Comprehensive Transcriptional Profiling and Mouse Phenotyping Reveals Dispensable Role for Adipose Tissue Selective Long Noncoding RNA Gm15551

. 2022 May 06 ; 8 (3) : . [epub] 20220506

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35645339

Grantová podpora
675014 European Research Council - International
00000 Danish Diabetes Academy
NNF18OC0033444 Novo Nordisk Foundation

Cold and nutrient-activated brown adipose tissue (BAT) is capable of increasing systemic energy expenditure via the uncoupled respiration and secretion of endocrine factors, thereby protecting mice against diet-induced obesity and improving insulin response and glucose tolerance in men. Long non-coding RNAs (lncRNAs) have recently been identified as fine-tuning regulators of cellular function. While certain lncRNAs have been functionally characterised in adipose tissue, their overall contribution in the activation of BAT remains elusive. We identified lncRNAs correlating to interscapular brown adipose tissue (iBAT) function in a high fat diet (HFD) and cold stressed mice. We focused on Gm15551, which has an adipose tissue specific expression profile, is highly upregulated during adipogenesis, and downregulated by β-adrenergic activation in mature adipocytes. Although we performed comprehensive transcriptional and adipocyte physiology profiling in vitro and in vivo, we could not detect an effect of gain or loss of function of Gm15551.

Zobrazit více v PubMed

NCD Risk Factor Collaboration (NCD-RisC) Trends in Adult Body-Mass Index in 200 Countries from 1975 to 2014: A Pooled Analysis of 1698 Population-Based Measurement Studies with 19·2 Million Participants. Lancet Lond. Engl. 2016;387:1377–1396. doi: 10.1016/S0140-6736(16)30054-X. PubMed DOI PMC

Angelantonio E.D., Bhupathiraju S.N., Wormser D., Gao P., Kaptoge S., de Gonzalez A.B., Cairns B.J., Huxley R., Jackson C.L., Joshy G., et al. Body-Mass Index and All-Cause Mortality: Individual-Participant-Data Meta-Analysis of 239 Prospective Studies in Four Continents. Lancet. 2016;388:776–786. doi: 10.1016/S0140-6736(16)30175-1. PubMed DOI PMC

Prospective Studies Collaboration Body-Mass Index and Cause-Specific Mortality in 900 000 Adults: Collaborative Analyses of 57 Prospective Studies. Lancet. 2009;373:1083–1096. doi: 10.1016/S0140-6736(09)60318-4. PubMed DOI PMC

Rosen E.D., Spiegelman B.M. What We Talk About When We Talk About Fat. Cell. 2014;156:20–44. doi: 10.1016/j.cell.2013.12.012. PubMed DOI PMC

Cannon B., Nedergaard J. Brown Adipose Tissue: Function and Physiological Significance. Physiol. Rev. 2004;84:277–359. doi: 10.1152/physrev.00015.2003. PubMed DOI

Betz M.J., Enerbäck S. Targeting Thermogenesis in Brown Fat and Muscle to Treat Obesity and Metabolic Disease. Nat. Rev. Endocrinol. 2018;14:77–87. doi: 10.1038/nrendo.2017.132. PubMed DOI

Klepac K., Georgiadi A., Tschöp M., Herzig S. The Role of Brown and Beige Adipose Tissue in Glycaemic Control. Mol. Aspects Med. 2019;68:90–100. doi: 10.1016/j.mam.2019.07.001. PubMed DOI

Scheele C., Wolfrum C. Brown Adipose Crosstalk in Tissue Plasticity and Human Metabolism. Endocr. Rev. 2020;41:53–65. doi: 10.1210/endrev/bnz007. PubMed DOI PMC

Zhang B., Yang Y., Xiang L., Zhao Z., Ye R. Adipose-Derived Exosomes: A Novel Adipokine in Obesity-Associated Diabetes. J. Cell. Physiol. 2019;234:16692–16702. doi: 10.1002/jcp.28354. PubMed DOI

Nedergaard J., Bengtsson T., Cannon B. Unexpected Evidence for Active Brown Adipose Tissue in Adult Humans. Am. J. Physiol. Endocrinol. Metab. 2007;293:E444–E452. doi: 10.1152/ajpendo.00691.2006. PubMed DOI

Djebali S., Davis C.A., Merkel A., Dobin A., Lassmann T., Mortazavi A., Tanzer A., Lagarde J., Lin W., Schlesinger F., et al. Landscape of Transcription in Human Cells. Nature. 2012;489:101–108. doi: 10.1038/nature11233. PubMed DOI PMC

Gil N., Ulitsky I. Regulation of Gene Expression by Cis -Acting Long Non-Coding RNAs. Nat. Rev. Genet. 2019;21:102–117. doi: 10.1038/s41576-019-0184-5. PubMed DOI

Yao R.-W., Wang Y., Chen L.-L. Cellular Functions of Long Noncoding RNAs. Nat. Cell Biol. 2019;21:542–551. doi: 10.1038/s41556-019-0311-8. PubMed DOI

Nguyen T.C., Zaleta-Rivera K., Huang X., Dai X., Zhong S. RNA, Action through Interactions. Trends Genet. TIG. 2018;34:867–882. doi: 10.1016/j.tig.2018.08.001. PubMed DOI PMC

Yi W., Li J., Zhu X., Wang X., Fan L., Sun W., Liao L., Zhang J., Li X., Ye J., et al. CRISPR-Assisted Detection of RNA–Protein Interactions in Living Cells. Nat. Methods. 2020;17:685–688. doi: 10.1038/s41592-020-0866-0. PubMed DOI

Derrien T., Johnson R., Bussotti G., Tanzer A., Djebali S., Tilgner H., Guernec G., Martin D., Merkel A., Knowles D.G., et al. The GENCODE v7 Catalog of Human Long Noncoding RNAs: Analysis of Their Gene Structure, Evolution, and Expression. Genome Res. 2012;22:1775–1789. doi: 10.1101/gr.132159.111. PubMed DOI PMC

Bai Z., Chai X., Yoon M.J., Kim H.-J., Lo K.A., Zhang Z., Xu D., Siang D.T.C., Walet A.C.E., Xu S., et al. Dynamic Transcriptome Changes during Adipose Tissue Energy Expenditure Reveal Critical Roles for Long Noncoding RNA Regulators. PLoS Biol. 2017;15:e2002176. doi: 10.1371/journal.pbio.2002176. PubMed DOI PMC

Schmidt E., Dhaouadi I., Gaziano I., Oliverio M., Klemm P., Awazawa M., Mitterer G., Fernandez-Rebollo E., Pradas-Juni M., Wagner W., et al. LincRNA H19 Protects from Dietary Obesity by Constraining Expression of Monoallelic Genes in Brown Fat. Nat. Commun. 2018;9:3622. doi: 10.1038/s41467-018-05933-8. PubMed DOI PMC

Bast-Habersbrunner A., Kiefer C., Weber P., Fromme T., Schießl A., Schwalie P.C., Deplancke B., Li Y., Klingenspor M. LncRNA Ctcflos Orchestrates Transcription and Alternative Splicing in Thermogenic Adipogenesis. EMBO Rep. 2021;22:e51289. doi: 10.15252/embr.202051289. PubMed DOI PMC

Alcalá M., Calderon-Dominguez M., Bustos E., Ramos P., Casals N., Serra D., Viana M., Herrero L. Increased Inflammation, Oxidative Stress and Mitochondrial Respiration in Brown Adipose Tissue from Obese Mice. Sci. Rep. 2017;7:16082. doi: 10.1038/s41598-017-16463-6. PubMed DOI PMC

Galarraga M., Campión J., Muñoz-Barrutia A., Boqué N., Moreno H., Martínez J.A., Milagro F., Ortiz-de-Solórzano C. Adiposoft: Automated Software for the Analysis of White Adipose Tissue Cellularity in Histological Sections. J. Lipid Res. 2012;53:2791–2796. doi: 10.1194/jlr.D023788. PubMed DOI PMC

Martin M. Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads. EMBnet. J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI

Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T.R. STAR: Ultrafast Universal RNA-Seq Aligner. Bioinformatics. 2013;29:15–21. doi: 10.1093/bioinformatics/bts635. PubMed DOI PMC

Patro R., Duggal G., Love M.I., Irizarry R.A., Kingsford C. Salmon Provides Fast and Bias-Aware Quantification of Transcript Expression. Nat. Methods. 2017;14:417–419. doi: 10.1038/nmeth.4197. PubMed DOI PMC

Langmead B., Salzberg S.L. Fast Gapped-Read Alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Alvarez-Dominguez J.R., Bai Z., Xu D., Yuan B., Lo K.A., Yoon M.J., Lim Y.C., Knoll M., Slavov N., Chen S., et al. De Novo Reconstruction of Adipose Tissue Transcriptomes Reveals Novel Long Non-Coding RNAs That Regulate Brown Adipocyte Development. Cell Metab. 2015;21:764–776. doi: 10.1016/j.cmet.2015.04.003. PubMed DOI PMC

Pradas-Juni M., Hansmeier N.R., Link J.C., Schmidt E., Larsen B.D., Klemm P., Meola N., Topel H., Loureiro R., Dhaouadi I., et al. A MAFG-LncRNA Axis Links Systemic Nutrient Abundance to Hepatic Glucose Metabolism. Nat. Commun. 2020;11:644. doi: 10.1038/s41467-020-14323-y. PubMed DOI PMC

Alexa A., Rahnenführer J., Lengauer T. Improved Scoring of Functional Groups from Gene Expression Data by Decorrelating GO Graph Structure. Bioinformatics. 2006;22:1600–1607. doi: 10.1093/bioinformatics/btl140. PubMed DOI

Yu G., He Q.-Y. ReactomePA: An R/Bioconductor Package for Reactome Pathway Analysis and Visualization. Mol. Biosyst. 2016;12:477–479. doi: 10.1039/C5MB00663E. PubMed DOI

Wang L., Park H.J., Dasari S., Wang S., Kocher J.-P., Li W. CPAT: Coding-Potential Assessment Tool Using an Alignment-Free Logistic Regression Model. Nucleic Acids Res. 2013;41:e74. doi: 10.1093/nar/gkt006. PubMed DOI PMC

Doench J.G., Hartenian E., Graham D.B., Tothova Z., Hegde M., Smith I., Sullender M., Ebert B.L., Xavier R.J., Root D.E. Rational Design of Highly Active SgRNAs for CRISPR-Cas9-Mediated Gene Inactivation. Nat. Biotechnol. 2014;32:1262–1267. doi: 10.1038/nbt.3026. PubMed DOI PMC

Konermann S., Brigham M.D., Trevino A.E., Joung J., Abudayyeh O.O., Barcena C., Hsu P.D., Habib N., Gootenberg J.S., Nishimasu H., et al. Genome-Scale Transcriptional Activation by an Engineered CRISPR-Cas9 Complex. Nature. 2015;517:583–588. doi: 10.1038/nature14136. PubMed DOI PMC

Love M.I., Huber W., Anders S. Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC

Zhu A., Ibrahim J.G., Love M.I. Heavy-Tailed Prior Distributions for Sequence Count Data: Removing the Noise and Preserving Large Differences. Bioinformatics. 2018;35:2084–2092. doi: 10.1093/bioinformatics/bty895. PubMed DOI PMC

Henriques F., Bedard A.H., Guilherme A., Kelly M., Chi J., Zhang P., Lifshitz L.M., Bellvé K., Rowland L.A., Yenilmez B., et al. Single-Cell RNA Profiling Reveals Adipocyte to Macrophage Signaling Sufficient to Enhance Thermogenesis. Cell Rep. 2020;32:107998. doi: 10.1016/j.celrep.2020.107998. PubMed DOI PMC

Natoli G., Andrau J.-C. Noncoding Transcription at Enhancers: General Principles and Functional Models. Annu. Rev. Genet. 2012;46:1–19. doi: 10.1146/annurev-genet-110711-155459. PubMed DOI

Anderson D.M., Anderson K.M., Chang C.-L., Makarewich C.A., Nelson B.R., McAnally J.R., Kasaragod P., Shelton J.M., Liou J., Bassel-Duby R., et al. A Micropeptide Encoded by a Putative Long Noncoding RNA Regulates Muscle Performance. Cell. 2015;160:595–606. doi: 10.1016/j.cell.2015.01.009. PubMed DOI PMC

Lundh M., Pluciñska K., Isidor M.S., Petersen P.S.S., Emanuelli B. Bidirectional Manipulation of Gene Expression in Adipocytes Using CRISPRa and SiRNA. Mol. Metab. 2017;6:1313–1320. doi: 10.1016/j.molmet.2017.07.001. PubMed DOI PMC

Rui L. Brown and Beige Adipose Tissues in Health and Disease. Compr. Physiol. 2017;7:1281–1306. doi: 10.1002/cphy.c170001. PubMed DOI PMC

Matsui M., Corey D.R. Perspectives: Noncoding RNAs as Drug Targets. Nat. Rev. Drug Discov. 2017;16:167–179. doi: 10.1038/nrd.2016.117. PubMed DOI PMC

Wahlestedt C. Targeting Long Non-Coding RNA to Therapeutically Upregulate Gene Expression. Nat. Rev. Drug Discov. 2013;12:433–446. doi: 10.1038/nrd4018. PubMed DOI

Sun L., Lin J.D. Function and Mechanism of Long Noncoding RNAs in Adipocyte Biology. Diabetes. 2019;68:887–896. doi: 10.2337/dbi18-0009. PubMed DOI PMC

Seale P., Kajimura S., Yang W., Chin S., Rohas L.M., Uldry M., Tavernier G., Langin D., Spiegelman B.M. Transcriptional Control of Brown Fat Determination by PRDM16. Cell Metab. 2007;6:38–54. doi: 10.1016/j.cmet.2007.06.001. PubMed DOI PMC

Seale P., Conroe H.M., Estall J., Kajimura S., Frontini A., Ishibashi J., Cohen P., Cinti S., Spiegelman B.M. Prdm16 Determines the Thermogenic Program of Subcutaneous White Adipose Tissue in Mice. J. Clin. Investig. 2011;121:96–105. doi: 10.1172/JCI44271. PubMed DOI PMC

Siersbæk M.S., Loft A., Aagaard M.M., Nielsen R., Schmidt S.F., Petrovic N., Nedergaard J., Mandrup S. Genome-Wide Profiling of Peroxisome Proliferator-Activated Receptor γ in Primary Epididymal, Inguinal, and Brown Adipocytes Reveals Depot-Selective Binding Correlated with Gene Expression. Mol. Cell. Biol. 2012;32:3452–3463. doi: 10.1128/MCB.00526-12. PubMed DOI PMC

Ji Z., Song R., Regev A., Struhl K. Many LncRNAs, 5′UTRs, and Pseudogenes Are Translated and Some Are Likely to Express Functional Proteins. eLife. 2015;4:e08890. doi: 10.7554/eLife.08890. PubMed DOI PMC

Gil N., Ulitsky I. Production of Spliced Long Noncoding RNAs Specifies Regions with Increased Enhancer Activity. Cell Syst. 2018;7:537–547. doi: 10.1016/j.cels.2018.10.009. PubMed DOI PMC

Maffei M., Barone I., Scabia G., Santini F. The Multifaceted Haptoglobin in the Context of Adipose Tissue and Metabolism. Endocr. Rev. 2016;37:403–416. doi: 10.1210/er.2016-1009. PubMed DOI

Sommer G., Weise S., Kralisch S., Scherer P.E., Lössner U., Blüher M., Stumvoll M., Fasshauer M. The Adipokine SAA3 Is Induced by Interleukin-1β in Mouse Adipocytes. J. Cell. Biochem. 2008;104:2241–2247. doi: 10.1002/jcb.21782. PubMed DOI

Sommer G., Weise S., Kralisch S., Lossner U., Bluher M., Stumvoll M., Fasshauer M. Lipocalin-2 Is Induced by Interleukin-1β in Murine Adipocytes in Vitro. J. Cell. Biochem. 2009;106:103–108. doi: 10.1002/jcb.21980. PubMed DOI

Guerra C., Navarro P., Valverde A.M., Arribas M., Brüning J., Kozak L.P., Kahn C.R., Benito M. Brown Adipose Tissue–Specific Insulin Receptor Knockout Shows Diabetic Phenotype without Insulin Resistance. J. Clin. Investig. 2001;108:1205–1213. doi: 10.1172/JCI13103. PubMed DOI PMC

Lowell B.B., S-Susulic V., Hamann A., Lawitts J.A., Himms-Hagen J., Boyer B.B., Kozak L.P., Flier J.S. Development of Obesity in Transgenic Mice after Genetic Ablation of Brown Adipose Tissue. Nature. 1993;366:740–742. doi: 10.1038/366740a0. PubMed DOI

Sun L., Goff L.A., Trapnell C., Alexander R., Lo K.A., Hacisuleyman E., Sauvageau M., Tazon-Vega B., Kelley D.R., Hendrickson D.G., et al. Long Noncoding RNAs Regulate Adipogenesis. Proc. Natl. Acad. Sci. USA. 2013;110:3387–3392. doi: 10.1073/pnas.1222643110. PubMed DOI PMC

Hughes M.R., Canals Hernaez D., Cait J., Refaeli I., Lo B.C., Roskelley C.D., McNagny K.M. A Sticky Wicket: Defining Molecular Functions for CD34 in Hematopoietic Cells. Exp. Hematol. 2020;86:1–14. doi: 10.1016/j.exphem.2020.05.004. PubMed DOI

Qian W., Liao B.-Y., Chang A.Y.-F., Zhang J. Maintenance of Duplicate Genes and Their Functional Redundancy by Reduced Expression. Trends Genet. 2010;26:425–430. doi: 10.1016/j.tig.2010.07.002. PubMed DOI PMC

Goudarzi M., Berg K., Pieper L.M., Schier A.F. Individual Long Non-Coding RNAs Have No Overt Functions in Zebrafish Embryogenesis, Viability and Fertility. eLife. 2019;8:e40815. doi: 10.7554/eLife.40815. PubMed DOI PMC

Han X., Luo S., Peng G., Lu J.Y., Cui G., Liu L., Yan P., Yin Y., Liu W., Wang R., et al. Mouse Knockout Models Reveal Largely Dispensable but Context-Dependent Functions of LncRNAs during Development. J. Mol. Cell Biol. 2018;10:175–178. doi: 10.1093/jmcb/mjy003. PubMed DOI

Palazzo A.F., Lee E.S. Non-Coding RNA: What Is Functional and What Is Junk? Front. Genet. 2015;6:2. doi: 10.3389/fgene.2015.00002. PubMed DOI PMC

Sanchez-Gurmaches J., Hung C.-M., Guertin D.A. Emerging Complexities in Adipocyte Origins and Identity. Trends Cell Biol. 2016;26:313–326. doi: 10.1016/j.tcb.2016.01.004. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...