Alteration of NCoR Corepressor Splicing in Mice Causes Increased Body Weight and Hepatosteatosis without Glucose Intolerance

REFERENCES

• Edwards DP. 2000. The role of coactivators and corepressors in the biology and mechanism of action of steroid hormone receptors. J. Mammary Gland Biol. Neoplasia 5:307–324. http://dx.doi.org/10.1023/A:1009503029176.
   PubMed Web of Science ®Google Scholar
• Privalsky ML. 2004. The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu. Rev. Physiol. 66:315–360. http://dx.doi.org/10.1146/annurev.physiol.66.032802.155556.
   PubMedGoogle Scholar
• Stanya KJ, Kao HY. 2009. New insights into the functions and regulation of the transcriptional corepressors SMRT and N-CoR. Cell Div. 4:7. http://dx.doi.org/10.1186/1747-1028-4-7.
   PubMedGoogle Scholar
• Chen JD, Evans RM. 1995. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 377:454–457. http://dx.doi.org/10.1038/377454a0.
   PubMed Web of Science ®Google Scholar
• Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK, Rosenfeld MG. 1995. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377:397–404. http://dx.doi.org/10.1038/377397a0.
   PubMed Web of Science ®Google Scholar
• Sande S, Privalsky ML. 1996. Identification of TRACs (T3 receptor-associating cofactors), a family of cofactors that associate with, and modulate the activity of, nuclear hormone receptors. Mol. Endocrinol. 10:813–825. http://dx.doi.org/10.1210/mend.10.7.8813722.
   PubMedGoogle Scholar
• Lazar MA. 2003. Nuclear receptor corepressors. Nucl. Recept. Signal. 1:e001. http://dx.doi.org/10.1621/nrs.01001.
   PubMedGoogle Scholar
• Goodson M, Jonas BA, Privalsky MA. 2005. Corepressors: custom tailoring and alterations while you wait. Nucl. Recept. Signal. 3:e003. http://dx.doi.org/10.1621/nrs.03003.
   PubMedGoogle Scholar
• Lonard DM, O'Malley BW. 2012. Nuclear receptor coregulators: modulators of pathology and therapeutic targets. Nat. Rev. Endocrinol. 8:598–604. http://dx.doi.org/10.1038/nrendo.2012.100.
   PubMed Web of Science ®Google Scholar
• Lonard DM, Lanz RB, O'Malley BW. 2007. Nuclear receptor coregulators and human disease. Endocr. Rev. 28:575–587. http://dx.doi.org/10.1210/er.2007-0012.
   PubMed Web of Science ®Google Scholar
• Graham A. 2000. The evolution of the vertebrates—genes and development. Curr. Opin. Genet. Dev. 10:624–628. http://dx.doi.org/10.1016/S0959-437X(00)00135-0.
   PubMedGoogle Scholar
• Sanchez-Pla A, Reverter F, Ruiz de Villa MC, Comabella M. 2012. Transcriptomics: mRNA and alternative splicing. J. Neuroimmunol. 248:23–31. http://dx.doi.org/10.1016/j.jneuroim.2012.04.008.
   PubMed Web of Science ®Google Scholar
• Malartre M, Short S, Sharpe C. 2004. Alternative splicing generates multiple SMRT transcripts encoding conserved repressor domains linked to variable transcription factor interaction domains. Nucleic Acids Res. 32:4676–4686. http://dx.doi.org/10.1093/nar/gkh786.
   PubMedGoogle Scholar
• Lahnalampi M, Heinaniemi M, Sinkkonen L, Wabitsch M, Carlberg C. 2010. Time-resolved expression profiling of the nuclear receptor superfamily in human adipogenesis. PLoS One 5:e12991. http://dx.doi.org/10.1371/journal.pone.0012991.
   PubMedGoogle Scholar
• Rosen ED, MacDougald OA. 2006. Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7:885–896. http://dx.doi.org/10.1038/nrm2066.
   PubMed Web of Science ®Google Scholar
• Goodson ML, Mengeling BJ, Jonas BA, Privalsky ML. 2011. Alternative mRNA splicing of corepressors generates variants that play opposing roles in adipocyte differentiation. J. Biol. Chem. 286:44988–44999. http://dx.doi.org/10.1074/jbc.M111.291625.
   PubMed Web of Science ®Google Scholar
• Jepsen K, Hermanson O, Onami TM, Gleiberman AS, Lunyak V, McEvilly RJ, Kurokawa R, Kumar V, Liu F, Seto E, Hedrick SM, Mandel G, Glass CK, Rose DW, Rosenfeld MG. 2000. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 102:753–763. http://dx.doi.org/10.1016/S0092-8674(00)00064-7.
   PubMedGoogle Scholar
• Jepsen K, Rosenfeld MG. 2002. Biological roles and mechanistic actions of co-repressor complexes. J. Cell Sci. 115:689–698.
   PubMed Web of Science ®Google Scholar
• Li P, Fan W, Xu J, Lu M, Yamamoto H, Auwerx J, Sears DD, Talukdar S, Oh D, Chen A, Bandyopadhyay G, Scadeng M, Ofrecio JM, Nalbandian S, Olefsky JM. 2011. Adipocyte NCoR knockout decreases PPARgamma phosphorylation and enhances PPARgamma activity and insulin sensitivity. Cell 147:815–826. http://dx.doi.org/10.1016/j.cell.2011.09.050.
   PubMed Web of Science ®Google Scholar
• Li P, Spann NJ, Kaikkonen MU, Lu M, Oh DY, Fox JN, Bandyopadhyay G, Talukdar S, Xu J, Lagakos WS, Patsouris D, Armando A, Quehenberger O, Dennis EA, Watkins SM, Auwerx J, Glass CK, Olefsky JM. 2013. NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids. Cell 155:200–214. http://dx.doi.org/10.1016/j.cell.2013.08.054.
   PubMed Web of Science ®Google Scholar
• Yamamoto H, Williams EG, Mouchiroud L, Canto C, Fan W, Downes M, Heligon C, Barish GD, Desvergne B, Evans RM, Schoonjans K, Auwerx J. 2011. NCoR1 is a conserved physiological modulator of muscle mass and oxidative function. Cell 147:827–839. http://dx.doi.org/10.1016/j.cell.2011.10.017.
   PubMedGoogle Scholar
• White JK, Gerdin AK, Karp NA, Ryder E, Buljan M, Bussell JN, Salisbury J, Clare S, Ingham NJ, Podrini C, Houghton R, Estabel J, Bottomley JR, Melvin DG, Sunter D, Adams NC, Sanger Institute Mouse Genetics Project, Tannahill D, Logan DW, Macarthur DG, Flint J, Mahajan VB, Tsang SH, Smyth I, Watt FM, Skarnes WC, Dougan G, Adams DJ, Ramirez-Solis R, Bradley A, Steel KP. 2013. Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154:452–464. http://dx.doi.org/10.1016/j.cell.2013.06.022.
   PubMed Web of Science ®Google Scholar
• Guan KL, Dixon JE. 1991. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262–267. http://dx.doi.org/10.1016/0003-2697(91)90534-Z.
   PubMed Web of Science ®Google Scholar
• Todaro GJ, Green H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299–313. http://dx.doi.org/10.1083/jcb.17.2.299.
   PubMed Web of Science ®Google Scholar
• Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36. http://dx.doi.org/10.1186/gb-2013-14-4-r36.
   PubMed Web of Science ®Google Scholar
• Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7:562–578. http://dx.doi.org/10.1038/nprot.2012.016.
   PubMed Web of Science ®Google Scholar
• Goodson ML, Farboud B, Privalsky ML. 2007. An improved high throughput protein-protein interaction assay for nuclear hormone receptors. Nucl. Recept. Signal. 5:e002. http://dx.doi.org/10.1621/nrs.05002.
   PubMedGoogle Scholar
• Mengeling BJ, Goodson ML, Bourguet W, Privalsky ML. 2012. SMRTepsilon, a corepressor variant, interacts with a restricted subset of nuclear receptors, including the retinoic acid receptors alpha and beta. Mol. Cell. Endocrinol. 351:306–316. http://dx.doi.org/10.1016/j.mce.2012.01.006.
   PubMedGoogle Scholar
• Wickham H. 2009. ggplot2: elegant graphics for data analysis. Springer, New York, NY.
   Google Scholar
• Fang S, Suh JM, Atkins AR, Hong SH, Leblanc M, Nofsinger RR, Yu RT, Downes M, Evans RM. 2011. Corepressor SMRT promotes oxidative phosphorylation in adipose tissue and protects against diet-induced obesity and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 108:3412–3417. http://dx.doi.org/10.1073/pnas.1017707108.
   PubMedGoogle Scholar
• Ghisletti S, Huang W, Jepsen K, Benner C, Hardiman G, Rosenfeld MG, Glass CK. 2009. Cooperative NCoR/SMRT interactions establish a corepressor-based strategy for integration of inflammatory and anti-inflammatory signaling pathways. Genes Dev. 23:681–693. http://dx.doi.org/10.1101/gad.1773109.
   PubMed Web of Science ®Google Scholar
• Guo J, Hall KD. 2011. Predicting changes of body weight, body fat, energy expenditure and metabolic fuel selection in C57BL/6 mice. PLoS One 6:e15961. http://dx.doi.org/10.1371/journal.pone.0015961.
   PubMedGoogle Scholar
• Lenti G. 1974. The diabetic disease (M.D.). Clinical picture and complications. Minerva Med. 65:3041–3057. (In Italian.)
   PubMedGoogle Scholar
• Capurso C, Capurso A. 2012. From excess adiposity to insulin resistance: the role of free fatty acids. Vascul. Pharmacol. 57:91–97. http://dx.doi.org/10.1016/j.vph.2012.05.003.
   PubMed Web of Science ®Google Scholar
• Farrell GC, Larter CZ. 2006. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43:S99–S112. http://dx.doi.org/10.1002/hep.20973.
   PubMed Web of Science ®Google Scholar
• Funaki M. 2009. Saturated fatty acids and insulin resistance. J. Med. Invest. 56:88–92. http://dx.doi.org/10.2152/jmi.56.88.
   PubMedGoogle Scholar
• Heilbronn LK, Campbell LV. 2008. Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr. Pharm. Des. 14:1225–1230. http://dx.doi.org/10.2174/138161208784246153.
   PubMed Web of Science ®Google Scholar
• Mlinar B, Marc J. 2011. New insights into adipose tissue dysfunction in insulin resistance. Clin. Chem. Lab. Med. 49:1925–1935. http://dx.doi.org/10.1515/CCLM.2011.697.
   PubMed Web of Science ®Google Scholar
• Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F, Jager J, Lazar MA. 2012. Rev-erbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev. 26:657–667. http://dx.doi.org/10.1101/gad.186858.112.
   PubMed Web of Science ®Google Scholar
• Sun Z, Miller RA, Patel RT, Chen J, Dhir R, Wang H, Zhang D, Graham MJ, Unterman TG, Shulman GI, Sztalryd C, Bennett MJ, Ahima RS, Birnbaum MJ, Lazar MA. 2012. Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration. Nat. Med. 18:934–942. http://dx.doi.org/10.1038/nm.2744.
   PubMed Web of Science ®Google Scholar
• You SH, Lim HW, Sun Z, Broache M, Won KJ, Lazar MA. 2013. Nuclear receptor co-repressors are required for the histone-deacetylase activity of HDAC3 in vivo. Nat. Struct. Mol. Biol. 20:182–187. http://dx.doi.org/10.1038/nsmb.2476.
   PubMedGoogle Scholar
• Sun Z, Feng D, Fang B, Mullican SE, You SH, Lim HW, Everett LJ, Nabel CS, Li Y, Selvakumaran V, Won KJ, Lazar MA. 2013. Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol. Cell 52:769–782. http://dx.doi.org/10.1016/j.molcel.2013.10.022.
   PubMed Web of Science ®Google Scholar
• Downes M, Burke LJ, Bailey PJ, Muscat GE. 1996. Two receptor interaction domains in the corepressor, N-CoR/RIP13, are required for an efficient interaction with Rev-erbA alpha and RVR: physical association is dependent on the E region of the orphan receptors. Nucleic Acids Res. 24:4379–4386. http://dx.doi.org/10.1093/nar/24.22.4379.
   PubMedGoogle Scholar
• Astapova I, Lee LJ, Morales C, Tauber S, Bilban M, Hollenberg AN. 2008. The nuclear corepressor, NCoR, regulates thyroid hormone action in vivo. Proc. Natl. Acad. Sci. U. S. A. 105:19544–19549. http://dx.doi.org/10.1073/pnas.0804604105.
   PubMedGoogle Scholar
• Ahmadian M, Suh JM, Hah N, Liddle C, Atkins AR, Downes M, Evans RM. 2013. PPARgamma signaling and metabolism: the good, the bad and the future. Nat. Med. 19:557–566. http://dx.doi.org/10.1038/nm.3159.
   PubMed Web of Science ®Google Scholar
• Guan HP, Ishizuka T, Chui PC, Lehrke M, Lazar MA. 2005. Corepressors selectively control the transcriptional activity of PPARgamma in adipocytes. Genes Dev. 19:453–461. http://dx.doi.org/10.1101/gad.1263305.
   PubMed Web of Science ®Google Scholar
• Yu C, Markan K, Temple KA, Deplewski D, Brady MJ, Cohen RN. 2005. The nuclear receptor corepressors NCoR and SMRT decrease peroxisome proliferator-activated receptor gamma transcriptional activity and repress 3T3-L1 adipogenesis. J. Biol. Chem. 280:13600–13605. http://dx.doi.org/10.1074/jbc.M409468200.
   PubMed Web of Science ®Google Scholar
• Seki G, Endo Y, Suzuki M, Yamada H, Horita S, Fujita T. 2012. Role of renal proximal tubule transport in thiazolidinedione-induced volume expansion. World J. Nephrol. 1:146–150.
   PubMedGoogle Scholar
• Choi JH, Banks AS, Estall JL, Kajimura S, Bostrom P, Laznik D, Ruas JL, Chalmers MJ, Kamenecka TM, Bluher M, Griffin PR, Spiegelman BM. 2010. Anti-diabetic drugs inhibit obesity-linked phosphorylation of PPARgamma by Cdk5. Nature 466:451–456. http://dx.doi.org/10.1038/nature09291.
   PubMed Web of Science ®Google Scholar