Lsd1 Ablation Triggers Metabolic Reprogramming of Brown Adipose Tissue

Cell Reports

Volumn 17, Issue 4, 2016, Pages 1008-1021

  Duteil, Delphine ^a   Tosic, Milica ^a   Lausecker, Franziska ^a   Nenseth, Hatice Z ^a   Müller, Judith M ^a   Urban, Sylvia ^a   Willmann, Dominica ^a   Petroll, Kerstin ^a,b   Messaddeq, Nadia ^c   Arrigoni, Laura ^d   Manke, Thomas ^d   Kornfeld, Jan Wilhelm ^e   Brüning, Jens C ^e   Zagoriy, Vyacheslav ^f   Meret, Michael ^f   Dengjel, Jörn ^g   Kanouni, Toufike ^h   Schüle, Roland ^a,i,j  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Centre for Biological Systems Analysis (ZBSA)   (Germany)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^e MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^f MetaSysX GmbH   (Germany)

^g UNIVERSITY OF FRIBOURG   (Switzerland)

^h CELGENE CORPORATION   (United States)

ⁱ UNIVERSITY OF FREIBURG   (Germany)

^j Deutsches Konsortium für Translationale Krebsforschungs dktk   (Germany)

more..

Author keywords

adipocyte; brown adipose tissue; carbohydrate metabolism; CoREST; epigenetics; lipid metabolism; lysine specific demethylase 1; obesity; thermogenesis; white adipose tissue

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); LYSINE SPECIFIC DEMETHYLASE 1; PROTEIN COREST; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1; UNCLASSIFIED DRUG; AOF2 PROTEIN, MOUSE; GLUCOSE; HISTONE DEMETHYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE DELETION; GENE EXPRESSION REGULATION; GLYCOLYSIS; MALE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATION; PRIORITY JOURNAL; PROTEIN DEPLETION; THERMOGENESIS; UPREGULATION; WHITE ADIPOCYTE; WHITE ADIPOSE TISSUE; ANIMAL; BIOLOGICAL MODEL; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; OXIDATION REDUCTION REACTION; WEIGHT GAIN;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; GENE DELETION; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOLYSIS; HISTONE DEMETHYLASES; LIPID METABOLISM; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; WEIGHT GAIN;

EID: 84994824112     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.09.053     Document Type: Article

References (37)

1. Betz, M.J., Enerbäck, S., Human Brown Adipose Tissue: What We Have Learned So Far. Diabetes 64 (2015), 2352–2360.
2. Birsoy, K., Wang, T., Chen, W.W., Freinkman, E., Abu-Remaileh, M., Sabatini, D.M., An Essential Role of the Mitochondrial Electron Transport Chain in Cell Proliferation Is to Enable Aspartate Synthesis. Cell 162 (2015), 540–551.
3. Cai, C., He, H.H., Gao, S., Chen, S., Yu, Z., Gao, Y., Chen, S., Chen, M.W., Zhang, J., Ahmed, M., et al. Lysine-specific demethylase 1 has dual functions as a major regulator of androgen receptor transcriptional activity. Cell Rep. 9 (2014), 1618–1627.
4. Cannon, B., Nedergaard, J., Brown adipose tissue: function and physiological significance. Physiol. Rev. 84 (2004), 277–359.
5. Cohen, P., Spiegelman, B.M., Brown and Beige Fat: Molecular Parts of a Thermogenic Machine. Diabetes 64 (2015), 2346–2351.
6. Duteil, D., Metzger, E., Willmann, D., Karagianni, P., Friedrichs, N., Greschik, H., Günther, T., Buettner, R., Talianidis, I., Metzger, D., Schüle, R., LSD1 promotes oxidative metabolism of white adipose tissue. Nat. Commun., 5, 2014, 4093.
7. Ellis, J.M., Li, L.O., Wu, P.C., Koves, T.R., Ilkayeva, O., Stevens, R.D., Watkins, S.M., Muoio, D.M., Coleman, R.A., Adipose acyl-CoA synthetase-1 directs fatty acids toward beta-oxidation and is required for cold thermogenesis. Cell Metab. 12 (2010), 53–64.
8. Feng, Z., Yao, Y., Zhou, C., Chen, F., Wu, F., Wei, L., Liu, W., Dong, S., Redell, M., Mo, Q., Song, Y., Pharmacological inhibition of LSD1 for the treatment of MLL-rearranged leukemia. J. Hematol. Oncol., 9, 2016, 24.
9. Fitzgibbons, T.P., Kogan, S., Aouadi, M., Hendricks, G.M., Straubhaar, J., Czech, M.P., Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am. J. Physiol. Heart Circ. Physiol. 301 (2011), H1425–H1437.
10. Giavalisco, P., Köhl, K., Hummel, J., Seiwert, B., Willmitzer, L., 13C isotope-labeled metabolomes allowing for improved compound annotation and relative quantification in liquid chromatography-mass spectrometry-based metabolomic research. Anal. Chem. 81 (2009), 6546–6551.
11. Giralt, M., Martin, I., Iglesias, R., Viñas, O., Villarroya, F., Mampel, T., Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5′-deiodinase activity is necessary for the response to environmental temperature at birth. Eur. J. Biochem. 193 (1990), 297–302.
12. Harms, M.J., Ishibashi, J., Wang, W., Lim, H.W., Goyama, S., Sato, T., Kurokawa, M., Won, K.J., Seale, P., Prdm16 is required for the maintenance of brown adipocyte identity and function in adult mice. Cell Metab. 19 (2014), 593–604.
13. Kleiner, S., Mepani, R.J., Laznik, D., Ye, L., Jurczak, M.J., Jornayvaz, F.R., Estall, J.L., Chatterjee Bhowmick, D., Shulman, G.I., Spiegelman, B.M., Development of insulin resistance in mice lacking PGC-1α in adipose tissues. Proc. Natl. Acad. Sci. USA 109 (2012), 9635–9640.
14. Langin, D., Recruitment of brown fat and conversion of white into brown adipocytes: strategies to fight the metabolic complications of obesity?. Biochim. Biophys. Acta 1801 (2010), 372–376.
15. Lee, M.G., Wynder, C., Cooch, N., Shiekhattar, R., An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437 (2005), 432–435.
16. Lee, Y.H., Jung, Y.S., Choi, D., Recent advance in brown adipose physiology and its therapeutic potential. Exp. Mol. Med., 46, 2014, e78.
17. Lee, Y.H., Mottillo, E.P., Granneman, J.G., Adipose tissue plasticity from WAT to BAT and in between. Biochim. Biophys. Acta 1842 (2014), 358–369.
18. Lee, J., Choi, J., Aja, S., Scafidi, S., Wolfgang, M.J., Loss of Adipose Fatty Acid Oxidation Does Not Potentiate Obesity at Thermoneutrality. Cell Rep. 14 (2016), 1308–1316.
19. Liu, X., Rossmeisl, M., McClaine, J., Riachi, M., Harper, M.E., Kozak, L.P., Paradoxical resistance to diet-induced obesity in UCP1-deficient mice. J. Clin. Invest. 111 (2003), 399–407.
20. Metzger, E., Wissmann, M., Yin, N., Müller, J.M., Schneider, R., Peters, A.H., Günther, T., Buettner, R., Schüle, R., LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437 (2005), 436–439.
21. Metzger, E., Willmann, D., McMillan, J., Forne, I., Metzger, P., Gerhardt, S., Petroll, K., von Maessenhausen, A., Urban, S., Schott, A.K., et al. Assembly of methylated KDM1A and CHD1 drives androgen receptor-dependent transcription and translocation. Nat. Struct. Mol. Biol. 23 (2016), 132–139.
22. Musri, M.M., Carmona, M.C., Hanzu, F.A., Kaliman, P., Gomis, R., Párrizas, M., Histone demethylase LSD1 regulates adipogenesis. J. Biol. Chem. 285 (2010), 30034–30041.
23. Peirce, V., Vidal-Puig, A., Regulation of glucose homoeostasis by brown adipose tissue. Lancet Diabetes Endocrinol. 1 (2013), 353–360.
24. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M., Spiegelman, B.M., A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (1998), 829–839.
25. Sambeat, A., Gulyaeva, O., Dempersmier, J., Tharp, K.M., Stahl, A., Paul, S.M., Sul, H.S., LSD1 Interacts with Zfp516 to Promote UCP1 Transcription and Brown Fat Program. Cell Rep. 15 (2016), 2536–2549.
26. Schoiswohl, G., Stefanovic-Racic, M., Menke, M.N., Wills, R.C., Surlow, B.A., Basantani, M.K., Sitnick, M.T., Cai, L., Yazbeck, C.F., Stolz, D.B., et al. Impact of Reduced ATGL-Mediated Adipocyte Lipolysis on Obesity-Associated Insulin Resistance and Inflammation in Male Mice. Endocrinology 156 (2015), 3610–3624.
27. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A., Casero, R.A., Shi, Y., Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119 (2004), 941–953.
28. Tiraby, C., Langin, D., Conversion from white to brown adipocytes: a strategy for the control of fat mass?. Trends Endocrinol. Metab. 14 (2003), 439–441.
29. Turpin, S.M., Nicholls, H.T., Willmes, D.M., Mourier, A., Brodesser, S., Wunderlich, C.M., Mauer, J., Xu, E., Hammerschmidt, P., Brönneke, H.S., et al. Obesity-induced CerS6-dependent C16:0 ceramide production promotes weight gain and glucose intolerance. Cell Metab. 20 (2014), 678–686.
30. Vernochet, C., Mourier, A., Bezy, O., Macotela, Y., Boucher, J., Rardin, M.J., An, D., Lee, K.Y., Ilkayeva, O.R., Zingaretti, C.M., et al. Adipose-specific deletion of TFAM increases mitochondrial oxidation and protects mice against obesity and insulin resistance. Cell Metab. 16 (2012), 765–776.
31. Vizcaíno, J.A., Csordas, A., del-Toro, N., Dianes, J.A., Griss, J., Lavidas, I., Mayer, G., Perez-Riverol, Y., Reisinger, F., Ternent, T., et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 44:D1 (2016), D447–D456.
32. Wu, M., Neilson, A., Swift, A.L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J., et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292 (2007), C125–C136.
33. Wu, J., Boström, P., Sparks, L.M., Ye, L., Choi, J.H., Giang, A.H., Khandekar, M., Virtanen, K.A., Nuutila, P., Schaart, G., et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150 (2012), 366–376.
34. Yang, P., Wang, Y., Chen, J., Li, H., Kang, L., Zhang, Y., Chen, S., Zhu, B., Gao, S., RCOR2 is a subunit of the LSD1 complex that regulates ESC property and substitutes for SOX2 in reprogramming somatic cells to pluripotency. Stem Cells 29 (2011), 791–801.
35. Zeng, X., Jedrychowski, M.P., Chen, Y., Serag, S., Lavery, G.G., Gygi, S.P., Spiegelman, B.M., Lysine-specific demethylase 1 promotes brown adipose tissue thermogenesis via repressing glucocorticoid activation. Genes Dev. 30 (2016), 1822–1836.
36. Zhang, Q., Wang, S.Y., Fleuriel, C., Leprince, D., Rocheleau, J.V., Piston, D.W., Goodman, R.H., Metabolic regulation of SIRT1 transcription via a HIC1:CtBP corepressor complex. Proc Natl Acad Sci USA 104 (2007), 829–833.
37. Zhu, D., Hölz, S., Metzger, E., Pavlovic, M., Jandausch, A., Jilg, C., Galgoczy, P., Herz, C., Moser, M., Metzger, D., et al. Lysine-specific demethylase 1 regulates differentiation onset and migration of trophoblast stem cells. Nat. Commun., 5, 2014, 3174.