The role of microRNAs in adipocyte differentiation
Rong Zhang, Di Wang, Zhuying Xia, Chao Chen, Peng Cheng, Hui Xie, Xianghang Luo
The role of microRNAs in adipocyte differentiation
Adipocytes differentiate from mesenchymal stem cells (MSCs) in a process known as adipogenesis. The programme of adipogenesis is regulated by the sequential activation of transcription factors and several signaling pathways. There is growing evidence indicating that a class of small non-coding single-stranded RNAs known as “microRNAs (miRNAs)” also are involved in this process. In this review, we summarize the biology and functional mechanisms of miRNAs in adipocyte differentiation. In addition, we further discuss the miRNAs profiling, the miRNAs function and miRNAs target prediction in the adipogenesis.
microRNA / adipocyte / differentiation / adipogenesis
[1] |
Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: tracking obesity to its source. Cell2007; 131(2): 242-256
CrossRef
Pubmed
Google scholar
|
[2] |
Otto TC, Lane MD. Adipose development: from stem cell to adipocyte. Crit Rev Biochem Mol Biol2005; 40(4): 229-242
CrossRef
Pubmed
Google scholar
|
[3] |
Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev1998; 78(3): 783-809
Pubmed
|
[4] |
Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev2000; 14(11): 1293-1307
Pubmed
|
[5] |
MacDougald OA, Mandrup S. Adipogenesis: forces that tip the scales. Trends Endocrinol Metab2002; 13(1): 5-11
CrossRef
Pubmed
Google scholar
|
[6] |
Blüher M, Michael MD, Peroni OD, Ueki K, Carter N, Kahn BB, Kahn CR. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell2002; 3(1): 25-38
CrossRef
Pubmed
Google scholar
|
[7] |
Smith PJ, Wise LS, Berkowitz R, Wan C, Rubin CS. Insulin-like growth factor-I is an essential regulator of the differentiation of 3T3-L1 adipocytes. J Biol Chem1988; 263(19): 9402-9408
Pubmed
|
[8] |
Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol2005; 6(5): 376-385
CrossRef
Pubmed
Google scholar
|
[9] |
[No authors listed]. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser2000; 894: i-xii, 1-253
Pubmed
|
[10] |
Li H, Xie H, Liu W, Hu R, Huang B, Tan YF, Xu K, Sheng ZF, Zhou HD, Wu XP, Luo XH. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest2009; 119(12): 3666-3677
CrossRef
Pubmed
Google scholar
|
[11] |
He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet2004; 5(7): 522-531
CrossRef
Pubmed
Google scholar
|
[12] |
Yang L, Cheng P, Chen C, He HB, Xie GQ, Zhou HD, Xie H, Wu XP, Luo XH. miR-93/Sp7 function loop mediates osteoblast mineralization. J Bone Miner Res2012; 27(7): 1598-1606
CrossRef
Pubmed
Google scholar
|
[13] |
Hu R, Liu W, Li H, Yang L, Chen C, Xia ZY, Guo LJ, Xie H, Zhou HD, Wu XP, Luo XH. A Runx2/miR-3960/miR-2861 regulatory feedback loop during mouse osteoblast differentiation. J Biol Chem2011; 286(14): 12328-12339
CrossRef
Pubmed
Google scholar
|
[14] |
Li H, Li WX, Ding SW. Induction and suppression of RNA silencing by an animal virus. Science2002; 296(5571): 1319-1321
CrossRef
Pubmed
Google scholar
|
[15] |
Zeng Y, Yi R, Cullen BR. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci USA2003; 100(17): 9779-9784
CrossRef
Pubmed
Google scholar
|
[16] |
Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. The nuclear RNase III Drosha initiates microRNA processing. Nature2003; 425(6956): 415-419
CrossRef
Pubmed
Google scholar
|
[17] |
Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev2003; 17(24): 3011-3016
CrossRef
Pubmed
Google scholar
|
[18] |
Lund E, Güttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science2004; 303(5654): 95-98
CrossRef
Pubmed
Google scholar
|
[19] |
Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The Microprocessor complex mediates the genesis of microRNAs. Nature2004; 432(7014): 235-240
CrossRef
Pubmed
Google scholar
|
[20] |
Tan GS, Garchow BG, Liu X, Yeung J, Morris JP 4th, Cuellar TL, McManus MT, Kiriakidou M. Expanded RNA-binding activities of mammalian Argonaute 2. Nucleic Acids Res2009; 37(22): 7533-7545
CrossRef
Pubmed
Google scholar
|
[21] |
Hutvágner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science2002; 297(5589): 2056-2060
CrossRef
Pubmed
Google scholar
|
[22] |
Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol2007; 17(3): 118-126
CrossRef
Pubmed
Google scholar
|
[23] |
Shingara J, Keiger K, Shelton J, Laosinchai-Wolf W, Powers P, Conrad R, Brown D, Labourier E. An optimized isolation and labeling platform for accurate microRNA expression profiling. RNA2005; 11(9): 1461-1470
CrossRef
Pubmed
Google scholar
|
[24] |
Hilton C, Neville MJ. Karpe F. MicroRNAs in adipose tissue: their role in adipogenesis and obesity. Int J Obes (Lond)2013;37:325-332
CrossRef
Pubmed
Google scholar
|
[25] |
Castoldi M, Schmidt S, Benes V, Noerholm M, Kulozik AE, Hentze MW, Muckenthaler MU. A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA). RNA2006; 12(5): 913-920
CrossRef
Pubmed
Google scholar
|
[26] |
Válóczi A, Hornyik C, Varga N, Burgyán J, Kauppinen S, Havelda Z. Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes. Nucleic Acids Res2004; 32(22): e175
CrossRef
Pubmed
Google scholar
|
[27] |
Neville MJ, Collins JM, Gloyn AL, McCarthy MI, Karpe F. Comprehensive human adipose tissue mRNA and microRNA endogenous control selection for quantitative real-time-PCR normalization. Obesity (Silver Spring)2011; 19(4): 888-892
CrossRef
Pubmed
Google scholar
|
[28] |
Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet2009; 10(1): 57-63
CrossRef
Pubmed
Google scholar
|
[29] |
Lee EJ, Baek M, Gusev Y, Brackett DJ, Nuovo GJ, Schmittgen TD. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA2008; 14(1): 35-42
CrossRef
Pubmed
Google scholar
|
[30] |
Kajimoto K, Naraba H, Iwai N. MicroRNA and 3T3-L1 pre-adipocyte differentiation. RNA2006; 12(9): 1626-1632
CrossRef
Pubmed
Google scholar
|
[31] |
Xie H, Lim B, Lodish HF. MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes2009; 58(5): 1050-1057
CrossRef
Pubmed
Google scholar
|
[32] |
Ailhaud G, Grimaldi P, Négrel R. Cellular and molecular aspects of adipose tissue development. Annu Rev Nutr1992; 12(1): 207-233
CrossRef
Pubmed
Google scholar
|
[33] |
Rosen ED, Spiegelman BM. Molecular regulation of adipogenesis. Annu Rev Cell Dev Biol2000; 16(1): 145-171
CrossRef
Pubmed
Google scholar
|
[34] |
Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol2006; 7(12): 885-896
CrossRef
Pubmed
Google scholar
|
[35] |
Tontonoz P, Hu E, Spiegelman BM. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell1994; 79(7): 1147-1156
CrossRef
Pubmed
Google scholar
|
[36] |
Tamori Y, Masugi J, Nishino N, Kasuga M. Role of peroxisome proliferator-activated receptor-gamma in maintenance of the characteristics of mature 3T3-L1 adipocytes. Diabetes2002; 51(7): 2045-2055
CrossRef
Pubmed
Google scholar
|
[37] |
Hamm JK, Park BH, Farmer SR. A role for C/EBPbeta in regulating peroxisome proliferator-activated receptor gamma activity during adipogenesis in 3T3-L1 preadipocytes. J Biol Chem2001; 276(21): 18464-18471
CrossRef
Pubmed
Google scholar
|
[38] |
Shao D, Lazar MA. Peroxisome proliferator activated receptor gamma, CCAAT/enhancer-binding protein alpha, and cell cycle status regulate the commitment to adipocyte differentiation. J Biol Chem1997; 272(34): 21473-21478
CrossRef
Pubmed
Google scholar
|
[39] |
Bennett CN, Ross SE, Longo KA, Bajnok L, Hemati N, Johnson KW, Harrison SD, MacDougald OA. Regulation of Wnt signaling during adipogenesis. J Biol Chem2002; 277(34): 30998-31004
CrossRef
Pubmed
Google scholar
|
[40] |
Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science2000; 289(5481): 950-953
CrossRef
Pubmed
Google scholar
|
[41] |
Arango NA, Szotek PP, Manganaro TF, Oliva E, Donahoe PK, Teixeira J. Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium. Dev Biol2005; 288(1): 276-283
CrossRef
Pubmed
Google scholar
|
[42] |
Choy L, Skillington J, Derynck R. Roles of autocrine TGF-beta receptor and Smad signaling in adipocyte differentiation. J Cell Biol2000; 149(3): 667-682
CrossRef
Pubmed
Google scholar
|
[43] |
Spiegelman BM, Ginty CA. Fibronectin modulation of cell shape and lipogenic gene expression in 3T3-adipocytes. Cell1983; 35(3 Pt 2): 657-666
CrossRef
Pubmed
Google scholar
|
[44] |
Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell2006; 126(4): 677-689
CrossRef
Pubmed
Google scholar
|
[45] |
Xu P, Vernooy SY, Guo M, Hay BA. The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol2003; 13(9): 790-795
CrossRef
Pubmed
Google scholar
|
[46] |
Esau C, Kang X, Peralta E, Hanson E, Marcusson EG, Ravichandran LV, Sun Y, Koo S, Perera RJ, Jain R, Dean NM, Freier SM, Bennett CF, Lollo B, Griffey R. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem2004; 279(50): 52361-52365
CrossRef
Pubmed
Google scholar
|
[47] |
Mendell JT. miRiad roles for the miR-17-92 cluster in development and disease. Cell2008; 133(2): 217-222
CrossRef
Pubmed
Google scholar
|
[48] |
Wang Q, Li YC, Wang J, Kong J, Qi Y, Quigg RJ, Li X. miR-17-92 cluster accelerates adipocyte differentiation by negatively regulating tumor-suppressor Rb2/p130. Proc Natl Acad Sci USA2008; 105(8): 2889-2894
CrossRef
Pubmed
Google scholar
|
[49] |
Richon VM, Lyle RE, McGehee RE Jr. Regulation and expression of retinoblastoma proteins p107 and p130 during 3T3-L1 adipocyte differentiation. J Biol Chem1997; 272(15): 10117-10124
CrossRef
Pubmed
Google scholar
|
[50] |
Prince AM, May JS, Burton GR, Lyle RE, McGehee RE Jr. Proteasomal degradation of retinoblastoma-related p130 during adipocyte differentiation. Biochem Biophys Res Commun2002; 290(3): 1066-1071
CrossRef
Pubmed
Google scholar
|
[51] |
Kim YJ, Hwang SJ, Bae YC, Jung JS. MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells2009; 27(12): 3093-3102
Pubmed
|
[52] |
Kim YJ, Hwang SH, Cho HH, Shin KK, Bae YC, Jung JS. MicroRNA 21 regulates the proliferation of human adipose tissue-derived mesenchymal stem cells and high-fat diet-induced obesity alters microRNA 21 expression in white adipose tissues. J Cell Physiol2012; 227(1): 183-193
CrossRef
Pubmed
Google scholar
|
[53] |
Martinelli R, Nardelli C, Pilone V, Buonomo T, Liguori R, Castanò I, Buono P, Masone S, Persico G, Forestieri P, Pastore L, Sacchetti L. miR-519d overexpression is associated with human obesity. Obesity (Silver Spring)2010; 18(11): 2170-2176
CrossRef
Pubmed
Google scholar
|
[54] |
Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science2000; 289(5481): 950-953
CrossRef
Pubmed
Google scholar
|
[55] |
Kennell JA, Gerin I, MacDougald OA, Cadigan KM. The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc Natl Acad Sci USA2008; 105(40): 15417-15422
CrossRef
Pubmed
Google scholar
|
[56] |
Qin L, Chen Y, Niu Y, Chen W, Wang Q, Xiao S, Li A, Xie Y, Li J, Zhao X, He Z, Mo D. A deep investigation into the adipogenesis mechanism: profile of microRNAs regulating adipogenesis by modulating the canonical Wnt/beta-catenin signaling pathway. BMC Genomics2010; 11(1): 320
CrossRef
Pubmed
Google scholar
|
[57] |
Zaragosi LE, Wdziekonski B, Brigand KL, Villageois P, Mari B, Waldmann R, Dani C, Barbry P. Small RNA sequencing reveals miR-642a-3p as a novel adipocyte-specific microRNA and miR-30 as a key regulator of human adipogenesis. Genome Biol2011; 12(7): R64
CrossRef
Pubmed
Google scholar
|
[58] |
Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells2010; 28(2): 357-364
Pubmed
|
[59] |
Ling HY, Wen GB, Feng SD, Tuo QH, Ou HS, Yao CH, Zhu BY, Gao ZP, Zhang L, Liao DF. MicroRNA-375 promotes 3T3-L1 adipocyte differentiation through modulation of extracellular signal-regulated kinase signalling. Clin Exp Pharmacol Physiol2011; 38(4): 239-246
CrossRef
Pubmed
Google scholar
|
[60] |
Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z. A role of miR-27 in the regulation of adipogenesis. FEBS J2009; 276(8): 2348-2358
CrossRef
Pubmed
Google scholar
|
[61] |
Kim SY, Kim AY, Lee HW, Son YH, Lee GY, Lee JW, Lee YS, Kim JB. miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun2010; 392(3): 323-328
CrossRef
Pubmed
Google scholar
|
[62] |
Karbiener M, Fischer C, Nowitsch S, Opriessnig P, Papak C, Ailhaud G, Dani C, Amri EZ, Scheideler M. microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun2009; 390(2): 247-251
CrossRef
Pubmed
Google scholar
|
[63] |
Lee EK, Lee MJ, Abdelmohsen K, Kim W, Kim MM, Srikantan S, Martindale JL, Hutchison ER, Kim HH, Marasa BS, Selimyan R, Egan JM, Smith SR, Fried SK, Gorospe M. miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol2011; 31(4): 626-638
CrossRef
Pubmed
Google scholar
|
[64] |
Sun T, Fu M, Bookout AL, Kliewer SA, Mangelsdorf DJ. MicroRNA let-7 regulates 3T3-L1 adipogenesis. Mol Endocrinol2009; 23(6): 925-931
CrossRef
Pubmed
Google scholar
|
[65] |
Anand A, Chada K. In vivo modulation of Hmgic reduces obesity. Nat Genet2000; 24(4): 377-380
CrossRef
Pubmed
Google scholar
|
[66] |
Kinoshita M, Ono K, Horie T, Nagao K, Nishi H, Kuwabara Y, Takanabe-Mori R, Hasegawa K, Kita T, Kimura T. Regulation of adipocyte differentiation by activation of serotonin (5-HT) receptors 5-HT2AR and 5-HT2CR and involvement of microRNA-448-mediated repression of KLF5. Mol Endocrinol2010; 24(10): 1978-1987
CrossRef
Pubmed
Google scholar
|
[67] |
Rajewsky N. microRNA target predictions in animals. Nat Genet2006; 38( Suppl): S8-S13
CrossRef
Pubmed
Google scholar
|
[68] |
John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol2004; 2(11): e363
CrossRef
Pubmed
Google scholar
|
[69] |
Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell2003; 115(7): 787-798
CrossRef
Pubmed
Google scholar
|
[70] |
Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet2005; 37(5): 495-500
CrossRef
Pubmed
Google scholar
|
[71] |
Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell2005; 120(1): 15-20
CrossRef
Pubmed
Google scholar
|
[72] |
Miranda KC, Huynh T, Tay Y, Ang YS, Tam WL, Thomson AM, Lim B, Rigoutsos I. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell2006; 126(6): 1203-1217
CrossRef
Pubmed
Google scholar
|
[73] |
Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature2005; 433(7027): 769-773
CrossRef
Pubmed
Google scholar
|
[74] |
Wang X, Wang X. Systematic identification of microRNA functions by combining target prediction and expression profiling. Nucleic Acids Res2006; 34(5): 1646-1652
CrossRef
Pubmed
Google scholar
|
[75] |
Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature2008; 455(7209): 64-71
CrossRef
Pubmed
Google scholar
|
[76] |
Kiriakidou M, Nelson PT, Kouranov A, Fitziev P, Bouyioukos C, Mourelatos Z, Hatzigeorgiou A. A combined computational-experimental approach predicts human microRNA targets. Genes Dev2004; 18(10): 1165-1178
CrossRef
Pubmed
Google scholar
|
[77] |
Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature2009; 460(7254): 479-486
Pubmed
|
[78] |
Stenvang J, Kauppinen S. MicroRNAs as targets for antisense-based therapeutics. Expert Opin Biol Ther2008; 8(1): 59-81
CrossRef
Pubmed
Google scholar
|
[79] |
Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods2007; 4(9): 721-726
CrossRef
Pubmed
Google scholar
|
[80] |
Liu Z, Sall A, Yang D. MicroRNA: An emerging therapeutic target and intervention tool. Int J Mol Sci2008; 9(6): 978-999
CrossRef
Pubmed
Google scholar
|
[81] |
Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with ‘antagomirs’. Nature2005; 438(7068): 685-689
CrossRef
Pubmed
Google scholar
|
[82] |
Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjärn M, Hansen HF, Berger U, Gullans S, Kearney P, Sarnow P, Straarup EM, Kauppinen S. LNA-mediated microRNA silencing in non-human primates. Nature2008; 452(7189): 896-899
CrossRef
Pubmed
Google scholar
|
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〈 | 〉 |