Browse > Article
http://dx.doi.org/10.5713/ab.21.0006

The role of long noncoding RNAs in livestock adipose tissue deposition - A review  

Wang, Lixue (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University)
Xie, Yuhuai (Department of Immunology, School of Basic Medical Sciences, Fudan University)
Chen, Wei (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University)
Zhang, Yu (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University)
Zeng, Yongqing (Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Technology, Shandong Agricultural University)
Publication Information
Animal Bioscience / v.34, no.7, 2021 , pp. 1089-1099 More about this Journal
Abstract
With the development of sequencing technology, numerous, long noncoding RNAs (lncRNAs) have been discovered and annotated. Increasing evidence has shown that lncRNAs play an essential role in regulating many biological and pathological processes, especially in cancer. However, there have been few studies on the roles of lncRNAs in livestock production. In animal products, meat quality and lean percentage are vital economic traits closely related to adipose tissue deposition. However, adipose tissue accumulation is also a pivotal contributor to obesity, diabetes, atherosclerosis, and many other diseases, as demonstrated by human studies. In livestock production, the mechanism by which lncRNAs regulate adipose tissue deposition is still unclear. In addition, the phenomenon that different animal species have different adipose tissue accumulation abilities is not well understood. In this review, we summarize the characteristics of lncRNAs and their four functional archetypes and review the current knowledge about lncRNA functions in adipose tissue deposition in livestock species. This review could provide theoretical significance to explore the functional mechanisms of lncRNAs in adipose tissue accumulation in animals.
Keywords
LncRNAs; Adipose Tissue Deposition; Livestock;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Dodson MV, Jiang Z, Chen J, et al. Allied industry approaches to alter intramuscular fat content and composition in beef animals. J Food Sci 2010;75:R1-R8. https://doi.org/10.1111/j.1750-3841.2009.01396.x   DOI
2 Neeland IJ, Ross R, Despres J, et al. Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement. Lancet Diabetes Endocrinol 2019;7:715-25. https://doi.org/10.1016/S2213-8587(19)30084-1   DOI
3 Guiu Jurado E, Unthan M, Bohler N, et al. Bone morphogenetic protein 2 (BMP2) may contribute to partition of energy storage into visceral and subcutaneous fat depots. Obesity 2016;24:2092-2100. https://doi.org/10.1002/oby.21571   DOI
4 Wang G, Du K, Hu S, et al. Genome-wide identification and characterization of long non-coding RNAs during postnatal development of rabbit adipose tissue. Lipids Health Dis 2018;17:271. https://doi.org/10.1186/s12944-018-0915-1   DOI
5 Zhang JW, Klemm DJ, Vinson C, Lane MD. Role of creb in transcriptional regulation of CCAAT/enhancer-binding protein β gene during adipogenesis. J Biol Chem 2004;279:4471-8. https://doi.org/10.1074/jbc.M311327200   DOI
6 Oishi Y, Manabe I, Tobe K, et al. Kruppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab 2005;1:27-39. https://doi.org/10.1016/j.cmet.2004.11.005   DOI
7 Flynn RA, Chang HY. Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell 2014;14:752-61. https://doi.org/10.1016/j.stem.2014.05.014   DOI
8 Cawthorn WP, Scheller EL, Macdougald OA. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J Lipid Res 2012;53:227-46. https://doi.org/10.1194/jlr.R021089   DOI
9 Huang H, Song T, Li X, et al. BMP signaling pathway is required for commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc Natl Acad Sci USA 2009;106:12670-5. https://doi.org/10.1073/pnas.0906266106   DOI
10 Fang X, Stroud MJ, Ouyang K, et al. Adipocyte-specific loss of PPARγ attenuates cardiac hypertrophy. JCI Insight 2016;1:e89908. https://doi.org/10.1172/jci.insight.89908   DOI
11 Li S, Wu J. TGF-β/SMAD signaling regulation of mesenchymal stem cells in adipocyte commitment. Stem Cell Res Ther 2020;11:41. https://doi.org/10.1186/s13287-020-1552-y   DOI
12 Wang J, Yang W, Chen Z, et al. Long noncoding RNA incSHGL recruits hnRNPA1 to suppress hepatic gluconeogenesis and lipogenesis. Diabetes 2018;67:581-93. https://doi.org/10.2337/db17-0799   DOI
13 Chen J, Bao C, Kim JT, Cho JS, Qiu S, Lee HJ. Sulforaphene inhibition of adipogenesis via Hedgehog signaling in 3T3-L1 adipocytes. J Agric Food Chem 2018;66:11926-34. https://doi.org/10.1021/acs.jafc.8b04330   DOI
14 Song B, Chi Y, Li X, et al. Inhibition of Notch signaling promotes the adipogenic differentiation of mesenchymal stem cells through autophagy activation and PTEN-PI3K/AKT/mTOR pathway. Cell Physiol Biochem 2015;36:1991-2002. https://doi.org/10.1159/000430167   DOI
15 Chen G, Yu D, Nian X, et al. LncRNA SRA promotes hepatic steatosis through repressing the expression of adipose triglyceride lipase (ATGL). Sci Rep-Uk 2016;6:35531. https://doi.org/10.1038/srep35531   DOI
16 Hausman GJ, Basu U, Du M, Fernyhough-Culver M, Dodson MV. Intermuscular and intramuscular adipose tissues: bad vs. Good adipose tissues. Adipocyte 2014;3:242-55. https://doi.org/10.4161/adip.28546   DOI
17 Li M, Xie Z, Wang P, et al. The long noncoding RNA GAS5 negatively regulates the adipogenic differentiation of MSCs by modulating the miR-18a/CTGF axis as a ceRNA. Cell Death Dis 2018;9:554. https://doi.org/10.1038/s41419-0180627-5   DOI
18 Xiao T, Liu L, Li H, et al. Long noncoding RNA ADINR regulates adipogenesis by transcriptionally activating C/EBPα. Stem Cell Rep 2015;5:856-65. https://doi.org/10.1016/j.stemcr.2015.09.007   DOI
19 Cai H, Li M, Jian W, et al. A novel lncRNA BADLNCR1 inhibits bovine adipogenesis by repressing GLRX5 expression. J Cell Mol Med 2020;24:7175-86. https://doi.org/10.1111/jcmm.15181   DOI
20 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. https://doi.org/10.1016/j.scr.2018.08.016   DOI
21 Alvarez-Dominguez JR, Bai Z, Xu D, et al. De novo reconstruction of adipose tissue transcriptomes reveals long noncoding RNA regulators of brown adipocyte development. Cell Metab 2015;21:764-76. https://doi.org/10.1016/j.cmet.2015.04.003   DOI
22 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;9:3622. https://doi.org/10.1038/s41467-018-05933-8   DOI
23 Johnsson P, Ackley A, Vidarsdottir L, et al. A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells. Nat Struct Mol Biol 2013;20:440-6. https://doi.org/10.1038/nsmb.2516   DOI
24 Pethick DW, Harper GS, Oddy VH. Growth, development and nutritional manipulation of marbling in cattle: a review. Aust J Exp Agric 2004;44:705-15.   DOI
25 Kosinska-Selbi B, Mielczarek M, Szyda J. Long non-coding RNA in livestock. Animal 2020;14:2003-13. https://doi.org/10.1017/S1751731120000841   DOI
26 Diederichs S. The four dimensions of noncoding RNA conservation. Trends Genet 2014;30:121-3. https://doi.org/10.1016/j.tig.2014.01.004   DOI
27 Guttman M, Amit I, Garber M, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009;458:223-7. https://doi.org/10.1038/nature07672   DOI
28 Chen YG, Satpathy AT, Chang HY. Gene regulation in the immune system by long noncoding RNAs. Nat Immunol 2017;18:962-72. https://doi.org/10.1038/ni.3771   DOI
29 Sun Y, Chen X, Qin J, Liu S, Zhao R. Comparative analysis of long noncoding RNAs expressed during intramuscular adipocytes adipogenesis in fat-type and lean-type pigs. J Agric Food Chem 2018;66:12122-30. https://doi.org/10.1021/acs.jafc.8b04243   DOI
30 Carninci P, Kasukawa T, Katayama S, et al. The transcriptional landscape of the mammalian genome. Science 2005;309:1559-63. https://doi.org/10.1126/science.1112014   DOI
31 Somarowthu S, Legiewicz M, Chillon I, Marcia M, Liu F, Pyle AM. HOTAIR forms an intricate and modular secondary structure. Mol Cell 2015;58:353-61. https://doi.org/10.1016/j.molcel.2015.03.006   DOI
32 Graf J, Kretz M. From structure to function: route to understanding lncRNA mechanism. Bioessays 2020;42:2000027. https://doi.org/10.1002/bies.202000027   DOI
33 Cabili MN, Trapnell C, Goff L, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Gene Dev 2011;25:191527. https://doi.org/10.1101/gad.17446611   DOI
34 Gupta PK. Competing endogenous RNA (ceRNA): a new class of RNA working as miRNA sponges. Curr Sci India 2014;106:823-9.
35 Cabili MN, Dunagin MC, Mcclanahan PD, et al. Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol 2015;16:20. https://doi.org/10.1186/s13059-015-0586-4   DOI
36 Ma M, Duan R, Shen L, et al. The lncRNA Gm15622 stimulates SREBP-1c expression and hepatic lipid accumulation by sponging the miR-742-3p in mice. J Lipid Res 2020;61:105264. https://doi.org/10.1194/jlr.RA120000664   DOI
37 Duan L, Min C, Niu Y, et al. Identification of a novel human long non-coding RNA that regulates hepatic lipid metabolism by inhibiting SREBP-1c. Int J Biol Sci 2017;13:349-57. https://doi.org/10.7150/ijbs.16635   DOI
38 Huang Y, Jin C, Zheng Y, et al. Knockdown of lncRNA MIR31HG inhibits adipocyte differentiation of human adiposederived stem cells via histone modification of FABP4. Sci Rep-Uk 2017;7:8080. https://doi.org/10.1038/s41598-01708131-6   DOI
39 Wang Y, Liu W, Liu Y, et al. Long noncoding RNA H19 mediates LCoR to impact the osteogenic and adipogenic differentiation of mBMSCs in mice through sponging miR-188. J Cell Physiol 2018;233:7435-46. https://doi.org/10.1002/jcp.26589   DOI
40 Zhang S, Kang Z, Cai H, et al. Identification of novel alternative splicing of bovine lncrna lncFAM200B and its effects on preadipocyte proliferation. J Cell Physiol 2020;236:60111. https://doi.org/10.1002/jcp.29887   DOI
41 Miao Z, Wang S, Zhang J, et al. Identification and comparison of long non-conding RNA in Jinhua and Landrace pigs. Biochem Biophys Res Commun 2018;506:765-71. https://doi.org/10.1016/j.bbrc.2018.06.028   DOI
42 Liu P, Jin L, Zhao L, et al. Identification of a novel antisense long non-coding RNA PLA2G16-AS that regulates the expression of PLA2G16 in pigs. Gene 2018;671:78-84. https://doi.org/10.1016/j.gene.2018.05.114   DOI
43 Jiang R, Li H, Huang Y, Lan X, Lei C, Chen H. Transcriptome profiling of lncRNA related to fat tissues of qinchuan cattle. Gene 2020;742:144587. https://doi.org/10.1016/j.gene.2020.144587   DOI
44 Xu L, Ma X, Verma NK, et al. Ablation of PPARγ in subcutaneous fat exacerbates age-associated obesity and metabolic decline. Aging Cell 2018;17:e12721. https://doi.org/10.1111/acel.12721   DOI
45 Corbin CH, O'Quinn TG, Garmyn AJ, et al. Sensory evaluation of tender beef strip loin steaks of varying marbling levels and quality treatments. Meat Sci 2015;100:24-31. https://doi.org/10.1016/j.meatsci.2014.09.009   DOI
46 Newcom DW, Baas TJ, Schwab CR, Stalder KJ. Genetic and phenotypic relationships between individual subcutaneous backfat layers and percentage of longissimus intramuscular fat in duroc swine. J Anim Sci 2005;83:316-23. https://doi.org/10.2527/2005.832316x   DOI
47 Hamdy O, Porramatikul S, Al-Ozairi E. Metabolic obesity: the paradox between visceral and subcutaneous fat. Curr Diabetes Rev 2006;2:367-73. https://doi.org/10.2174/1573399810602040367   DOI
48 Latorre J, Fernandez-Real JM. LncRNAs in adipose tissue from obese and insulin-resistant subjects: new targets for therapy? Ebiomedicine 2018;30:10-1. https://doi.org/10.1016/j.ebiom.2018.03.023   DOI
49 Li M, Sun X, Cai H, et al. Long non-coding RNA ADNCR suppresses adipogenic differentiation by targeting miR-204. Biochim Biophys Acta Gene Regul Mech 2016;1859:871-82. https://doi.org/10.1016/j.bbagrm.2016.05.003   DOI
50 Huang P, Huang F, Liu H, Zhang T, Yang M, Sun C. LncRNA MEG3 functions as a ceRNA in regulating hepatic lipogenesis by competitively binding to miR-21 with LRP6. Metabolism 2019;94:1-8. https://doi.org/10.1016/j.metabol.2019.01.018   DOI
51 Cai B, Li Z, Ma M, et al. LncRNA-Six1 encodes a micropeptide to activate Six1 in cis and is involved in cell proliferation and muscle growth. Front Physiol 2017;8:230. https://doi.org/10.3389/fphys.2017.00230   DOI
52 Huang J, Zheng Q, Wang S, Wei X, Li F, Ma Y. High-throughput RNA sequencing reveals NDUFC2-AS lncRNA promotes adipogenic differentiation in chinese buffalo (Bubalus bubalis L.). Genes-Basel 2019;10:689. https://doi.org/10.3390/genes10090689   DOI
53 Choi JY, Shin D, Lee HJ, Oh JD. Comparison of long noncoding RNA between muscles and adipose tissues in Hanwoo beef cattle. Anim Cells Syst 2019;23:50-8. https://doi.org/10.1080/19768354.2018.1512522   DOI
54 Li M, Gao Q, Tian Z, et al. MIR221HG is a novel long noncoding RNA that inhibits bovine adipocyte differentiation. Genes-Basel 2020;11:29. https://doi.org/10.3390/genes11010029   DOI
55 Li A, Hu Y, Liu X, Zhao L, Tian Q, Du M. PSXV-9 a novel anti-sense lncRNA of CEBPA inhibits bovine adipogenic differentiation. J Anim Sci 2018;96(Suppl 3):245. https://doi.org/10.1093/jas/sky404.535   DOI
56 Chen M, Wang J, Wang Y, Wu Y, Fu J, Liu J. Genome-wide detection of selection signatures in chinese indigenous laiwu pigs revealed candidate genes regulating fat deposition in muscle. BMC Genet 2018;19:31. https://doi.org/10.1186/s12863-018-0622-y   DOI
57 Bouchi R, Takeuchi T, Akihisa M, et al. High visceral fat with low subcutaneous fat accumulation as a determinant of atherosclerosis in patients with type 2 diabetes. Cardiovasc Diabetol 2015;14:136. https://doi.org/10.1186/s12933-0150302-4   DOI
58 Caprio S, Perry R, Kursawe R. Adolescent obesity and insulin resistance: roles of ectopic fat accumulation and adipose inflammation. Gastroenterology 2017;152:1638-46. https://doi.org/10.1053/j.gastro.2016.12.051   DOI
59 Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol 2011;21:354-61. https://doi.org/10.1016/j.tcb.2011.04.001   DOI
60 Cui JX, Zeng QF, Chen W, Zhang H, Zeng YQ. Analysis and preliminary validation of the molecular mechanism of fat deposition in fatty and lean pigs by high-throughput sequencing. Mamm Genome 2019;30:71-80. https://doi.org/10.1007/s00335-019-09795-3   DOI
61 Tang QQ, Lane MD. Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem 2012;81:715-36. https://doi.org/10.1146/annurev-biochem-052110-115718   DOI
62 Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Gene Dev 2000;14:1293-307.   DOI
63 Hardouin P, Rharass T, Lucas S. Bone marrow adipose tissue: to be or not to be a typical adipose tissue? Front Endocrinol 2016;7:85. https://doi.org/10.3389/fendo.2016.00085   DOI
64 Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 2011;147:1537-50. https://doi.org/10.1016/j.cell.2011.11.055   DOI
65 Weikard R, Demasius W, Kuehn C. Mining long noncoding RNA in livestock. Anim Genet 2017;48:3-18. https://doi.org/10.1111/age.12493   DOI
66 Sun Y, Cai R, Wang Y, Zhao R, Qin J, Pang W. A newly identified lncrna lncIMF4 controls adipogenesis of porcine intramuscular preadipocyte through attenuating autophagy to inhibit lipolysis. Animals 2020;10:926. https://doi.org/10.3390/ani10060926   DOI
67 Wang J, Chen M, Chen J, et al. LncRNA IMFlnc1 promotes porcine intramuscular adipocyte adipogenesis by sponging miR-199a-5p to up-regulate CAV-1. BMC Mol Cell Biol 2020;21:77. https://doi.org/10.1186/s12860-020-00324-8   DOI
68 Muret K, Klopp C, Wucher V, et al. Long noncoding RNA repertoire in chicken liver and adipose tissue. Genet Sel Evol 2017;49:6. https://doi.org/10.1186/s12711-016-0275-0   DOI
69 Ma L, Zhang M, Jin Y, et al. Comparative transcriptome profiling of mRNA and lncRNA related to tail adipose tissues of sheep. Front Genet 2018;9:365. https://doi.org/10.3389/fgene.2018.00365   DOI
70 Zhang M, Li F, Sun JW, et al. LncRNA IMFNCR promotes intramuscular adipocyte differentiation by sponging miR-128-3p and miR-27b-3p. Front Genet 2019;10:42. https://doi.org/10.3389/fgene.2019.00042   DOI
71 Liu F, Somarowthu S, Pyle AM. Visualizing the secondary and tertiary architectural domains of lncRNA Repa. Nat Chem Biol 2017;13:282-9. https://doi.org/10.1038/nchembio.2272   DOI
72 Derrien T, Johnson R, Bussotti G, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012;22:1775-89. https://doi.org/10.1101/gr.132159.111   DOI
73 Cristancho AG, Lazar MA. Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol 2011;12:722-34. https://doi.org/10.1038/nrm3198   DOI
74 Louveau I, Perruchot M, Bonnet M, Gondret F. Invited review: Pre-and postnatal adipose tissue development in farm animals: from stem cells to adipocyte physiology. Animal 2016;10:1839-47. https://doi.org/10.1017/S1751731116000872   DOI
75 Kanazawa A, Tsukada S, Kamiyama M, Yanagimoto T, Nakajima M, Maeda S. Wnt5b partially inhibits canonical Wnt/ β-catenin signaling pathway and promotes adipogenesis in 3T3-L1 preadipocytes. Biochem Biophys Res Commun 2005;330:505-10. https://doi.org/10.1016/j.bbrc.2005.03.007   DOI
76 Laurent GS, Wahlestedt C, Kapranov P. The landscape of long noncoding RNA classification. Trends Genet 2015;31:239-51. https://doi.org/10.1016/j.tig.2015.03.007   DOI
77 Quinn JJ, Zhang QC, Georgiev P, Ilik IA, Akhtar A, Chang HY. Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Gene Dev 2016;30:191-207. https://doi.org/10.1101/gad.272187.115   DOI
78 Chen J, Liu Y, Lu S, et al. The role and possible mechanism of lncRNA U90926 in modulating 3T3-L1 preadipocyte differentiation. Int J Obes 2017;41:299-308. https://doi.org/10.1038/ijo.2016.189   DOI
79 Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 2011;146:353-8. https://doi.org/10.1016/j.cell.2011.07.014   DOI
80 Wei N, Wang Y, Xu RX, et al. PU.1 antisense lnc RNA against its mRNA translation promotes adipogenesis in porcine preadipocytes. Anim Genet 2015;46:133-40. https://doi.org/10.1111/age.12275   DOI
81 Smith A, Yu X, Yin L. Diazinon exposure activated transcriptional factors CCAAT-enhancer-binding proteins α (C/EBPα) and peroxisome proliferator-activated receptor γ (PPARγ) and induced adipogenesis in 3T3-L1 preadipocytes. Pestic Biochem Physiol 2018;150:48-58. https://doi.org/10.1016/j.pestbp.2018.07.003   DOI