Browning of white fat: Does irisin play a role in humans?

Journal of Endocrinology

Volumn 222, Issue 1, 2014, Pages

  Elsen, Manuela ^a   Raschke, Silja ^a   Eckel, Jürgen ^a  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

Author keywords

Adipocyte; Diabetes; Exercise; Muscle; Obesity

Indexed keywords

FIBRONECTIN TYPE III DOMAIN CONTAINING PROTEIN 5; IRISIN; MESSENGER RNA; OSTEOGENIC PROTEIN 1; PEPTIDE; PROTEIN; PROTEIN PGC1 ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; BROWN ADIPOSE TISSUE; ELISA KIT; EXERCISE; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; METABOLIC DISORDER; MUSCLE CONTRACTION; OBESITY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SKELETAL MUSCLE; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

ADIPOCYTE; DIABETES; EXERCISE; MUSCLE; OBESITY;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; DIABETES MELLITUS, TYPE 2; EXERCISE; FIBRONECTINS; HUMANS; OBESITY;

EID: 84904417022     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0189     Document Type: Review

References (61)

1. Al-Daghri NM, Alkharfy KM, Rahman S, Amer OE, Vinodson B, Sabico S, Milan P, Harte AL, McTernan PG, Alokail MS et al. 2013 Irisin as a predictor of glucose metabolism in children: sexually dimorphic effects. European Journal of Clinical Investigation [in press]. (doi:10.1111/eci.12196)
2. Aydin S, Aydin S, Kuloglu T, Yilmaz M, Kalayci M, Sahin I & Cicek D 2013 Alterations of irisin concentrations in saliva and serum of obese and normal-weight subjects, before and after 45min of a Turkish bath or running. Peptides 50 13-18. (doi:10.1016/j.peptides.2013.09.011)
3. Besse-Patin A, Montastier E, Vinel C, Castan-Laurell I, Louche K, Dray C, Daviaud D, Mir L, Marques MA, Thalamas C et al. 2014 Effect of endurance training on skeletal muscle myokine expression in obese men: identification of apelin as a novel myokine. International Journal of Obesity 38 707-713. (doi:10.1038/ijo.2013.158)
4. Bordicchia M, Liu D, Amri EZ, Ailhaud G, Dessi-Fulgheri P, Zhang C, Takahashi N, Sarzani R & Collins S 2012 Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. Journal of Clinical Investigation 122 1022-1036. (doi:10.1172/JCI59701)
5. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ et al. 2012a A PGC1-a-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481 463-468. (doi:10.1038/nature10777)
6. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ et al. 2012b Boström et al. reply. Nature 488 E10-E11. (doi:10.1038/nature11365)
7. Cannon B & Nedergaard J 2004 Brown adipose tissue: function and physiological significance. Physiological Reviews 84 277-359. (doi:10.1152/physrev.00015.2003)
8. Choi YK, Kim MK, Bae KH, Seo HA, Jeong JY, Lee WK, Kim JG, Lee IK & Park KG 2013 Serum irisin levels in new-onset type 2 diabetes. Diabetes Research and Clinical Practice 100 96-101. (doi:10.1016/j.diabres.2013. 01.007)
9. Crujeiras AB, Pardo M, Arturo RR, Santiago NC, Zulet MA, Martinez JA & Casanueva FF 2014a Longitudinal variation of circulating irisin after an energy restriction-induced weight loss and following weight regain in obese men and women. American Journal of Human Biology 26 198-207. (doi:10.1002/ajhb.22493)
10. Crujeiras AB, Zulet MA, Lopez-Legarrea P, de la Iglesia I, Pardo M, Carreira MC, Martinez JA & Casanueva FF 2014b Association between circulating irisin levels and the promotion of insulin resistance during the weight maintenance period after a dietary weight-lowering program in obese patients. Metabolism 63 520-531. (doi:10.1016/j. metabol.2013.12.007)
11. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A et al. 2009 Identification and importance of brown adipose tissue in adult humans. New England Journal of Medicine 360 1509-1517. (doi:10.1056/NEJMoa0810780)
12. Cypess AM, White AP, Vernochet C, Schulz TJ, Xue R, Sass CA, Huang TL, Roberts-Toler C, Weiner LS, Sze C et al. 2013 Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nature Medicine 19 635-639. (doi:10.1038/nm.3112)
13. De Matteis R, Lucertini F, GuesciniM, Polidori E, Zeppa S, Stocchi V, Cinti S & Cuppini R 2013 Exercise as a new physiological stimulus for brown adipose tissue activity. Nutrition, Metabolism, and Cardiovascular Diseases 23 582-590. (doi:10.1016/j.numecd.2012.01.013)
14. Ebert T, Focke D, PetroffD, Wurst U, Richter J, Bachmann A, Lossner U, Kralisch S, Kratzsch J, Beige J et al. 2014a Serum levels of the myokine irisin in relation to metabolic and renal function. European Journal of Endocrinology 170 501-506. (doi:10.1530/EJE-13-1053)
15. Ebert T, Stepan H, Schrey S, Kralisch S, Hindricks J, Hopf L, Platz M, Lossner U, Jessnitzer B, Drewlo S et al. 2014b Serum levels of irisin in gestational diabetes mellitus during pregnancy and after delivery. Cytokine 65 153-158. (doi:10.1016/j.cyto.2013.11.009)
16. Elsen M, Raschke S, Tennagels N, Schwahn U, Jelenik T, Roden M, Romacho T & Eckel J 2014 BMP4 and BMP7 induce the white-to-brown transition of primary human adipose stem cells. American Journal of Physiology. Cell Physiology 306 C431-C440. (doi:10.1152/ajpcell. 00290.2013)
17. Erickson HP 2013 Irisin and FNDC5 in retrospect: an exercise hormone or a transmembrane receptor? Adipocytes 2 289-293. (doi:10.4161/adip. 26082)
18. Goto M, Terada S, Kato M, Katoh M, Yokozeki T, Tabata I & Shimokawa T 2000 cDNA cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochemical and Biophysical Research Communications 274 350-354. (doi:10.1006/bbrc.2000.3134)
19. Gouni-Berthold I, Berthold HK, Huh JY, Berman R, Spenrath N, KroneW& Mantzoros CS 2013 Effects of lipid-lowering drugs on irisin in human subjects in vivo and in human skeletal muscle cells ex vivo. PLoS ONE 8 e72858. (doi:10.1371/journal.pone.0072858)
20. Hecksteden A, Wegmann M, Steffen A, Kraushaar J, Morsch A, Ruppenthal S, Kaestner L & Meyer T 2013 Irisin and exercise training in humans - results from a randomized controlled training trial. BMC Medicine 11 235. (doi:10.1186/1741-7015-11-235)
21. Huh JY, Panagiotou G, Mougios V, Brinkoetter M, Vamvini MT, Schneider BE & Mantzoros CS 2012 FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism 61 1725-1738. (doi:10.1016/j.metabol.2012. 09.002)
22. de la Iglesia R, Lopez-Legarrea P, Crujeiras AB, Pardo M, Casanueva FF, Zulet MA & Martinez JA 2013 Plasma irisin depletion under energy restriction is associated with improvements in lipid profile inmetabolic syndrome patients. Clinical Endocrinology [in press]. (doi:10.1111/cen. 12383)
23. Ivanov IP, Firth AE, Michel AM, Atkins JF & Baranov PV 2011 Identification of evolutionarily conserved non-AUG-initiated N-terminal extensions in human coding sequences. Nucleic Acids Research 39 4220-4234. (doi:10.1093/nar/gkr007)
24. Jespersen NZ, Larsen TJ, Peijs L, Daugaard S, Homoe P, Loft A, de Jong JJ, Mathur N, Cannon B, Nedergaard J et al. 2013 A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metabolism 17 798-805. (doi:10.1016/j. cmet.2013.04.011)
25. Kelly DP 2012 Irisin, light my fire. Science 336 42-43. (doi:10.1126/science. 1221688)
26. Kraemer RR, Shockett P, Webb ND, Shah U & Castracane VD 2014 A transient elevated irisin blood concentration in response to prolonged, moderate aerobic exercise in young men and women. Hormone and Metabolic Research 46 150-154. (doi:10.1055/s-0033-1355381)
27. Kurdiova T, Balaz M, Vician M, Maderova D, Vlcek M, Valkovic L, Srbecky M, Imrich R, Kyselovicova O, Belan V et al. 2014 Effects of obesity, diabetes and exercise on Fndc5 gene expression and irisin release in human skeletal muscle and adipose tissue: in vivo and in vitro studies. Journal of Physiology 592 1091-1107. (doi:10.1113/jphysiol. 2013.264655)
28. Lambernd S, Taube A, Schober A, Platzbecker B, Gorgens SW, Schlich R, Jeruschke K, Weiss J, Eckardt K & Eckel J 2012 Contractile activity of human skeletal muscle cells prevents insulin resistance by inhibiting pro-inflammatory signalling pathways. Diabetologia 55 1128-1139. (doi:10.1007/s00125-012-2454-z)
29. Lee P, Linderman JD, Smith S, Brychta RJ, Wang J, Idelson C, Perron RM, Werner CD, Phan GQ, Kammula US et al. 2014 Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metabolism 19 302-309. (doi:10.1016/j.cmet.2013.12.017)
30. Lidell ME, Betz MJ, Dahlqvist LO, Heglind M, Elander L, Slawik M, Mussack T, Nilsson D, Romu T, Nuutila P et al. 2013 Evidence for two types of brown adipose tissue in humans. Nature Medicine 19 631-634. (doi:10.1038/nm.3017)
31. Liu JJ, Wong MD, Toy WC, Tan CS, Liu S, Ng XW, Tavintharan S, Sum CF & Lim SC 2013 Lower circulating irisin is associated with type 2 diabetes mellitus. Journal of Diabetes and its Complications 27 365-369. (doi:10.1016/j.jdiacomp.2013.03.002)
32. Liu JJ, Liu S, Wong MD, Tan CS, Tavintharan S, Sum CF & Lim SC 2014 Relationship between circulating irisin, renal function and body composition in type 2 diabetes. Journal of Diabetes and its Complications 28 208-213. (doi:10.1016/j.jdiacomp.2013.09.011)
33. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P & Teule GJ 2009 Cold-activated brown adipose tissue in healthy men. New England Journal of Medicine 360 1500-1508. (doi:10.1056/NEJMoa0808718)
34. Moraes C, Leal VO, Marinho SM, Barroso SG, Rocha GS, Boaventura GT & Mafra D 2013 Resistance exercise training does not affect plasma irisin levels of hemodialysis patients. Hormone and Metabolic Research 45 900-904. (doi:10.1055/s-0033-1354402)
35. Moreno-Navarrete JM, Ortega F, Serrano M, Guerra E, Pardo G, Tinahones F, RicartW& Fernandez-Real JM 2013 Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. Journal of Clinical Endocrinology and Metabolism 98 E769-E778. (doi:10.1210/jc.2012-2749)
36. Norheim F, Langleite TM, Hjorth M, Holen T, Kielland A, Stadheim HK, Gulseth HL, Birkeland KI, Jensen J & Drevon CA 2014 The effects of acute and chronic exercise on PGC-1a, irisin and browning of subcutaneous adipose tissue in humans. FEBS Letters 281 739-749. (doi:10.1111/febs.12619)
37. Ouellet V, Labbe SM, Blondin DP, Phoenix S, Guerin B, Haman F, Turcotte EE, Richard D & Carpentier AC 2012 Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. Journal of Clinical Investigation 122 545-552. (doi:10.1172/JCI60433)
38. Park KH, Zaichenko L, Brinkoetter M, Thakkar B, Sahin-Efe A, Joung KE, Tsoukas MA, Geladari EV, Huh JY, Dincer F et al. 2013 Circulating irisin in relation to insulin resistance and the metabolic syndrome. Journal of Clinical Endocrinology and Metabolism 98 4899-4907. (doi:10.1210/jc. 2013-2373)
39. Park KH, Zaichenko L, Peter P, Davis CR, Crowell JA & Mantzoros CS 2014 Diet quality is associated with circulating C-reactive protein but not irisin levels in humans. Metabolism 63 233-241. (doi:10.1016/j. metabol.2013.10.011)
40. Pekkala S, Wiklund PK, Hulmi JJ, Ahtiainen JP, Horttanainen M, Pollanen E, Makela KA, Kainulainen H, Hakkinen K, Nyman K et al. 2013 Are skeletal muscle FNDC5 gene expression and irisin release regulated by exercise and related to health? Journal of Physiology 591 5393-5400. (doi:10.1113/jphysiol.2013.263707)
41. 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. Journal of Biological Chemistry 285 7153-7164. (doi:10.1074/jbc. M109.053942)
42. Pilegaard H, Saltin B & Neufer PD 2003 Exercise induces transient transcriptional activation of the PGC-1a gene in human skeletal muscle. Journal of Physiology 546 851-858. (doi:10.1113/jphysiol.2002. 034850)
43. Polyzos SA, Kountouras J, Anastasilakis AD, Geladari EV & Mantzoros CS 2014 Irisin in patients with nonalcoholic fatty liver disease. Metabolism 63 207-217. (doi:10.1016/j.metabol.2013.09.013)
44. Raschke S, Elsen M, Gassenhuber H, Sommerfeld M, Schwahn U, Brockmann B, Jung R, WisloffU, Tjonna AE, Raastad T et al. 2013 Evidence against a beneficial effect of irisin in humans. PLoS ONE 8 e73680. (doi:10.1371/journal.pone.0073680)
45. Roca-Rivada A, Castelao C, Senin LL, Landrove MO, Baltar J, Belen CA, Seoane LM, Casanueva FF & Pardo M 2013FNDC5/irisin is not only a myokine but also an adipokine. PLoS ONE 8 e60563. (doi:10.1371/journal.pone.0060563)
46. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K et al. 2009 High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58 1526-1531. (doi:10.2337/db09-0530)
47. Scarpace PJ, Yenice S& Tumer N 1994 Influence of exercise training and age on uncoupling protein mRNA expression in brown adipose tissue. Pharmacology, Biochemistry, and Behavior 49 1057-1059. (doi:10.1016/0091-3057(94)90264-X)
48. Schulz TJ, Huang TL, Tran TT, Zhang H, Townsend KL, Shadrach JL, Cerletti M, McDougall LE, Giorgadze N, Tchkonia T et al. 2011 Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. PNAS 108 143-148. (doi:10.1073/pnas. 1010929108)
49. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H et al. 2008 PRDM16 controls a brown fat/skeletal muscle switch. Nature 454 961-967. (doi:10.1038/nature07182)
50. Segawa M, Oh-Ishi S, Kizaki T, Ookawara T, Sakurai T, Izawa T, Nagasawa J, Kawada T, Fushiki T & Ohno H 1998 Effect of running training on brown adipose tissue activity in rats: a reevaluation. Research Communications in Molecular Pathology and Pharmacology 100 77-82.
51. Shan T, Liang X, Bi P & Kuang S 2013 Myostatin knockout drives browning of white adipose tissue through activating the AMPK-PGC1a-Fndc5 pathway in muscle. FASEB Journal 27 1981-1989. (doi:10.1096/fj.12-225755)
52. Stengel A, Hofmann T, Goebel-Stengel M, Elbelt U, Kobelt P & Klapp BF 2013 Circulating levels of irisin in patients with anorexia nervosa and different stages of obesity - correlation with body mass index. Peptides 39 125-130. (doi:10.1016/j.peptides.2012.11.014)
53. Timmons JA, Baar K, Davidsen PK & Atherton PJ 2012 Is irisin a human exercise gene? Nature 488 E9-10. (doi:10.1038/nature11364)
54. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerback S et al. 2009 Functional brown adipose tissue in healthy adults. New England Journal of Medicine 360 1518-1525. (doi:10.1056/NEJMoa0808949)
55. Walden TB, Hansen IR, Timmons JA, Cannon B & Nedergaard J 2012 Recruited vs. nonrecruited molecular signatures of brown, "brite", and white adipose tissues. American Journal of Physiology. Endocrinology and Metabolism 302 E19-E31. (doi:10.1152/ajpendo.00249.2011)
56. Wen MS, Wang CY, Lin SL & Hung KC 2013 Decrease in irisin in patients with chronic kidney disease. PLoS ONE 8 e64025. (doi:10.1371/journal. pone.0064025)
57. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G et al. 2012 Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 366-376. (doi:10.1016/j.cell.2012.05.016)
58. Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, Tzan K, Wang A, Parthasarathy S, He G et al. 2011 Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 300 R1115-R1125. (doi:10.1152/ajpregu.00806.2010)
59. Zhang HJ, Zhang XF, Ma ZM, Pan LL, Chen Z, Han HW, Han CK, Zhuang XJ, Lu Y, Li XJ et al. 2013 Irisin is inversely associated with intrahepatic triglyceride contents in obese adults. Journal of Hepatology 59 557-562. (doi:10.1016/j.jhep.2013.04.030)
60. Zhang Y, Li R, Meng Y, Li S, Donelan W, Zhao Y, Qi L, Zhang M, Wang X, Cui T et al. 2014 Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes 63 514-525. (doi:10.2337/db13-1106)
61. Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, Nedergaard J & Cinti S 2009 The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB Journal 23 3113-3120. (doi:10.1096/fj.09-133546)