral or cold-exposed rats. FEBS Lett. 1999;444:181–5.CrossrefGoogle Scholar

  • [79]

    BowersRR. Sympathetic innervation of white adipose tissue and its regulation of fat cell number. AJP Regul Integr Comp Physiol. 2004;286:R1167–75.CrossrefGoogle Scholar

  • [80]

    AtgiéC, D’AllaireF, BukowieckiLJ. Role of beta1- and beta3-adrenoceptors in the regulation of lipolysis and thermogenesis in rat brown adipocytes. Am J Physiol. 1997;273:C1136–42.Google Scholar

  • [81]

    FlierlMA, RittirschD, NadeauBA, ChenAJ, SarmaJV, ZetouneFS, et al. Phagocyte-derived catecholamines enhance acute inflammatory injury. Nature. 2007;449:721–5.CrossrefGoogle Scholar

  • [82]

    FischerK, RuizHH, JhunK, FinanB, OberlinDJ, van der HeideV, et al. Alternatively activated macrophages do not synthesize catecholamines or contribute to adipose tissue adaptive thermogenesis. Nat Med. 2017;23:623–30.CrossrefGoogle Scholar

  • [83]

    BurkeyBF, DongM, GagenK, EckhardtM, DragonasN, ChenW, et al. Effects of pioglitazone on promoting energy storage, not expenditure, in brown adipose tissue of obese fa/fa zucker rats: comparison to CL 316,243. Metabolism. 2000;49:1301–8.CrossrefGoogle Scholar

  • [84]

    RongJX, QiuY, HansenMK, ZhuL, ZhangV, XieM, et al. Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes. 2007;56:1751–60.CrossrefGoogle Scholar

  • [85]

    FestucciaWT, OztezcanS, LaplanteM, BerthiaumeM, MichelC, DohguS, et al. Peroxisome proliferator-activated receptor-γ-mediated positive energy balance in the rat is associated with reduced sympathetic drive to adipose tissues and thyroid status. Endocrinology. 2008;149:2121–30.CrossrefGoogle Scholar

  • [86]

    LiY-L, LiX, JiangT-T, FanJ-M, ZhengX-L, ShiX-E, et al. An additive effect of promoting thermogenic gene expression in mice adipose-derived stromal vascular cells by combination of rosiglitazone and CL316,243. Int J Mol Sci. 2017;18:1002.CrossrefGoogle Scholar

  • [87]

    McElroyJF, WadeGN. Short photoperiod stimulates brown adipose tissue growth and thermogenesis but not norepinephrine turnover in Syrian hamsters. Physiol Behav. 1986;37:307–11.CrossrefGoogle Scholar

  • [88]

    SigurdsonSL, Himms-HagenJ. Control of norepinephrine turnover in brown adipose tissue of Syrian hamsters. Am J Physiol. 1988;254:R960–68.Google Scholar

  • [89]

    GriggioMA. The participation of shivering and nonshivering thermogenesis in warm and cold-acclimated rats. Comp Biochem Physiol Part A Physiol. 1982;73:481–4.CrossrefGoogle Scholar

  • [90]

    KalinovichAV, de JongJM, CannonB, NedergaardJ. UCP1 in adipose tissues: two steps to full browning. Biochimie. 2017;134:127–37.CrossrefGoogle Scholar

About the article

Received: 2017-06-13

Accepted: 2017-07-17

Published Online: 2017-09-01


Author Statement

Research funding: This work was supported by grants from São Paulo Research Foundation (FAPESP #2015/19530-5) and National Counsel of Science and Technology Development (CNPq #443492/2014-0) to WTF. EC and TEO are recipients of FAPESP fellowships (#2016/23169-9 and 2016/07062-0, respectively).

Conflict of interest: The authors state no conflict of interest.

Informed consent: Informed consent is not applicable.

Ethical approval: The conducted research is not related to either human or animal use.


Citation Information: Hormone Molecular Biology and Clinical Investigation, ISSN (Online) 1868-1891, DOI: https://doi.org/10.1515/hmbci-2017-0042.

Export Citation

©2017 Walter de Gruyter GmbH, Berlin/Boston. Copyright Clearance Center

Comments (0)

Please log in or register to comment.
Log in