Identification of the transcription factor ZEB1 as a central component of the adipogenic gene regulatory network

eLife

Volumn 3, Issue August2014, 2014, Pages 1-30

  Gubelmann, Carine ^a   Schwalie, Petra C ^a   Raghav, Sunil K ^a,d   Röder, Eva ^b   Delessa, Tenagne ^b   Kiehlmann, Elke ^b   Waszak, Sebastian M ^a,e   Corsinotti, Andrea ^a,f   Udin, Gilles ^a   Holcombe, Wiebke ^a   Rudofsky, Gottfried ^c   Trono, Didier ^a   Wolfrum, Christian ^b   Deplancke, Bart ^a  

^a EPFL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c KANTONSSPITAL   (Switzerland)

^d INSTITUTE OF LIFE SCIENCES   (India)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; HOMEODOMAIN PROTEIN; KRUPPEL LIKE FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN BINDING; TRANSCRIPTION FACTOR; ZEB1 PROTEIN, MOUSE;

3T3 CELL LINE; ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL; C3H MOUSE; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; CYTOLOGY; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETICS; HUMAN; METABOLISM; MOUSE; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; GENE EXPRESSION; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C3H; PPAR GAMMA; PROTEIN BINDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84922762247     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03346     Document Type: Article

References (91)

1. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11:R106. doi: 10.1186/gb-2010-11-10-r106.
2. Asada M, Rauch A, Shimizu H, Maruyama H, Miyaki S, Shibamori M, Kawasome H, Ishiyama H, Tuckermann J, Asahara H. 2011. DNA binding-dependent glucocorticoid receptor activity promotes adipogenesis via Krüppel-like factor 15 gene expression. Laboratory Investigation 91:203-215. doi: 10.1038/labinvest.2010.170.
3. Bailey TL, Williams N, Misleh C, Li WW. 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research 34:W369-W373. doi: 10.1093/nar/gkl198.
4. Barde I, Salmon P, Trono D. 2010. Production and titration of lentiviral vectors. Current Protocols in Neuroscience Chapter 4, Unit 4.21. doi: 10.1002/0471142301.ns0421s53.
5. Barde I, Zanta-Boussif MA, Paisant S, Leboeuf M, Rameau P, Delenda C, Danos O. 2006. Efficient control of gene expression in the hematopoietic system using a single Tet-on inducible lentiviral vector. Molecular Therapy 13:382-390. doi: 10.1016/j.ymthe.2005.09.012.
6. Billon N, Kolde R, Reimand J, Monteiro MC, Kull M, Peterson H, Tretyakov K, Adler P, Wdziekonski B, Vilo J, Dani C. 2010. Comprehensive transcriptome analysis of mouse embryonic stem cell adipogenesis unravels new processes of adipocyte development. Genome Biology 11:R80. doi: 10.1186/gb-2010-11-8-r80.
7. Birsoy K, Chen Z, Friedman J. 2008. Transcriptional regulation of adipogenesis by KLF4. Cell Metabolism 7:339-347. doi: 10.1016/j.cmet.2008.02.001.
8. Bryne JC, Valen E, Tang MH, Marstrand T, Winther O, da Piedade I, Krogh A, Lenhard B, Sandelin A. 2008. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Research 36:D102-D106. doi: 10.1093/nar/gkm955.
9. Cawthorn WP, Scheller EL, MacDougald OA. 2012. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. Journal of Lipid Research 53:227-246. doi: 10.1194/jlr.R021089.
10. Cheng SL, Shao JS, Charlton-Kachigian N, Loewy AP, Towler DA. 2003. MSX2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. Journal of Biological Chemistry 278:45969-45977. doi: 10.1074/jbc.M306972200.
11. Cristancho AG, Schupp M, Lefterova MI, Cao S, Cohen DM, Chen CS, Steger DJ, Lazar MA. 2011. Repressor transcription factor 7-like 1 promotes adipogenic competency in precursor cells. Proceedings of the National Academy of Sciences of USA 108:16271-16276. doi: 10.1073/pnas.1109409108.
12. Eguchi J, Yan QW, Schones DE, Kamal M, Hsu CH, Zhang MQ, Crawford GE, Rosen ED. 2008. Interferon regulatory factors are transcriptional regulators of adipogenesis. Cell Metabolism 7:86-94. doi: 10.1016/j.cmet.2007.11.002.
13. ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57-74. doi: 10.1038/nature11247.
14. Fajas L, Auboeuf D, Raspé E, Schoonjans K, Lefebvre AM, Saladin R, Najib J, Laville M, Fruchart JC, Deeb S, Vidal-Puig A, Flier J, Briggs MR, Staels B, Vidal H, Auwerx J. 1997. The organization, promoter analysis, and expression of the human PPARgamma gene. The Journal of Biological Chemistry 272:18779-18789. doi: 10.1074/jbc.272.30.18779.
15. Fajas L, Egler V, Reiter R, Hansen J, Kristiansen K, Debril MB, Miard S, Auwerx J. 2002. The retinoblastoma-histone deacetylase 3 complex inhibits PPARgamma and adipocyte differentiation. Developmental Cell 3:903-910. doi: 10.1016/S1534-5807(02)00360-X.
16. Farmer SR. 2006. Transcriptional control of adipocyte formation. Cell Metabolism 4:263-273. doi: 10.1016/j.cmet.2006.07.001.
17. Floyd ZE, Stephens JM. 2003. STAT5A promotes adipogenesis in nonprecursor cells and associates with the glucocorticoid receptor during adipocyte differentiation. Diabetes 52:308-314. doi: 10.2337/diabetes.52.2.308.
18. Funahashi J, Kamachi Y, Goto K, Kondoh H. 1991. Identification of nuclear factor delta EF1 and its binding site essential for lens-specific activity of the delta 1-crystallin enhancer. Nucleic Acids Research 19:3543-3547. doi: 10.1093/nar/19.13.3543.
19. Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, Min R, Alves P, Abyzov A, Addleman N, Bhardwaj N, Boyle AP, Cayting P, Charos A, Chen DZ, Cheng Y, Clarke D, Eastman C, Euskirchen G, Frietze S, Fu Y, Gertz J, Grubert F, Harmanci A, Jain P, Kasowski M, Lacroute P, Leng J, Lian J, Monahan H, O'Geen H, Ouyang Z, Partridge EC, Patacsil D, Pauli F, Raha D, Ramirez L, Reddy TE, Reed B, Shi M, Slifer T, Wang J, Wu L, Yang X, Yip KY, Zilberman-Schapira G, Batzoglou S, Sidow A, Farnham PJ, Myers RM, Weissman SM, Snyder M. 2012. Architecture of the human regulatory network derived from ENCODE data. Nature 489:91-100. doi: 10.1038/nature11245.
20. Gheldof A, Hulpiau P, van Roy F, De Craene B, Berx G. 2012. Evolutionary functional analysis and molecular regulation of the ZEB transcription factors. Cellular and Molecular Life Sciences 69:2527-2541. doi: 10.1007/s00018-012-0935-3.
21. Green H, Kehinde O. 1975. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5:19-27. doi: 10.1016/0092-8674(75)90087-2.
22. Green H, Kehinde O. 1976. Spontaneous heritable changes leading to increased adipose conversion in 3T3 cells. Cell 7:105-113. doi: 10.1016/0092-8674(76)90260-9.
23. Green H, Kehinde O. 1979. Formation of normally differentiated subcutaneous fat pads by an established preadipose cell line. Journal of Cellular Physiology 101:169-171. doi: 10.1002/jcp.1041010119.
24. Gubelmann C, Gattiker A, Massouras A, Hens K, David F, Decouttere F, Rougemont J, Deplancke B. 2011. GETPrime: a gene-or transcript-specific primer database for quantitative real-time PCR. Database 2011:bar040. doi: 10.1093/database/bar040.
25. Gubelmann C, Schwalie PC, Raghav SK, Röder E, Delessa T, Kiehlmann E, Waszak SM, Corsinotti A, Udin G, Holcombe W, Rudofsky G, Trono D, Wolfrum C, Deplancke B. 2014. Data from: Identification of ZEB1 as a central component of the adipogenic gene regulatory network. Dryad Digital Repository. doi: 10.5061/dryad.j966f.
26. Gubelmann C, Waszak SM, Isakova A, Holcombe W, Hens K, Iagovitina A, Feuz JD, Raghav SK, Simicevic J, Deplancke B. 2013. A yeast one-hybrid and microfluidics-based pipeline to map mammalian gene regulatory networks. Molecular Systems Biology 9:682. doi: 10.1038/msb.2013.38.
27. Gupta RK, Arany Z, Seale P, Mepani RJ, Ye L, Conroe HM, Roby YA, Kulaga H, Reed RR, Spiegelman BM. 2010. Transcriptional control of preadipocyte determination by Zfp423. Nature 464:619-623. doi: 10.1038/nature08816.
28. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS. 2007. Quantifying similarity between motifs. Genome Biology 8:R24. doi: 10.1186/gb-2007-8-2-r24.
29. Hager J, Dina C, Francke S, Dubois S, Houari M, Vatin V, Vaillant E, Lorentz N, Basdevant A, Clement K, Guy-Grand B, Froguel P. 1998. A genome-wide scan for human obesity genes reveals a major susceptibility locus on chromosome 10. Nature Genetics 20:304-308. doi: 10.1038/3123.
30. Heid IM, Jackson AU, Randall JC, Winkler TW, Qi L, Steinthorsdottir V, Thorleifsson G, Zillikens MC, Speliotes EK, Mägi R, Workalemahu T, White CC, Bouatia-Naji N, Harris TB, Berndt SI, Ingelsson E, Willer CJ, Weedon MN, Luan J, Vedantam S, Esko T, Kilpeläinen TO, Kutalik Z, Li S, Monda KL, Dixon AL, Holmes CC, Kaplan LM, Liang L, Min JL, Moffatt MF, Molony C, Nicholson G, Schadt EE, Zondervan KT, Feitosa MF, Ferreira T, Lango Allen HL, Weyant RJ, Wheeler E, Wood AR, MAGIC, Estrada K, Goddard ME, Lettre G, Mangino M, Nyholt DR, Purcell S, Smith AV, Visscher PM, Yang J, McCarroll SA, Nemesh J, Voight BF, Absher D, Amin N, Aspelund T, Coin L, Glazer NL, Hayward C, Heard-Costa NL, Hottenga JJ, Johansson A, Johnson T, Kaakinen M, Kapur K, Ketkar S, Knowles JW, Kraft P, Kraja AT, Lamina C, Leitzmann MF, McKnight B, Morris AP, Ong KK, Perry JR, Peters MJ, Polasek O, Prokopenko I, Rayner NW, Ripatti S, Rivadeneira F, Robertson NR, Sanna S, Sovio U, Surakka I, Teumer A, van Wingerden S, Vitart V, Zhao JH, Cavalcanti-Proenca C, Chines PS, Fisher E, Kulzer JR, Lecoeur C, Narisu N, Sandholt C, Scott LJ, Silander K, Stark K, Tammesoo ML, Teslovich TM, Timpson NJ, Watanabe RM, Welch R, Chasman DI, Cooper MN, Jansson JO, Kettunen J, Lawrence RW, Pellikka N, Perola M, Vandenput L, Alavere H, Almgren P, Atwood LD, Bennett AJ, Biffar R, Bonnycastle LL, Bornstein SR, Buchanan TA, Campbell H, Day IN, Dei M, Dörr M, Elliott P, Erdos MR, Eriksson JG, Freimer NB, Fu M, Gaget S, Geus EJ, Gjesing AP, Grallert H, Grässler J, Groves CJ, Guiducci C, Hartikainen AL, Hassanali N, Havulinna AS, Herzig KH, Hicks AA, Hui J, Igl W, Jousilahti P, Jula A, Kajantie E, Kinnunen L, Kolcic I, Koskinen S, Kovacs P, Kroemer HK, Krzelj V, Kuusisto J, Kvaloy K, Laitinen J, Lantieri O, Lathrop GM, Lokki ML, Luben RN, Ludwig B, McArdle WL, McCarthy A, Morken MA, Nelis M, Neville MJ, Paré G, Parker AN, Peden JF, Pichler I, Pietiläinen KH, Platou CG, Pouta A, Ridderstråle M, Samani NJ, Saramies J, Sinisalo J, Smit JH, Strawbridge RJ, Stringham HM, Swift AJ, Teder-Laving M, Thomson B, Usala G, van Meurs JB, van Ommen GJ, Vatin V, Volpato CB, Wallaschofski H, Walters GB, Widen E, Wild SH, Willemsen G, Witte DR, Zgaga L, Zitting P, Beilby JP, James AL, Kähönen M, Lehtimäki T, Nieminen MS, Ohlsson C, Palmer LJ, Raitakari O, Ridker PM, Stumvoll M, Tönjes A, Viikari J, Balkau B, Ben-Shlomo Y, Bergman RN, Boeing H, Smith GD, Ebrahim S, Froguel P, Hansen T, Hengstenberg C, Hveem K, Isomaa B, Jørgensen T, Karpe F, Khaw KT, Laakso M, Lawlor DA, Marre M, Meitinger T, Metspalu A, Midthjell K, Pedersen O, Salomaa V, Schwarz PE, Tuomi T, Tuomilehto J, Valle TT, Wareham NJ, Arnold AM, Beckmann JS, Bergmann S, Boerwinkle E, Boomsma DI, Caulfield MJ, Collins FS, Eiriksdottir G, Gudnason V, Gyllensten U, Hamsten A, Hattersley AT, Hofman A, Hu FB, Illig T, Iribarren C, Jarvelin MR, Kao WH, Kaprio J, Launer LJ, Munroe PB, Oostra B, Penninx BW, Pramstaller PP, Psaty BM, Quertermous T, Rissanen A, Rudan I, Shuldiner AR, Soranzo N, Spector TD, Syvanen AC, Uda M, Uitterlinden A, Völzke H, Vollenweider P, Wilson JF, Witteman JC, Wright AF, Abecasis GR, Boehnke M, Borecki IB, Deloukas P, Frayling TM, Groop LC, Haritunians T, Hunter DJ, Kaplan RC, North KE, O'Connell JR, Peltonen L, Schlessinger D, Strachan DP, Hirschhorn JN, Assimes TL, Wichmann HE, Thorsteinsdottir U, van Duijn CM, Stefansson K, Cupples LA, Loos RJ, Barroso I, McCarthy MI, Fox CS, Mohlke KL, Lindgren CM. 2010. Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution. Nature Genetics 42:949-960. doi: 10.1038/ng.685.
31. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell 38:576-589. doi: 10.1016/j.molcel.2010.05.004.
32. Higashi Y, Moribe H, Takagi T, Sekido R, Kawakami K, Kikutani H, Kondoh H. 1997. Impairment of T cell development in δEF1 Mutant mice. The Journal of Experimental Medicine 185:1467-1479. doi: 10.1084/jem.185.8.1467.
33. Ishibashi J, Firtina Z, Rajakumari S, Wood KH, Conroe HM, Steger DJ, Seale P. 2012. An Evi1-C/EBPbeta complex controls peroxisome proliferator-activated receptor gamma2 gene expression to initiate white fat cell differentiation. Molecular and Cellular Biology 32:2289-2299. doi: 10.1128/MCB.06529-11.
34. James AW. 2013. Review of Signaling Pathways Governing MSC Osteogenic and Adipogenic Differentiation. Scientifica 2013:684736. doi: 10.1155/2013/684736.
35. Jimenez MA, Akerblad P, Sigvardsson M, Rosen ED. 2007. Critical role for Ebf1 and Ebf2 in the adipogenic transcriptional cascade. Molecular and Cellular Biology 27:743-757. doi: 10.1128/MCB.01557-06.
36. Kapushesky M, Adamusiak T, Burdett T, Culhane A, Farne A, Filippov A, Holloway E, Klebanov A, Kryvych N, Kurbatova N, Kurnosov P, Malone J, Melnichuk O, Petryszak R, Pultsin N, Rustici G, Tikhonov A, Travillian RS, Williams E, Zorin A, Parkinson H, Brazma A. 2012. Gene Expression Atlas update-a value-added database of microarray and sequencing-based functional genomics experiments. Nucleic Acids Research 40:D1077-D1081. doi: 10.1093/nar/gkr913.
37. Kawaguchi N, Toriyama K, Nicodemou-Lena E, Inou K, Torii S, Kitagawa Y. 1998. De novo adipogenesis in mice at the site of injection of basement membrane and basic fibroblast growth factor. Proceedings of the National Academy of Sciences of USA 95:1062-1066. doi: 10.1073/pnas.95.3.1062.
38. Kelder T, van Iersel MP, Hanspers K, Kutmon M, Conklin BR, Evelo CT, Pico AR. 2012. WikiPathways: building research communities on biological pathways. Nucleic Acids Research 40:D1301-D1307. doi: 10.1093/nar/gkr1074.
39. Kilpinen H, Waszak SM, Gschwind AR, Raghav SK, Witwicki RM, Orioli A, Migliavacca E, Wiederkehr M, Gutierrez-Arcelus M, Panousis NI, Yurovsky A, Lappalainen T, Romano-Palumbo L, Planchon A, Bielser D, Bryois J, Padioleau I, Udin G, Thurnheer S, Hacker D, Core LJ, Lis JT, Hernandez N, Reymond A, Deplancke B, Dermitzakis ET. 2013. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342:744-747. doi: 10.1126/science.1242463.
40. Kim JB, Wright HM, Wright M, Spiegelman BM. 1998. ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proceedings of the National Academy of Sciences of USA 95:4333-4337. doi: 10.1073/pnas.95.8.4333.
41. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, Flynn J, Shekar M, Wang H, Park J, Cui W, Wall GD, Wisotzkey R, Alag S, Akhtari S, Ronaghi M. 2010. Ontology-based meta-analysis of global collections of high-throughput public data. PLOS ONE 5:e13066. doi: 10.1371/journal.pone.0013066.
42. Kurima K, Hertzano R, Gavrilova O, Monahan K, Shpargel KB, Nadaraja G, Kawashima Y, Lee KY, Ito T, Higashi Y, Eisenman DJ, Strome SE, Griffith AJ. 2011. A noncoding point mutation of Zeb1 causes multiple developmental malformations and obesity in Twirler mice. PLOS Genetics 7:e1002307. doi: 10.1371/journal.pgen.1002307.
43. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357-359. doi: 10.1038/nmeth.1923.
44. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nature Biotechnology 28:495-501. doi: 10.1038/nbt.1630.
45. Meissburger B, Ukropec J, Roeder E, Beaton N, Geiger M, Teupser D, Civan B, Langhans W, Nawroth PP, Gasperikova D, Rudofsky G, Wolfrum C. 2011. Adipogenesis and insulin sensitivity in obesity are regulated by retinoid-related orphan receptor gamma. EMBO Molecular Medicine 3:637-651. doi: 10.1002/emmm.201100172.
46. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES, Rosen ED. 2010. Comparative epigenomic analysis of murine and human adipogenesis. Cell 143:156-169. doi: 10.1016/j.cell.2010.09.006.
47. Mori T, Sakaue H, Iguchi H, Gomi H, Okada Y, Takashima Y, Nakamura K, Nakamura T, Yamauchi T, Kubota N, Kadowaki T, Matsuki Y, Ogawa W, Hiramatsu R, Kasuga M. 2005. Role of Krüppel-like factor 15 (KLF15) in transcriptional regulation of adipogenesis. The Journal of Biological Chemistry 280:12867-12875. doi: 10.1074/jbc.M410515200.
48. Murad JM, Place CS, Ran C, Hekmatyar SK, Watson NP, Kauppinen RA, Israel MA. 2010. Inhibitor of DNA binding 4 (ID4) regulation of adipocyte differentiation and adipose tissue formation in mice. Journal of Biological Chemistry 285:24164-24173. doi: 10.1074/jbc.M110.128744.
49. Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, Wang R, Green DR, Tessarollo L, Casellas R, Zhao K, Levens D. 2012. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151:68-79. doi: 10.1016/j.cell.2012.08.033.
50. Nielsen R, Pedersen TA, Hagenbeek D, Moulos P, Siersbaek R, Megens E, Denissov S, Borgesen M, Francoijs KJ, Mandrup S, Stunnenberg HG. 2008. Genome-wide profiling of PPARgamma:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes & Development 22:2953-2967. doi: 10.1101/gad.501108.
51. Nishimura G, Manabe I, Tsushima K, Fujiu K, Oishi Y, Imai Y, Maemura K, Miyagishi M, Higashi Y, Kondoh H, Nagai R. 2006. δEF1 mediates TGF-β signaling in vascular smooth muscle cell differentiation. Developmental Cell 11:93-104. doi: 10.1016/j.devcel.2006.05.011.
52. Oishi Y, Manabe I, Tobe K, Tsushima K, Shindo T, Fujiu K, Nishimura G, Maemura K, Yamauchi T, Kubota N, Suzuki R, Kitamura T, Akira S, Kadowaki T, Nagai R. 2005. Krüppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metabolism 1:27-39. doi: 10.1016/j.cmet.2004.11.005.
53. Pérez-Mancera PA, Bermejo-Rodríguez C, González-Herrero I, Herranz M, Flores T, Jiménez R, Sánchez-García I. 2007. Adipose tissue mass is modulated by SLUG (SNAI2). Human Molecular Genetics 16:2972-2986. doi: 10.1093/hmg/ddm278.
54. Pinney DF, Emerson CP Jr. 1989. 10T1/2 cells: an in vitro model for molecular genetic analysis of mesodermal determination and differentiation. Environmental Health Perspectives 80:221-227. doi: 10.1289/ehp.8980221.
55. Raghav SK, Deplancke B. 2012. Genome-wide profiling of DNA-binding proteins using barcode-based multiplex Solexa sequencing. Methods in Molecular Biology 786:247-262. doi: 10.1007/978-1-61779-292-2_15.
56. Raghav SK, Waszak SM, Krier I, Gubelmann C, Isakova A, Mikkelsen TS, Deplancke B. 2012. Integrative genomics identifies the corepressor SMRT as a gatekeeper of adipogenesis through the transcription factors C/EBPβ and KAISO. Molecular Cell 46:335-350. doi: 10.1016/j.molcel.2012.03.017.
57. Rawnsley DR, Xiao J, Lee JS, Liu X, Mericko-Ishizuka P, Kumar V, He J, Basu A, Lu M, Lynn FC, Pack M, Gasa R, Kahn ML. 2013. The transcription factor Atonal homolog 8 regulates Gata4 and Friend of Gata-2 during vertebrate development. The Journal of Biological Chemistry 288:24429-24440. doi: 10.1074/jbc.M113.463083.
58. Roberts R, Hodson L, Dennis AL, Neville MJ, Humphreys SM, Harnden KE, Micklem KJ, Frayn KN. 2009. Markers of de novo lipogenesis in adipose tissue: associations with small adipocytes and insulin sensitivity in humans. Diabetologia 52:882-890. doi: 10.1007/s00125-009-1300-4.
59. Rosen ED, MacDougald OA. 2006. Adipocyte differentiation from the inside out. Nature Reviews Molecular Cell Biology 7:885-896. doi: 10.1038/nrm2066.
60. Rosen ED, Spiegelman BM. 2000. Molecular regulation of adipogenesis. Annual Review of Cell and Developmental Biology 16:145-171. doi: 10.1146/annurev.cellbio.16.1.145.
61. Rosen ED, Spiegelman BM. 2014. What we talk about when we talk about fat. Cell 156:20-44. doi: 10.1016/j.cell.2013.12.012.
62. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. 2000. Transcriptional regulation of adipogenesis. Genes & Development 14:1293-1307.
63. Rustici G, Kolesnikov N, Brandizi M, Burdett T, Dylag M, Emam I, Farne A, Hastings E, Ison J, Keays M, Kurbatova N, Malone J, Mani R, Mupo A, Pedro Pereira R, Pilicheva E, Rung J, Sharma A, Tang YA, Ternent T, Tikhonov A, Welter D, Williams E, Brazma A, Parkinson H, Sarkans U. 2013. ArrayExpress update-trends in database growth and links to data analysis tools. Nucleic Acids Research 41:D987-D990. doi: 10.1093/nar/gks1174.
64. Saykally JN, Dogan S, Cleary MP, Sanders MM. 2009. The ZEB1 transcription factor is a novel repressor of adiposity in female mice. PLOS ONE 4:e8460. doi: 10.1371/journal.pone.0008460.
65. Siersbæk R, Mandrup S. 2011. Transcriptional networks controlling adipocyte differentiation. Cold Spring Harbor Symposia on Quantitative Biology 76:247-255. doi: 10.1101/sqb.2011.76.010512.
66. Siersbæk R, Nielsen R, John S, Sung MH, Baek S, Loft A, Hager GL, Mandrup S. 2011. Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. The EMBO Journal 30:1459-1472. doi: 10.1038/emboj.2011.65.
67. Siersbæk R, Nielsen R, Mandrup S. 2012. Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends in Endocrinology and Metabolism 23:56-64. doi: 10.1016/j.tem.2011.10.001.
68. Siersbæk R, Rabiee A, Nielsen R, Sidoli S, Traynor S, Loft A, La Cour Poulsen L, Rogowska-Wrzesinska A, Jensen ON, Mandrup S. 2014. Transcription factor cooperativity in early adipogenic hotspots and super-enhancers. Cell Reports 7:1443-1455. doi: 10.1016/j.celrep.2014.04.042.
69. Simicevic J, Schmid AW, Gilardoni PA, Zoller B, Raghav SK, Krier I, Gubelmann C, Lisacek F, Naef F, Moniatte M, Deplancke B. 2013. Absolute quantification of transcription factors during cellular differentiation using multiplexed targeted proteomics. Nature Methods 10:570-576. doi: 10.1038/nmeth.2441.
70. Söhle J, Machuy N, Smailbegovic E, Holtzmann U, Grönniger E, Wenck H, Stäb F, Winnefeld M. 2012. Identification of new genes involved in human adipogenesis and fat storage. PLOS ONE 7:e31193. doi: 10.1371/journal.pone.0031193.
71. Soukas A, Socci ND, Saatkamp BD, Novelli S, Friedman JM. 2001. Distinct transcriptional profiles of adipogenesis in vivo and in vitro. The Journal of Biological Chemistry 276:34167-34174. doi: 10.1074/jbc.M104421200.
72. Steger DJ, Grant GR, Schupp M, Tomaru T, Lefterova MI, Schug J, Manduchi E, Stoeckert CJ Jnr, Lazar MA. 2010. Propagation of adipogenic signals through an epigenomic transition state. Genes & Development 24:1035-1044. doi: 10.1101/gad.1907110.
73. Stephens JM. 2012. The fat controller: adipocyte development. PLOS Biology 10:e1001436. doi: 10.1371/journal.pbio.100143.
74. Tang QQ, Lane MD. 2012. Adipogenesis: from stem cell to adipocyte. Annual Review of Biochemistry 81:715-736. doi: 10.1146/annurev-biochem-052110-115718.
75. Tang QQ, Otto TC, Lane MD. 2003. Mitotic clonal expansion: a synchronous process required for adipogenesis. Proceedings of the National Academy of Sciences of USA 100:44-49. doi: 10.1073/pnas.0137044100.
76. Tang QQ, Otto TC, Lane MD. 2004. Commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proceedings of the National Academy of Sciences of USA 101:9607-9611. doi: 10.1073/pnas.0403100101.
77. Tilg H, Moschen AR. 2006. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature Reviews Immunology 6:772-783. doi: 10.1038/nri1937.
78. Tong Q, Dalgin G, Xu H, Ting CN, Leiden JM, Hotamisligil GS. 2000. Function of GATA transcription factors in preadipocyte-adipocyte transition. Science 290:134-138. doi: 10.1126/science.290.5489.134.
79. Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes & Development 8:1224-1234. doi: 10.1101/gad.8.10.1224.
80. Turro E, Su SY, Gonçalves Â, Coin LJ, Richardson S, Lewin A. 2011. Haplotype and isoform specific expression estimation using multi-mapping RNA-seq reads. Genome Biology 12:R13. doi: 10.1186/gb-2011-12-2-r13.
81. Urrutia R. 2003. KRAB-containing zinc-finger repressor proteins. Genome Biology 4:231. doi: 10.1186/gb-2003-4-10-231.
82. van Iersel MP, Kelder T, Pico AR, Hanspers K, Coort S, Conklin BR, Evelo C. 2008. Presenting and exploring biological pathways with PathVisio. BMC Bioinformatics 9:399. doi: 10.1186/1471-2105-9-399.
83. Vandewalle C, Van Roy F, Berx G. 2009. The role of the ZEB family of transcription factors in development and disease. Cellular and Molecular Life Sciences 66:773-787. doi: 10.1007/s00018-008-8465-8.
84. Villanueva CJ, Waki H, Godio C, Nielsen R, Chou WL, Vargas L, Wroblewski K, Schmedt C, Chao LC, Boyadjian R, Mandrup S, Hevener A, Saez E, Tontonoz P. 2011. TLE3 is a dual-function transcriptional coregulator of adipogenesis. Cell Metabolism 13:413-427. doi: 10.1016/j.cmet.2011.02.014.
85. von Ruesten A, Steffen A, Floegel A, van der A DL, Masala G, Tjønneland A, Halkjaer J, Palli D, Wareham NJ, Loos RJ, Sorensen TI, Boeing H. 2011. Trend in obesity prevalence in European adult cohort populations during follow-up since 1996 and their predictions to 2015. PLOS ONE 6:e27455. doi: 10.1371/journal.pone.0027455.
86. Waki H, Nakamura M, Yamauchi T, Wakabayashi K, Yu J, Hirose-Yotsuya L, Take K, Sun W, Iwabu M, Okada-Iwabu M, Fujita T, Aoyama T, Tsutsumi S, Ueki K, Kodama T, Sakai J, Aburatani H, Kadowaki T. 2011. Global mapping of cell type-specific open chromatin by FAIRE-seq reveals the regulatory role of the NFI family in adipocyte differentiation. PLOS Genetics 7:e1002311. doi: 10.1371/journal.pgen.1002311.
87. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M, Weng Z. 2012. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Research 22:1798-1812. doi: 10.1101/gr.139105.112.
88. Winkler JK, Schultz JH, Woehning A, Piel D, Gartner L, Hildebrand M, Roeder E, Nawroth PP, Wolfrum C, Rudofsky G. 2013. Effectiveness of a low-calorie weight loss program in moderately and severely obese patients. Obesity Facts 6:469-480. doi: 10.1159/000355822.
89. Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, McKeon C, Darlington GJ, Spiegelman BM. 1999. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Molecular Cell 3:151-158. doi: 10.1016/S1097-2765(00)80306-8.
90. Xu H, Handoko L, Wei X, Ye C, Sheng J, Wei CL, Lin F, Sung WK. 2010. A signal-noise model for significance analysis of ChIP-seq with negative control. Bioinformatics 26:1199-1204. doi: 10.1093/bioinformatics/btq128.
91. Zhou H, Kaplan T, Li Y, Grubisic I, Zhang Z, Wang PJ, Eisen MB, Tjian R. 2013. Dual functions of TAF7L in adipocyte differentiation. eLife 2:e00170. doi: 10.7554/eLife.00170.