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Pulling the trigger: Noncoding RNAs in white adipose tissue browning

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Abstract

White adipose tissue (WAT) serves as the primary site for energy storage and endocrine regulation in mammals, while brown adipose tissue (BAT) is specialized for thermogenesis and energy expenditure. The conversion of white adipocytes to brown-like fat cells, known as browning, has emerged as a promising therapeutic strategy for reversing obesity and its associated co-morbidities. Noncoding RNAs (ncRNAs) are a class of transcripts that do not encode proteins but exert regulatory functions on gene expression at various levels. Recent studies have shed light on the involvement of ncRNAs in adipose tissue development, differentiation, and function. In this review, we aim to summarize the current understanding of ncRNAs in adipose biology, with a focus on their role and intricate mechanisms in WAT browning. Also, we discuss the potential applications and challenges of ncRNA-based therapies for overweight and its metabolic disorders, so as to combat the obesity epidemic in the future.

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Data availability

Data availability is not applicable to this article as no new data were created or analyzed in this study.

Abbreviations

ATGL:

Adipose triglyceride lipase

BAT:

Brown adipose tissue

CEBPα:

CCAAT/enhancer-binding protein α

ceRNAs:

Competitive endogenous RNAs

eWAT:

Epididymal WAT

FGF21:

Fibroblast growth factor 21

HSL:

Hormone-sensitive lipase

IGF-1:

Insulin-like growth factor-1

IL-6:

Interleukin-6

iWAT:

Inguinal WAT

m1A:

N1-methyladenosine

m6A:

N6-methyladenosine

miRNAs:

MicroRNAs

NcRNAs:

Noncoding RNAs

PGC1α:

Peroxisome proliferator-activated receptor gamma coactivator 1 Alpha

Prdm16:

Positive regulatory domain containing 16

RBP:

RNA-binding protein

RISC:

RNA-induced silencing complex

SREBP1:

Sterol-regulatory element binding proteins

UCP1:

Uncoupling protein 1

WAT:

White adipose tissue

ASOs:

Antisense oligonucleotides

CDS:

Coding regions

Celf1:

CUGBP Elav-Like Family Member 1

circRNAs:

Circular RNAs

FABP4:

Fatty acid binding protein 4

FGFR1:

FGF21 receptor

HuR:

Hu antigen R

IL-4:

Interleukin-4

IL-13:

Interleukin-13

lncRNAs:

Long noncoding RNAs

m5C:

5-Methylcytosine

m7G:

7-Methyl guanosine

mRNAs:

Messenger RNAs

NRG-4:

Neuregulin 4

PPARγ:

Peroxisome proliferator-activated receptor γ

PTBP1:

Polypyrimidine tract-binding protein 1

RIP140:

Receptor-interacting protein 140

siRNA:

Small interfering RNA

TNF-α:

Tumor necrosis factor-alpha

UTR:

Untranslated region

ZBTB7B:

Zinc finger and BTB domain containing 7B

References

  1. Jaacks LM, Vandevijvere S, Pan A, McGowan CJ, Wallace C, Imamura F, Mozaffarian D, Swinburn B, Ezzati M. The obesity transition: Stages of the global epidemic. Lancet Diabetes Endocrinol. 2019;7(3):231–40. https://doi.org/10.1016/S2213-8587(19)30026-9.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ghaben AL, Scherer PE. Adipogenesis and metabolic health. Nat Rev Mol Cell Biol. 2019;20(4):242–58. https://doi.org/10.1038/s41580-018-0093-z.

    Article  CAS  PubMed  Google Scholar 

  3. Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML, Gortmaker SL. The global obesity pandemic: Shaped by global drivers and local environments. Lancet. 2011;378(9793):804–14. https://doi.org/10.1016/S0140-6736(11)60813-1.

    Article  PubMed  Google Scholar 

  4. Whitehead A, Krause FN, Moran A, MacCannell ADV, Scragg JL, McNally BD, Boateng E, Murfitt SA, Virtue S, Wright J, et al. Brown and beige adipose tissue regulate systemic metabolism through a metabolite interorgan signaling axis. Nat Commun. 2021;12(1):1905. https://doi.org/10.1038/s41467-021-22272-3.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  5. Kurylowicz A, Puzianowska-Kuznicka M. Induction of adipose tissue browning as a strategy to combat obesity. Int J Mol Sci. 2020;21(17):6241. https://doi.org/10.3390/ijms21176241.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cech TR, Steitz JA. The noncoding RNA revolution-trashing old rules to forge new ones. Cell. 2014;157(1):77–94. https://doi.org/10.1016/j.cell.2014.03.008.

    Article  CAS  PubMed  Google Scholar 

  7. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature. 2007;447(7146):799–816. https://doi.org/10.1038/nature05874.

    Article  CAS  ADS  Google Scholar 

  8. Squillaro T, Peluso G, Galderisi U, Di Bernardo G. Long non-coding RNAs in regulation of adipogenesis and adipose tissue function. Elife. 2020;9:e59053. https://doi.org/10.7554/eLife.59053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Huang Y, Zheng Y, Jin C, Li X, Jia L, Li W. Long non-coding RNA H19 inhibits adipocyte differentiation of bone marrow mesenchymal stem cells through epigenetic modulation of histone deacetylases. Sci Rep. 2016;6:28897. https://doi.org/10.1038/srep28897.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  10. Long J-K, Dai W, Zheng Y-W, Zhao S-P. miR-122 promotes hepatic lipogenesis via inhibiting the LKB1/AMPK pathway by targeting Sirt1 in non-alcoholic fatty liver disease. Mol Med. 2019;25(1):26. https://doi.org/10.1186/s10020-019-0085-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Xu G, Li M, Wu J, Qin C, Tao Y, He H. Circular RNA circNRIP1 sponges microRNA-138-5p to maintain hypoxia-induced resistance to 5-fluorouracil through HIF-1α-dependent glucose metabolism in gastric carcinoma. Cancer Manag Res. 2020;12:2789–802. https://doi.org/10.2147/CMAR.S246272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Osuna-Prieto FJ, Martinez-Tellez B, Segura-Carretero A, Ruiz JR. Activation of brown adipose tissue and promotion of white adipose tissue browning by plant-based dietary components in rodents: A systematic review. Adv Nutr. 2021;12:2147–56. https://doi.org/10.1093/advances/nmab084.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Scheja L, Heeren J. The endocrine function of adipose tissues in health and cardiometabolic disease. Nat Rev Endocrinol. 2019;15:507–24. https://doi.org/10.1038/s41574-019-0230-6.

    Article  CAS  PubMed  Google Scholar 

  14. Auger C, Kajimura S. Adipose tissue remodeling in pathophysiology. Annu Rev Pathol. 2023;18:71–93. https://doi.org/10.1146/annurev-pathol-042220-023633.

    Article  CAS  PubMed  Google Scholar 

  15. Bartelt A, Heeren J. Adipose tissue browning and metabolic health. Nat Rev Endocrinol. 2014;10:24–36. https://doi.org/10.1038/nrendo.2013.204.

    Article  CAS  PubMed  Google Scholar 

  16. Schulz TJ, Huang P, Huang TL, Xue R, McDougall LE, Townsend KL, Cypess AM, Mishina Y, Gussoni E, Tseng YH. Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature. 2013;495:379–83. https://doi.org/10.1038/nature11943.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  17. Rui L. Brown and beige adipose tissues in health and disease. Compr Physiol. 2017;7:1281–306. https://doi.org/10.1002/cphy.c170001.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Chen Y, Wu Z, Huang S, Wang X, He S, Liu L, Hu Y, Chen L, Chen P, Liu S, et al. Adipocyte IRE1alpha promotes PGC1alpha mRNA decay and restrains adaptive thermogenesis. Nat Metab. 2022;4:1166–84. https://doi.org/10.1038/s42255-022-00631-8.

    Article  CAS  PubMed  ADS  Google Scholar 

  19. Ikeda K, Kang Q, Yoneshiro T, Camporez JP, Maki H, Homma M, Shinoda K, Chen Y, Lu X, Maretich P, et al. UCP1-independent signaling involving SERCA2b-mediated calcium cycling regulates beige fat thermogenesis and systemic glucose homeostasis. Nat Med. 2017;23:1454–65. https://doi.org/10.1038/nm.4429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lowell BB, S-Susulic V, Hamann A, Lawitts JA, Himms-Hagen J, Boyer BB, Kozak LP, Flier JS. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature. 1993;366:740–2. https://doi.org/10.1038/366740a0.

    Article  CAS  PubMed  ADS  Google Scholar 

  21. Sidossis L, Kajimura S. Brown and beige fat in humans: Thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015;125:478–86. https://doi.org/10.1172/JCI78362.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Yoneshiro T, Aita S, Matsushita M, Okamatsu-Ogura Y, Kameya T, Kawai Y, Miyagawa M, Tsujisaki M, Saito M. Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity (Silver Spring). 2011;19:1755–60. https://doi.org/10.1038/oby.2011.125.

    Article  PubMed  Google Scholar 

  23. Mancuso P, Bouchard B. The impact of aging on adipose function and adipokine synthesis. Front Endocrinol (Lausanne). 2019;10:137. https://doi.org/10.3389/fendo.2019.00137.

    Article  PubMed  Google Scholar 

  24. Rogers NH. Brown adipose tissue during puberty and with aging. Ann Med. 2015;47:142–9. https://doi.org/10.3109/07853890.2014.914807.

    Article  CAS  PubMed  Google Scholar 

  25. Li Y, Wang D, Ping X, Zhang Y, Zhang T, Wang L, Jin L, Zhao W, Guo M, Shen F, et al. Local hyperthermia therapy induces browning of white fat and treats obesity. Cell. 2022;185(949–966):e919. https://doi.org/10.1016/j.cell.2022.02.004.

    Article  CAS  Google Scholar 

  26. Wang L, Liu X, Liu S, Niu Y, Fu L. Sestrin2 ablation attenuates the exercise-induced browning of white adipose tissue in C57BL/6J mice. Acta Physiol (Oxf). 2022;234:e13785. https://doi.org/10.1111/apha.13785.

    Article  CAS  PubMed  Google Scholar 

  27. Song Y, Zan W, Qin L, Han S, Ye L, Wang M, Jiang B, Fang P, Liu Q, Shao C. Ablation of ORMDL3 impairs adipose tissue thermogenesis and insulin sensitivity by increasing ceramide generation. Mol Metabol. 2022;56:101423. https://doi.org/10.1016/j.molmet.2021.101423.

    Article  CAS  Google Scholar 

  28. Vargas-Castillo A, Fuentes-Romero R, Rodriguez-Lopez LA, Torres N, Tovar AR. Understanding the biology of thermogenic fat: Is browning a new approach to the treatment of obesity? Arch Med Res. 2017;48:401–13. https://doi.org/10.1016/j.arcmed.2017.10.002.

    Article  CAS  PubMed  Google Scholar 

  29. Kajimura S, Spiegelman BM, Seale P. Brown and beige fat: Physiological roles beyond heat generation. Cell Metab. 2015;22:546–59. https://doi.org/10.1016/j.cmet.2015.09.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17:200–5. https://doi.org/10.1038/nm.2297.

    Article  CAS  PubMed  Google Scholar 

  31. Kajimura S, Seale P, Spiegelman BM. Transcriptional control of brown fat development. Cell Metab. 2010;11:257–62. https://doi.org/10.1016/j.cmet.2010.03.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Stanford KI, Middelbeek RJ, Goodyear LJ. Erratum. Exercise Effects on White Adipose Tissue: Beiging and Metabolic Adaptations. Diabetes. 2015;64:2361–2368. Diabetes 64:3334. https://doi.org/10.2337/db15-er09.

  33. Cheng L, Wang J, Dai H, Duan Y, An Y, Shi L, Lv Y, Li H, Wang C, Ma Q, et al. Brown and beige adipose tissue: A novel therapeutic strategy for obesity and type 2 diabetes mellitus. Adipocyte. 2021;10:48–65. https://doi.org/10.1080/21623945.2020.1870060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mottillo EP, Balasubramanian P, Lee YH, Weng C, Kershaw EE, Granneman JG. Coupling of lipolysis and de novo lipogenesis in brown, beige, and white adipose tissues during chronic beta3-adrenergic receptor activation. J Lipid Res. 2014;55:2276–86. https://doi.org/10.1194/jlr.M050005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Desjardins EM, Steinberg GR. Emerging role of AMPK in brown and Beige Adipose Tissue (BAT): Implications for obesity, insulin resistance, and type 2 diabetes. Curr Diab Rep. 2018;18:80. https://doi.org/10.1007/s11892-018-1049-6.

    Article  CAS  PubMed  Google Scholar 

  36. Cuevas-Ramos D, Mehta R, Aguilar-Salinas CA. Fibroblast growth factor 21 and browning of white adipose tissue. Front Physiol. 2019;10:37. https://doi.org/10.3389/fphys.2019.00037.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pydi SP, Jain S, Barella LF, Zhu L, Sakamoto W, Meister J, Wang L, Lu H, Cui Y, Gavrilova O, et al. Beta-arrestin-1 suppresses myogenic reprogramming of brown fat to maintain euglycemia. Sci Adv. 2020;6:eaba1733. https://doi.org/10.1126/sciadv.aba1733.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  38. Villarroya F, Cereijo R, Villarroya J, Giralt M. Brown adipose tissue as a secretory organ. Nat Rev Endocrinol. 2017;13:26–35. https://doi.org/10.1038/nrendo.2016.136.

    Article  CAS  PubMed  Google Scholar 

  39. Shi L, Li Y, Xu X, Cheng Y, Meng B, Xu J, Xiang L, Zhang J, He K, Tong J, et al. Brown adipose tissue-derived Nrg4 alleviates endothelial inflammation and atherosclerosis in male mice. Nat Metab. 2022;4:1573–90. https://doi.org/10.1038/s42255-022-00671-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Schlein C, Talukdar S, Heine M, Fischer AW, Krott LM, Nilsson SK, Brenner MB, Heeren J, Scheja L. FGF21 lowers plasma triglycerides by accelerating lipoprotein catabolism in white and brown adipose tissues. Cell Metab. 2016;23:441–53. https://doi.org/10.1016/j.cmet.2016.01.006.

    Article  CAS  PubMed  Google Scholar 

  41. Gunawardana SC, Piston DW. Insulin-independent reversal of type-1 diabetes following transplantation of adult brown adipose tissue supplemented with IGF-1. Transplant Direct. 2019;5:e500. https://doi.org/10.1097/TXD.0000000000000945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Qiu Y, Nguyen KD, Odegaard JI, Cui X, Tian X, Locksley RM, Palmiter RD, Chawla A. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell. 2014;157:1292–308. https://doi.org/10.1016/j.cell.2014.03.066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tang Y, Ma D, Liang M, Hou Y, Zhang M, Wang J, Yuan C, Li M, Sun C, Xie J, et al. Stress-inducible IL-6 is regulated by KLF7 in brown adipocytes. Heliyon. 2023;9:e14931. https://doi.org/10.1016/j.heliyon.2023.e14931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, Markan KR, Nakano K, Hirshman MF, Tseng YH, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123:215–23. https://doi.org/10.1172/JCI62308.

    Article  CAS  PubMed  Google Scholar 

  45. Cinti S. The adipose organ at a glance. Dis Model Mech. 2012;5:588–94. https://doi.org/10.1242/dmm.009662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sharp LZ, Shinoda K, Ohno H, Scheel DW, Tomoda E, Ruiz L, Hu H, Wang L, Pavlova Z, Gilsanz V, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS ONE. 2012;7:e49452. https://doi.org/10.1371/journal.pone.0049452.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  47. Dandare A, Khan MJ, Naeem A, Liaquat A. Clinical relevance of circulating non-coding RNAs in metabolic diseases: Emphasis on obesity, diabetes, cardiovascular diseases and metabolic syndrome. Genes Dis. 2023;10:2393–413. https://doi.org/10.1016/j.gendis.2022.05.022.

    Article  CAS  PubMed  Google Scholar 

  48. Liu N, Pan T. RNA epigenetics. Transl Res. 2015;165:28–35. https://doi.org/10.1016/j.trsl.2014.04.003.

    Article  CAS  PubMed  Google Scholar 

  49. Rong D, Sun G, Wu F, Cheng Y, Sun G, Jiang W, Li X, Zhong Y, Wu L, Zhang C, et al. Epigenetics: Roles and therapeutic implications of non-coding RNA modifications in human cancers. Mol Ther Nucleic Acids. 2021;25:67–82. https://doi.org/10.1016/j.omtn.2021.04.021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yan Y, Peng J, Liang Q, Ren X, Cai Y, Peng B, Chen X, Wang X, Yi Q, Xu Z. Dynamic m6A-ncRNAs association and their impact on cancer pathogenesis, immune regulation and therapeutic response. Genes Dis. 2023;10:135–50. https://doi.org/10.1016/j.gendis.2021.10.004.

    Article  CAS  PubMed  Google Scholar 

  51. Alarcon CR, Lee H, Goodarzi H, Halberg N, Tavazoie SF. N6-methyladenosine marks primary microRNAs for processing. Nature. 2015;519:482–5. https://doi.org/10.1038/nature14281.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  52. Song H, Zhang J, Liu B, Xu J, Cai B, Yang H, Straube J, Yu X, Ma T. Biological roles of RNA m(5)C modification and its implications in cancer immunotherapy. Biomark Res. 2022;10:15. https://doi.org/10.1186/s40364-022-00362-8.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Cusenza VY, Tameni A, Neri A, Frazzi R. The lncRNA epigenetics: The significance of m6A and m5C lncRNA modifications in cancer. Front Oncol. 2023;13:1063636. https://doi.org/10.3389/fonc.2023.1063636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Xiao T, Liu L, Li H, Sun Y, Luo H, Li T, Wang S, Dalton S, Zhao RC, Chen R. Long noncoding RNA ADINR regulates adipogenesis by transcriptionally activating C/EBPalpha. Stem Cell Reports. 2021;16:1006–8. https://doi.org/10.1016/j.stemcr.2021.03.024.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Xu J, Zhang L, Shu G, Wang B. microRNA-16–5p promotes 3T3-L1 adipocyte differentiation through regulating EPT1. Biochem Biophys Res Commun. 2019;514:1251–6. https://doi.org/10.1016/j.bbrc.2019.04.179.

    Article  CAS  PubMed  Google Scholar 

  56. Zhang Y, Tian Z, Ye H, Sun X, Zhang H, Sun Y, Mao Y, Yang Z, Li M. Emerging functions of circular RNA in the regulation of adipocyte metabolism and obesity. Cell Death Discov. 2022;8:268. https://doi.org/10.1038/s41420-022-01062-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Sun L, Lin JD. Function and mechanism of long noncoding RNAs in adipocyte biology. Diabetes. 2019;68:887–96. https://doi.org/10.2337/dbi18-0009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Statello L, Guo CJ, Chen LL, Huarte M. Author Correction: Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 2021;22:159. https://doi.org/10.1038/s41580-021-00330-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Xiong Y, Yue F, Jia Z, Gao Y, Jin W, Hu K, Zhang Y, Zhu D, Yang G, Kuang S. 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 (BBA)-Mol Cell Biol Lipids. 2018;1863(4):409–19. https://doi.org/10.1016/j.bbalip.2018.01.008.

    Article  CAS  Google Scholar 

  60. Iwase M, Sakai S, Seno S, Yeh Y-S, Kuo T, Takahashi H, Nomura W, Jheng H-F, Horton P, Osato N. Long non-coding RNA 2310069B03Rik functions as a suppressor of Ucp1 expression under prolonged cold exposure in murine beige adipocytes. Biosci Biotechnol Biochem. 2020;84(2):305–13. https://doi.org/10.1080/09168451.2019.1677451.

    Article  CAS  PubMed  Google Scholar 

  61. Giroud M, Kotschi S, Kwon Y, Le Thuc O, Hoffmann A, Gil-Lozano M, Karbiener M, Higareda-Almaraz JC, Khani S, Tews D. The obesity-linked human lncRNA AATBC stimulates mitochondrial function in adipocytes. EMBO Rep. 2023;24(10):e57600. https://doi.org/10.15252/embr.202357600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Huang R, Shi C, Liu G. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation. Open Life Sci. 2023;18(1):20220552. https://doi.org/10.1515/biol-2022-0552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Cai R, Sun Y, Qimuge N, Wang G, Wang Y, Chu G, Yu T, Yang G, Pang W. Adiponectin AS lncRNA inhibits adipogenesis by transferring from nucleus to cytoplasm and attenuating Adiponectin mRNA translation. Biochim Biophys Acta (BBA)-Mol Cell Biolo Lipids. 2018;1863(4):420–32. https://doi.org/10.1016/j.bbalip.2018.01.005.

    Article  CAS  Google Scholar 

  64. Alvarez-Dominguez JR, Bai Z, Xu D, Yuan B, Lo KA, Yoon MJ, Lim YC, Knoll M, Slavov N, Chen S. De novo reconstruction of adipose tissue transcriptomes reveals long non-coding RNA regulators of brown adipocyte development. Cell Metab. 2015;21(5):764–76. https://doi.org/10.1016/j.cmet.2015.04.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Li S, Mi L, Yu L, Yu Q, Liu T, Wang G-X, Zhao X-Y, Wu J, Lin JD. Zbtb7b engages the long noncoding RNA Blnc1 to drive brown and beige fat development and thermogenesis. Proc Natl Acad Sci. 2017;114(34):E7111–20. https://doi.org/10.1073/pnas.1703494114.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  66. Mi L, Zhao X-Y, Li S, Yang G, Lin JD. Conserved function of the long noncoding RNA Blnc1 in brown adipocyte differentiation. Mol Metabol. 2017;6(1):101–10. https://doi.org/10.1016/j.molmet.2016.10.010.

    Article  CAS  Google Scholar 

  67. Shen L, Han J, Wang H, Meng Q, Chen L, Liu Y, Feng Y, Wu G. 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):1809–21. https://doi.org/10.1002/ijc.32236.

    Article  CAS  PubMed  Google Scholar 

  68. Bast-Habersbrunner A, Kiefer C, Weber P, Fromme T, Schießl A, Schwalie PC, Deplancke B, Li Y, Klingenspor M. LncRNA Ctcflos orchestrates transcription and alternative splicing in thermogenic adipogenesis. EMBO Rep. 2021;22(7):e51289. https://doi.org/10.15252/embr.202051289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Liu Y, Wang J, Shou Y, Xu W, Huang Z, Xu J, Chen K, Liu J, Liu D, Liang H. Restoring the epigenetically silenced lncRNA COL18A1-AS1 represses ccRCC progression by lipid browning via miR-1286/KLF12 axis. Cell Death Dis. 2022;13(7):578. https://doi.org/10.1038/s41419-022-04996-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Chen Y-T, Yang Q-Y, Hu Y, Liu X-D, de Avila JM, Zhu M-J, Nathanielsz PW, Du M. Imprinted lncRNA Dio3os preprograms intergenerational brown fat development and obesity resistance. Nat Commun. 2021;12(1):6845. https://doi.org/10.1038/s41467-021-27171-1.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  71. Wang Y, Hua S, Cui X, Cao Y, Wen J, Chi X, Ji C, Pang L, You L. The effect of FOXC2-AS1 on white adipocyte browning and the possible regulatory mechanism. Front Endocrinol (Lausanne). 2020;11:565483. https://doi.org/10.3389/fendo.2020.565483.

    Article  PubMed  PubMed Central  Google Scholar 

  72. You L, Zhou Y, Cui X, Wang X, Sun Y, Gao Y, Wang X, Wen J, Xie K, Tang R. GM13133 is a negative regulator in mouse white adipocytes differentiation and drives the characteristics of brown adipocytes. J Cell Physiol. 2018;233(1):313–24. https://doi.org/10.1002/jcp.25878.

    Article  CAS  PubMed  Google Scholar 

  73. Liu W, Ma C, Yang B, Yin C, Zhang B, Xiao Y. LncRNA Gm15290 sponges miR-27b to promote PPARγ-induced fat deposition and contribute to body weight gain in mice. Biochem Biophys Res Commun. 2017;493(3):1168–75. https://doi.org/10.1016/j.bbrc.2017.09.114.

    Article  CAS  PubMed  Google Scholar 

  74. Schmidt E, Dhaouadi I, Gaziano I, Oliverio M, Klemm P, Awazawa M, Mitterer G, Fernandez-Rebollo E, Pradas-Juni M, Wagner W. LincRNA H19 protects from dietary obesity by constraining expression of monoallelic genes in brown fat. Nat Commun. 2018;9(1):3622. https://doi.org/10.1038/s41467-018-05933-8.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  75. Guo Y-F, Sun J-Y, Liu Y, Liu Z-Y, Huang Y, Xiao Y, Su T. LncRNA Hnscr regulates lipid metabolism by mediating adipocyte lipolysis. Endocrinology. 2023;164(2):bqad147. https://doi.org/10.1210/endocr/bqad147.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Zhang Z, Cui Y, Su V, Wang D, Tol MJ, Cheng L, Wu X, Kim J, Rajbhandari P, Zhang S. A PPAR γ/long noncoding RNA axis regulates adipose thermoneutral remodeling in mice. J Clin Investig. 2023;133(21):e170072. https://doi.org/10.1172/JCI170072.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Tran K-V, Brown EL, DeSouza T, Jespersen NZ, Nandrup-Bus C, Yang Q, Yang Z, Desai A, Min SY, Rojas-Rodriguez R. Human thermogenic adipocyte regulation by the long noncoding RNA LINC00473. Nat Metab. 2020;2(5):397–412. https://doi.org/10.1038/s42255-020-0205-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Bai Z, Chai X-R, Yoon MJ, Kim H-J, Lo KA, Zhang Z-C, Xu D, Siang DTC, Walet ACE, Xu S-H. Dynamic transcriptome changes during adipose tissue energy expenditure reveal critical roles for long noncoding RNA regulators. PLoS Biol. 2017;15(8):e2002176. https://doi.org/10.1371/journal.pbio.2002176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Liu X, Huang C, Jiang T, Sun X, Zhan S, Zhong T, Guo J, Dai D, Wang Y, Li L. LncDGAT2 is a novel positive regulator of the goat adipocyte thermogenic gene program. Int J Biol Macromol. 2023;245:125465. https://doi.org/10.1016/j.ijbiomac.2023.125465.

    Article  CAS  PubMed  Google Scholar 

  80. Ma J, Wu Y, Cen L, Wang Z, Jiang K, Lian B, Sun C. Cold‐inducible lncRNA266 promotes browning and the thermogenic program in white adipose tissue. EMBO Rep. 2023;e55467. https://doi.org/10.15252/embr.202255467.

  81. Huang Y, Jin C, Zheng Y, Li X, Zhang S, Zhang Y, Jia L, Li W. Knockdown of lncRNA MIR31HG inhibits adipocyte differentiation of human adipose-derived stem cells via histone modification of FABP4. Sci Rep. 2017;7(1):8080. https://doi.org/10.1038/s41598-017-08131-6.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  82. Tang T, Jiang G, Shao J, Wang M, Zhang X, Xia S, Sun W, Jia X, Wang J, Lai S. lncRNA MSTRG4710 promotes the proliferation and differentiation of preadipocytes through miR-29b-3p/IGF1 Axis. Int J Mol Sci. 2023;24(21):15715. https://doi.org/10.3390/ijms242115715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Tang J, Liu X, Su D, Jiang T, Zhan S, Zhong T, Guo J, Cao J, Li L, Zhang H. A Novel LncRNA MSTRG. 310246.1 Promotes differentiation and thermogenesis in goat brown adipocytes. Genes. 2023;14(4):833. https://doi.org/10.3390/genes14040833.

  84. Zhang Y, Ma Y, Gu M, Peng Y. lncRNA TUG1 promotes the brown remodeling of white adipose tissue by regulating miR-204-targeted SIRT1 in diabetic mice. Int J Mol Med. 2020;46(6):2225–34. https://doi.org/10.3892/ijmm.2020.4741.

    Article  CAS  PubMed  Google Scholar 

  85. Cui X, You L, Li Y, Zhu L, Zhang F, Xie K, Cao Y, Ji C, Guo X. A transcribed ultraconserved noncoding RNA, uc. 417, serves as a negative regulator of brown adipose tissue thermogenesis. FASEB J. 2016;30(12):4301–12. https://doi.org/10.1096/fj.201600694R.

    Article  CAS  PubMed  Google Scholar 

  86. Wu C, Fang S, Zhang H, Li X, Du Y, Zhang Y, Lin X, Wang L, Ma X, Xue Y. Long noncoding RNA XIST regulates brown preadipocytes differentiation and combats high-fat diet induced obesity by targeting C/EBPα. Mol Med. 2022;28(1):6. https://doi.org/10.1186/s10020-022-00434-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2016;17:47–62. https://doi.org/10.1038/nrg.2015.10.

    Article  CAS  PubMed  Google Scholar 

  88. Zhang P, Wu S, He Y, Li X, Zhu Y, Lin X, Chen L, Zhao Y, Niu L, Zhang S, et al. LncRNA-mediated adipogenesis in different adipocytes. Int J Mol Sci. 2022;23. https://doi.org/10.3390/ijms23137488.

  89. Zhao X-Y, Li S, DelProposto JL, Liu T, Mi L, Porsche C, Peng X, Lumeng CN, Lin JD. The long noncoding RNA Blnc1 orchestrates homeostatic adipose tissue remodeling to preserve metabolic health. Molecular metabolism. 2018;14:60–70. https://doi.org/10.1016/j.molmet.2018.06.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Zhao XY, Li S, Wang GX, Yu Q, Lin JD. A long noncoding RNA transcriptional regulatory circuit drives thermogenic adipocyte differentiation. Mol Cell. 2014;55:372–82. https://doi.org/10.1016/j.molcel.2014.06.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97. https://doi.org/10.1016/s0092-8674(04)00045-5.

    Article  CAS  PubMed  Google Scholar 

  92. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15(8):509–24. https://doi.org/10.1038/nrm3838.

    Article  MathSciNet  CAS  PubMed  Google Scholar 

  93. Ru W, Zhang S, Liu J, Liu W, Huang B, Chen H. Non-coding RNAs and adipogenesis. Int J Mol Sci. 2023;24(12):9978. https://doi.org/10.3390/ijms24129978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Trajkovski M, Ahmed K, Esau CC, Stoffel M. MyomiR-133 regulates brown fat differentiation through Prdm16. Nat Cell Biol. 2012;14(12):1330–5. https://doi.org/10.1038/ncb2612.

    Article  CAS  PubMed  Google Scholar 

  95. Zhao J, Hu L, Gui W, Xiao L, Wang W, Xia J, Fan H, Li Z, Zhu Q, Hou X. Hepatocyte TGF-β signaling inhibiting WAT browning to promote NAFLD and obesity is associated with Let-7b-5p. Hepatol Commun. 2022;6(6):1301–21. https://doi.org/10.1002/hep4.1892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Giroud M, Karbiener M, Pisani DF, Ghandour RA, Beranger GE, Niemi T, Taittonen M, Nuutila P, Virtanen KA, Langin D. Let-7i-5p represses brite adipocyte function in mice and humans. Sci Rep. 2016;6:28613. https://doi.org/10.1038/srep28613.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  97. Cho YK, Son Y, Kim S-N, Song H-D, Kim M, Park J-H, Jung Y-S, Ahn S-Y, Saha A, Granneman JG. MicroRNA-10a-5p regulates macrophage polarization and promotes therapeutic adipose tissue remodeling. Mol Metabol. 2019;29:86–98. https://doi.org/10.1016/j.molmet.2019.08.015.

    Article  CAS  Google Scholar 

  98. Giroud M, Pisani DF, Karbiener M, Barquissau V, Ghandour RA, Tews D, Fischer-Posovszky P, Chambard J-C, Knippschild U, Niemi T. miR-125b affects mitochondrial biogenesis and impairs brite adipocyte formation and function. Mole Metabol. 2016;5(8):615–25. https://doi.org/10.1016/j.molmet.2016.06.005.

    Article  CAS  Google Scholar 

  99. Lee EK, Lee MJ, Abdelmohsen K, Kim W, Kim MM, Srikantan S, Martindale JL, Hutchison ER, Kim HH, Marasa BS. miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor γ expression. Mol Cell Biol. 2011;31(4):626–38. https://doi.org/10.1128/MCB.00894-10.

    Article  CAS  PubMed  Google Scholar 

  100. Luo W, Kim Y, Jensen ME, Herlea-Pana O, Wang W, Rudolph MC, Friedman JE, Chernausek SD, Jiang S. miR-130b/301b is a negative regulator of beige adipogenesis and energy metabolism in vitro and in vivo. Diabetes. 2022;71(11):2360–71. https://doi.org/10.2337/db22-0205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Liang J, Jia Y, Yu H, Yan H, Shen Q, Xu Y, Li Y, Yang M. 5-Aza-2′-deoxycytidine regulates white adipocyte browning by modulating miRNA-133a/Prdm16. Metabolites. 2022;12(11):1131. https://doi.org/10.3390/metabo12111131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Liu J, Liu J, Zeng D, Wang H, Wang Y, Xiong J, Chen X, Luo J, Chen T, Xi Q. miR-143-null is against diet-induced obesity by promoting BAT thermogenesis and inhibiting WAT adipogenesis. Int J Mol Sci. 2022;23(21):13058. https://doi.org/10.3390/ijms232113058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Liu J, Wei L, Chen T, Wang H, Luo J, Chen X, Jiang Q, Xi Q, Sun J, Zhang L, et al. MiR-143 targets SYK to regulate NEFA uptake and contribute to thermogenesis in male mice. Endocrinology. 2023;164(9):bqad114. https://doi.org/10.1210/endocr/bqad114.

    Article  PubMed  Google Scholar 

  104. Di W, Zhang W, Zhu B, Li X, Tang Q, Zhou Y. Colorectal cancer prompted adipose tissue browning and cancer cachexia through transferring exosomal miR-146b-5p. J Cell Physiol. 2021;236(7):5399–410. https://doi.org/10.1002/jcp.30245.

    Article  CAS  PubMed  Google Scholar 

  105. Pan X-X, Cao J-M, Cai F, Ruan C-C, Wu F, Gao P-J. Loss of miR-146b-3p inhibits perivascular adipocyte browning with cold exposure during aging. Cardiovasc Drugs Ther. 2018;32(5):511–8. https://doi.org/10.1007/s10557-018-6814-x.

    Article  CAS  PubMed  Google Scholar 

  106. Ding H, Zheng S, Garcia-Ruiz D, Hou D, Wei Z, Liao Z, Li L, Zhang Y, Han X, Zen K. Fasting induces a subcutaneous-to-visceral fat switch mediated by microRNA-149-3p and suppression of PRDM16. Nat Commun. 2016;7:11533. https://doi.org/10.1038/ncomms11533.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  107. Chou C-F, Lin Y-Y, Wang H-K, Zhu X, Giovarelli M, Briata P, Gherzi R, Garvey WT, Chen C-Y. KSRP ablation enhances brown fat gene program in white adipose tissue through reduced miR-150 expression. Diabetes. 2014;63(9):2949–61. https://doi.org/10.2337/db13-1901.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Chen Y, Siegel F, Kipschull S, Haas B, Fröhlich H, Meister G, Pfeifer A. miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat Commun. 2013;4:1769. https://doi.org/10.1038/ncomms274.

    Article  PubMed  ADS  Google Scholar 

  109. Huang Y, Zhang H, Dong M, Zhang L, Lin J, Ye R, Zhou H, Liu X, Jin W. miR17–92 cluster drives white adipose tissue browning. J Mol Endocrinol. 2020;65(3):97–107. https://doi.org/10.1530/JME-20-0032.

    Article  CAS  PubMed  Google Scholar 

  110. Huang Y, Xiao Y, Liu Y, Guo M, Guo Q, Zhou F, Liu T, Su T, Xiao Y, Luo XH. MicroRNA-188 regulates aging-associated metabolic phenotype. Aging Cell. 2020;19(1):e13077. https://doi.org/10.1111/acel.13077.

    Article  CAS  PubMed  Google Scholar 

  111. Lv Y-F, Yu J, Sheng Y-L, Huang M, Kong X-C, Di W-J, Liu J, Zhou H, Liang H. Ding G-X Glucocorticoids suppress the browning of adipose tissue via miR-19b in male mice. Endocrinology. 2018;159(1):310–22. https://doi.org/10.1210/en.2017-00566.

    Article  CAS  PubMed  Google Scholar 

  112. Mori M, Nakagami H, Rodriguez-Araujo G, Nimura K, Kaneda Y. Essential role for miR-196a in brown adipogenesis of white fat progenitor cells. PLoS Biol. 2012;10(4):e1001314. https://doi.org/10.1371/journal.pbio.1001314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Di W, Amdanee N, Zhang W, Zhou Y. Long-term exercise-secreted extracellular vesicles promote browning of white adipocytes by suppressing miR-191a-5p. Life Sci. 2020;263:118464. https://doi.org/10.1016/j.lfs.2020.118464.

    Article  CAS  PubMed  Google Scholar 

  114. Sun L, Xie H, Mori MA, Alexander R, Yuan B, Hattangadi SM, Liu Q, Kahn CR, Lodish HF. Mir193b–365 is essential for brown fat differentiation. Nat Cell Biol. 2011;13(8):958–65. https://doi.org/10.1038/ncb2286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. He L, Tang M, Xiao T, Liu H, Liu W, Li G, Zhang F, Xiao Y, Zhou Z, Liu F. Obesity-associated miR-199a/214 cluster inhibits adipose browning via PRDM16–PGC-1α transcriptional network. Diabetes. 2018;67(12):2585–600. https://doi.org/10.2337/db18-0626.

    Article  PubMed  Google Scholar 

  116. Gao Y, Cao Y, Cui X, Wang X, Zhou Y, Huang F, Wang X, Wen J, Xie K, Xu P. miR-199a-3p regulates brown adipocyte differentiation through mTOR signaling pathway. Mol Cell Endocrinol. 2018;476:155–64. https://doi.org/10.1016/j.mce.2018.05.005.

    Article  CAS  PubMed  Google Scholar 

  117. Guo X, Zhang Z, Zeng T, Lim YC, Wang Y, Xie X, Yang S, Huang C, Xu M, Tao L. cAMP-MicroRNA-203-IFNγ network regulates subcutaneous white fat browning and glucose tolerance. Mol Metabol. 2019;28:36–47. https://doi.org/10.1016/j.molmet.2019.07.002.

    Article  CAS  Google Scholar 

  118. Hu Y, Liu L, Chen Y, Zhang X, Zhou H, Hu S, Li X, Li M, Li J, Cheng S. Cancer-cell-secreted miR-204-5p induces leptin signalling pathway in white adipose tissue to promote cancer-associated cachexia. Nat Commun. 2023;14(1):5179. https://doi.org/10.1038/s41467-023-40571-9.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  119. Wang H, Chen Y, Mao X, Du M. Maternal obesity impairs fetal mitochondriogenesis and brown adipose tissue development partially via upregulation of miR-204–5p. Biochim Biophys Acta (BBA)-Mol Basis Disease. 2019;1865(10):2706–15. https://doi.org/10.1016/j.bbadis.2019.07.012.

    Article  CAS  Google Scholar 

  120. Lhamyani S, Gentile A-M, Giráldez-Pérez RM, Feijóo-Cuaresma M, Romero-Zerbo SY, Clemente-Postigo M, Zayed H, Oliva-Olivera W, Bermúdez-Silva FJ, Salas J. miR-21 mimic blocks obesity in mice: A novel therapeutic option. Mol Ther-Nucleic Acids. 2021;26:401–16. https://doi.org/10.1016/j.omtn.2021.06.019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Zhang Y, Song K, Qi G, Yan R, Yang Y, Li Y, Wang S, Bai Z, Ge R-L. Adipose-derived exosomal miR-210/92a cluster inhibits adipose browning via the FGFR-1 signaling pathway in high-altitude hypoxia. Sci Rep. 2020;10(1):14390. https://doi.org/10.1038/s41598-020-71345-8.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  122. Panella R, Petri A, Desai BN, Fagoonee S, Cotton CA, Nguyen PK, Lundin EM, Wagshal A, Wang D-Z, Näär AM, et al. MicroRNA-22 is a key regulator of lipid and metabolic homeostasis. Int J Mol Sci. 2023;24(16):12870. https://doi.org/10.3390/ijms241612870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Karbiener M, Pisani DF, Frontini A, Oberreiter LM, Lang E, Vegiopoulos A, Mössenböck K, Bernhardt GA, Mayr T, Hildner F. MicroRNA-26 family is required for human adipogenesis and drives characteristics of brown adipocytes. Stem cells. 2014;32(6):1578–90. https://doi.org/10.1002/stem.1603.

    Article  CAS  PubMed  Google Scholar 

  124. Lv Y, Xia F, Yu J, Sheng Y, Jin Y, Li Y, Ding G. Distinct response of adipocyte progenitors to glucocorticoids determines visceral obesity via the TEAD1-miR-27b-PRDM16 axis. Obesity. 2023;31(9):2335–48. https://doi.org/10.1002/oby.23839.

    Article  CAS  PubMed  Google Scholar 

  125. Yu J, Lv Y, Wang F, Kong X, Di W, Liu J, Sheng Y, Lv S, Ding G. MiR-27b-3p inhibition enhances browning of epididymal fat in high-fat diet induced obese mice. Front Endocrinol. 2019;10:38. https://doi.org/10.3389/fendo.2019.00038.

    Article  Google Scholar 

  126. Yu J, Lv Y, Di W, Liu J, Kong X, Sheng Y, Huang M, Lv S, Qi H, Gao M. MiR-27b-3p Regulation in browning of human visceral adipose related to central obesity. Obesity. 2018;26(2):387–96. https://doi.org/10.1002/oby.22104.

    Article  CAS  PubMed  Google Scholar 

  127. Sun L, Trajkovski M. MiR-27 orchestrates the transcriptional regulation of brown adipogenesis. Metabolism. 2014;63(2):272–82. https://doi.org/10.1016/j.metabol.2013.10.004.

    Article  CAS  PubMed  Google Scholar 

  128. Lian W-S, Wu R-W, Chen Y-S, Ko J-Y, Wang S-Y, Jahr H, Wang F-S. MicroRNA-29a in osteoblasts represses high-fat diet-mediated osteoporosis and body adiposis through targeting leptin. Int J Mol Sci. 2021;22(17):9135. https://doi.org/10.3390/ijms22179135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Saha PK, Hamilton MP, Rajapakshe K, Putluri V, Felix JB, Masschelin P, Cox AR, Bajaj M, Putluri N, Coarfa C. miR-30a targets gene networks that promote browning of human and mouse adipocytes. Am J Physiol-Endocrinol Metabol. 2020;319(4):E667–77. https://doi.org/10.1152/ajpendo.00045.2020.

    Article  CAS  Google Scholar 

  130. Koh EH, Chen Y, Bader DA, Hamilton MP, He B, York B, Kajimura S, McGuire SE, Hartig SM. Mitochondrial activity in human white adipocytes is regulated by the ubiquitin carrier protein 9/microRNA-30a axis. J Biol Chem. 2016;291(47):24747–55. https://doi.org/10.1074/jbc.M116.749408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Hu F, Wang M, Xiao T, Yin B, He L, Meng W, Dong M, Liu F. miR-30 promotes thermogenesis and the development of beige fat by targeting RIP140. Diabetes. 2015;64(6):2056–68. https://doi.org/10.2337/db14-1117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Ng R, Hussain NA, Zhang Q, Chang C, Li H, Fu Y, Cao L, Han W, Stunkel W, Xu F. miRNA-32 drives brown fat thermogenesis and trans-activates subcutaneous white fat browning in mice. Cell Rep. 2017;19(6):1229–46. https://doi.org/10.1016/j.celrep.2017.04.035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Li D, Liu Y, Gao W, Han J, Yuan R, Zhang M, Pang W. Inhibition of miR-324-5p increases PM20D1-mediated white and brown adipose loss and reduces body weight in juvenile mice. Eur J Pharmacol. 2019;863:172708. https://doi.org/10.1016/j.ejphar.2019.172708.

    Article  CAS  PubMed  Google Scholar 

  134. Fischer C, Seki T, Lim S, Nakamura M, Andersson P, Yang Y, Honek J, Wang Y, Gao Y, Chen F. A miR-327–FGF10–FGFR2-mediated autocrine signaling mechanism controls white fat browning. Nat Commun. 2017;8(1):2079. https://doi.org/10.1038/s41467-017-02158-z.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  135. Afonso MS, Verma N, van Solingen C, Cyr Y, Sharma M, Perie L, Corr EM, Schlegel M, Shanley LC, Peled D. MicroRNA-33 inhibits adaptive thermogenesis and adipose tissue beiging. Arterioscler Thromb Vasc Biol. 2021;41(4):1360–73. https://doi.org/10.1161/ATVBAHA.120.315798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Vonhögen IG, El Azzouzi H, Olieslagers S, Vasilevich A, de Boer J, Tinahones FJ, da Costa Martins PA, de Windt LJ, Murri M. MiR-337-3p promotes adipocyte browning by inhibiting TWIST1. Cells. 2020;9(4):1056. https://doi.org/10.3390/cells9041056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Tsai N-P, Lin Y-L, Wei L-N. MicroRNA mir-346 targets the 5′-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression. Biochem J. 2009;424(3):411–8. https://doi.org/10.1042/BJ20090915.

    Article  CAS  PubMed  Google Scholar 

  138. Kiskinis E, Chatzeli L, Curry E, Kaforou M, Frontini A, Cinti S, Montana G, Parker MG, Christian M. RIP140 represses the “brown-in-white” adipocyte program including a futile cycle of triacyclglycerol breakdown and synthesis. Mol Endocrinol. 2014;28(3):344–56. https://doi.org/10.1210/me.2013-1254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Fu T, Seok S, Choi S, Huang Z, Suino-Powell K, Xu HE, Kemper B, Kemper JK. MicroRNA 34a inhibits beige and brown fat formation in obesity in part by suppressing adipocyte fibroblast growth factor 21 signaling and SIRT1 function. Mol Cell Biol. 2014;34(22):4130–42. https://doi.org/10.1128/MCB.00596-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Rocha A, de Lima T, de Souza G, Corrêa R, Ferrucci D, Rodrigues B, Lopes-Ramos C, Nilsson D, Knittel T, Castro P. Enoxacin induces oxidative metabolism and mitigates obesity by regulating adipose tissue miRNA expression. Sci Adv. 2020;6(49):eabc6250. https://doi.org/10.1126/sciadv.abc6250.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  141. Ge X, Sathiakumar D, Lua B, Kukreti H, Lee M, McFarlane C. Myostatin signals through miR-34a to regulate Fndc5 expression and browning of white adipocytes. Int J Obes. 2017;41(1):137–48. https://doi.org/10.1038/ijo.2016.110.

    Article  CAS  Google Scholar 

  142. Seeliger C, Krauss T, Honecker J, Mengel LA, Buekens L, Mesas-Fernández A, Skurk T, Claussnitzer M, Hauner H. miR-375 is cold exposure sensitive and drives thermogenesis in visceral adipose tissue derived stem cells. Sci Rep. 2022;12(1):9557. https://doi.org/10.1038/s41598-022-13610-6.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  143. Pan D, Mao C, Quattrochi B, Friedline RH, Zhu LJ, Jung DY, Kim JK, Lewis B, Wang Y-X. MicroRNA-378 controls classical brown fat expansion to counteract obesity. Nat Commun. 2014;5:4725. https://doi.org/10.1038/ncomms5725.

    Article  CAS  PubMed  ADS  Google Scholar 

  144. Abdollahi M, Kato M, Lanting L, Tunduguru R, Wang M, Wang Y, Fueger PT, Wang Q, Huang W, Natarajan R. miR-379 mediates insulin resistance and obesity through impaired angiogenesis and adipogenesis regulated by ER stress. Mol Ther Nucleic Acids. 2022;30:115–30. https://doi.org/10.1016/j.omtn.2022.09.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Choi WH, Ahn J, Jung CH, Jang YJ, Ha TY. β-Lapachone prevents diet-induced obesity by increasing energy expenditure and stimulating the browning of white adipose tissue via downregulation of miR-382 expression. Diabetes. 2016;65(9):2490–501. https://doi.org/10.2337/db15-1423.

    Article  CAS  PubMed  Google Scholar 

  146. Wang M, Shao J, Zhang X, Liu Z, Tang T, Chen G, Xia S, Zhao K, Kang Z, Sun W. miR-383-5p regulates preadipocyte proliferation and differentiation by targeting RAD51AP1. Int J Mol Sci. 2023;24(18):14025. https://doi.org/10.3390/ijms241814025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Ye C, Duan J, Zhang X, Yao L, Song Y, Wang G, Li Q, Wang B, Ai D, Wang C. Cold-induced Yes-associated-protein expression through miR-429 mediates the browning of white adipose tissue. Sci China Life Sci. 2021;64(3):404–18. https://doi.org/10.1007/s11427-020-1779-2.

    Article  CAS  PubMed  ADS  Google Scholar 

  148. Liu X, Zhu Y, Zhan S, Zhong T, Guo J, Cao J, Li L, Zhang H, Wang L. RNA-Seq reveals miRNA role in thermogenic regulation in brown adipose tissues of goats. BMC Genomics. 2022;23(1):186. https://doi.org/10.1186/s12864-022-08401-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Zhang H, Guan M, Townsend KL, Huang TL, An D, Yan X, Xue R, Schulz TJ, Winnay J, Mori M. Micro RNA-455 regulates brown adipogenesis via a novel HIF 1an-AMPK-PGC 1α signaling network. EMBO Rep. 2015;16:1378–93. https://doi.org/10.15252/embr.201540837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Lemecha M, Morino K, Imamura T, Iwasaki H, Ohashi N, Ida S, Sato D, Sekine O, Ugi S, Maegawa H. MiR-494-3p regulates mitochondrial biogenesis and thermogenesis through PGC1-α signalling in beige adipocytes. Sci Rep. 2018;8(1):15096. https://doi.org/10.1038/s41598-018-33438-3.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  151. Man XF, Hu N, Tan SW, Tang HN, Guo Y, Tang CY, Liu YQ, Tang J, Zhou CL, Wang F. Insulin receptor substrate-1 inhibits high-fat diet-induced obesity by browning of white adipose tissue through miR-503. FASEB J. 2020;34(9):12308–23. https://doi.org/10.1096/fj.201903283RR.

    Article  CAS  PubMed  Google Scholar 

  152. Tan X, Zhu T, Zhang L, Fu L, Hu Y, Li H, Li C, Zhang J, Liang B, Liu J. miR-669a-5p promotes adipogenic differentiation and induces browning in preadipocytes. Adipocyte. 2022;11(1):120–32. https://doi.org/10.1080/21623945.2022.2030570.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Chen Y, Buyel JJ, Hanssen MJ, Siegel F, Pan R, Naumann J, Schell M, Van Der Lans A, Schlein C, Froehlich H. Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity. Nat Commun. 2016;7:11420. https://doi.org/10.1038/ncomms11420.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  154. Goody D, Pfeifer A. MicroRNAs in brown and beige fat. Biochim Biophys Acta Mol Cell Biol Lipids. 2019;1864:29–36. https://doi.org/10.1016/j.bbalip.2018.05.003.

    Article  CAS  PubMed  Google Scholar 

  155. Rani V, Sengar RS. Biogenesis and mechanisms of microRNA-mediated gene regulation. Biotechnol Bioeng. 2022;119:685–92. https://doi.org/10.1002/bit.28029.

    Article  CAS  PubMed  Google Scholar 

  156. Isaac R, Reis FCG, Ying W, Olefsky JM. Exosomes as mediators of intercellular crosstalk in metabolism. Cell Metab. 2021;33:1744–62. https://doi.org/10.1016/j.cmet.2021.08.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. O’Brien J, Hayder H, Zayed Y, Peng C. Overview of MicroRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402. https://doi.org/10.3389/fendo.2018.00402.

    Article  CAS  PubMed  Google Scholar 

  158. Thomou T, Mori MA, Dreyfuss JM, Konishi M, Sakaguchi M, Wolfrum C, Rao TN, Winnay JN, Garcia-Martin R, Grinspoon SK, et al. Corrigendum: Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature. 2017;545:252. https://doi.org/10.1038/nature22319.

    Article  CAS  PubMed  ADS  Google Scholar 

  159. Kristensen LS, Andersen MS, Stagsted LVW, Ebbesen KK, Hansen TB, Kjems J. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20:675–91. https://doi.org/10.1038/s41576-019-0158-7.

    Article  CAS  PubMed  Google Scholar 

  160. Thomson DW, Dinger ME. Endogenous microRNA sponges: Evidence and controversy. Nat Rev Genet. 2016;17:272–83. https://doi.org/10.1038/nrg.2016.20.

    Article  CAS  PubMed  Google Scholar 

  161. Liu K, Liu X, Deng Y, Li Z, Tang A. CircRNA-mediated regulation of brown adipose tissue adipogenesis. Front Nutr. 2022;9:926024. https://doi.org/10.3389/fnut.2022.926024.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Shao J, Wang M, Zhang A, Liu Z, Jiang G, Tang T, Wang J, Jia X, Lai S. Interference of a mammalian circRNA regulates lipid metabolism reprogramming by targeting miR-24–3p/Igf2/PI3K-AKT-mTOR and Igf2bp2/Ucp1 axis. Cell Mol Life Sci. 2023;80(9):252. https://doi.org/10.1007/s00018-023-04899-1.

    Article  CAS  PubMed  Google Scholar 

  163. Hu C, Feng X, Ma Y, Wei D, Zhang L, Wang S, Ma Y. CircADAMTS16 inhibits differentiation and promotes proliferation of bovine adipocytes by targeting miR-10167-3p. Cells. 2023;12(8):1175. https://doi.org/10.3390/cells12081175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Song X-H, He N, Xing Y-T, Jin X-Q, Li Y-W, Liu S-S, Gao Z-Y, Guo C, Wang J-J, Huang Y-Y. A novel age-related circular RNA circ-ATXN2 inhibits proliferation, promotes cell death and adipogenesis in rat adipose tissue-derived stromal cells. Frontiers in Genetics. 2021;12:761926. https://doi.org/10.3389/fgene.2021.761926.

  165. Zhang S, Jiang E, Kang Z, Bi Y, Liu H, Xu H, Wang Z, Lei C, Chen H, Lan X. CircRNA profiling reveals an abundant circBDP1 that regulates bovine fat development by sponging miR-181b/miR-204 targeting Sirt1/TRARG1. J Agric Food Chem. 2022;70:14312–28. https://doi.org/10.1021/acs.jafc.2c05939.

    Article  CAS  PubMed  Google Scholar 

  166. Tian W, Liu Y, Zhang W, Nie R, Ling Y, Zhang B, Zhang H, Wu C. CircDOCK7 facilitates the proliferation and adipogenic differentiation of chicken abdominal preadipocytes through the gga-miR-301b-3p/ACSL1 axis. J Anim Sci Biotechnol. 2023;14:91. https://doi.org/10.1186/s40104-023-00891-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Zhu Y, Gui W, Lin X, Li H. Knock-down of circular RNA H19 induces human adipose-derived stem cells adipogenic differentiation via a mechanism involving the polypyrimidine tract-binding protein 1. Exp Cell Res. 2020;387:111753. https://doi.org/10.1016/j.yexcr.2019.111753.

    Article  CAS  PubMed  Google Scholar 

  168. Chen S, Song P, Wang Y, Wang Z, Xue J, Jiang Y, Zhou Y, Zhao J, Tang L. CircMAPK9 promotes adipogenesis through modulating hsa-miR-1322/FTO axis in obesity. Iscience. 2023;26(10):107756. https://doi.org/10.1016/j.isci.2023.107756.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  169. Zhang T, Zhang Z, Xia T, Liu C, Sun C. circNrxn2 promoted WAT browning via sponging miR-103 to relieve its inhibition of FGF10 in HFD mice. Mol Ther-Nucleic Acids. 2019;17:551–62. https://doi.org/10.1016/j.omtn.2019.06.019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Ding Z, Sun D, Han J, Shen L, Yang F, Sah S, Sui X, Wu G. Novel noncoding RNA CircPTK2 regulates lipolysis and adipogenesis in cachexia. Mol Metab. 2021;53:101310. https://doi.org/10.1016/j.molmet.2021.101310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Liu Y, Liu H, Li Y, Mao R, Yang H, Zhang Y, Zhang Y, Guo P, Zhan D, Zhang T. Circular RNA SAMD4A controls adipogenesis in obesity through the miR-138-5p/EZH2 axis. Theranostics. 2020;10:4705. https://doi.org/10.7150/thno.42417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Yue X, Fan M, Liang Y, Qiao L, Liu J, Pan Y, Yang K, Liu W. circITGB1 regulates adipocyte proliferation and differentiation via the miR-23a/ARRB1 pathway. Int J Mol Sci. 2023;24:1976. https://doi.org/10.3390/ijms24031976.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Chen H, Zhang J, Yang L, Li Y, Wang Z, Ye C. circ-ZEB1 regulates epithelial-mesenchymal transition and chemotherapy resistance of colorectal cancer through acting on miR-200c-5p. Transl Oncol. 2023;28:101604. https://doi.org/10.1016/j.tranon.2022.101604.

    Article  CAS  PubMed  Google Scholar 

  174. Zhi F, Ding Y, Wang R, Yang Y, Luo K, Hua F. Correction: Exosomal hsa_circ_0006859 is a potential biomarker for postmenopausal osteoporosis and enhances adipogenic versus osteogenic differentiation in human bone marrow mesenchymal stem cells by sponging miR-431-5p. Stem Cell Res Ther. 2022;13:381. https://doi.org/10.1186/s13287-022-03096-4.

    Article  PubMed  PubMed Central  Google Scholar 

  175. Zhang X, Chen L, Xiao B, Liu H, Su Y. Circ_0075932 in adipocyte-derived exosomes induces inflammation and apoptosis in human dermal keratinocytes by directly binding with PUM2 and promoting PUM2-mediated activation of AuroraA/NF-kappaB pathway. Biochem Biophys Res Commun. 2019;511:551–8. https://doi.org/10.1016/j.bbrc.2019.02.082.

    Article  CAS  PubMed  Google Scholar 

  176. Winkle M, El-Daly SM, Fabbri M, Calin GA. Noncoding RNA therapeutics - challenges and potential solutions. Nat Rev Drug Discov. 2021;20:629–51. https://doi.org/10.1038/s41573-021-00219-z.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Yang J, Meng X, Pan J, Jiang N, Zhou C, Wu Z, Gong Z. CRISPR/Cas9-mediated noncoding RNA editing in human cancers. RNA Biol. 2018;15:35–43. https://doi.org/10.1080/15476286.2017.1391443.

    Article  PubMed  Google Scholar 

  178. Ratti M, Lampis A, Ghidini M, Salati M, Mirchev MB, Valeri N, Hahne JC. MicroRNAs (miRNAs) and long non-coding RNAs (lncRNAs) as new tools for cancer therapy: First steps from bench to bedside. Target Oncol. 2020;15:261–78. https://doi.org/10.1007/s11523-020-00717-x.

    Article  PubMed  PubMed Central  Google Scholar 

  179. Li C, Zhang L. Noncoding RNAs in human cancer: One step forward in diagnosis and treatment. Brief Funct Genomics. 2016;15:165–6. https://doi.org/10.1093/bfgp/elw004.

    Article  PubMed  PubMed Central  Google Scholar 

  180. Zhao R, Fu J, Zhu L, Chen Y, Liu B. Designing strategies of small-molecule compounds for modulating non-coding RNAs in cancer therapy. J Hematol Oncol. 2022;15:14. https://doi.org/10.1186/s13045-022-01230-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Ortega FJ, Mercader JM, Catalan V, Moreno-Navarrete JM, Pueyo N, Sabater M, Gomez-Ambrosi J, Anglada R, Fernandez-Formoso JA, Ricart W, et al. Targeting the circulating microRNA signature of obesity. Clin Chem. 2013;59:781–92. https://doi.org/10.1373/clinchem.2012.195776.

    Article  CAS  PubMed  Google Scholar 

  182. Lorente-Cebrian S, Gonzalez-Muniesa P, Milagro FI, Martinez JA. MicroRNAs and other non-coding RNAs in adipose tissue and obesity: Emerging roles as biomarkers and therapeutic targets. Clin Sci (Lond). 2019;133:23–40. https://doi.org/10.1042/CS20180890.

    Article  CAS  PubMed  Google Scholar 

  183. Perez-Hernandez J, Riffo-Campos AL, Ortega A, Martinez-Arroyo O, Perez-Gil D, Olivares D, Solaz E, Martinez F, Martinez-Hervas S, Chaves FJ, et al. Urinary- and plasma-derived exosomes reveal a distinct MicroRNA signature associated with albuminuria in hypertension. Hypertension. 2021;77:960–71. https://doi.org/10.1161/HYPERTENSIONAHA.120.16598.

    Article  CAS  PubMed  Google Scholar 

  184. Vonhogen IGC, Mohseni Z, Winkens B, Xiao K, Thum T, Calore M, da Costa Martins PA, de Windt LJ, Spaanderman MEA, Ghossein-Doha C. Circulating miR-216a as a biomarker of metabolic alterations and obesity in women. Noncoding RNA Res. 2020;5:144–52. https://doi.org/10.1016/j.ncrna.2020.08.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Zhang K, Wan X, Khan MA, Sun X, Yi X, Wang Z, Chen K, Peng L. Peripheral blood circRNA microarray profiling identities hsa_circ_0001831 and hsa_circ_0000867 as two novel circRNA biomarkers for early type 2 diabetic nephropathy. Diabetes Metab Syndr Obes. 2022;15:2789–801. https://doi.org/10.2147/DMSO.S384054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Amri EZ, Scheideler M. Small non coding RNAs in adipocyte biology and obesity. Mol Cell Endocrinol. 2017;456:87–94. https://doi.org/10.1016/j.mce.2017.04.009.

    Article  CAS  PubMed  Google Scholar 

  187. Hueso M, Mallen A, Sune-Pou M, Aran JM, Sune-Negre JM, Navarro E. ncRNAs in Therapeutics: Challenges and limitations in nucleic acid-based drug delivery. Int J Mol Sci. 2021;22. https://doi.org/10.3390/ijms222111596.

  188. Pierce JB, Zhou H, Simion V, Feinberg MW. Long noncoding RNAs as therapeutic targets. Adv Exp Med Biol. 2022;1363:161–75. https://doi.org/10.1007/978-3-030-92034-0_9.

    Article  CAS  PubMed  Google Scholar 

  189. Schachner-Nedherer A-L, Fuchs J, Vidakovic I, Höller O, Schratter G, Almer G, Fröhlich E, Zimmer A, Wabitsch M, Kornmueller K. Lipid nanoparticles as a shuttle for anti-adipogenic miRNAs to human adipocytes. Pharmaceutics. 2023;15:1983. https://doi.org/10.3390/pharmaceutics15071983.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Dowdy SF. Overcoming cellular barriers for RNA therapeutics. Nat Biotechnol. 2017;35:222–9. https://doi.org/10.1038/nbt.3802.

    Article  CAS  PubMed  Google Scholar 

  191. Jiang L, Li J. lncRNA GMDS-AS1 upregulates IL-6, TNF-alpha and IL-1beta, and induces apoptosis in human monocytic THP-1 cells via miR-96-5p/caspase 2 signaling. Mol Med Rep. 2022;25(2):67. https://doi.org/10.3892/mmr.2022.12583.

    Article  MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

  192. Chini A, Guha P, Malladi VS, Guo Z, Mandal SS. Novel long non-coding RNAs associated with inflammation and macrophage activation in human. Sci Rep. 2023;13:4036. https://doi.org/10.1038/s41598-023-30568-1.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  193. Li N, Liu Y, Cai J. LncRNA MIR155HG regulates M1/M2 macrophage polarization in chronic obstructive pulmonary disease. Biomed Pharmacother. 2019;117:109015. https://doi.org/10.1016/j.biopha.2019.109015.

    Article  CAS  PubMed  Google Scholar 

  194. Li Z, Rana TM. Therapeutic targeting of microRNAs: Current status and future challenges. Nat Rev Drug Discov. 2014;13:622–38. https://doi.org/10.1038/nrd4359.

    Article  CAS  PubMed  Google Scholar 

  195. Guan S, Zhang Z, Wu J. Non-coding RNA delivery for bone tissue engineering: Progress, challenges, and potential solutions. iScience. 2022;25:104807. https://doi.org/10.1016/j.isci.2022.104807.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  196. Scheideler M, Vidakovic I, Prassl R. Lipid nanocarriers for microRNA delivery. Chem Phys Lipids. 2020;226:104837. https://doi.org/10.1016/j.chemphyslip.2019.104837.

    Article  CAS  PubMed  Google Scholar 

  197. Toden S, Zumwalt TJ, Goel A. Non-coding RNAs and potential therapeutic targeting in cancer. Biochim Biophys Acta Rev Cancer. 2021;1875(1):188491. https://doi.org/10.1016/j.bbcan.2020.188491.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the Chinese Academy of Medical Sciences (CAMS) Innovation Fund for Medical Sciences (CIFMS) (2021-I2M-1–008) for Dr. Guoping Li, National Natural Science Foundation of China (82370877, 81970739) and National High Level Hospital Clinical Research Funding (BJ-2023–237).

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Liang Dehuan wrote the main manuscript text and prepared the figure; Li Guoping critically revised the article.

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Liang, D., Li, G. Pulling the trigger: Noncoding RNAs in white adipose tissue browning. Rev Endocr Metab Disord 25, 399–420 (2024). https://doi.org/10.1007/s11154-023-09866-6

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