Browning of white adipose cells by intermediate metabolites: An adaptive mechanism to alleviate redox pressure

Diabetes

Volumn 63, Issue 10, 2014, Pages 3253-3265

  Carrière, Audrey ^a,b,c,d   Jeanson, Yannick ^a,b,c,d   Berger Müller, Sandra ^a,b,c,d   André, Mireille ^a,b,c,d   Chenouard, Vanessa ^a,b,c,d   Arnaud, Emmanuelle ^a,b,c,d   Barreau, Corinne ^a,b,c,d   Walther, Romy ^a,b,c,d   Galinier, Anne ^a,b,c,d   Wdziekonski, Brigitte ^e   Villageois, Phi ^e   Louche, Katie ^f   Collas, Philippe ^g   Moro, Cédric ^f   Dani, Christian ^e   Villarroya, Francesc ^h   Casteilla, Louis ^a,b,c,d  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c INSERM   (France)

^d ETABLISSEMENT FRANÇAIS DU SANG   (France)

^e UNIVERSITÉ CÔTE D'AZUR   (France)

^f Université de Toulouse   (France)

^g UNIVERSITY OF OSLO   (Norway)

^h UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ADIPONECTIN; FATTY ACID BINDING PROTEIN 4; FIBROBLAST GROWTH FACTOR 21; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KETONE BODY; LACTIC ACID; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCOUPLING PROTEIN 1; VASCULOTROPIN;

ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EPIDIDYMIS FAT; FATTY ACID OXIDATION; GENE EXPRESSION; GLUCOSE INTAKE; GLYCATION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; LACTATE BLOOD LEVEL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PHENOTYPE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THERMOGENESIS; UPREGULATION; WHITE ADIPOSE TISSUE; ANIMAL; C57BL MOUSE; ENERGY METABOLISM; METABOLISM; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PHYSIOLOGY; STEM CELL;

ADIPOCYTES, BROWN; ADIPOCYTES, WHITE; ADIPOGENESIS; ANIMALS; ENERGY METABOLISM; HUMANS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PPAR GAMMA; STEM CELLS;

EID: 84907485620     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1885     Document Type: Article

References (48)

1. Algire C, Medrikova D, Herzig S. White and brown adipose stem cells: from signaling to clinical implications. Biochim Biophys Acta 2013;1831:896-904
2. Nicholls DG, Locke RM. Thermogenic mechanisms in brown fat. Physiol Rev 1984;64:1-64
3. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359
4. Bouillaud F, Villarroya F, Hentz E, Raimbault S, Cassard AM, Ricquier D. Detection of brown adipose tissue uncoupling protein mRNA in adult patients by a human genomic probe. Clin Sci (Lond) 1988;75:21-27
5. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Coldactivated brown adipose tissue in healthy men. N Engl J Med 2009;360:1500-1508
6. Loncar D. Convertible adipose tissue in mice. Cell Tissue Res 1991;266: 149-161
7. Cousin B, Cinti S, Morroni M, et al. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci 1992;103:931-942
8. Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev 2013;27:234-250
9. Barte It A, Bruns OT, Reimer R, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med 2011;17:200-205
10. Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol 2014;10:24-36
11. Kopecky J, Clarke G, Enerbäck S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 1995;96:2914-2923
12. Haiestrap AP. The SLC16 gene family - structure, role and regulation in health and disease. Mol Aspects Med 2013;34:337-349
13. Hajduch E, Heyes RR, Watt PW, Hundal HS. Lactate transport in rat adipocytes: identification of monocarboxylate transporter 1 (MCT1) and its modulation during streptozotocin-induced diabetes. FEES Lett 2000;479:89-92
14. Iwanaga T, Kuchiiwa T, Saito M. Histochemical demonstration of monocarboxylate transporters in mouse brown adipose tissue. Biomed Res 2009;30: 217-225
15. De Matteis R, Lucertini F, Guescini M, et al. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr Metab Cardiovasc Dis 2013;23: 582-590
16. Pérez de Heredia F, Wood IS, Trayhurn P. Hypoxia stimulates lactate release and modulates monocarboxylate transporter (MCT1, MCT2, and MCT4) expression in human adipocytes. Pflugers Arch 2010;459:509-518
17. Ahmed K, Tunaru S, Offermanns S. GPR109A, GPR109B and GPR81, a family of hydroxy-carboxylic acid receptors. Trends Pharmacol Sci 2009;30: 557-562
18. Leverve XM, Mustafa I. Lactate: A key metabolite in the intercellular metabolic interplay. Grit Care 2002;6:284-285
19. Brooks GA. Cell-cell and intracellular lactate shuttles. J Physiol 2009;587: 5591-5600
20. Pellerin L, Magistretti PJ. Sweet sixteen for ANLS. J Cereb Blood Flow Metab 2012;32:1152-1166
21. Sonveaux P, Végran F, Schroeder T, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008;118:3930-3942
22. Sonveaux P, Copetti T, De Saedeleer CJ, et al. Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis. PLoS ONE 2012;7:e33418
23. Végran F, Boidot R, Michiels C, Sonveaux P, Feron O. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 2011;71:2550-2560
24. Hashimoto T, Hussien R, Oommen S, Gohil K, Brooks GA. Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis. FASEB J 2007;21:2602-2612
25. Form by B, Stern R. Lactate-sensitive response elements in genes involved in hyaluronan catabolism. Biochem Biophys Res Commun 2003;305:203-208
26. Samuvel DJ, Sundararaj KP, Nareika A, Lopes-Virella MF, Huang Y. Lactate boosts TLR4 signaling and NF-kappaB pathway-mediated gene transcription in macrophages via monocarboxylate transporters and MD-2 up-regulation. J Immunol 2009;182:2476-2484
27. Planat-Benard V, Silvestre JS, Cousin B, et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 2004;109:656-663
28. Brown SE, Tong W, Krebsbach PH. The derivation of mesenchymal stem cells from human embryonic stem cells. Cells Tissues Organs 2009;189:256-260
29. Taura D, Noguchi M, Sone M, et al. Adipogenic differentiation of human induced pluripotent stem cells: comparison with that of human embryonic stem cells. FEBS Lett 2009;583:1029-1033
30. (a). Mohsen-Kanson T, Hafner AL, Wdziekonski B, et al. Differentiation of human induced pluripotent stem cells into brown and white adipocytes: role of Pax3. Stem Cells 2014;32:1459-1467
31. Carrière A, Carmona MC, Fernandez Y, et al. Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. J Biol Chem 2004;279: 40462-40469
32. Dimmer KS, Friedrich B, Lang F, Deitmer JW, Bröer S. The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem J 2000;350:219-227
33. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007;129:111-122
34. Brahimi-Horn MC, Bellot G, Pouysségur J. Hypoxia and energetic tumour metabolism. Curr Opin Genet Dev 2011;21:67-72
35. Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. 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 2010 285 7153-7164 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;285:7153-7164
36. Ohno H, Shinoda K, Spiegelman BM, Kajimura S. PPARγy agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab 2012;15:395-404
37. Liu C, Kuei C, Zhu J, et al. 3,5-Dihydroxybenzoic acid, a specific agonist for hydroxycarboxylic acid 1, inhibits lipolysis in adipocytes. J Pharmacol Exp Ther 2012;341:794-801
38. Kennedy KM, Dewhirst MW. Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol 2010;6:127 -148
39. Philp A, Macdonald AL, Watt PW. Lactate-a signal coordinating cell and systemic function. J Exp Biol 2005;208:4561-4575
40. Walenta S, Schroeder T, Mueller-Klieser W. Lactate in solid malignant tumors: potential basis of a metabolic classification in clinical oncology. Curr Med Chem 2004;11:2195-2204
41. Ahmed K, Tunaru S, Tang C, et al. An autocrine lactate loop mediates insulindependent inhibition of lipolysis through GPR81. Cell Metab 2010;11:311-319
42. Chiarugi A, Dölle C, Felici R, Ziegler M. The NAD metabolome-a key determinant of cancer cell biology. Nat Rev Cancer 2012;12:741-752
43. Kajimura S, Seale P, Tomaru T, et al. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev 2008;22:1397-1409
44. Zhang Q, Wang SY, Nottke AC, Rocheleau JV, Piston DW, Goodman RH. Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc Natl Acad Sci USA 2006;103:9029-9033
45. Qiang L, Wang L, Kon N, et al. Brown remodeling of white adipose tissue by SirT 1 -dependent deacetylation of Ppar-γ. Cell 2012;150:620-632
46. Boström P, Wu J, Jedrychowski MP, et al. A PGC1 -a-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012;481:463-468
47. Srivastava S, Kashiwaya Y, King MT, et al. Mitochondrial biogenesis and increased uncoupling protein 1 in brown adipose tissue of mice fed a ketone ester diet. FASEB J 2012;26:2351-2362
48. Bougneres PF, Lemmel C, Ferré P, Bier DM. Ketone body transport in the human neonate and infant. J Clin Invest 1986;77:42-48