Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity

Nature Communications

Volumn 7, Issue , 2016, Pages

  Chen, Yong ^a   Buyel, Joschka J ^a,b   Hanssen, Mark J W ^c   Siegel, Franziska ^a   Pan, Ruping ^a   Naumann, Jennifer ^a   Schell, Michael ^a   Van Der Lans, Anouk ^c   Schlein, Christian ^d   Froehlich, Holger ^b   Heeren, Joerg ^d   Virtanen, Kirsi A ^e,f   Van Marken Lichtenbelt, Wouter ^c   Pfeifer, Alexander ^a,b  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e TURKU UNIVERSITY HOSPITAL   (Finland)

^f UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 92A; UNCLASSIFIED DRUG; MIRN92 MICRORNA, HUMAN; MIRN92 MICRORNA, MOUSE;

BIOMARKER; COHORT ANALYSIS; CONCENTRATION (COMPOSITION); FAT; GENETIC MARKER; MUSCLE; RADIATION EXPOSURE; RNA; RODENT; SERUM; TOMOGRAPHY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD LEVEL; BROWN ADIPOCYTE; COLD EXPOSURE; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; EXOSOME; FEMALE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEWBORN; NONHUMAN; SERUM; ANIMAL; BLOOD; BROWN ADIPOSE TISSUE; C57BL MOUSE; COHORT ANALYSIS; METABOLISM; YOUNG ADULT;

MUS;

ADIPOSE TISSUE, BROWN; ADULT; ANIMALS; COHORT STUDIES; EXOSOMES; FEMALE; HUMANS; MALE; MICE, INBRED C57BL; MICRORNAS; YOUNG ADULT;

EID: 84964690999     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11420     Document Type: Article

References (70)

1. Cannon, B. & Nedergaard, J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (2004).
2. Pfeifer, A. & Hoffmann, L. S. Brown, beige, and white: The new color code of fat and its pharmacological implications. Annu. Rev. Pharmacol. Toxicol. 55, 207-227 (2015).
3. Rosen, E. D. & Spiegelman, B. M. What we talk about when we talk about fat. Cell 156, 20-44 (2014).
4. Harms, M. & Seale, P. Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19, 1252-1263 (2013).
5. Enerback, S. Human brown adipose tissue. Cell Metab. 11, 248-252 (2010).
6. Cypess, A. M. et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517 (2009).
7. Saito, M. et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58, 1526-1531 (2009).
8. van Marken Lichtenbelt, W. D. et al. Cold-Activated brown adipose tissue in healthy men. N. Engl. J. Med. 360, 1500-1508 (2009).
9. Virtanen, K. A. et al. Functional brown adipose tissue in healthy adults. N. Engl. J. Med. 360, 1518-1525 (2009).
10. Gnad, T. et al. Adenosine activates brown adipose tissue and recruits beige adipocytes via A2A receptors. Nature 516, 395-399 (2014).
11. Frontini, A. & Cinti, S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 11, 253-256 (2010).
12. Lo, K. A. & Sun, L. Turning WAT into BAT: A review on regulators controlling the browning of white adipocytes. Biosci. Rep. 33, 711-719 (2013).
13. Jespersen, N. Z. et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 17, 798-805 (2013).
14. Sharp, L. Z. et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS ONE 7, e49452 (2012).
15. Wu, J. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376 (2012).
16. Cypess, A. M. et al. Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat. Med. 19, 635-639 (2013).
17. Shabalina, I. G. et al. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 5, 1196-1203 (2013).
18. Meister, G. & Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343-349 (2004).
19. Mello, C. C. & Conte, Jr D. Revealing the world of RNA interference. Nature 431, 338-342 (2004).
20. Pfeifer, A. & Lehmann, H. Pharmacological potential of RNAi-focus on miRNA. Pharmacol. Ther. 126, 217-227 (2010).
21. Trajkovski, M. & Lodish, H. MicroRNA networks regulate development of brown adipocytes. Trends Endocrinol. Metab. 24, 442-450 (2013).
22. Wu, Y. et al. Identification of miR-106b-93 as a negative regulator of brown adipocyte differentiation. Biochem. Biophys. Res. Commun. 438, 575-580 (2013).
23. Trajkovski, M., Ahmed, K., Esau, C. C. & Stoffel, M. MyomiR-133 regulates brown fat differentiation through Prdm16. Nat. Cell Biol. 14, 1330-1335 (2012).
24. Pan, D. et al. MicroRNA-378 controls classical brown fat expansion to counteract obesity. Nat. Commun. 5, 4725 (2014).
25. Chen, Y. et al. miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat. Commun. 4, 1769 (2013).
26. Mori, M., Nakagami, H., Rodriguez-Araujo, G., Nimura, K. & Kaneda, Y. Essential role for miR-196a in brown adipogenesis of white fat progenitor cells. PLoS Biol. 10, e1001314 (2012).
27. Raposo, G. & Stoorvogel, W. Extracellular vesicles: exosomes, microvesicles, and friends. J. Cell Biol. 200, 373-383 (2013).
28. Vlassov, A. V., Magdaleno, S., Setterquist, R. & Conrad, R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta 1820, 940-948 (2012).
29. Zhang, J. et al. Exosome and exosomal microRNA: Trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13, 17-24 (2015).
30. Mause, S. F. & Weber, C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 107, 1047-1057 (2010).
31. Thery, C., Zitvogel, L. & Amigorena, S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579 (2002).
32. Seale, P. et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121, 96-105 (2011).
33. Petrovic, N. et al. 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 (2010).
34. Keller, P. et al. Gene-chip studies of adipogenesis-regulated microRNAs in mouse primary adipocytes and human obesity. BMC Endocr Disord 11, 7 (2011).
35. van der Lans, A. A. et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J. Clin. Invest. 123, 3395-3403 (2013).
36. Villarroya, J., Cereijo, R. & Villarroya, F. An endocrine role for brown adipose tissue? Am. J. Physiol. Endocrinol. Metab. 305, E567-E572 (2013).
37. Pfeifer, A. NRG4: An endocrine link between brown adipose tissue and liver. Cell Metab. 21, 13-14 (2015).
38. Haas, B. et al. Protein kinase g controls brown fat cell differentiation and mitochondrial biogenesis. Sci. Signal. 2, ra78 (2009).
39. Nisoli, E. et al. Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide. Science 299, 896-899 (2003).
40. Lee, P. et al. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab. 19, 302-309 (2014).
41. Fisher, F. M. et al. FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 26, 271-281 (2012).
42. Wang, G. X. et al. The brown fat-enriched secreted factor Nrg4 preserves metabolic homeostasis through attenuation of hepatic lipogenesis. Nat. Med. 20, 1436-1443 (2014).
43. Zhou, W. et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 25, 501-515 (2014).
44. Fabbri, M. et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl Acad. Sci. USA 109, E2110-E2116 (2012).
45. Cortez, M. A. et al. MicroRNAs in body fluids-The mix of hormones and biomarkers. Nat. Rev. Clin. Oncol. 8, 467-477 (2011).
46. Ogata-Kawata, H. et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS ONE 9, e92921 (2014).
47. Wu, L. et al. Profiling peripheral microRNAs in obesity and type 2 diabetes mellitus. APMIS 123, 580-585 (2015).
48. Pescador, N. et al. Serum circulating microRNA profiling for identification of potential type 2 diabetes and obesity biomarkers. PLoS ONE 8, e77251 (2013).
49. Al-Kafaji, G. et al. Peripheral blood microRNA-15a is a potential biomarker for type 2 diabetes mellitus and pre-diabetes. Mol. Med. Rep. 12, 7485-7490 (2015).
50. Santovito, D. et al. Plasma exosome microRNA profiling unravels a new potential modulator of adiponectin pathway in diabetes: effect of glycemic control. J. Clin. Endocrinol. Metab. 99, E1681-E1685 (2014).
51. Woods, K., Thomson, J. M. & Hammond, S. M. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J. Biol. Chem. 282, 2130-2134 (2007).
52. Mogilyansky, E. & Rigoutsos, I. The miR-17/92 cluster: A comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ. 20, 1603-1614 (2013).
53. Ventura, A. et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132, 875-886 (2008).
54. He, L. et al. A microRNA polycistron as a potential human oncogene. Nature 435, 828-833 (2005).
55. Tanaka, M. et al. Downregulation of miR-92 in human plasma is a novel marker for acute leukemia patients. PLoS ONE 4, e5532 (2009).
56. Al-Nakhle, H. et al. Estrogen receptor {beta}1 expression is regulated by miR-92 in breast cancer. Cancer Res. 70, 4778-4784 (2010).
57. Shigoka, M. et al. Deregulation of miR-92a expression is implicated in hepatocellular carcinoma development. Pathol. Int. 60, 351-357 (2010).
58. Bonauer, A. et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324, 1710-1713 (2009).
59. Iaconetti, C. et al. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res. Cardiol. 107, 296 (2012).
60. Loyer, X. et al. Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ. Res. 114, 434-443 (2014).
61. Penzkofer, D. et al. Phenotypic characterization of miR-92a-/-mice reveals an important function of miR-92a in skeletal development. PLoS ONE 9, e101153 (2014).
62. Wang, Q. et al. miR-17-92 cluster accelerates adipocyte differentiation by negatively regulating tumor-suppressor Rb2/p130. Proc. Natl Acad. Sci. USA 105, 2889-2894 (2008).
63. Fischer, A. P., Seeger, D., Bonauer, T., Zeiher, A. & Dimmeler, S. Genetic deletion and pharmacological inhibition of MiR-92a reduce obesity. Circulation 130: A16501 (2014).
64. Nedergaard, J., Bengtsson, T. & Cannon, B. Unexpected evidence for active brown adipose tissue in adult humans. Am. J. Physiol. Endocrinol. Metab. 293, E444-E452 (2007).
65. Mitschke, M. M. et al. Increased cGMP promotes healthy expansion and browning of white adipose tissue. FASEB J. 27, 1621-1630 (2013).
66. Hanssen, M. J. et al. Glucose uptake in human brown adipose tissue is impaired upon fasting-induced insulin resistance. Diabetologia 58, 586-595 (2015).
67. Vosselman, M. J. et al. Systemic beta-Adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes 61, 3106-3113 (2012).
68. van der Lans, A. A. et al. Cold-Activated brown adipose tissue in human adults: methodological issues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307, R103-R113 (2014).
69. Orava, J. et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 14, 272-279 (2011).
70. Orava, J. et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring) 21, 2279-2287 (2013).