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Novel Mediators of Adipose Tissue and Muscle Crosstalk

  • Metabolism (P Trayhurn, Section Editor)
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Abstract

The crosstalk between adipose tissue and skeletal muscle has gained considerable interest, since this process, specifically in obesity, substantially drives the pathogenesis of muscle insulin resistance. In this review, we discuss novel concepts and targets of this bidirectional organ communication system. This includes adipo-myokines like apelin and FGF21, inflammasomes, autophagy, and microRNAs (miRNAs). Literature analysis shows that the crosstalk between fat and muscle involves both extracellular molecules and intracellular organelles. We conclude that integration of these multiple crosstalk elements into one network will be required to better understand this process.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Trayhurn P, Drevon CA, Eckel J. Secreted proteins from adipose tissue and skeletal muscle—adipokines, myokines and adipose/muscle cross-talk. Arch Physiol Biochem. 2011;117(2):47–56.

    Article  CAS  PubMed  Google Scholar 

  2. Raschke S, Eckel J. Adipo-myokines: two sides of the same coin—mediators of inflammation and mediators of exercise. Mediators Inflamm. 2013;2013:320724.

    Article  PubMed Central  PubMed  Google Scholar 

  3. Tatemoto K, Hosoya M, Habata Y, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun. 1998;251(2):471–6.

    Article  CAS  PubMed  Google Scholar 

  4. Hosoya M, Kawamata Y, Fukusumi S, et al. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem. 2000;275(28):21061–7.

    Article  CAS  PubMed  Google Scholar 

  5. Zhang BH, Guo CX, Wang HX, et al. Cardioprotective effects of adipokine apelin on myocardial infarction. Heart Vessels. 2014;29(5):679–89.

    Article  CAS  PubMed  Google Scholar 

  6. Catalan V, Gomez-Ambrosi J, Rodriguez A, et al. Increased circulating and visceral adipose tissue expression levels of YKL-40 in obesity-associated type 2 diabetes are related to inflammation: impact of conventional weight loss and gastric bypass. J Clin Endocrinol Metab. 2011;96(1):200–9.

    Article  CAS  PubMed  Google Scholar 

  7. Castan-Laurell I, Boucher J, Dray C, et al. Apelin, a novel adipokine over-produced in obesity: friend or foe? Mol Cell Endocrinol. 2005;245(1–2):7–9.

    Article  CAS  PubMed  Google Scholar 

  8. Boucher J, Masri B, Daviaud D, et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology. 2005;146(4):1764–71.

    Article  CAS  PubMed  Google Scholar 

  9. Wei L, Hou X, Tatemoto K. Regulation of apelin mRNA expression by insulin and glucocorticoids in mouse 3T3-L1 adipocytes. Regul Pept. 2005;132(1–3):27–32.

    Article  CAS  PubMed  Google Scholar 

  10. Higuchi K, Masaki T, Gotoh K, et al. Apelin, an APJ receptor ligand, regulates body adiposity and favors the messenger ribonucleic acid expression of uncoupling proteins in mice. Endocrinology. 2007;148(6):2690–7.

    Article  CAS  PubMed  Google Scholar 

  11. Dray C, Knauf C, Daviaud D, et al. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 2008;8(5):437–45.

    Article  CAS  PubMed  Google Scholar 

  12. Attane C, Daviaud D, Dray C, et al. Apelin stimulates glucose uptake but not lipolysis in human adipose tissue ex vivo. J Mol Endocrinol. 2011;46(1):21–8.

    Article  CAS  PubMed  Google Scholar 

  13. Guo M, Chen F, Lin T, et al. Apelin-13 decreases lipid storage in hypertrophic adipocytes in vitro through the upregulation of AQP7 expression by the PI3K signaling pathway. Med Sci Monit. 2014;20:1345–52.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Besse-Patin A, Montastier E, Vinel C, et al. Effect of endurance training on skeletal muscle myokine expression in obese men: identification of apelin as a novel myokine. Int J Obes (Lond). 2014;38(5):707–13. The data of this work identify apelin as a new exercise-regulated myokine in humans, involved in the improvement of whole-body insulin sensitivity of obese subjects.

    Article  CAS  Google Scholar 

  15. Yue P, Jin H, Aillaud M, et al. Apelin is necessary for the maintenance of insulin sensitivity. Am J Physiol Endocrinol Metab. 2010;298(1):E59–67.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Attane C, Foussal C, Le GS, et al. Apelin treatment increases complete fatty acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes. 2012;61(2):310–20.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Mohammadi M, Olsen SK, Ibrahimi OA. Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 2005;16(2):107–37.

    Article  CAS  PubMed  Google Scholar 

  18. Suzuki M, Uehara Y, Motomura-Matsuzaka K, et al. betaKlotho is required for fibroblast growth factor (FGF) 21 signaling through FGF receptor (FGFR) 1c and FGFR3c. Mol Endocrinol. 2008;22(4):1006–14.

    Article  CAS  PubMed  Google Scholar 

  19. Mashili FL, Austin RL, Deshmukh AS, et al. Direct effects of FGF21 on glucose uptake in human skeletal muscle: implications for type 2 diabetes and obesity. Diabetes Metab Res Rev. 2011;27(3):286–97.

    Article  CAS  PubMed  Google Scholar 

  20. Nishimura T, Nakatake Y, Konishi M, et al. Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim Biophys Acta. 2000;1492(1):203–6.

    Article  CAS  PubMed  Google Scholar 

  21. Izumiya Y, Bina HA, Ouchi N, et al. FGF21 is an Akt-regulated myokine. FEBS Lett. 2008;582(27):3805–10.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Hojman P, Pedersen M, Nielsen AR, et al. Fibroblast growth factor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes. 2009;58(12):2797–801.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8(8):457–65.

    Article  CAS  PubMed  Google Scholar 

  24. Muise ES, Azzolina B, Kuo DW, et al. Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferator-activated receptor gamma and altered metabolic states. Mol Pharmacol. 2008;74(2):403–12.

    Article  CAS  PubMed  Google Scholar 

  25. Fon TK, Bookout AL, Ding X, et al. Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol Endocrinol. 2010;24(10):2050–64.

    Article  Google Scholar 

  26. Keipert S, Ost M, Johann K, et al. Skeletal muscle mitochondrial uncoupling drives endocrine cross-talk through the induction of FGF21 as a myokine. Am J Physiol Endocrinol Metab. 2014;306(5):E469–82.

    Article  CAS  PubMed  Google Scholar 

  27. Chavez AO, Molina-Carrion M, Abdul-Ghani MA, et al. Circulating fibroblast growth factor-21 is elevated in impaired glucose tolerance and type 2 diabetes and correlates with muscle and hepatic insulin resistance. Diabetes Care. 2009;32(8):1542–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Zhang X, Yeung DC, Karpisek M, et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes. 2008;57(5):1246–53.

    Article  CAS  PubMed  Google Scholar 

  29. Chen W, Hoo RL, Konishi M, et al. Growth hormone induces hepatic production of fibroblast growth factor 21 through a mechanism dependent on lipolysis in adipocytes. J Biol Chem. 2011;286(40):34559–66.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Arner P, Pettersson A, Mitchell PJ, et al. FGF21 attenuates lipolysis in human adipocytes—a possible link to improved insulin sensitivity. FEBS Lett. 2008;582(12):1725–30.

    Article  CAS  PubMed  Google Scholar 

  31. Kharitonenkov A, Shiyanova TL, Koester A, et al. FGF-21 as a novel metabolic regulator. J Clin Invest. 2005;115(6):1627–35.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Lee DV, Li D, Yan Q, et al. Fibroblast growth factor 21 improves insulin sensitivity and synergizes with insulin in human adipose stem cell-derived (hASC) adipocytes. PLoS One. 2014;9(11):e111767.

    Article  PubMed Central  PubMed  Google Scholar 

  33. Murata Y, Nishio K, Mochiyama T, et al. Fgf21 impairs adipocyte insulin sensitivity in mice fed a low-carbohydrate, high-fat ketogenic diet. PLoS One. 2013;8(7):e69330.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Xu J, Lloyd DJ, Hale C, et al. Fibroblast growth factor 21 reverses hepatic steatosis, increases energy expenditure, and improves insulin sensitivity in diet-induced obese mice. Diabetes. 2009;58(1):250–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Cuevas-Ramos D, Almeda-Valdes P, Meza-Arana CE, et al. Exercise increases serum fibroblast growth factor 21 (FGF21) levels. PLoS One. 2012;7(5):e38022.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Kim KH, Kim SH, Min YK, et al. Acute exercise induces FGF21 expression in mice and in healthy humans. PLoS One. 2013;8(5):e63517.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Yang SJ, Hong HC, Choi HY, et al. Effects of a three-month combined exercise programme on fibroblast growth factor 21 and fetuin-A levels and arterial stiffness in obese women. Clin Endocrinol (Oxf). 2011;75(4):464–9.

    Article  CAS  Google Scholar 

  38. Luo Y, McKeehan WL. Stressed liver and muscle call on adipocytes with FGF21. Front Endocrinol (Lausanne). 2013;4:194.

    Google Scholar 

  39. Lin Z, Tian H, Lam KS, et al. Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metab. 2013;17(5):779–89. This study describes adipose tissue-derived FGF21 as an inducer of adiponectin with glucose-lowering and insulin-sensitizing impact, coupling adipose tissue to liver and skeletal muscle.

    Article  CAS  PubMed  Google Scholar 

  40. Lee MS, Choi SE, Ha ES, et al. Fibroblast growth factor-21 protects human skeletal muscle myotubes from palmitate-induced insulin resistance by inhibiting stress kinase and NF-kappaB. Metabolism. 2012;61(8):1142–51.

    Article  CAS  PubMed  Google Scholar 

  41. Stienstra R, Joosten LA, Koenen T, et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 2010;12(6):593–605.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Goossens GH, Blaak EE, Theunissen R, et al. Expression of NLRP3 inflammasome and T cell population markers in adipose tissue are associated with insulin resistance and impaired glucose metabolism in humans. Mol Immunol. 2012;50(3):142–9.

    Article  CAS  PubMed  Google Scholar 

  43. Vandanmagsar B, Youm YH, Ravussin A, et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011;17(2):179–88.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Stienstra R, van Diepen JA, Tack CJ, et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci U S A. 2011;108(37):15324–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Wen H, Gris D, Lei Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011;12(5):408–15.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Nov O, Kohl A, Lewis EC, et al. Interleukin-1beta may mediate insulin resistance in liver-derived cells in response to adipocyte inflammation. Endocrinology. 2010;151(9):4247–56.

    Article  CAS  PubMed  Google Scholar 

  47. Rawat R, Cohen TV, Ampong B, et al. Inflammasome up-regulation and activation in dysferlin-deficient skeletal muscle. Am J Pathol. 2010;176(6):2891–900.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Otis JS, Niccoli S, Hawdon N, et al. Pro-inflammatory mediation of myoblast proliferation. PLoS One. 2014;9(3):e92363.

    Article  PubMed Central  PubMed  Google Scholar 

  49. Li W, Moylan JS, Chambers MA, et al. Interleukin-1 stimulates catabolism in C2C12 myotubes. Am J Physiol Cell Physiol. 2009;297(3):C706–14.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Schmidt J, Barthel K, Wrede A, et al. Interrelation of inflammation and APP in sIBM: IL-1 beta induces accumulation of beta-amyloid in skeletal muscle. Brain. 2008;131(Pt 5):1228–40.

    PubMed Central  PubMed  Google Scholar 

  51. Scheler M, Irmler M, Lehr S, et al. Cytokine response of primary human myotubes in an in vitro exercise model. Am J Physiol Cell Physiol. 2013;305(8):C877–86.

    Article  CAS  PubMed  Google Scholar 

  52. Larsen CM, Faulenbach M, Vaag A, et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007;356(15):1517–26.

    Article  CAS  PubMed  Google Scholar 

  53. Berchtold LA, Larsen CM, A V, et al. IL-1 receptor antagonism and muscle gene expression in patients with type 2 diabetes. Eur Cytokine Netw. 2009;20(2):81–7.

    CAS  PubMed  Google Scholar 

  54. Galluzzi L, Pietrocola F, Levine B, et al. Metabolic control of autophagy. Cell. 2014;159(6):1263–76.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Kim KH, Jeong YT, Oh H, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med. 2013;19(1):83–92. This study provides an insight into the complicated role of autophagy regarding the regulation of energy homeostasis by use of an autophagy-deficient mouse model. They also highlight the impact of autophagy-induced FGF21 as a mediator of inter-organ crosstalk.

    Article  CAS  PubMed  Google Scholar 

  56. Lum JJ, Bauer DE, Kong M, et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell. 2005;120(2):237–48.

    Article  CAS  PubMed  Google Scholar 

  57. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221(1):3–12.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Deter RL, De DC. Influence of glucagon, an inducer of cellular autophagy, on some physical properties of rat liver lysosomes. J Cell Biol. 1967;33(2):437–49.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Kim KH, Lee MS. Autophagy as a crosstalk mediator of metabolic organs in regulation of energy metabolism. Rev Endocr Metab Disord. 2014;15(1):11–20.

    Article  CAS  PubMed  Google Scholar 

  60. Yang L, Li P, Fu S, et al. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010;11(6):467–78.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Jansen HJ, Van Essen P, Koenen T, et al. Autophagy activity is up-regulated in adipose tissue of obese individuals and modulates proinflammatory cytokine expression. Endocrinology. 2012;153(12):5866–74.

    Article  CAS  PubMed  Google Scholar 

  62. Liu Y, Palanivel R, Rai E, et al. Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice. Diabetes. 2015;64(1):36–48.

    Article  CAS  PubMed  Google Scholar 

  63. Zhang Y, Goldman S, Baerga R, et al. Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proc Natl Acad Sci U S A. 2009;106(47):19860–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Dumortier O, Hinault C, Van OE. MicroRNAs and metabolism crosstalk in energy homeostasis. Cell Metab. 2013;18(3):312–24.

    Article  CAS  PubMed  Google Scholar 

  65. Friedlander MR, Lizano E, Houben AJ, et al. Evidence for the biogenesis of more than 1,000 novel human microRNAs. Genome Biol. 2014;15(4):R57.

    Article  PubMed Central  PubMed  Google Scholar 

  66. Zhu L, Shi C, Ji C, et al. FFAs and adipokine-mediated regulation of hsa-miR-143 expression in human adipocytes. Mol Biol Rep. 2013;40(10):5669–75.

    Article  CAS  PubMed  Google Scholar 

  67. Herrera BM, Lockstone HE, Taylor JM, et al. Global microRNA expression profiles in insulin target tissues in a spontaneous rat model of type 2 diabetes. Diabetologia. 2010;53(6):1099–109.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Hilton C, Neville MJ, Karpe F. MicroRNAs in adipose tissue: their role in adipogenesis and obesity. Int J Obes (Lond). 2013;37(3):325–32.

    Article  CAS  Google Scholar 

  69. Takanabe R, Ono K, Abe Y, et al. Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet. Biochem Biophys Res Commun. 2008;376(4):728–32.

    Article  CAS  PubMed  Google Scholar 

  70. Zhuang G, Meng C, Guo X, et al. A novel regulator of macrophage activation: miR-223 in obesity-associated adipose tissue inflammation. Circulation. 2012;125(23):2892–903.

    Article  CAS  PubMed  Google Scholar 

  71. Chen YH, Heneidi S, Lee JM, et al. miRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes. 2013;62(7):2278–86. This manuscript presents a detailed mechanistic study on how a single miRNA can affect insulin sensitivity in polycystic ovary syndrome.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Ishida M, Shimabukuro M, Yagi S, et al. MicroRNA-378 regulates adiponectin expression in adipose tissue: a new plausible mechanism. PLoS One. 2014;9(11):e111537.

    Article  PubMed Central  PubMed  Google Scholar 

  73. Mori MA, Thomou T, Boucher J, et al. Altered miRNA processing disrupts brown/white adipocyte determination and associates with lipodystrophy. J Clin Invest. 2014;124(8):3339–51.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  74. Yin H, Pasut A, Soleimani VD, et al. MicroRNA-133 controls brown adipose determination in skeletal muscle satellite cells by targeting Prdm16. Cell Metab. 2013;17(2):210–24.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  75. Liu W, Bi P, Shan T, et al. miR-133a regulates adipocyte browning in vivo. PLoS Genet. 2013;9(7). e1003626.

  76. Gallagher IJ, Scheele C, Keller P, et al. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med. 2010;2(2):9.

    Article  PubMed Central  PubMed  Google Scholar 

  77. Yang WM, Jeong HJ, Park SY, et al. Induction of miR-29a by saturated fatty acids impairs insulin signaling and glucose uptake through translational repression of IRS-1 in myocytes. FEBS Lett. 2014;588(13):2170–6.

    Article  CAS  PubMed  Google Scholar 

  78. Zhang Y, Yang L, Gao YF, et al. MicroRNA-106b induces mitochondrial dysfunction and insulin resistance in C2C12 myotubes by targeting mitofusin-2. Mol Cell Endocrinol. 2013;381(1–2):230–40.

    Article  CAS  PubMed  Google Scholar 

  79. Rivas DA, Lessard SJ, Rice NP. et al. Diminished skeletal muscle microRNA expression with aging is associated with attenuated muscle plasticity and inhibition of IGF-1 signaling. FASEB J. 2014.

  80. He A, Zhu L, Gupta N, et al. Overexpression of micro ribonucleic acid 29, highly up-regulated in diabetic rats, leads to insulin resistance in 3T3-L1 adipocytes. Mol Endocrinol. 2007;21(11):2785–94.

    Article  CAS  PubMed  Google Scholar 

  81. Wang YC, Li Y, Wang XY, et al. Circulating miR-130b mediates metabolic crosstalk between fat and muscle in overweight/obesity. Diabetologia. 2013;56(10):2275–85. This manuscript describes evidence for an endocrine mediation between adipose tissue and skeletal muscle via miRNAs.

    Article  CAS  PubMed  Google Scholar 

  82. Pan S, Yang X, Jia Y, et al. Microvesicle-shuttled miR-130b reduces fat deposition in recipient primary cultured porcine adipocytes by inhibiting PPAR-g expression. J Cell Physiol. 2014;229(5):631–9.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Ministeriumfür Wissenschaft und Forschung des Landes Nordrhein-Westfalen (Ministry of Science and Research of the State of North Rhine-Westphalia) and the Bundesministeriumfür Gesundheit (Federal Ministry of Health).

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Conflict of Interest

Ira Indrakusuma, Henrike Sell, and Jürgen Eckel declare that they have no conflict of interest.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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  1. Paul-Langerhans-Group for Integrative Physiology, German Diabetes Center (DDZ), Auf‘m Hennekamp 65, 40225, Düsseldorf, Germany

    Ira Indrakusuma, Henrike Sell & Jürgen Eckel

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  1. Ira Indrakusuma
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  2. Henrike Sell
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  3. Jürgen Eckel
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Correspondence to Henrike Sell.

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This article is part of the Topical Collection on Metabolism

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Indrakusuma, I., Sell, H. & Eckel, J. Novel Mediators of Adipose Tissue and Muscle Crosstalk. Curr Obes Rep 4, 411–417 (2015). https://doi.org/10.1007/s13679-015-0174-7

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