1932

Abstract

Long noncoding RNAs (lncRNAs) are sensitive to changing environments and play key roles in health and disease. Emerging evidence indicates that lncRNAs regulate gene expression to shape metabolic processes in response to changing nutritional cues. Here we review various lncRNAs sensitive to fasting, feeding, and high-fat diet in key metabolic tissues (liver, adipose, and muscle), highlighting regulatory mechanisms that trigger expression changes of lncRNAs themselves, and how these lncRNAs regulate gene expression of key metabolic genes in specific cell types or across tissues. Determining how lncRNAs respond to changes in nutrition is critical for our understanding of the complex downstream cascades following dietary changes and can shape how we treat metabolic disease. Furthermore, investigating sex biases that might influence lncRNA-regulated responses will likely reveal contributions toward the observed disparities between the sexes in metabolic diseases.

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2022-08-22
2024-12-14
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Literature Cited

  1. 1.
    Agliano F, Rathinam VA, Medvedev AE, Vanaja SK, Vella AT. 2019. Long noncoding RNAs in host-pathogen interactions. Trends Immunol. 40:6492–510
    [Google Scholar]
  2. 2.
    Al-Rugeebah A, Alanazi M, Parine NR. 2019. MEG3: an oncogenic long non-coding RNA in different cancers. Pathol. Oncol. Res. 25:3859–74
    [Google Scholar]
  3. 3.
    Anderson DM, Anderson KM, Chang C-L, Makarewich CA, Nelson BR et al. 2015. A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 160:4595–606
    [Google Scholar]
  4. 4.
    Audas TE, Lee S. 2016. Stressing out over long noncoding RNA. Biochim. Biophys. Acta Gene Regul. Mech. 1859:1184–91
    [Google Scholar]
  5. 5.
    Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N. 1991. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349:630484–87
    [Google Scholar]
  6. 6.
    Bartolomei MS, Zemel S, Tilghman SM. 1991. Parental imprinting of the mouse H19 gene. Nature 351:6322153–55
    [Google Scholar]
  7. 7.
    Berletch JB, Ma W, Yang F, Shendure J, Noble WS et al. 2015. Escape from X inactivation varies in mouse tissues. PLOS Genet 11:3e1005079
    [Google Scholar]
  8. 8.
    Borsani G, Tonlorenzi R, Simmler MC, Dandolo L, Arnaud D et al. 1991. Characterization of a murine gene expressed from the inactive X chromosome. Nature 351:6324325–29
    [Google Scholar]
  9. 9.
    Braconi C, Kogure T, Valeri N, Huang N, Nuovo G et al. 2011. microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30:474750–56
    [Google Scholar]
  10. 10.
    Brockdorff N, Ashworth A, Kay GF, Cooper P, Smith S et al. 1991. Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome. Nature 351:6324329–31
    [Google Scholar]
  11. 11.
    Brown CJ, Willard HF. 1994. The human X-inactivation centre is not required for maintenance of X-chromosome inactivation. Nature 368:6467154–56
    [Google Scholar]
  12. 12.
    Calkin AC, Tontonoz P. 2012. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat. Rev. Mol. Cell Biol. 13:4213–24
    [Google Scholar]
  13. 13.
    Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:7031400–4
    [Google Scholar]
  14. 14.
    Cava C, Bertoli G, Castiglioni I. 2019. Portrait of tissue-specific coexpression networks of noncoding RNAs (miRNA and lncRNA) and mRNAs in normal tissues. Comput. Math. Methods Med. 2019:9029351
    [Google Scholar]
  15. 15.
    Cech TR, Steitz JA. 2014. The noncoding RNA revolution—trashing old rules to forge new ones. Cell 157:177–94
    [Google Scholar]
  16. 16.
    Chadwick BP, Willard HF. 2004. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. PNAS 101:5017450–55
    [Google Scholar]
  17. 17.
    Chen G, Yu D, Nian X, Liu J, Koenig RJ et al. 2016. LncRNA SRA promotes hepatic steatosis through repressing the expression of adipose triglyceride lipase (ATGL). Sci. Rep. 6:135531
    [Google Scholar]
  18. 18.
    Chen X, McClusky R, Chen J, Beaven SW, Tontonoz P et al. 2012. The number of X chromosomes causes sex differences in adiposity in mice. PLOS Genet 8:5e1002709
    [Google Scholar]
  19. 19.
    Clemson CM, McNeil JA, Willard HF, Lawrence JB. 1996. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132:3259–75
    [Google Scholar]
  20. 20.
    Csankovszki G, Nagy A, Jaenisch R. 2001. Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation. J. Cell Biol. 153:4773–84
    [Google Scholar]
  21. 21.
    Cui X, Tan J, Shi Y, Sun C, Li Y et al. 2018. The long non-coding RNA Gm10768 activates hepatic gluconeogenesis by sequestering microRNA-214 in mice. J. Biol. Chem. 293:114097–109
    [Google Scholar]
  22. 22.
    Dalsgaard T, Cecchi CR, Askou AL, Bak RO, Andersen PO et al. 2018. Improved lentiviral gene delivery to mouse liver by hydrodynamic vector injection through tail vein. Mol. Ther. Nucleic Acids 12:672–83
    [Google Scholar]
  23. 23.
    de Aguiar Vallim TQ, Tarling EJ, Edwards PA. 2013. Pleiotropic roles of bile acids in metabolism. Cell Metab. 17:5657–69
    [Google Scholar]
  24. 24.
    Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S et al. 2012. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22:91775–89
    [Google Scholar]
  25. 25.
    Du K, Herzig S, Kulkarni RN, Montminy M. 2003. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300:56251574–77
    [Google Scholar]
  26. 26.
    Ezkurdia I, Juan D, Rodriguez JM, Frankish A, Diekhans M et al. 2014. Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes. Hum. Mol. Genet. 23:225866–78
    [Google Scholar]
  27. 27.
    Fang S, Zhang L, Guo J, Niu Y, Wu Y et al. 2018. NONCODEV5: a comprehensive annotation database for long non-coding RNAs. Nucleic Acids Res. 46:D1D308–14
    [Google Scholar]
  28. 28.
    Ferreira CR, van Karnebeek CDM, Vockley J, Blau N. 2019. A proposed nosology of inborn errors of metabolism. Genet. Med. 21:1102–6
    [Google Scholar]
  29. 29.
    Gabory A, Jammes H, Dandolo L. 2010. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 32:6473–80
    [Google Scholar]
  30. 30.
    Gao Y, Wu F, Zhou J, Yan L, Jurczak MJ et al. 2014. The H19/let-7 double-negative feedback loop contributes to glucose metabolism in muscle cells. Nucleic Acids Res. 42:2213799–811
    [Google Scholar]
  31. 31.
    Geng T, Liu Y, Xu Y, Jiang Y, Zhang N et al. 2018. H19 lncRNA promotes skeletal muscle insulin sensitivity in part by targeting AMPK. Diabetes 67:112183–98
    [Google Scholar]
  32. 32.
    Ghafouri-Fard S, Esmaeili M, Taheri M. 2020. H19 lncRNA: roles in tumorigenesis. Biomed. Pharmacother. 123:109774
    [Google Scholar]
  33. 33.
    Ghafouri-Fard S, Taheri M. 2019. Maternally expressed gene 3 (MEG3): a tumor suppressor long non coding RNA. Biomed. Pharmacother. 118:109129
    [Google Scholar]
  34. 34.
    Go G. 2015. Low-density lipoprotein receptor-related protein 6 (LRP6) is a novel nutritional therapeutic target for hyperlipidemia, non-alcoholic fatty liver disease, and atherosclerosis. Nutrients 7:64453–64
    [Google Scholar]
  35. 35.
    Hernandez-Munoz I, Lund AH, van der Stoop P, Boutsma E, Muijrers I et al. 2005. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. PNAS 102:217635–40
    [Google Scholar]
  36. 36.
    Horton JD, Goldstein JL, Brown MS. 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Investig. 109:91125–31
    [Google Scholar]
  37. 37.
    Huang P, Huang F, Liu H, Zhang T, Yang M, Sun C 2019. LncRNA MEG3 functions as a ceRNA in regulating hepatic lipogenesis by competitively binding to miR-21 with LRP6. Metabolism 94:1–8
    [Google Scholar]
  38. 38.
    Int. Hum. Genome Seq. Consort 2004. Finishing the euchromatic sequence of the human genome. Nature 431:7011931–45
    [Google Scholar]
  39. 39.
    Int. Hum. Genome Seq. Consort 2001. Initial sequencing and analysis of the human genome. Nature 409:6822860–921
    [Google Scholar]
  40. 40.
    Jiang S, Cheng S-J, Ren L-C, Wang Q, Kang Y-J et al. 2019. An expanded landscape of human long noncoding RNA. Nucleic Acids Res. 47:157842–56
    [Google Scholar]
  41. 41.
    Kallen AN, Zhou X-B, Xu J, Qiao C, Ma J et al. 2013. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol. Cell 52:1101–12
    [Google Scholar]
  42. 42.
    Komatsu M, Waguri S, Chiba T, Murata S, Iwata J et al. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:7095880–84
    [Google Scholar]
  43. 43.
    Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H et al. 2004. The role of autophagy during the early neonatal starvation period. Nature 432:70201032–36
    [Google Scholar]
  44. 44.
    Kung JTY, Colognori D, Lee JT. 2013. Long noncoding RNAs: past, present, and future. Genetics 193:3651–69
    [Google Scholar]
  45. 45.
    Lee EB, Lee VM-Y, Trojanowski JQ. 2012. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci. 13:138–50
    [Google Scholar]
  46. 46.
    Li K, Zhang J, Yu J, Liu B, Guo Y et al. 2015. MicroRNA-214 suppresses gluconeogenesis by targeting activating transcriptional factor 4. J. Biol. Chem. 290:138185–95
    [Google Scholar]
  47. 47.
    Li P, Ruan X, Yang L, Kiesewetter K, Zhao Y et al. 2015. A liver-enriched long non-coding RNA, lncLSTR, regulates systemic lipid metabolism in mice. Cell Metab. 21:3455–67
    [Google Scholar]
  48. 48.
    Li S, Li Y, Chen B, Zhao J, Yu S et al. 2018. exoRBase: a database of circRNA, lncRNA and mRNA in human blood exosomes. Nucleic Acids Res. 46:D1D106–12
    [Google Scholar]
  49. 49.
    Li S, Mi L, Yu L, Yu Q, Liu T et al. 2017. Zbtb7b engages the long noncoding RNA Blnc1 to drive brown and beige fat development and thermogenesis. PNAS 114:34E7111–20
    [Google Scholar]
  50. 50.
    Li Y, Chen X, Sun H, Wang H. 2018. Long non-coding RNAs in the regulation of skeletal myogenesis and muscle diseases. Cancer Lett. 417:58–64
    [Google Scholar]
  51. 51.
    Link JC, Reue K. 2017. Genetic basis for sex differences in obesity and lipid metabolism. Annu. Rev. Nutr. 37:1225–45
    [Google Scholar]
  52. 52.
    Liu S, Sheng L, Miao H, Saunders TL, MacDougald OA et al. 2014. SRA gene knockout protects against diet-induced obesity and improves glucose tolerance. J. Biol. Chem. 289:1913000–9
    [Google Scholar]
  53. 53.
    Lo KA, Huang S, Walet ACE, Zhang Z, Leow MK-S et al. 2018. Adipocyte long-noncoding RNA transcriptome analysis of obese mice identified Lnc-leptin, which regulates leptin. Diabetes 67:61045–56
    [Google Scholar]
  54. 54.
    Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:4773373–74
    [Google Scholar]
  55. 55.
    Ma M, Duan R, Shen L, Liu M, Ji Y et al. 2020. The lncRNA Gm15622 stimulates SREBP-1c expression and hepatic lipid accumulation by sponging the miR-742-3p in mice. J. Lipid Res. 61:71052–64
    [Google Scholar]
  56. 56.
    Mahpour A, Mullen AC. 2021. Our emerging understanding of the roles of long non-coding RNAs in normal liver function, disease, and malignancy. JHEP Rep 3:1100177
    [Google Scholar]
  57. 57.
    Marahrens Y, Panning B, Dausman J, Strauss W, Jaenisch R. 1997. Xist-deficient mice are defective in dosage compensation but not spermatogenesis. Genes Dev. 11:2156–66
    [Google Scholar]
  58. 58.
    Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA et al. 2011. The human mitochondrial transcriptome. Cell 146:4645–58
    [Google Scholar]
  59. 59.
    Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T et al. 2014. The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505:7485635–40
    [Google Scholar]
  60. 60.
    Nelson BR, Makarewich CA, Anderson DM, Winders BR, Troupes CD et al. 2016. A peptide encoded by a transcript annotated as long noncoding RNA enhances SERCA activity in muscle. Science 351:6270271–75
    [Google Scholar]
  61. 61.
    Nilsson E, Matte A, Perfilyev A, de Mello VD, Käkelä P et al. 2015. Epigenetic alterations in human liver from subjects with type 2 diabetes in parallel with reduced folate levels. J. Clin. Endocrinol. Metab. 100:11E1491–501
    [Google Scholar]
  62. 62.
    Ong KT, Mashek MT, Bu SY, Greenberg AS, Mashek DG. 2011. Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 53:1116–26
    [Google Scholar]
  63. 63.
    Pennisi E. 2012. ENCODE project writes eulogy for junk DNA. Science 337:60991159–61
    [Google Scholar]
  64. 64.
    Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorfft BN. 1996. Requirement for Xist in X chromosome inactivation. Nature 379:6561131–37
    [Google Scholar]
  65. 65.
    Pradas-Juni M, Hansmeier NR, Link JC, Schmidt E, Larsen BD et al. 2020. A MAFG-lncRNA axis links systemic nutrient abundance to hepatic glucose metabolism. Nat. Commun. 11:1644
    [Google Scholar]
  66. 66.
    Pyfrom S, Paneru B, Knoxx JJ, Cancro MP, Posso S et al. 2021. The dynamic epigenetic regulation of the inactive X chromosome in healthy human B cells is dysregulated in lupus patients. PNAS 118:24e2024624118
    [Google Scholar]
  67. 67.
    Recena Aydos L, Aparecida do Amaral L, Serafim de Souza R, Jacobowski AC, Freitas dos Santos E, Rodrigues Macedo ML. 2019. Nonalcoholic fatty liver disease induced by high-fat diet in C57bl/6 models. Nutrients 11:123067
    [Google Scholar]
  68. 68.
    Reik W, Brown KW, Slatter RE, Sartor P, Elliott M, Maher ER. 1994. Allelic methylation of H19 and IGF2 in the Beckwith–Wiedemann syndrome. Hum. Mol. Genet. 3:81297–1301
    [Google Scholar]
  69. 69.
    Ruan X, Li P, Cangelosi A, Yang L, Cao H 2016. A long non-coding RNA, lncLGR, regulates hepatic glucokinase expression and glycogen storage during fasting. Cell Rep. 14:81867–75
    [Google Scholar]
  70. 70.
    Ruan X, Li P, Ma Y, Jiang C, Chen Y et al. 2021. Identification of human long noncoding RNAs associated with nonalcoholic fatty liver disease and metabolic homeostasis. J. Clin. Investig. 131:1e136336
    [Google Scholar]
  71. 71.
    Schultz JR. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14:222831–38
    [Google Scholar]
  72. 72.
    Shabgah AG, Norouzi F, Hedayati-Moghadam M, Soleimani D, Pahlavani N, Navashenaq JG. 2021. A comprehensive review of long non-coding RNAs in the pathogenesis and development of non-alcoholic fatty liver disease. Nutr. Metab. 18:122
    [Google Scholar]
  73. 73.
    Shen X, Zhang Y, Zhang X, Yao Y, Zheng Y et al. 2019. Long non-coding RNA Bhmt-AS attenuates hepatic gluconeogenesis via modulation of Bhmt expression. Biochem. Biophys. Res. Commun. 516:1215–21
    [Google Scholar]
  74. 74.
    Sun C, Liu X, Yi Z, Xiao X, Yang M et al. 2015. Genome-wide analysis of long noncoding RNA expression profiles in patients with non-alcoholic fatty liver disease: lncRNAs role in NAFLD. IUBMB Life 67:11847–52
    [Google Scholar]
  75. 75.
    Sun L, Goff LA, Trapnell C, Alexander R, Lo KA et al. 2013. Long noncoding RNAs regulate adipogenesis. PNAS 110:93387–92
    [Google Scholar]
  76. 76.
    Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. 1988. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37:91163–67
    [Google Scholar]
  77. 77.
    Syrett CM, Paneru B, Sandoval-Heglund D, Wang J, Banerjee S et al. 2019. Altered X-chromosome inactivation in T cells may promote sex-biased autoimmune diseases. JCI Insight 4:7e126751
    [Google Scholar]
  78. 78.
    Syrett CM, Sierra I, Beethem ZT, Dubin AH, Anguera MC. 2019. Loss of epigenetic modifications on the inactive X chromosome and sex-biased gene expression profiles in B cells from NZB/W F1 mice with lupus-like disease. J. Autoimmun. 107:102357
    [Google Scholar]
  79. 79.
    Syrett CM, Sindhava V, Hodawadekar S, Myles A, Liang G et al. 2017. Loss of Xist RNA from the inactive X during B cell development is restored in a dynamic YY1-dependent two-step process in activated B cells. PLOS Genet 13:10e1007050
    [Google Scholar]
  80. 80.
    Teng Y-W, Ellis JM, Coleman RA, Zeisel SH. 2012. Mouse betaine-homocysteine S-methyltransferase deficiency reduces body fat via increasing energy expenditure and impairing lipid synthesis and enhancing glucose oxidation in white adipose tissue. J. Biol. Chem. 287:2016187–98
    [Google Scholar]
  81. 81.
    Tukiainen T, Villani A-C, Yen A, Rivas MA, Marshall JL et al. 2017. Landscape of X chromosome inactivation across human tissues. Nature 550:7675244–48
    [Google Scholar]
  82. 82.
    Uchida S, Kauppinen S. 2020. Long non-coding RNAs in liver cancer and nonalcoholic steatohepatitis. Noncoding RNA 6:334
    [Google Scholar]
  83. 83.
    Ulitsky I. 2016. Evolution to the rescue: using comparative genomics to understand long non-coding RNAs. Nat. Rev. Genet. 17:10601–14
    [Google Scholar]
  84. 84.
    Wang J, Syrett CM, Kramer MC, Basu A, Atchison ML, Anguera MC. 2016. Unusual maintenance of X chromosome inactivation predisposes female lymphocytes for increased expression from the inactive X. PNAS 113:14E2029–38
    [Google Scholar]
  85. 85.
    Wang J, Yang W, Chen Z, Chen J, Meng Y et al. 2018. Long noncoding RNA lncSHGL recruits hnRNPA1 to suppress hepatic gluconeogenesis and lipogenesis. Diabetes 67:4581–93
    [Google Scholar]
  86. 86.
    Wang Y, Hu Y, Sun C, Zhuo S, He Z et al. 2016. Down-regulation of Risa improves insulin sensitivity by enhancing autophagy. FASEB J. 30:93133–45
    [Google Scholar]
  87. 87.
    Williams KJ. 2008. Molecular processes that handle—and mishandle—dietary lipids. J. Clin. Investig. 118:103247–59
    [Google Scholar]
  88. 88.
    Xu B, Gerin I, Miao H, Vu-Phan D, Johnson CN et al. 2010. Multiple roles for the non-coding RNA SRA in regulation of adipogenesis and insulin sensitivity. PLOS ONE 5:12e14199
    [Google Scholar]
  89. 89.
    Yan B, Yao J, Liu J-Y, Li X-M, Wang X-Q et al. 2015. lncRNA-MIAT regulates microvascular dysfunction by functioning as a competing endogenous RNA. Circ. Res. 116:71143–56
    [Google Scholar]
  90. 90.
    Yan C, Li J, Feng S, Li Y, Tan L. 2018. Long noncoding RNA Gomafu upregulates Foxo1 expression to promote hepatic insulin resistance by sponging miR-139-5p. Cell Death Dis 9:3289
    [Google Scholar]
  91. 91.
    Yang L, Li P, Yang W, Ruan X, Kiesewetter K et al. 2016. Integrative transcriptome analyses of metabolic responses in mice define pivotal lncRNA metabolic regulators. Cell Metab. 24:4627–39
    [Google Scholar]
  92. 92.
    Yang L, Yildirim E, Kirby JE, Press W, Lee JT. 2020. Widespread organ tolerance to Xist loss and X reactivation except under chronic stress in the gut. PNAS 117:84262–72
    [Google Scholar]
  93. 93.
    Yao Z, Liu C, Yu X, Meng J, Teng B et al. 2019. Microarray profiling and coexpression network analysis of long noncoding RNAs in adipose tissue of obesity-T2DM mouse. Obesity 27:101644–51
    [Google Scholar]
  94. 94.
    Yildirim E. 2013. Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152:727–42
    [Google Scholar]
  95. 95.
    Zemel S, Bartolomei MS, Tilghman SM. 1992. Physical linkage of two mammalian imprinted genes, H19 and insulin-like growth factor 2. Nat. Genet. 2:161–65
    [Google Scholar]
  96. 96.
    Zhang J, Chen M, Chen J, Lin S, Cai D et al. 2017. Long non-coding RNA MIAT acts as a biomarker in diabetic retinopathy by absorbing miR-29b and regulating cell apoptosis. Biosci. Rep. 37:2BSR20170036
    [Google Scholar]
  97. 97.
    Zhang N, Geng T, Wang Z, Zhang R, Cao T et al. 2018. Elevated hepatic expression of H19 long noncoding RNA contributes to diabetic hyperglycemia. JCI Insight 3:10e120304
    [Google Scholar]
  98. 98.
    Zhao X-Y, Li S, Wang G-X, Yu Q, Lin JD 2014. A long noncoding RNA transcriptional regulatory circuit drives thermogenic adipocyte differentiation. Mol. Cell 55:3372–82
    [Google Scholar]
  99. 99.
    Zhao X-Y, Xiong X, Liu T, Mi L, Peng X et al. 2018. Long noncoding RNA licensing of obesity-linked hepatic lipogenesis and NAFLD pathogenesis. Nat. Commun. 9:12986
    [Google Scholar]
  100. 100.
    Zhou X, Yuan P, Liu Q, Liu Z. 2017. LncRNA MEG3 regulates imatinib resistance in chronic myeloid leukemia via suppressing microRNA-21. Biomol. Ther. 25:5490–96
    [Google Scholar]
  101. 101.
    Zhou X, Zhang W, Jin M, Chen J, Xu W, Kong X 2017. lncRNA MIAT functions as a competing endogenous RNA to upregulate DAPK2 by sponging miR-22-3p in diabetic cardiomyopathy. Cell Death Dis 8:7e2929
    [Google Scholar]
  102. 102.
    Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP et al. 2011. The Lin28/let-7 axis regulates glucose metabolism. Cell 147:181–94
    [Google Scholar]
  103. 103.
    Zhu X, Wu YB, Zhou J, Kang DM. 2016. Upregulation of lncRNA MEG3 promotes hepatic insulin resistance via increasing FoxO1 expression. Biochem. Biophys. Res. Commun. 469:2319–25
    [Google Scholar]
  104. 104.
    Żylicz JJ, Heard E. 2020. Molecular mechanisms of facultative heterochromatin formation: an X-chromosome perspective. Annu. Rev. Biochem. 89:255–82
    [Google Scholar]
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