Skip to main content
SpringerLink
Log in

Brown Adipokines

  • Chapter
  • First Online:
Brown Adipose Tissue

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 251))

Abstract

Brown adipokines are regulatory factors secreted by brown and beige adipocytes that exhibit endocrine, paracrine, and autocrine actions. Peptidic and non-peptidic molecules, including miRNAs and lipids, are constituents of brown adipokines. Brown adipose tissue remodeling to meet thermogenic needs is dependent on the secretory properties of brown/beige adipocytes. The association between brown fat activity and a healthy metabolic profile, in relation to energy balance and glucose and lipid homeostasis, is influenced by the endocrine actions of brown adipokines. A comprehensive knowledge of the brown adipocyte secretome is still lacking. Advancements in the identification and characterization of brown adipokines will facilitate therapeutic interventions for metabolic diseases, as these molecules are obvious candidates to therapeutic agents. Moreover, identification of brown adipokines as circulating biomarkers of brown adipose tissue activity may be particularly useful for noninvasive assessment of brown adipose tissue alterations in human pathologies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD et al (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 102:3324–3329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blüher M, Mantzoros CS (2015) From leptin to other adipokines in health and disease: facts and expectations at the beginning of the 21st century. Metabolism 64:131–145

    Article  PubMed  CAS  Google Scholar 

  • Boon MR, Kooijman S, van Dam AD, Pelgrom LR, Berbée JF, Visseren CA et al (2014) Peripheral cannabinoid 1 receptor blockade activates brown adipose tissue and diminishes dyslipidemia and obesity. FASEB J 28:5361–5375

    Article  CAS  PubMed  Google Scholar 

  • Braga M, Reddy ST, Vergnes L, Pervin S, Grijalva V, Stout D et al (2014) Follistatin promotes adipocyte differentiation, browning, and energy metabolism. J Lipid Res 55:375–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burysek L, Houstek J (1997) β-Adrenergic stimulation of interleukin-1α and interleukin-6 expression in mouse brown adipocytes. FEBS Lett 411:83–86

    Article  CAS  PubMed  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–259

    Article  CAS  PubMed  Google Scholar 

  • Chartoumpekis DV, Habeos IG, Ziros PG, Psyrogiannis AI, Kyriazopoulou VE, Papavassiliou AG (2011) Brown adipose tissue responds to cold and adrenergic stimulation by induction of FGF21. Mol Med 17:736–740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G et al (2009) Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ Res 104:541–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen KY, Cypess AM, Laughlin MR, Haft CR, Hu HH, Bredella MA et al (2014) Brown adipose reporting criteria in imaging studies (BARCIST 1.0): recommendations for standardized FDG-PET/CT experiments in humans. Cell Metab 24:210–222

    Article  CAS  Google Scholar 

  • Chen Y, Buyel JJ, Hanssen MJ, Siegel F, Pan R, Naumann J et al (2016) Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity. Nat Commun 7:11420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Wang GX, Ma SL, Jung DY, Ha H, Altamimi T et al (2017) Nrg4 promotes fuel oxidation and a healthy adipokine profile to ameliorate diet-induced metabolic disorders. Mol Metab 6:863–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Franco A, Guasti D, Squecco R, Mazzanti B, Rossi F, Idrizaj E et al (2016) Searching for classical brown fat in humans: development of a novel human fetal brown stem cell model. Stem Cells 34:1679–1691

    Article  PubMed  CAS  Google Scholar 

  • Duchamp C, Burton KA, Géloën A, Dauncey MJ (1997) Transient upregulation of IGF-I gene expression in brown adipose tissue of cold-exposed rats. Am J Physiol 272:E453–EE60

    CAS  PubMed  Google Scholar 

  • Fernandez JA, Mampel T, Villarroya F, Iglesias R (1987) Direct assessment of brown adipose tissue as a site of systemic tri-iodothyronine production in the rat. Biochem J 243:281–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitzgibbons TP, Kogan S, Aouadi M, Hendricks GM, Straubhaar J, Czech MP (2011) Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am J Physiol Heart Circ Physiol 301:H1425–H1437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fournier B, Murray B, Gutzwiller S, Marcaletti S, Marcellin D, Bergling S et al (2012) Blockade of the activin receptor IIb activates functional brown adipogenesis and thermogenesis by inducing mitochondrial oxidative metabolism. Mol Cell Biol 32:2871–2879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friederich-Persson M, Nguyen Dinh Cat A, Persson P, Montezano AC, Touyz RM (2017) Brown adipose tissue regulates small artery function through NADPH oxidase 4-derived hydrogen peroxide and redox-sensitive protein kinase G-1α. Arterioscler Thromb Vasc Biol 37:455–465

    Article  CAS  PubMed  Google Scholar 

  • Fu Z, Yao F, Abou-Samra AB, Zhang R (2013) Lipasin, thermoregulated in brown fat, is a novel but atypical member of the angiopoietin-like protein family. Biochem Biophys Res Commun 430:1126–1131

    Article  CAS  PubMed  Google Scholar 

  • Gaich G, Chien JY, Fu H, Glass LC, Deeg MA, Holland WL et al (2013) The effects of LY2405319, an FGF21 analog, in obese human subjects with type 2 diabetes. Cell Metab 18:333–340

    Article  CAS  PubMed  Google Scholar 

  • García-Alonso V, Clària J (2014) Prostaglandin E2 signals white-to-brown adipogenic differentiation. Adipocytes 3:290–296

    Article  CAS  Google Scholar 

  • García-Alonso V, López-Vicario C, Titos E, Morán-Salvador E, González-Périz A, Rius B et al (2013) Coordinate functional regulation between microsomal prostaglandin E synthase-1 (mPGES-1) and peroxisome proliferator activated receptor γ (PPARγ) in the conversion of white-to-brown adipocytes. J Biol Chem 288:28230–28242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Alonso V, Titos E, Alcaraz-Quiles J, Rius B, Lopategi A, López-Vicario C et al (2016) Prostaglandin E2 exerts multiple regulatory actions on human obese adipose tissue remodeling, inflammation, adaptive thermogenesis and lipolysis. PLoS One 11:e0153751

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gesta S, Tseng YH, Kahn CR (2007) Developmental origin of fat: tracking obesity to its source. Cell 131:242–256

    Article  CAS  PubMed  Google Scholar 

  • Giralt M, Gavaldà-Navarro A, Villarroya F (2015) Fibroblast growth factor-21, energy balance and obesity. Mol Cell Endocrinol 418:66–63

    Article  CAS  PubMed  Google Scholar 

  • Gnad T, Scheibler S, von Kügelgen I, Scheele C, Kilić A, Glöde A et al (2014) Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors. Nature 516:395–399

    Article  CAS  PubMed  Google Scholar 

  • Gunawardana SC, Piston DW (2012) Reversal of type 1 diabetes in mica by brown adipose tissue transplant. Diabetes 61:674–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunawardana SC, Piston DW (2015) Insulin-independent reversal of type 1 diabetes in nonobese diabetic mice with brown adipose tissue transplant. Am J Physiol Endocrinol Metab 308:E1043–E1055

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hansen IR, Jansson KM, Cannon B, Nedergaard J (2014) Contrasting effects of cold acclimation versus obesogenic diets on chemerin gene expression in brown and brite adipose tissues. Biochim Biophys Acta 1841:1691–1699

    Article  CAS  PubMed  Google Scholar 

  • Hanssen MJ, Broeders E, Samms RJ, Vosselman MJ, van der Lans AA, Cheng CC et al (2015) Serum FGF21 levels are associated with brown adipose tissue activity in humans. Sci Rep 5:10275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hondares E, Iglesias R, Giralt A, Gonzalez FJ, Giralt M, Mampel T et al (2011) Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J Biol Chem 286:12983–12990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hondares E, Gallego-Escuredo JM, Flachs P, Frontini A, Cereijo R, Goday A et al (2014) Fibroblast growth factor-21 is expressed in neonatal and pheochromocytoma-induced adult human brown adipose tissue. Metabolism 63:312–317

    Article  CAS  PubMed  Google Scholar 

  • Jorge AS, Jorge GC, Paraíso AF, Franco RM, Vieira LJ, Hilzenderger AM et al (2017) Brown and White adipose tissue expression of IL6, UCP1 and SIRT1 are associated with alterations in clinical, metabolic and anthropometric parameters in obese humans. Exp Clin Endocrinol Diabetes 125:163–170

    Article  CAS  PubMed  Google Scholar 

  • Kang YE, Choung S, Lee JH, Kim HJ, Ku BJ (2017) The role of circulating Slit2, the one of the newly Batokines, in human diabetes mellitus. Endocrinol Metab (Seoul) 32:383–388

    Article  CAS  Google Scholar 

  • Kazak L, Chouchani ET, Jedrychowski MP, Erickson BK, Shinoda K, Cohen P et al (2015) A creatine-driven substrate cycle enhances energy expenditure and thermogenesis in beige fat. Cell 163:643–655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keipert S, Kutschke M, Lamp D, Brachthäuser L, Neff F, Meyer CW et al (2015) Genetic disruption of uncoupling protein 1 in mice renders brown adipose tissue a significant source of FGF21 secretion. Mol Metab 4:537–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klepac K, Kilić A, Gnad T, Brown LM, Herrmann B, Wilderman A et al (2016) The Gq signalling pathway inhibits brown and beige adipose tissue. Nat Commun 7:10895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kralisch S, Hoffmann A, Kratzsch J, Blüher M, Stumvoll M, Fasshauer M et al (2017) The brown-fat-secreted adipokine neuregulin 4 is decreased in gestational diabetes mellitus. Diabetes Metab. pii: S1262-3636(17)30465-2

    Google Scholar 

  • Krings A, Rahman S, Huang S, Lu Y, Czernik PJ, Lecka-Czernik B (2012) Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone 50:546–552

    Article  CAS  PubMed  Google Scholar 

  • Krott LM, Piscitelli F, Heine M, Borrino S, Scheja L, Silvestri C et al (2016) Endocannabinoid regulation in white and brown adipose tissue following thermogenic activation. J Lipid Res 57:464–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee P, Linderman JD, Smith S, Brychta RJ, Wang J, Idelson C et al (2014) Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab 19:302–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lidell ME, Enerbäck S (2015) Brown adipose tissue and bone. Int J Obes Suppl 5:S23–S27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long JZ, Svensson KJ, Bateman LA, Lin H, Kamenecka T, Lokurkar IA et al (2016) The secreted enzyme PM20D1 regulates lipidated amino acid uncouplers of mitochondria. Cell 166:424–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenzo M, Valverde AM, Teruel T, Benito M (1993) IGF-I is a mitogen also involved in differentiation related gene expression in fetal brown adipocytes. J Cell Biol 123:1567–1575

    Article  CAS  PubMed  Google Scholar 

  • Lynes MD, Leiria LO, Lundh M, Bartelt A, Shamsi F, Huang TL et al (2017) The cold-induced lipokine 12,13-diHOME promotes fatty acid transport into brown adipose tissue. Nat Med 23:631–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahdaviani K, Chess D, Wu Y, Shirihai O, Aprahamian TR (2016) Autocrine effect of vascular endothelial growth factor-A is essential for mitochondrial function in brown adipocytes. Metabolism 65:26–35

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Perez B, Ejarque M, Gutierrez C, Nuñez-Roa C, Roche K, Vila-Bedmar R et al (2016) Angiopoietin-like protein 8 (ANGPTL8) in pregnancy: a brown adipose tissue-derived endocrine factor with a potential role in fetal growth. Transl Res 178:1–12

    Article  CAS  PubMed  Google Scholar 

  • Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD et al (2014) Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin. Nat Immunol 15:423–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Min SY, Kady J, Nam M, Rojas-Rodriguez R, Berkenwald A, Kim JH et al (2016) Human “brite/beige” adipocytes develop from capillary networks, and their implantation improves metabolic homeostasis in mice. Nat Med 22:312–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murano I, Barbatelli G, Giordano A, Cinti S (2009) Noradrenergic parenchymal nerve fiber branching after cold acclimatisation correlates with brown adipocyte density in mouse adipose organ. J Anat 214:171–178

    Article  CAS  PubMed  Google Scholar 

  • Néchad M, Ruka E, Thibault J (1994) Production of nerve growth factor by brown fat in culture: relation with the in vivo developmental stage of the tissue. Comp Biochem Physiol Comp Physiol 107:381–388

    Article  PubMed  Google Scholar 

  • Nguyen KD, Qiu Y, Cui X, Goh YP, Mwangi J, David T et al (2011) Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature 480:104–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nisoli E, Tonello C, Benarese M, Liberini P, Carruba MO (1996) Expression of nerve growth factor in brown adipose tissue: implications for thermogenesis and obesity. Endocrinology 137:495–503

    Article  CAS  PubMed  Google Scholar 

  • Nisoli E, Tonello C, Briscini L, Carruba MO (1997) Inducible nitric oxide synthase in rat brown adipocytes: implications for blood flow to brown adipose tissue. Endocrinology 138:676–682

    Article  CAS  PubMed  Google Scholar 

  • Nisoli E, Clementi E, Tonello C, Sciorati C, Briscini L, Carruba MO (1998) Effects of nitric oxide on proliferation and differentiation of rat brown adipocytes in primary cultures. Br J Pharmacol 125:888–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T et al (2011) Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab 14:272–279

    Article  CAS  PubMed  Google Scholar 

  • Pal M, Febbraio MA, Whitham M (2014) From cytokine to myokine: the emerging role of interleukin-6 in metabolic regulation. Immunol Cell Biol 92:331–339

    Article  CAS  PubMed  Google Scholar 

  • Pellegrinelli V, Carobbio S, Vidal-Puig A (2016) Adipose tissue plasticity: how fat depots respond differently to pathophysiological cues. Diabetologia 59:1075–1088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J (2010) 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 285:7153–7164

    Article  CAS  PubMed  Google Scholar 

  • Qian SW, Tang Y, Li X, Liu Y, Zhang YY, Huang HY et al (2013) BMP4-mediated brown fat-like changes in white adipose tissue alter glucose and energy homeostasis. Proc Natl Acad Sci U S A 110:E798–E807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rabelo R, Schifman A, Rubio A, Sheng X, Silva JE (1995) Delineation of thyroid hormone-responsive sequences within a critical enhancer in the rat uncoupling protein gene. Endocrinology 136:1003–1013

    Article  CAS  PubMed  Google Scholar 

  • Rahman S, Lu Y, Czernik PJ, Rosen CJ, Enerback S, Lecka-Czernik B (2013) Inducible brown adipose tissue, or beige fat, is anabolic for the skeleton. Endocrinology 154:2687–2701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao RR, Long JZ, White JP, Svensson KJ, Lou J, Lokurkar I et al (2014) Meteorin-like is a hormone that regulates immune adipose interactions to increase beige fat thermogenesis. Cell 157:1279–1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts LD, Ashmore T, Kotwica AO, Murfitt SA, Fernandez BO, Feelisch M et al (2015) Inorganic nitrate promotes the browning of white adipose tissue through the nitrate-nitrite-nitric oxide pathway. Diabetes 64:471–484

    Article  CAS  PubMed  Google Scholar 

  • Rosell M, Hondares E, Iwamoto S, Gonzalez FJ, Wabitsch M, Staels B et al (2012) Peroxisome proliferator-activated receptors-alpha and -gamma, and cAMP-mediated pathways, control retinol-binding protein-4 gene expression in brown adipose tissue. Endocrinology 153:1162–1173

    Article  CAS  PubMed  Google Scholar 

  • Rosell M, Kaforou M, Frontini A, Okolo A, Chan YW, Nikolopoulou E et al (2014) Brown and white adipose tissues: intrinsic differences in gene expression and response to cold exposure in mice. Am J Physiol Endocrinol Metab 306:E945–E964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rourke JL, Muruganandan S, Dranse HJ, McMullen NM, Sinal CJ (2014) Gpr1 is an active chemerin receptor influencing glucose homeostasis in obese mice. J Endocrinol 222:201–215

    Article  CAS  PubMed  Google Scholar 

  • Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H et al (2013) Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab 98:E1448–E1455

    Article  CAS  PubMed  Google Scholar 

  • Schulz TJ, Huang P, Huang TL, Xue R, McDougall LE, Townsend KL et al (2013) Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 495:379–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shabalina IG, Petrovic N, de Jong JM, Kalinovich AV, Cannon B, Nedergaard J (2013) UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep 5:1196–1203

    Article  CAS  PubMed  Google Scholar 

  • Shimizu I, Aprahamian T, Kikuchi R, Shimizu A, Papanicolaou KN, MacLauchlan S et al (2014) Vascular rarefaction mediates whitening of brown fat in obesity. J Clin Invest 124:2099–2112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva JE, Larsen PR (1985) Potential 520 of brown adipose tissue type II thyroxine 5′-deiodinase as a local and systemic source of triiodothyronine in rats. J Clin Invest 76:2296–2305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh R, Braga M, Pervin S (2014) Regulation of brown adipocyte metabolism by myostatin/follistatin signaling. Front Cell Dev Biol 2:60

    PubMed  PubMed Central  Google Scholar 

  • Singh R, Braga M, Reddy ST, Lee SJ, Parveen M, Grijalva V et al (2017) Follistatin targets distinct pathways to promote brown adipocyte characteristics in brown and white adipose tissues. Endocrinology 158:1217–1230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM et al (2013) Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest 123:215–223

    Article  CAS  PubMed  Google Scholar 

  • Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM et al (2016) AgRP neurons control systemic insulin sensitivity via myostatin expression in brown adipose tissue. Cell 165:125–138

    Article  CAS  Google Scholar 

  • Sun K, Kusminski CM, Luby-Phelps K, Spurgin SB, An YA, Wang QA et al (2014) Brown adipose tissue derived VEGF-A modulates cold tolerance and energy expenditure. Mol Metab 3:474–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svensson KJ, Long JZ, Jedrychowski MP, Cohen P, Lo JC, Serag S et al (2016) A secreted Slit2 fragment regulates adipose tissue thermogenesis and metabolic function. Cell Metab 23:454–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomou T, Mori MA, Dreyfuss JM, Konishi M, Sakaguchi M, Wolfrum C et al (2017) Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature 542:450–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tseng YH, Kokkotou E, Schulz TJ, Huang TL, Winnay JN, Taniguchi CM et al (2008) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454:1000–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vegiopoulos A, Müller-Decker K, Strzoda D, Schmitt I, Chichelnitskiy E, Ostertag A et al (2010) Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science 328:1158–1161

    Article  CAS  PubMed  Google Scholar 

  • Villarroya F, Giralt M (2015) The beneficial effects of brown fat transplantation: further evidence of an endocrine role of brown adipose tissue. Endocrinology 156:2368–2370

    Article  CAS  PubMed  Google Scholar 

  • Villarroya F, Vidal-Puig A (2013) Beyond the sympathetic tone: the new brown fat activators. Cell Metab 17:638–643

    Article  CAS  PubMed  Google Scholar 

  • Villarroya F, Cereijo R, Villarroya J, Giralt M (2017) Brown adipose tissue as a secretory organ. Nat Rev Endocrinol 13:26–35

    Article  CAS  PubMed  Google Scholar 

  • Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T et al (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525

    Article  CAS  PubMed  Google Scholar 

  • Virtue S, Feldmann H, Christian M, Tan CY, Masoodi M, Dale M et al (2012) A new role for lipocalin prostaglandin D synthase in the regulation of brown adipose tissue substrate utilization. Diabetes 61:3139–3147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang GX, Zhao XY, Meng ZX, Kern M, Dietrich A, Chen Z et al (2014) The brown fat-enriched secreted factor Nrg4 preserves metabolic homeostasis through attenuation of hepatic lipogenesis. Nat Med 20:1436–1443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittle AJ, Carobbio S, Martins L, Slawik M, Hondares E, Vázquez MJ et al (2012) BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell 149:871–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittle AJ, Jiang M, Peirce V, Relat J, Virtue S, Ebinuma H et al (2015) Soluble LR11/SorLA represses thermogenesis in adipose tissue and correlates with BMI in humans. Nat Commun 6:8951

    Article  CAS  PubMed  Google Scholar 

  • Wright WS, Longo KA, Dolinsky VW, Gerin I, Kang S, Bennett CN et al (2007) Wnt10b inhibits obesity in ob/ob and agouti mice. Diabetes 56:295–303

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH et al (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150:366–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue Y, Petrovic N, Cao R, Larsson O, Lim S, Chen S et al (2009) Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metab 9:99–109

    Article  CAS  PubMed  Google Scholar 

  • Yamashita H, Sato Y, Kizaki T, Oh S, Nagasawa J, Ohno H (1994) Basic fibroblast growth factor (bFGF) contributes to the enlargement of brown adipose tissue during cold acclimation. Pflugers Arch 428:352–356

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Abou-Samra AB (2013) Emerging roles of lipasin as a critical lipid regulator. Biochem Biophys Res Commun 432:401–405

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work has been supported by Grants SAF2017-85722-R from the Ministerio de Ciencia e Innovación (MINECO) and PI17/00420 from the Instituto de Salud Carlos III, Spain, cofinanced by the European Regional Development Fund (ERDF), and Fundació Marató de TV3 (grant 201612-30). M.P. and J.V. are “Juan de la Cierva” researchers (MINECO, Spain).

Author information

Authors and Affiliations

  1. Departament de Bioquímica i Biomedicina Molecular, Institut de Biomedicina, Universitat de Barcelona, Barcelona, Catalonia, Spain

    Francesc Villarroya, Aleix Gavaldà-Navarro, Marion Peyrou, Joan Villarroya & Marta Giralt

  2. CIBER Fisiopatología de la Obesidad y Nutrición, Barcelona, Spain

    Francesc Villarroya, Aleix Gavaldà-Navarro, Marion Peyrou & Marta Giralt

  3. Hospital de la Santa Creu I Sant Pau, Barcelona, Spain

    Joan Villarroya

Authors
  1. Francesc Villarroya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleix Gavaldà-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marion Peyrou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joan Villarroya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marta Giralt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesc Villarroya .

Editor information

Editors and Affiliations

  1. Institute of Pharmacology & Toxicology, University Hospital Bonn, University of Bonn, Bonn, Germany

    Alexander Pfeifer

  2. Institute of Molecular Nutritional Medicine, TU München, Freising, Bayern, Germany

    Martin Klingenspor

  3. Institute for Diabetes and Cancer IDC, Helmholtz Center München, Neuherberg, Germany

    Stephan Herzig

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Villarroya, F., Gavaldà-Navarro, A., Peyrou, M., Villarroya, J., Giralt, M. (2018). Brown Adipokines. In: Pfeifer, A., Klingenspor, M., Herzig, S. (eds) Brown Adipose Tissue. Handbook of Experimental Pharmacology, vol 251. Springer, Cham. https://doi.org/10.1007/164_2018_119

Download citation

Publish with us

Policies and ethics

Search

Navigation