TGR5 signalling promotes mitochondrial fission and beige remodelling of white adipose tissue

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Velazquez Villegas, Laura A ^a   Perino, Alessia ^a   Lemos, Vera ^a,b   Zietak, Marika ^a,c   Nomura, Mitsunori ^a   Pols, Thijs Willem Hendrik ^a   Schoonjans, Kristina ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF PORTO   (Portugal)

^c INSTITUTE OF ANIMAL REPRODUCTION AND FOOD RESEARCH   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; FATTY ACID; MEMBRANE RECEPTOR; G PROTEIN COUPLED RECEPTOR; GPBAR1 PROTEIN, MOUSE;

BIOMARKER; CELL; DISABILITY; ENVIRONMENTAL CUE; FAT; FATTY ACID; FEEDING; MEMBRANE; MITOCHONDRION; OXIDATION;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEIGE ADIPOSE TISSUE; CALORIC INTAKE; CELL DIFFERENTIATION; CONTROLLED STUDY; FATTY ACID OXIDATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; THERMOGENESIS; WHITE ADIPOSE TISSUE; 3T3-L1 CELL LINE; ANIMAL; BEIGE ADIPOCYTE; CELL LINE; CYTOLOGY; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRIAL DYNAMICS; SUBCUTANEOUS FAT; TEMPERATURE; WHITE ADIPOCYTE;

MUS;

3T3-L1 CELLS; ADIPOCYTES, BEIGE; ADIPOCYTES, WHITE; ADIPOSE TISSUE, BEIGE; ADIPOSE TISSUE, WHITE; ANIMALS; CELL DIFFERENTIATION; CELL LINE; FATTY ACIDS, NONESTERIFIED; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIAL DYNAMICS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; TEMPERATURE;

EID: 85040824941     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02068-0     Document Type: Article

References (70)

1. Giralt, M. & Villarroya, F. White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154, 2992-3000 (2013).
2. Wu, J. et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376 (2012).
3. Fedorenko, A., Lishko, P. V. & Kirichok, Y. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151, 400-413 (2012).
4. Matthias, A. et al. Thermogenic responses in brown fat cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. J. Biol. Chem. 275, 25073-25081 (2000).
5. Nedergaard, J. & Cannon, B. The Browning of white adipose tissue: some burning issues. Cell Metab. 20, 396-407 (2014).
6. Shabalina, I. G. et al. UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep. 5, 1196-1203 (2013).
7. Sidossis, L. & Kajimura, S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J. Clin. Invest. 125, 478-486 (2015).
8. Farmer, S. R. Transcriptional control of adipocyte formation. Cell Metab. 4, 263-273 (2006).
9. Gesta, S., Tseng, Y. H. & Kahn, C. R. Developmental origin of fat: tracking obesity to its source. Cell 131, 242-256 (2007).
10. Kajimura, S. et al. Initiation of myoblast to brown fat switch by a PRDM16-C/ EBP-beta transcriptional complex. Nature 460, 1154-1158 (2009).
11. Seale, P. et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967 (2008).
12. Seale, P. et al. Transcriptional control of brown fat determination by PRDM16. Cell Metab. 6,38-54 (2007).
13. Barbera, M. J. et al. Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene. A link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J. Biol. Chem. 276, 1486-1493 (2001).
14. Cannon, B. & Nedergaard, J. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359 (2004).
15. Desautels, M. & Himms-Hagen, J. Roles of noradrenaline and protein synthesis in the cold-induced increase in purine nucleotide binding by rat brown adipose tissue mitochondria. Can. J. Biochem. 57, 968-976 (1979).
16. Nahmias, C. et al. Molecular characterization of the mouse beta 3-adrenergic receptor: relationship with the atypical receptor of adipocytes. EMBO J. 10, 3721-3727 (1991).
17. Worthmann, A. et al. Cold-induced conversion of cholesterol to bile acids in mice shapes the gut microbiome and promotes adaptive thermogenesis. Nat. Med. 23, 839-849 (2017).
18. Zietak, M. et al. Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab. 23, 1216-1223 (2016).
19. Watanabe, M. et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439, 484-489 (2006).
20. Kuipers, F., Bloks, V. W. & Groen, A. K. Beyond intestinal soap-bile acids in metabolic control. Nat. Rev. Endocrinol. 10, 488-498 (2014).
21. Lefebvre, P., Cariou, B., Lien, F., Kuipers, F. & Staels, B. Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89, 147-191 (2009).
22. Thomas, C., Pellicciari, R., Pruzanski, M., Auwerx, J. & Schoonjans, K. Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov. 7, 678-693 (2008).
23. Perino, A. & Schoonjans, K. TGR5 and Immunometabolism: insights from physiology and pharmacology. Trends Pharmacol. Sci. 36, 847-857 (2015).
24. Watanabe, M. et al. Bile acid binding resin improves metabolic control through the induction of energy expenditure. PLoS ONE 7, e38286 (2012).
25. Perino, A. et al. TGR5 reduces macrophage migration through mTOR-induced C/EBPbeta differential translation. J. Clin. Invest. 124, 5424-5436 (2014).
26. Thomas, C. et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10, 167-177 (2009).
27. Pols, T. W. et al. TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab. 14, 747-757 (2011).
28. Broeders, E. P. et al. The bile acid chenodeoxycholic acid increases human brown adipose tissue activity. Cell Metab. 22, 418-426 (2015).
29. Rosell, M. et al. 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 (2014).
30. Van der Lans, A. A. et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J. Clin. Invest. 123, 3395-3403 (2013).
31. Garcia-Ruiz, E. et al. The intake of high-fat diets induces the acquisition of brown adipocyte gene expression features in white adipose tissue. Int. J. Obes. 39, 1619-1629 (2015).
32. van de Peppel, J. et al. Identification of three early phases of cell-fate determination during osteogenic and adipogenic differentiation by transcription factor dynamics. Stem Cell Rep. 8, 947-960 (2017).
33. Fischer-Posovszky, P., Newell, F. S., Wabitsch, M. & Tornqvist, H. E. Human SGBS cells - a unique tool for studies of human fat cell biology. Obes. Facts 1 , 184-189 (2008).
34. Wabitsch, M. et al. Characterization of a human preadipocyte cell strain with high capacity for adipose differentiation. Int. J. Obes. Relat. Metab. Disord. 25, 8-15 (2001).
35. Yeo, C. R. et al. SGBS cells as a model of human adipocyte browning: a comprehensive comparative study with primary human white subcutaneous adipocytes. Sci. Rep. 7, 4031 (2017).
36. Wikstrom, J. D. et al. Hormone-induced mitochondrial fission is utilized by brown adipocytes as an amplification pathway for energy expenditure. EMBO J. 33, 418-436 (2014).
37. Fu, L. et al. SIRT4 inhibits malignancy progression of NSCLCs, through mitochondrial dynamics mediated by the ERK-Drp1 pathway. Oncogene 36, 2724-2736 (2017).
38. Prieto, J. et al. Early ERK1/2 activation promotes DRP1-dependent mitochondrial fission necessary for cell reprogramming. Nat. Commun. 7, 11124 (2016).
39. Chou, C. H. et al. GSK3beta-mediated Drp1 phosphorylation induced elongated mitochondrial morphology against oxidative stress. PLoS ONE 7, e49112 (2012).
40. Li, X. et al. cAMP signalling prevents podocyte apoptosis via activation of protein kinase A and mitochondrial fusion. PLoS ONE 9, e92003 (2014).
41. Loh, J. K. et al. GSKIP- and GSK3-mediated anchoring strengthens cAMP/ PKA/Drp1 axis signalling in the regulation of mitochondrial elongation. Biochim. Biophys. Acta 1853, 1796-1807 (2015).
42. Gandre-Babbe, S. & van der Bliek, A. M. The novel tail-anchored membrane protein Mff controls mitochondrial and peroxisomal fission in mammalian cells. Mol. Biol. Cell 19, 2402-2412 (2008).
43. Loson, O. C., Song, Z., Chen, H. & Chan, D. C. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659-667 (2013).
44. Otera, H. et al. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191, 1141-1158 (2010).
45. Kelly, D. P. & Scarpulla, R. C. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368 (2004).
46. Wu, Z. et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124 (1999).
47. Liesa, M. & Shirihai, O. S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 17, 491-506 (2013).
48. Qian, S., Huang, H. & Tang, Q. Brown and beige fat: the metabolic function, induction, and therapeutic potential. Front. Med. 9, 162-172 (2015).
49. Aune, U. L., Ruiz, L. & Kajimura, S. Isolation and differentiation of stromal vascular cells to beige/brite cells. J. Vis. Exp. https://doi.org/10.3791/50191 (2013).
50. Bayindir, I. et al. Transcriptional pathways in cPGI2-induced adipocyte progenitor activation for browning. Front. Endocrinol. 6, 129 (2015).
51. Matsukawa, T., Villareal, M. O., Motojima, H. & Isoda, H. Increasing cAMP levels of preadipocytes by cyanidin-3-glucoside treatment induces the formation of beige phenotypes in 3T3-L1 adipocytes. J. Nutr. Biochem. 40, 77-85 (2017).
52. McGlashon, J. M. et al. Central serotonergic neurons activate and recruit thermogenic brown and beige fat and regulate glucose and lipid homeostasis. Cell Metab. 21, 692-705 (2015).
53. Zhu, Y. et al. Connexin 43 mediates white adipose tissue beiging by facilitating the propagation of sympathetic neuronal signals. Cell Metab. 24, 420-433 (2016).
54. Liu, P. S., Lin, Y. W., Burton, F. H. & Wei, L. N. M1-M2 balancing act in white adipose tissue browning - a new role for RIP140. Adipocyte 4, 146-148 (2015).
55. Man, K., Kutyavin, V. I. & Chawla, A. Tissue immunometabolism: development, physiology, and pathobiology. Cell Metab. 25,11-26 (2017).
56. Wu, D. et al. Eosinophils sustain adipose alternatively activated macrophages associated with glucose homeostasis. Science 332, 243-247 (2011).
57. Zietak, M. & Kozak, L. P. Bile acids induce uncoupling protein 1-dependent thermogenesis and stimulate energy expenditure at thermoneutrality in mice. Am. J. Physiol. Endocrinol. Metab. 310, E346-E354 (2016).
58. Liesa, M., Palacin, M. & Zorzano, A. Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 89, 799-845 (2009).
59. Twig, G., Hyde, B. & Shirihai, O. S. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim. Biophys. Acta 1777, 1092-1097 (2008).
60. Divakaruni, A. S., Humphrey, D. M. & Brand, M. D. Fatty acids change the conformation of uncoupling protein 1 (UCP1). J. Biol. Chem. 287, 36845-36853 (2012).
61. Shabalina, I. G., Backlund, E. C., Bar-Tana, J., Cannon, B. & Nedergaard, J. Within brown-fat cells, UCP1-mediated fatty acid-induced uncoupling is independent of fatty acid metabolism. Biochim. Biophys. Acta 1777, 642-650 (2008).
62. Chenette, E. J. Generating energy with mitochondrial fission. Nat. Cell Biol. 16, 307-307 (2014).
63. Dutia, R. et al. Temporal changes in bile acid levels and 12alpha-hydroxylation after Roux-en-Y gastric bypass surgery in type 2 diabetes. Int. J. Obes. 39, 806-813 (2015).
64. Kaska, L., Sledzinski, T., Chomiczewska, A., Dettlaff-Pokora, A. & Swierczynski, J. Improved glucose metabolism following bariatric surgery is associated with increased circulating bile acid concentrations and remodelling of the gut microbiome. World J. Gastroenterol. 22, 8698-8719 (2016).
65. Pournaras, D. J. et al. The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology 153, 3613-3619 (2012).
66. Steinert, R. E. et al. Bile acids and gut peptide secretion after bariatric surgery: a 1-year prospective randomized pilot trial. Obesity 21 , E660-E668 (2013).
67. Sato, H. et al. Novel potent and selective bile acid derivatives as TGR5 agonists: biological screening, structure-activity relationships, and molecular modeling studies. J. Med. Chem. 51, 1831-1841 (2008).
68. Galarraga, M. et al. Adiposoft: automated software for the analysis of white adipose tissue cellularity in histological sections. J. Lipid Res. 53, 2791-2796 (2012) .
69. Nguyen, D. Quantifying chromogen intensity in immunohistochemistry via reciprocal intensity. Protoc. Exch. https://doi.org/10.1038/protex.2013.097 (2013) .
70. Arques, O., Chicote, I., Tenbaum, S., Puig, I. & Palmer, H. G. Standardized relative quantification of immunofluorescence tissue staining. Protoc. Exch. https://doi.org/10.1038/protex.2014.018 (2012).