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Review

Long Non-Coding RNAs in Brown Adipose Tissue

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Pages 3193-3204 | Published online: 15 Sep 2020

References

  • You W, Henneberg M. Relaxed natural selection contributes to global obesity increase more in males than in females due to more environmental modifications in female body mass. PLoS One. 2018;13(7):e0199594. doi:10.1371/journal.pone.0199594
  • Prentice AM. The emerging epidemic of obesity in developing countries. Int J Epidemiol. 2006;35(1):93–99. doi:10.1093/ije/dyi272
  • Fox CS, Massaro JM, Hoffmann U, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham heart study. Circulation. 2007;116(1):39–48. doi:10.1161/CIRCULATIONAHA.106.675355
  • Kim HJ, Kwon H, Jeong SM, Hwang SE, Park JH. Effects of abdominal visceral fat compared with those of subcutaneous fat on the association between PM10 and hypertension in Korean men: A cross-sectional study. Sci Rep. 2019;9(1):5951. doi:10.1038/s41598-019-42398-1
  • Ogden CL, Carroll MD, Flegal KM. Prevalence of obesity in the United States. JAMA. 2014;312(2):189–190. doi:10.1001/jama.2014.6228
  • Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol. 2006;7(12):885–896. doi:10.1038/nrm2066
  • Cai R, Tang G, Zhang Q, et al. A novel lnc-RNA, named lnc-ORA, is identified by RNA-Seq analysis, and its knockdown inhibits adipogenesis by regulating the PI3K/AKT/mTOR signaling pathway. Cells. 2019;8(5):E477. doi:10.3390/cells8050477
  • Zhang L, Zhang D, Qin ZY, Li J, Shen ZY. The role and possible mechanism of long noncoding RNA PVT1 in modulating 3T3-L1 preadipocyte proliferation and differentiation. IUBMB Life. 2020;72(7):1460–1467. doi:10.1002/iub.2269
  • Shen L, Han J, Wang H, et al. Cachexia-related long noncoding RNA, CAAlnc1, suppresses adipogenesis by blocking the binding of HuR to adipogenic transcription factor mRNAs. Int J Cancer. 2019;145(7):1809–1821. doi:10.1002/ijc.32236
  • Bhatt PS, Dhillo WS, Salem V. Human brown adipose tissue-function and therapeutic potential in metabolic disease. Curr Opin Pharmacol. 2017;37:1–9. doi:10.1016/j.coph.2017.07.004
  • Schmidt E, Dhaouadi I, Gaziano I, et al. LincRNA H19 protects from dietary obesity by constraining expression of monoallelic genes in brown fat. Nat Commun. 2018;9(1):3622. doi:10.1038/s41467-018-05933-8
  • Ding C, Lim YC, Chia SY, et al. De novo reconstruction of human adipose transcriptome reveals conserved lncRNAs as regulators of brown adipogenesis. Nat Commun. 2018;9(1):1329. doi:10.1038/s41467-018-03754-3
  • Peirce V, Carobbio S, Vidal-Puig A. The different shades of fat. Nature. 2014;510(7503):76–83. doi:10.1038/nature13477
  • Roesler A, Kazak L. UCP1-independent thermogenesis. Biochem J. 2020;477(3):709–725. doi:10.1042/BCJ20190463
  • Bargmann W, V. Hehn G, Lindner E. Über die Zellen des braunen Fettgewebes und ihre Innervation. Zeitschrift für Zellforschung und Mikroskopische Anatomie. 1968;85(4):601–613. doi:10.1007/BF00324749
  • Zhu Q, Glazier BJ, Hinkel BC, et al. Neuroendocrine regulation of energy metabolism involving different types of adipose tissues. Int J Mol Sci. 2019;20(11):2707. doi:10.3390/ijms20112707
  • Young P, Arch JR, Ashwell M. Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett. 1984;167(1):10–14. doi:10.1016/0014-5793(84)80822-4
  • Himms-Hagen J, Cui J, Danforth E Jr, et al. Effect of CL-316,243, a thermogenic beta 3-agonist, on energy balance and brown and white adipose tissues in rats. Am J Physiol. 1994;266(4 Pt 2):R1371–1382. doi:10.1152/ajpregu.1994.266.4.R1371
  • Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360(15):1509–1517. doi:10.1056/NEJMoa0810780
  • Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9(2):203–209. doi:10.1016/j.cmet.2008.12.014
  • Lowell BB, SS V, Hamann A, et al. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature. 1993;366(6457):740–742. doi:10.1038/366740a0
  • Farmer SR. Molecular determinants of brown adipocyte formation and function. Genes Dev. 2008;22(10):1269–1275. doi:10.1101/gad.1681308
  • Kajimura S, Seale P, Spiegelman BM. Transcriptional control of brown fat development. Cell Metab. 2010;11(4):257–262. doi:10.1016/j.cmet.2010.03.005
  • Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 2013;27(3):234–250. doi:10.1101/gad.211649.112
  • Li S, Mi L, Yu L, et al. Zbtb7b engages the long noncoding RNA Blnc1 to drive brown and beige fat development and thermogenesis. Proc Natl Acad Sci U S A. 2017;114(34):E7111–e7120. doi:10.1073/pnas.1703494114
  • Xu B, Gerin I, Miao H, et al. Multiple roles for the non-coding RNA SRA in regulation of adipogenesis and insulin sensitivity. PLoS One. 2010;5(12):e14199. doi:10.1371/journal.pone.0014199
  • Stamatoyannopoulos JA, Snyder M, Hardison R, et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol. 2012;13(8):418. doi:10.1186/gb-2012-13-8-418
  • Devaux Y, Zangrando J, Schroen B, et al. Long noncoding RNAs in cardiac development and ageing. Nat Rev Cardiol. 2015;12(7):415–425.
  • Peng WX, Koirala P, Mo YY. LncRNA-mediated regulation of cell signaling in cancer. Oncogene. 2017;36(41):5661–5667. doi:10.1038/onc.2017.184
  • Zeng Y, Ren K, Zhu X, Zheng Z, Yi G. Long noncoding RNAs: advances in lipid metabolism. Adv Clin Chem. 2018;87:1–36.
  • Alvarez-Dominguez JR, Bai Z, Xu D, et al. De novo reconstruction of adipose tissue transcriptomes reveals long non-coding RNA regulators of brown adipocyte development. Cell Metab. 2015;21(5):764–776. doi:10.1016/j.cmet.2015.04.003
  • Bai Z, Chai XR, Yoon MJ, et al. Dynamic transcriptome changes during adipose tissue energy expenditure reveal critical roles for long noncoding RNA regulators. PLoS Biol. 2017;15(8):e2002176. doi:10.1371/journal.pbio.2002176
  • Xiong Y, Yue F, Jia Z, et al. A novel brown adipocyte-enriched long non-coding RNA that is required for brown adipocyte differentiation and sufficient to drive thermogenic gene program in white adipocytes. Biochim Biophys Acta Mol Cell Biol Lipids. 2018;1863(4):409–419. doi:10.1016/j.bbalip.2018.01.008
  • Zhao XY, Li S, Wang GX, Yu Q, Lin JD. A long noncoding RNA transcriptional regulatory circuit drives thermogenic adipocyte differentiation. Mol Cell. 2014;55(3):372–382. doi:10.1016/j.molcel.2014.06.004
  • Cui X, You L, Li Y, et al. A transcribed ultraconserved noncoding RNA, uc.417, serves as a negative regulator of brown adipose tissue thermogenesis. FASEB J. 2016;30(12):4301–4312. doi:10.1096/fj.201600694R
  • Cai R, Sun Y, Qimuge N, et al. Adiponectin AS lncRNA inhibits adipogenesis by transferring from nucleus to cytoplasm and attenuating Adiponectin mRNA translation. Biochim Biophys Acta Mol Cell Biol Lipids. 2018;1863(4):420–432. doi:10.1016/j.bbalip.2018.01.005
  • You L, Zhou Y, Cui X, et al. GM13133 is a negative regulator in mouse white adipocytes differentiation and drives the characteristics of brown adipocytes. J Cell Physiol. 2018;233(1):313–324. doi:10.1002/jcp.25878
  • Watson JD, Crick FH. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature. 1953;171(4356):737–738. doi:10.1038/171737a0
  • Doolittle WF. Is junk DNA bunk? A critique of ENCODE. Proc Natl Acad Sci U S A. 2013;110(14):5294–5300. doi:10.1073/pnas.1221376110
  • Stein LD. Human genome: end of the beginning. Nature. 2004;431(7011):915–916. doi:10.1038/431915a
  • Siepel A. Finishing the euchromatic sequence of the human genome. Nature. 2005;50(2):931–945.
  • Batista PJ, Chang HY. Long noncoding RNAs: cellular address codes in development and disease. Cell. 2013;152(6):1298–1307. doi:10.1016/j.cell.2013.02.012
  • Tong C, Chen Q, Zhao L, Ma J, Ibeagha-Awemu EM, Zhao X. Identification and characterization of long intergenic noncoding RNAs in bovine mammary glands. BMC Genomics. 2017;18(1):468. doi:10.1186/s12864-017-3858-4
  • Reik W, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629–641. doi:10.1016/j.cell.2009.02.006
  • Ambros V. The functions of animal microRNAs. Nature. 2004;431(7006):350–355. doi:10.1038/nature02871
  • Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell. 2011;146(3):353–358. doi:10.1016/j.cell.2011.07.014
  • Cesana M, Cacchiarelli D, Legnini I, et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011;147(2):358–369. doi:10.1016/j.cell.2011.09.028
  • Gong C, Li Z, Ramanujan K, et al. A long non-coding RNA, LncMyoD, regulates skeletal muscle differentiation by blocking IMP2-mediated mRNA translation. Dev Cell. 2015;34(2):181–191. doi:10.1016/j.devcel.2015.05.009
  • Zhou J, Yang L, Zhong T, et al. H19 lncRNA alters DNA methylation genome wide by regulating S-adenosylhomocysteine hydrolase. Nat Commun. 2015;6:10221. doi:10.1038/ncomms10221
  • Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013;152(6):1308–1323. doi:10.1016/j.cell.2013.02.016
  • Dey BK, Pfeifer K, Dutta A. The H19 long noncoding RNA gives rise to microRNAs miR-675-3p and miR-675-5p to promote skeletal muscle differentiation and regeneration. Genes Dev. 2014;28(5):491–501. doi:10.1101/gad.234419.113
  • Tripathi V, Ellis JD, Shen Z, et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010;39(6):925–938. doi:10.1016/j.molcel.2010.08.011
  • Sun L, Goff LA, Trapnell C, et al. Long noncoding RNAs regulate adipogenesis. Proc Natl Acad Sci U S A. 2013;110(9):3387–3392. doi:10.1073/pnas.1222643110
  • Hacisuleyman E, Goff LA, Trapnell C, et al. Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nat Struct Mol Biol. 2014;21(2):198–206. doi:10.1038/nsmb.2764
  • Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–15550. doi:10.1073/pnas.0506580102
  • Amaya Ramirez CC, Hubbe P, Mandel N, Béthune J. 4EHP-independent repression of endogenous mRNAs by the RNA-binding protein GIGYF2. Nucleic Acids Res. 2018;46(11):5792–5808. doi:10.1093/nar/gky198
  • Okazaki Y, Furuno M, Kasukawa T, et al. Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature. 2002;420(6915):563–573.
  • Cornelis G, Souquere S, Vernochet C, Heidmann T, Pierron G. Functional conservation of the lncRNA NEAT1 in the ancestrally diverged marsupial lineage: evidence for NEAT1 expression and associated paraspeckle assembly during late gestation in the opossum Monodelphis domestica. RNA Biol. 2016;13(9):826–836. doi:10.1080/15476286.2016.1197482
  • Huang Y. The novel regulatory role of lncRNA-miRNA-mRNA axis in cardiovascular diseases. J Cell Mol Med. 2018;22(12):5768–5775. doi:10.1111/jcmm.13866
  • Kutter C, Watt S, Stefflova K, et al. Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet. 2012;8(7):e1002841. doi:10.1371/journal.pgen.1002841
  • Mi L, Zhao XY, Li S, Yang G, Lin JD. Conserved function of the long noncoding RNA Blnc1 in brown adipocyte differentiation. Mol Metab. 2017;6(1):101–110. doi:10.1016/j.molmet.2016.10.010
  • Somarowthu S, Legiewicz M, Chillón I, Marcia M, Liu F, Pyle AM. HOTAIR forms an intricate and modular secondary structure. Mol Cell. 2015;58(2):353–361. doi:10.1016/j.molcel.2015.03.006
  • Xue Z, Hennelly S, Doyle B, et al. A G-rich motif in the lncRNA braveheart interacts with a zinc-finger transcription factor to specify the cardiovascular lineage. Mol Cell. 2016;64(1):37–50. doi:10.1016/j.molcel.2016.08.010
  • Ghafouri-Fard S, Esmaeili M, Taheri MH. 19 lncRNA: roles in tumorigenesis. Biomed Pharmacother. 2020;123:109774. doi:10.1016/j.biopha.2019.109774
  • Xu X, Ji S, Li W, et al. LncRNA H19 promotes the differentiation of bovine skeletal muscle satellite cells by suppressing Sirt1/FoxO1. Cell Mol Biol Lett. 2017;22(1):10. doi:10.1186/s11658-017-0040-6
  • Chen L, Wang Y, He J, Zhang C, Chen J, Shi D. Long non-coding RNA H19 promotes proliferation and invasion in human glioma cells by downregulating miR-152. Oncol Res. 2018;26:1419–1428.
  • Li X, Wang H, Zhang Y, et al. Overexpression of lncRNA H19 changes basic characteristics and affects immune response of bovine mammary epithelial cells. Peer J. 2019;7:e6715. doi:10.7717/peerj.6715
  • Nordin M, Bergman D, Halje M, Engström W, Ward A. Epigenetic regulation of the Igf2/H19 gene cluster. Cell Prolif. 2014;47(3):189–199. doi:10.1111/cpr.12106
  • Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360(15):1518–1525. doi:10.1056/NEJMoa0808949
  • Ranzani V, Rossetti G, Panzeri I, Arrigoni A, Pagani M. The long intergenic noncoding RNA landscape of human lymphocytes highlights the regulation of T cell differentiation by linc-MAF-4. Nat Immunol. 2015;16(3):318. doi:10.1038/ni.3093
  • Amin V, Harris RA, Onuchic V, et al. Epigenomic footprints across 111 reference epigenomes reveal tissue-specific epigenetic regulation of lincRNAs. Nat Commun. 2015;6:6370. doi:10.1038/ncomms7370
  • Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57. doi:10.1038/nprot.2008.211
  • Zhang B, Arun G, Mao YS, et al. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2012;2(1):111–123. doi:10.1016/j.celrep.2012.06.003
  • Yan P, Luo S, Lu JY, Shen X. Cis- and trans-acting lncRNAs in pluripotency and reprogramming. Curr Opin Genet Dev. 2017;46:170–178. doi:10.1016/j.gde.2017.07.009
  • Wang GX, Zhao XY, Lin JD. The brown fat secretome: metabolic functions beyond thermogenesis. Trends Endocrinol Metab. 2015;26(5):231–237. doi:10.1016/j.tem.2015.03.002
  • Magistri M, Faghihi MA, St Laurent G 3rd, Wahlestedt C. Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet. 2012;28(8):389–396. doi:10.1016/j.tig.2012.03.013
  • Halley P, Kadakkuzha BM, Faghihi MA, et al. Regulation of the apolipoprotein gene cluster by a long noncoding RNA. Cell Rep. 2014;6(1):222–230. doi:10.1016/j.celrep.2013.12.015
  • Stern JH, Rutkowski JM, Scherer PE. Adiponectin, leptin, and fatty acids in the maintenance of metabolic homeostasis through adipose tissue crosstalk. Cell Metab. 2016;23(5):770–784. doi:10.1016/j.cmet.2016.04.011
  • Wang GZ, Du K, Hu SQ, et al. Genome-wide identification and characterization of long non-coding RNAs during postnatal development of rabbit adipose tissue. Lipids Health Dis. 2018;17(1):271. doi:10.1186/s12944-018-0915-1
  • Huang X, Fu C, Liu W, et al. Chemerin-induced angiogenesis and adipogenesis in 3 T3-L1 preadipocytes is mediated by lncRNA Meg3 through regulating Dickkopf-3 by sponging miR-217. Toxicol Appl Pharmacol. 2019;385:114815. doi:10.1016/j.taap.2019.114815
  • Liu Y, Wang Y, He X, et al. LncRNA TINCR/miR-31-5p/C/EBP-α feedback loop modulates the adipogenic differentiation process in human adipose tissue-derived mesenchymal stem cells. Stem Cell Res. 2018;32:35–42. doi:10.1016/j.scr.2018.08.016
  • Liu H, Li H, Jin L, et al. Long noncoding RNA GAS5 suppresses 3T3-L1 cells adipogenesis through miR-21a-5p/PTEN signal pathway. DNA Cell Biol. 2018;37(9):767–777. doi:10.1089/dna.2018.4264
  • Li FP, Lin DQ, Gao LY. LncRNA TUG1 promotes proliferation of vascular smooth muscle cell and atherosclerosis through regulating miRNA-21/PTEN axis. Eur Rev Med Pharmacol Sci. 2018;22(21):7439–7447. doi:10.26355/eurrev_201811_16284
  • Burl RB, Ramseyer VD, Rondini EA, Pique-Regi R, Lee YH, Granneman JG. Deconstructing adipogenesis induced by β3-adrenergic receptor activation with single-cell expression profiling. Cell Metab. 2018;28(2):300–309.e304. doi:10.1016/j.cmet.2018.05.025
  • Wang J, Zibetti C, Shang P, et al. ATAC-Seq analysis reveals a widespread decrease of chromatin accessibility in age-related macular degeneration. Nat Commun. 2018;9(1):1364. doi:10.1038/s41467-018-03856-y
  • Suzuki A, Terao C, Yamamoto K. Linking of genetic risk variants to disease-specific gene expression via multi-omics studies in rheumatoid arthritis. Semin Arthritis Rheum. 2019;49(3s):S49–S53. doi:10.1016/j.semarthrit.2019.09.007
  • Guo H, Liu J, Ben Q, et al. The aspirin-induced long non-coding RNA OLA1P2 blocks phosphorylated STAT3 homodimer formation. Genome Biol. 2016;17:24. doi:10.1186/s13059-016-0892-5
  • Khvorova A, Watts JK. The chemical evolution of oligonucleotide therapies of clinical utility. Nat Biotechnol. 2017;35(3):238–248. doi:10.1038/nbt.3765
  • van Heesch S, van Iterson M, Jacobi J, et al. Extensive localization of long noncoding RNAs to the cytosol and mono- and polyribosomal complexes. Genome Biol. 2014;15(1):R6. doi:10.1186/gb-2014-15-1-r6