Generation of Functional Brown Adipocytes from Human Pluripotent Stem Cells via Progression through a Paraxial Mesoderm State

Cell Stem Cell - Tập 27 - Trang 784-797.e11 - 2020
Liang Zhang1,2, John Avery1,2, Amelia Yin1,2, Amar M. Singh1,2, Timothy S. Cliff1,2, Hang Yin1,2, Stephen Dalton1,2
1Center for Molecular Medicine, University of Georgia, 325 Riverbend Road, Athens, GA 30605, USA
2Department of Biochemistry and Molecular Biology, University of Georgia, 325 Riverbend Road, Athens, GA 30605, USA

Tài liệu tham khảo

Ahfeldt, 2012, Programming human pluripotent stem cells into white and brown adipocytes, Nat. Cell Biol., 14, 209, 10.1038/ncb2411 Altshuler-Keylin, 2016, Beige adipocyte maintenance is regulated by autophagy-induced mitochondrial clearance, Cell Metab., 24, 402, 10.1016/j.cmet.2016.08.002 An, 2017, A molecular switch regulating cell fate choice between muscle progenitor cells and brown adipocytes, Dev. Cell, 41, 382, 10.1016/j.devcel.2017.04.012 Angueira, 2020, Early B cell factor activity controls developmental and adaptive thermogenic gene programming in adipocytes, Cell Rep., 30, 2869, 10.1016/j.celrep.2020.02.023 Atit, 2006, β-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse, Dev. Biol., 296, 164, 10.1016/j.ydbio.2006.04.449 Bartelt, 2011, Brown adipose tissue activity controls triglyceride clearance, Nat. Med., 17, 200, 10.1038/nm.2297 Beers, 2012, Passaging and colony expansion of human pluripotent stem cells by enzyme-free dissociation in chemically defined culture conditions, Nat. Protoc., 7, 2029, 10.1038/nprot.2012.130 Blighe K (2019). EnhancedVolcano: publication-ready volcano plots with enhanced colouring and labeling. R package version 1.2.0. https://github.com/kevinblighe/EnhancedVolcano. Bolstad, B. (2020). preprocessCore: A collection of pre-processing functions. R package version 1.50.0, https://github.com/bmbolstad/preprocessCore. Chal, 2017, Making muscle: skeletal myogenesis in vivo and in vitro, Development, 144, 2104, 10.1242/dev.151035 Cheng, 2018, Prediction of adipose browning capacity by systematic integration of transcriptional profiles, Cell Rep., 23, 3112, 10.1016/j.celrep.2018.05.021 Chondronikola, 2014, Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans, Diabetes, 63, 4089, 10.2337/db14-0746 Cinti, 2009, The adipose organ, 11 Cliff, 2017, MYC controls human pluripotent stem cell fate decisions through regulation of metabolic flux, Cell Stem Cell, 21, 502, 10.1016/j.stem.2017.08.018 Corces, 2018, The chromatin accessibility landscape of primary human cancers, Science, 362, 362, 10.1126/science.aav1898 Cypess, 2009, Identification and importance of brown adipose tissue in adult humans, N. Engl. J. Med., 360, 1509, 10.1056/NEJMoa0810780 Din, 2018, Postprandial oxidative metabolism of human brown fat indicates thermogenesis, Cell Metab., 28, 207, 10.1016/j.cmet.2018.05.020 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Gunawardana, 2012, Reversal of type 1 diabetes in mice by brown adipose tissue transplant, Diabetes, 61, 674, 10.2337/db11-0510 Hafner, 2018, Differentiation of brown adipocyte progenitors derived from human induced pluripotent stem cells, Methods Mol. Biol., 1773, 31, 10.1007/978-1-4939-7799-4_4 Hanssen, 2015, Short-term cold acclimation improves insulin sensitivity in patients with type 2 diabetes mellitus, Nat. Med., 21, 863, 10.1038/nm.3891 Heinz, 2010, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Mol. Cell, 38, 576, 10.1016/j.molcel.2010.05.004 Ikeda, 2018, The common and distinct features of brown and beige adipocytes, Trends Endocrinol. Metab., 29, 191, 10.1016/j.tem.2018.01.001 Inagaki, 2016, Transcriptional and epigenetic control of brown and beige adipose cell fate and function, Nat. Rev. Mol. Cell Biol., 17, 480, 10.1038/nrm.2016.62 Kajimura, 2015, Brown and beige fat: physiological roles beyond heat generation, Cell Metab., 22, 546, 10.1016/j.cmet.2015.09.007 Kishida, 2015, Reprogrammed functional brown adipocytes ameliorate insulin resistance and dyslipidemia in diet-induced obesity and type 2 diabetes, Stem Cell Reports, 5, 569, 10.1016/j.stemcr.2015.08.007 Kolde Kurtenbach, 2019, SparK: a publication-quality NGS visualization tool, bioRxiv, 10.1101/845529 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Laurila, 2016, USF1 deficiency activates brown adipose tissue and improves cardiometabolic health, Sci. Transl. Med., 8, 323ra13, 10.1126/scitranslmed.aad0015 Lee, 2015, Cellular origins of cold-induced brown adipocytes in adult mice, FASEB J., 29, 286, 10.1096/fj.14-263038 Lee, 2016, Brown adipose tissue exhibits a glucose-responsive thermogenic biorhythm in humans, Cell Metab., 23, 602, 10.1016/j.cmet.2016.02.007 Li, 2011, RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome, BMC Bioinformatics, 12, 323, 10.1186/1471-2105-12-323 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Loh, 2016, Mapping the pairwise choices leading from pluripotency to human bone, heart, and other mesoderm cell types, Cell, 166, 451, 10.1016/j.cell.2016.06.011 Long, 2014, A smooth muscle-like origin for beige adipocytes, Cell Metab., 19, 810, 10.1016/j.cmet.2014.03.025 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Lusk, 1928 Maier, 2004, Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription, Nat. Immunol., 5, 1069, 10.1038/ni1119 McCarthy, 2012, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation, Nucleic Acids Res., 40, 4288, 10.1093/nar/gks042 Miccheli, 2006, Metabolic profiling by 13C-NMR spectroscopy:[1, 2-13C2] glucose reveals a heterogeneous metabolism in human leukemia T cells, Biochimie, 88, 437, 10.1016/j.biochi.2005.10.004 Mohsen-Kanson, 2014, Differentiation of human induced pluripotent stem cells into brown and white adipocytes: role of Pax3, Stem Cells, 32, 1459, 10.1002/stem.1607 Moisan, 2015, White-to-brown metabolic conversion of human adipocytes by JAK inhibition, Nat. Cell Biol., 17, 57, 10.1038/ncb3075 Mottillo, 2012, Lipolytic products activate peroxisome proliferator-activated receptor (PPAR) α and δ in brown adipocytes to match fatty acid oxidation with supply, J. Biol. Chem., 287, 25038, 10.1074/jbc.M112.374041 Nedergaard, 2013, UCP1 mRNA does not produce heat, Biochim. Biophys. Acta, 1831, 943, 10.1016/j.bbalip.2013.01.009 Nishio, 2012, Production of functional classical brown adipocytes from human pluripotent stem cells using specific hemopoietin cocktail without gene transfer, Cell Metab., 16, 394, 10.1016/j.cmet.2012.08.001 Orava, 2011, Different metabolic responses of human brown adipose tissue to activation by cold and insulin, Cell Metab., 14, 272, 10.1016/j.cmet.2011.06.012 Pan, 2011, A role for Zic1 and Zic2 in Myf5 regulation and somite myogenesis, Dev. Biol., 351, 120, 10.1016/j.ydbio.2010.12.037 Ritchie, 2015, limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007 Roberts, 1986, Brown adipose tissue triacylglycerol fatty acids of obese and lean mice: in situ and in transplants, Lipids, 21, 195, 10.1007/BF02534821 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Rosenwald, 2013, Bi-directional interconversion of brite and white adipocytes, Nat. Cell Biol., 15, 659, 10.1038/ncb2740 Saito, 2009, High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity, Diabetes, 58, 1526, 10.2337/db09-0530 Sanchez-Gurmaches, 2014, Adipocytes arise from multiple lineages that are heterogeneously and dynamically distributed, Nat. Commun., 5, 4099, 10.1038/ncomms5099 Seale, 2008, PRDM16 controls a brown fat/skeletal muscle switch, Nature, 454, 961, 10.1038/nature07182 Shannon, 2003, Cytoscape: a software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Shapira, 2019, Transcriptional control of brown and beige fat development and function, Obesity (Silver Spring), 27, 13, 10.1002/oby.22334 Shinoda, 2015, Genetic and functional characterization of clonally derived adult human brown adipocytes, Nat. Med., 21, 389, 10.1038/nm.3819 Sidossis, 2015, Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis, J. Clin. Invest., 125, 478, 10.1172/JCI78362 Singh, 2018, What can ‘Brown-ing’ do for you?, Trends Endocrinol. Metab., 29, 349, 10.1016/j.tem.2018.03.002 Singh, 2015, Cell-cycle control of bivalent epigenetic domains regulates the exit from pluripotency, Stem Cell Reports, 5, 323, 10.1016/j.stemcr.2015.07.005 Si-Tayeb, 2010, Generation of human induced pluripotent stem cells by simple transient transfection of plasmid DNA encoding reprogramming factors, BMC Dev Biol., 10, 81, 10.1186/1471-213X-10-81 Stanford, 2013, Brown adipose tissue regulates glucose homeostasis and insulin sensitivity, J. Clin. Invest., 123, 215, 10.1172/JCI62308 Su, 2018, A renewable source of human beige adipocytes for development of therapies to treat metabolic syndrome, Cell Rep., 25, 3215, 10.1016/j.celrep.2018.11.037 Szklarczyk, 2019, STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets, Nucleic Acids Res., 47, D607, 10.1093/nar/gky1131 Toenhake, 2018, Chromatin accessibility-based characterization of the gene regulatory network underlying Plasmodium falciparum blood-stage development, Cell Host Microbe, 23, 557, 10.1016/j.chom.2018.03.007 Townsend, 2014, Brown fat fuel utilization and thermogenesis, Trends Endocrinol. Metab., 25, 168, 10.1016/j.tem.2013.12.004 Virtanen, 2009, Functional brown adipose tissue in healthy adults, N. Engl. J. Med., 360, 1518, 10.1056/NEJMoa0808949 Wang, 2013, Tracking adipogenesis during white adipose tissue development, expansion and regeneration, Nat. Med., 19, 1338, 10.1038/nm.3324 Warnes Weir, 2018, Substantial metabolic activity of human brown adipose tissue during warm conditions and cold-induced lipolysis of local triglycerides, Cell Metab., 27, 1348, 10.1016/j.cmet.2018.04.020 Wickham, 2016 Xi, 2017, In vivo human somitogenesis guides somite development from hPSCs, Cell Rep., 18, 1573, 10.1016/j.celrep.2017.01.040 Xue, 2015, Clonal analyses and gene profiling identify genetic biomarkers of the thermogenic potential of human brown and white preadipocytes, Nat. Med., 21, 760, 10.1038/nm.3881 Yu, 2002, Cold elicits the simultaneous induction of fatty acid synthesis and β-oxidation in murine brown adipose tissue: prediction from differential gene expression and confirmation in vivo, FASEB J., 16, 155, 10.1096/fj.01-0568com Yuan, 2019, Ex vivo and in vivo stable isotope labelling of central carbon metabolism and related pathways with analysis by LC-MS/MS, Nat. Protoc., 14, 313, 10.1038/s41596-018-0102-x Zhang, 2008, Model-based analysis of ChIP-Seq (MACS), Genome Biol., 9, R137, 10.1186/gb-2008-9-9-r137 Zhu, 2014, Enhanced sympathetic activity in mice with brown adipose tissue transplantation (transBATation), Physiol. Behav., 125, 21, 10.1016/j.physbeh.2013.11.008