Adipocytes fail to maintain cellular identity during obesity due to reduced PPARγ activity and elevated TGFβ-SMAD signaling

Molecular Metabolism - Tập 42 - Trang 101086 - 2020
Hyun Cheol Roh1,2,3, Manju Kumari1, Solaema Taleb3, Danielle Tenen1,2, Christopher Jacobs1,2, Anna Lyubetskaya1,2, Linus T.-Y. Tsai1,2, Evan D. Rosen1,2
1Division of Endocrinology, Diabetes and Obesity, Beth Israel Deaconess Medical Center, Boston, MA, 02215, USA
2Broad Institute, Cambridge, MA 02142, USA
3Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN 46202, USA

Tài liệu tham khảo

World Health Organization Pi-Sunyer, 2002, The medical risks of obesity, Obesity Surgery, 12, S6, 10.1007/BF03342140 Kusminski, 2016, Targeting adipose tissue in the treatment of obesity-associated diabetes, Nature Reviews Drug Discovery, 15, 639, 10.1038/nrd.2016.75 Tontonoz, 2008, Fat and beyond: the diverse biology of PPARgamma, Annual Review of Biochemistry, 77, 289, 10.1146/annurev.biochem.77.061307.091829 Siersbæk, 2010, PPARγ in adipocyte differentiation and metabolism - novel insights from genome-wide studies, FEBS Letters, 584, 3242, 10.1016/j.febslet.2010.06.010 Tamori, 2002, Role of peroxisome proliferator-activated receptor-γ in maintenance of the characteristics of mature 3T3-L1 adipocytes, Diabetes, 51, 2045, 10.2337/diabetes.51.7.2045 Wang, 2013, Lipoatrophy and severe metabolic disturbance in mice with fat-specific deletion of PPARγ, Proceedings of the National Academy of Sciences of the United States of America, 110, 18656, 10.1073/pnas.1314863110 Soccio, 2017, Targeting PPARγ in the epigenome rescues genetic metabolic defects in mice, Journal of Clinical Investigation, 127, 1, 10.1172/JCI91211 Soccio, 2014, Thiazolidinediones and the promise of insulin sensitization in type 2 diabetes, Cell Metabolism, 20, 573, 10.1016/j.cmet.2014.08.005 Lynes, 2018, Deciphering adipose tissue heterogeneity, Annals of the New York Academy of Sciences, 1411, 5, 10.1111/nyas.13398 Roh, 2017, Simultaneous transcriptional and epigenomic profiling from specific cell types within heterogeneous tissues in vivo, Cell Reports, 18, 1048, 10.1016/j.celrep.2016.12.087 Reilly, 2017, Adapting to obesity with adipose tissue inflammation, Nature Reviews Endocrinology, 13, 633, 10.1038/nrendo.2017.90 Rodbell, 1964, Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis, Journal of Biological Chemistry, 239, 375, 10.1016/S0021-9258(18)51687-2 Ebke, 2014, Tight association between macrophages and adipocytes in obesity: implications for adipocyte preparation, Obesity, 22, 1246, 10.1002/oby.20634 Ruan, 2003, Standard isolation of primary adipose cells from mouse epididymal fat pads induces inflammatory mediators and down-regulates adipocyte genes, Journal of Biological Chemistry, 278, 47585, 10.1074/jbc.M305257200 Roh, 2018, Warming induces significant reprogramming of beige, but not Brown, adipocyte cellular identity, Cell Metabolism, 27, 1121, 10.1016/j.cmet.2018.03.005 Eguchi, 2011, Transcriptional control of adipose lipid handling by IRF4, Cell Metabolism, 13, 249, 10.1016/j.cmet.2011.02.005 Kim, 2019, Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype, Nature Biotechnology, 37, 907, 10.1038/s41587-019-0201-4 Liao, 2014, FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Robinson, 2009, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Zhou, 2019, Metascape provides a biologist-oriented resource for the analysis of systems-level datasets, Nature Communications, 10 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nature Methods, 9, 357, 10.1038/nmeth.1923 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Zhang, 2008, Model-based analysis of ChIP-seq (MACS), Genome Biology, 9, 10.1186/gb-2008-9-9-r137 Quinlan, 2010, BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, 26, 841, 10.1093/bioinformatics/btq033 Zhou, 2012, Using the wash U epigenome browser to examine genome-wide sequencing data, Current Protocols in Bioinformatics, 40, 10.10.1, 10.1002/0471250953.bi1010s40 Kent, 2010, BigWig and BigBed: enabling browsing of large distributed datasets, Bioinformatics, 26, 2204, 10.1093/bioinformatics/btq351 Ramírez, 2016, deepTools2: a next generation web server for deep-sequencing data analysis, Nucleic Acids Research, 44, W160, 10.1093/nar/gkw257 Heinz, 2010, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Molecular Cell, 38, 576, 10.1016/j.molcel.2010.05.004 Grant, 2011, FIMO: scanning for occurrences of a given motif, Bioinformatics, 27, 1017, 10.1093/bioinformatics/btr064 Mathelier, 2014, JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles, Nucleic Acids Research, 42, 142, 10.1093/nar/gkt997 Wang, 2013, Tracking adipogenesis during white adipose tissue development, expansion and regeneration, Nature Medicine, 19, 1338, 10.1038/nm.3324 Sun, 2011, Adipose tissue remodeling and obesity, Journal of Clinical Investigation, 121, 2094, 10.1172/JCI45887 Heiman, 2008, A translational profiling approach for the molecular characterization of CNS cell types, Cell, 135, 738, 10.1016/j.cell.2008.10.028 Wernstedt Asterholm, 2014, Adipocyte inflammation is essential for healthy adipose tissue expansion and remodeling, Cell Metabolism, 20, 103, 10.1016/j.cmet.2014.05.005 Ye, 2015, Impact of tamoxifen on adipocyte lineage tracing: inducer of adipogenesis and prolonged nuclear translocation of Cre recombinase, Molecular Metabolism, 4, 771, 10.1016/j.molmet.2015.08.004 Samad, 1997, Elevated expression of transforming growth factor-beta in adipose tissue from obese mice, Molecular Medicine (Cambridge, Mass.), 3, 37 Shen, 2017, Adipocyte glucocorticoid receptor is important in lipolysis and insulin resistance due to exogenous steroids, but not insulin resistance caused by high fat feeding, Molecular Metabolism, 10.1016/j.molmet.2017.06.013 Marcelin, 2017, A PDGFRα-mediated switch toward CD9high adipocyte progenitors controls obesity-induced adipose tissue fibrosis, Cell Metabolism, 25, 673, 10.1016/j.cmet.2017.01.010 Datta, 2018, Fat fibrosis: friend or foe? Find the latest version, JCI Insight, 3, 10.1172/jci.insight.122289 Vidal-Puig, 1997, Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids, Journal of Clinical Investigation, 99, 2416, 10.1172/JCI119424 Auboeuf, 1997, Tissue distribution and quantification of the expression of mRNAs of peroxisome proliferator–activated receptors and liver X receptor-α in humans: No alteration in adipose tissue of obese and NIDDM patients, Diabetes, 46, 1319, 10.2337/diab.46.8.1319 Rieusset, 1999, Insulin acutely regulates the expression of the peroxisome proliferator-activated receptor-gamma in human adipocytes, Diabetes, 48, 699, 10.2337/diabetes.48.4.699 Giusti, 2003, Expression of peroxisome proliferator – activated tissue of obese women, Diabetes, 52, 1673, 10.2337/diabetes.52.7.1673 Kang, 2015, Identification of nuclear hormone receptor pathways causing insulin resistance by transcriptional and epigenomic analysis, Nature Cell Biology, 17, 10.1038/ncb3080 Tang, 2010, Uncoupling of inflammation and insulin resistance by NF-κB in transgenic mice through elevated energy expenditure, Journal of Biological Chemistry, 285, 4637, 10.1074/jbc.M109.068007 Gao, 2015, P65 inactivation in adipocytes and macrophages attenuates adipose inflammatory response in lean but not in obese mice, American Journal of Physiology - Endocrinology and Metabolism, 308, E496, 10.1152/ajpendo.00532.2014 Kumari, 2016, IRF3 promotes adipose inflammation and insulin resistance and represses browning, Journal of Clinical Investigation, 126, 2839, 10.1172/JCI86080 Nakae, 2008, Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure, Diabetes, 57, 563, 10.2337/db07-0698 Lee, 2014, Increased adipocyte O2 consumption triggers HIF-1α, causing inflammation and insulin resistance in obesity, Cell, 157, 1339, 10.1016/j.cell.2014.05.012 Vijayakumar, 2017, Absence of carbohydrate response element binding protein in adipocytes causes systemic insulin resistance and impairs glucose transport, Cell Reports, 21, 1021, 10.1016/j.celrep.2017.09.091 Mikkelsen, 2010, Comparative epigenomic analysis of murine and human adipogenesis, Cell, 143, 156, 10.1016/j.cell.2010.09.006 Alessi, 2000, Plasminogen activator inhibitor 1, transforming growth factor-β1, and BMI are closely associated in human adipose tissue during morbid obesity, Diabetes, 49, 1374, 10.2337/diabetes.49.8.1374 Tsurutani, 2011, The roles of transforming growth factor-β and Smad3 signaling in adipocyte differentiation and obesity, Biochemical and Biophysical Research Communications, 407, 68, 10.1016/j.bbrc.2011.02.106 Choy, 2003, Transforming growth factor-β inhibits adipocyte differentiation by Smad3 interacting with CCAAT/enhancer-binding protein (C/EBP) and repressing C/EBP transactivation function, Journal of Biological Chemistry, 278, 9609, 10.1074/jbc.M212259200 Yadav, 2011, Protection from obesity and diabetes by blockade of TGF-??/Smad3 signaling, Cell Metabolism, 14, 67, 10.1016/j.cmet.2011.04.013 Tan, 2011, Smad3 deficiency in mice protects against insulin resistance and obesity induced by a high-fat diet, Diabetes, 60, 464, 10.2337/db10-0801 Lin, 2017, Transforming growth factor-β signaling pathway-associated genes SMAD2 and TGFBR2 are implicated in metabolic syndrome in a Taiwanese population, Scientific Reports, 7, 1 Perry, 2009, Interrogating type 2 diabetes genome-wide association data using a biological pathway-based approach, Diabetes, 58, 1463, 10.2337/db08-1378 Evans, 2003, TGF-β1-mediated fibroblast–myofibroblast terminal differentiation—the role of smad proteins, Experimental Cell Research, 282, 90, 10.1016/S0014-4827(02)00015-0 Akhurst, 2012, Targeting the TGFβ signalling pathway in disease, Nature Reviews Drug Discovery, 11, 790, 10.1038/nrd3810 Yang, 2014, BSCL2/seipin regulates adipogenesis through actin cytoskeleton, Remodelling, 23, 502 Schiller, 2013, Adipogenesis of adipose-derived stem cells may be regulated via the cytoskeleton at physiological oxygen levels in vitro, Stem Cell Research & Therapy, 4, 10.1186/scrt230 McBeath, 2004, Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment, Developmental Cell, 6, 483, 10.1016/S1534-5807(04)00075-9 Hansson, 2019, Adipose cell size changes are associated with a drastic actin remodeling, Scientific Reports, 9, 1, 10.1038/s41598-019-49418-0 Kim, 2019, During adipocyte remodeling, lipid droplet configurations regulate insulin sensitivity through F-actin and G-actin reorganization, Molecular and Cellular Biology, 39, e00210, 10.1128/MCB.00210-19 Yonashiro, 2009, Mutant SOD1 and attenuates mutant SOD1-induced reactive oxygen species generation, Molecular Biology of the Cell, 20, 4524, 10.1091/mbc.e09-02-0112 Kanzaki, 2001, Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling, Journal of Biological Chemistry, 276, 42436, 10.1074/jbc.M108297200 Rosenwald, 2013, Bi-directional interconversion of brite and white adipocytes, Nature Cell Biology, 15, 1 Wang, 2018, Reversible de-differentiation of mature white adipocytes into preadipocyte-like precursors during lactation, Cell Metabolism, 1 Matsumoto, 2008, Mature adipocyte-derived de-differentiated fat cells exhibit multilineage potential, Journal of Cellular Physiology, 215, 210, 10.1002/jcp.21304 Shook, 2020, Dermal adipocyte lipolysis and myofibroblast conversion are required for efficient skin repair, Cell Stem Cell, 1 Marangoni, 2015, Myofibroblasts in murine cutaneous fibrosis originate from adiponectin-positive intradermal progenitors, Arthritis and Rheumatology, 67, 1062, 10.1002/art.38990 Korman, 2018, Adipocyte-specific repression of PPAR-gamma by NCoR contributes to scleroderma skin fibrosis, Arthritis Research and Therapy, 20, 1, 10.1186/s13075-018-1630-z Li, 2011, Adipocyte NCoR knockout decreases PPARγ phosphorylation and enhances PPARγ activity and insulin sensitivity, Cell, 147, 815, 10.1016/j.cell.2011.09.050 Zhang, 2019, Dermal adipose tissue has high plasticity and undergoes reversible de-differentiation in mice, Journal of Clinical Investigation, 129, 5327, 10.1172/JCI130239 Talchai, 2012, Pancreatic β cell de-differentiation as a mechanism of diabetic β cell failure, Cell, 150, 1223, 10.1016/j.cell.2012.07.029 Li, 2020, Cell plasticity in liver regeneration, Trends in Cell Biology, 30, 329, 10.1016/j.tcb.2020.01.007