MicroRNAs and their roles in osteoclast differentiation

Zhuying Xia, Chao Chen, Peng Chen, Hui Xie, Xianghang Luo

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Front. Med. ›› 2011, Vol. 5 ›› Issue (4) : 414-419. DOI: 10.1007/s11684-011-0168-0
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MicroRNAs and their roles in osteoclast differentiation

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Abstract

Osteoclasts, which are derived from monocyte-macrophage precursors, are exclusive bone resorption cells. Limited evidence indicates that a class of small non-coding single-stranded RNAs known as “microRNAs” (miRNAs) is also involved in bone resorption. Although various miRNAs regulate cell proliferation and differentiation, few miRNAs have been reported to play a key role in the regulation of osteoclast differentiation. In this short review, the biology and functional mechanisms of miRNAs in osteoclastogenesis are summarized. The profiling, function, and target prediction of miRNAs are discussed as well.

Keywords

miRNA / osteoclast differentiation / antagomirs

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Zhuying Xia, Chao Chen, Peng Chen, Hui Xie, Xianghang Luo. MicroRNAs and their roles in osteoclast differentiation. Front Med, 2011, 5(4): 414‒419 https://doi.org/10.1007/s11684-011-0168-0

References

[1]
Suda T, Udagawa N, Nakamura I, Miyaura C, Takahashi N. Modulation of osteoclast differentiation by local factors. Bone 1995; 17(2 Suppl 1): S87–S91
CrossRef Pubmed Google scholar
[2]
Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2002; 2(4): 389–406
CrossRef Pubmed Google scholar
[3]
Tanaka S, Nakamura K, Takahasi N, Suda T. Role of RANKL in physiological and pathological bone resorption and therapeutics targeting the RANKL-RANK signaling system. Immunol Rev 2005; 208(1): 30–49
CrossRef Pubmed Google scholar
[4]
Soriano P, Montgomery C, Geske R, Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 1991; 64(4): 693–702
CrossRef Pubmed Google scholar
[5]
Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF. c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 1994; 266(5184): 443–448
CrossRef Pubmed Google scholar
[6]
Tondravi MM, McKercher SR, Anderson K, Erdmann JM, Quiroz M, Maki R, Teitelbaum SL. Osteopetrosis in mice lacking haematopoietic transcription factor PU.1. Nature 1997; 386(6620): 81–84
CrossRef Pubmed Google scholar
[7]
Iotsova V, Caamaño J, Loy J, Yang Y, Lewin A, Bravo R. Osteopetrosis in mice lacking NF-κB1 and NF-κB2. Nat Med 1997; 3(11): 1285–1289
CrossRef Pubmed Google scholar
[8]
Takayanagi H, Kim S, Koga T, Nishina H, Isshiki M, Yoshida H, Saiura A, Isobe M, Yokochi T, Inoue J, Wagner EF, Mak TW, Kodama T, Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 2002; 3(6): 889–901
CrossRef Pubmed Google scholar
[9]
Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005; 6(5): 376–385
CrossRef Pubmed Google scholar
[10]
Mizuno Y, Yagi K, Tokuzawa Y, Kanesaki-Yatsuka Y, Suda T, Katagiri T, Fukuda T, Maruyama M, Okuda A, Amemiya T, Kondoh Y, Tashiro H, Okazaki Y. miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 2008; 368(2): 267–272
CrossRef Pubmed Google scholar
[11]
Luzi E, Marini F, Sala SC, Tognarini I, Galli G, Brandi ML. Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res 2008; 23(2): 287–295
CrossRef Pubmed Google scholar
[12]
Li ZY, Hassan MQ, Volinia S, van Wijnen AJ, Stein JL, Croce CM, Lian JB, Stein GS. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 2008; 105(37): 13906–13911
CrossRef Pubmed Google scholar
[13]
Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010; 28(2): 357–364
Pubmed
[14]
Kapinas K, Kessler CB, Delany AM. miR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem 2009; 108(1): 216–224
CrossRef Pubmed Google scholar
[15]
Itoh T, Nozawa Y, Akao Y. MicroRNA-141 and -200a are involved in bone morphogenetic protein-2-induced mouse pre-osteoblast differentiation by targeting distal-less homeobox 5. J Biol Chem 2009; 284(29): 19272–19279
CrossRef Pubmed Google scholar
[16]
Inose H, Ochi H, Kimura A, Fujita K, Xu R, Sato S, Iwasaki M, Sunamura S, Takeuchi Y, Fukumoto S, Saito K, Nakamura T, Siomi H, Ito H, Arai Y, Shinomiya K, Takeda S. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci USA 2009; 106(49): 20794–20799
CrossRef Pubmed Google scholar
[17]
Li ZY, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 2009; 284(23): 15676–15684
CrossRef Pubmed Google scholar
[18]
Mizuno Y, Tokuzawa Y, Ninomiya Y, Yagi K, Yatsuka-Kanesaki Y, Suda T, Fukuda T, Katagiri T, Kondoh Y, Amemiya T, Tashiro H, Okazaki Y. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 2009; 583(13): 2263–2268
CrossRef Pubmed Google scholar
[19]
Kim YJ, Bae SW, Yu SS, Bae YC, Jung JS. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 2009; 24(5): 816–825
CrossRef Pubmed Google scholar
[20]
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 Invest 2009; 119(12): 3666–3677
CrossRef Pubmed Google scholar
[21]
Xu XH, Dong SS, Guo Y, Yang TL, Lei SF, Papasian CJ, Zhao M, Deng HW. Molecular genetic studies of gene identification for osteoporosis: the 2009 update. Endocr Rev 2010; 31(4): 447–505
CrossRef Pubmed Google scholar
[22]
Ambros V, Chen X. The regulation of genes and genomes by small RNAs. Development 2007; 134(9): 1635–1641
CrossRef Pubmed Google scholar
[23]
Cullen BR. Transcription and processing of human microRNA precursors. Mol Cell 2004; 16(6): 861–865
CrossRef Pubmed Google scholar
[24]
Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, Bentwich Z. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 2005; 37(7): 766–770
CrossRef Pubmed Google scholar
[25]
Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001; 294(5543): 853–858
CrossRef Pubmed Google scholar
[26]
Lee Y, Jeon K, Lee JT, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002; 21(17): 4663–4670
CrossRef Pubmed Google scholar
[27]
Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res 2004; 14( 10A): 1902–1910
CrossRef Pubmed Google scholar
[28]
Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136(4): 642–655
CrossRef Pubmed Google scholar
[29]
Bushati N, Cohen SM. microRNA functions. Annu Rev Cell Dev Biol 2007; 23(1): 175–205
CrossRef Pubmed Google scholar
[30]
Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R. The microprocessor complex mediates the genesis of microRNAs. Nature 2004; 432(7014): 235–240
CrossRef Pubmed Google scholar
[31]
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 Res 2009; 37(22): 7533–7545
CrossRef Pubmed Google scholar
[32]
Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol 2007; 17(3): 118–126
CrossRef Pubmed Google scholar
[33]
Zeng Y, Yi R, Cullen BR. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci USA 2003; 100(17): 9779–9784
CrossRef Pubmed Google scholar
[34]
Yekta S, Shih IH, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004; 304(5670): 594–596
CrossRef Pubmed Google scholar
[35]
Krützfeldt J, Poy MN, Stoffel M. Strategies to determine the biological function of microRNAs. Nat Genet 2006; 38(Suppl): S14–S19
CrossRef Pubmed Google scholar
[36]
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). RNA 2006; 12(5): 913–920
CrossRef Pubmed Google scholar
[37]
Kauppinen S, Vester B, Wengel J. Locked nucleic acid: high-affinity targeting of complementary RNA for RNomics. Handb Exp Pharmacol 2006; (173): 405–422
[38]
Auer H, Newsom DL, Kornacker K. Expression profiling using Affymetrix GeneChip microarrays. Methods Mol Biol 2009; 509: 35–46
CrossRef Pubmed Google scholar
[39]
Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR, Golub TR. MicroRNA expression profiles classify human cancers. Nature 2005; 435(7043): 834–838
CrossRef Pubmed Google scholar
[40]
Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, Elton TS, Chen C. Real-time PCR quantification of precursor and mature microRNA. Methods 2008; 44(1): 31–38
CrossRef Pubmed Google scholar
[41]
Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005; 33(20): e179
CrossRef Pubmed Google scholar
[42]
Sugatani T, Vacher J, Hruska KA. A microRNA expression signature of osteoclastogenesis. Blood 2011; 117(13): 3648–3657
CrossRef Pubmed Google scholar
[43]
Marzia M, Sims NA, Voit S, Migliaccio S, Taranta A, Bernardini S, Faraggiana T, Yoneda T, Mundy GR, Boyce BF, Baron R, Teti A. Decreased c-Src expression enhances osteoblast differentiation and bone formation. J Cell Biol 2000; 151(2): 311–320
CrossRef Pubmed Google scholar
[44]
Del Fattore A, Teti A, Rucci N. Osteoclast receptors and signaling. Arch Biochem Biophys 2008; 473(2): 147–160
CrossRef Pubmed Google scholar
[45]
Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, Brown KD, Leonardi A, Tran T, Boyce BF, Siebenlist U. Requirement for NF-κB in osteoclast and B-cell development. Genes Dev 1997; 11(24): 3482–3496
CrossRef Pubmed Google scholar
[46]
Ishida N, Hayashi K, Hoshijima M, Ogawa T, Koga S, Miyatake Y, Kumegawa M, Kimura T, Takeya T. Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator. J Biol Chem 2002; 277(43): 41147–41156
CrossRef Pubmed Google scholar
[47]
Takayanagi H, Kim S, Koga T, Nishina H, Isshiki M, Yoshida H, Saiura A, Isobe M, Yokochi T, Inoue J, Wagner EF, Mak TW, Kodama T, Taniguchi T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 2002; 3(6): 889–901
CrossRef Pubmed Google scholar
[48]
Takayanagi H, Kim S, Matsuo K, Suzuki H, Suzuki T, Sato K, Yokochi T, Oda H, Nakamura K, Ida N, Wagner EF, Taniguchi T. RANKL maintains bone homeostasis through c-Fos-dependent induction of interferon-beta. Nature 2002; 416(6882): 744–749
CrossRef Pubmed Google scholar
[49]
Weilbaecher KN, Motyckova G, Huber WE, Takemoto CM, Hemesath TJ, Xu Y, Hershey CL, Dowland NR, Wells AG, Fisher DE. Linkage of M-CSF signaling to Mitf, TFE3, and the osteoclast defect in Mitf(mi/mi) mice. Mol Cell 2001; 8(4): 749–758
CrossRef Pubmed Google scholar
[50]
Sugatani T, Hruska KA. Impaired micro-RNA pathways diminish osteoclast differentiation and function. J Biol Chem 2009; 284(7): 4667–4678
CrossRef Pubmed Google scholar
[51]
Keen R. Osteoporosis: strategies for prevention and management. Best Pract Res Clin Rheumatol 2007; 21(1): 109–122
CrossRef Pubmed Google scholar
[52]
Lakshmipathy U, Hart RP. Concise review: microRNA expression in multipotent mesenchymal stromal cells. Stem Cells 2008; 26(2): 356–363
CrossRef Pubmed Google scholar
[53]
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136(2): 215–233
CrossRef Pubmed Google scholar
[54]
Yue D, Liu H, Huang Y. Survey of computational algorithms for microRNA target prediction. Curr Genomics 2009; 10(7): 478–492
CrossRef Pubmed Google scholar
[55]
Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120(1): 15–20
CrossRef Pubmed Google scholar
[56]
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 Genet 2005; 37(5): 495–500
CrossRef Pubmed Google scholar
[57]
John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol 2004; 2(11): e363
CrossRef Pubmed Google scholar
[58]
Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006; 34(Suppl 1): D140–D144
CrossRef Pubmed Google scholar
[59]
Hsu PW, Huang HD, Hsu SD, Lin LZ, Tsou AP, Tseng CP, Stadler PF, Washietl S, Hofacker IL. miRNAMap: genomic maps of microRNA genes and their target genes in mammalian genomes. Nucleic Acids Res 2006; 34(Suppl 1): D135–D139
CrossRef Pubmed Google scholar
[60]
Megraw M, Sethupathy P, Corda B, Hatzigeorgiou AG. miRGen: a database for the study of animal microRNA genomic organization and function. Nucleic Acids Res 2007; 35(Suppl 1): D149–D155
CrossRef Pubmed Google scholar
[61]
Meister G, Landthaler M, Dorsett Y, Tuschl T. Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA 2004; 10(3): 544–550
CrossRef Pubmed Google scholar
[62]
Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with ‘antagomirs’. Nature 2005; 438(7068): 685–689
CrossRef Pubmed Google scholar
[63]
Krützfeldt J, Kuwajima S, Braich R, Rajeev KG, Pena J, Tuschl T, Manoharan M, Stoffel M. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res 2007; 35: 2885–2892
CrossRef Pubmed Google scholar
[64]
Horwich MD, Zamore PD. Design and delivery of antisense oligonucleotides to block microRNA function in cultured Drosophila and human cells. Nat Protoc 2008; 3(10): 1537–1549
CrossRef Pubmed Google scholar
[65]
Nasevicius A, Ekker SC. Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 2000; 26(2): 216–220
CrossRef Pubmed Google scholar
[66]
Zellweger T, Miyake H, Cooper S, Chi K, Conklin BS, Monia BP, Gleave ME. Antitumor activity of antisense clusterin oligonucleotides is improved in vitro and in vivo by incorporation of 2′-O-(2-methoxy)ethyl chemistry. J Pharmacol Exp Ther 2001; 298(3): 934–940
Pubmed
[67]
Dean NM, Bennett CF. Antisense oligonucleotide-based therapeutics for cancer. Oncogene 2003; 22(56): 9087–9096
CrossRef Pubmed Google scholar
[68]
Kastelein JJ, Wedel MK, Baker BF, Su J, Bradley JD, Yu RZ, Chuang E, Graham MJ, Crooke RM. Potent reduction of apolipoprotein B and low-density lipoprotein cholesterol by short-term administration of an antisense inhibitor of apolipoprotein B. Circulation 2006; 114(16): 1729–1735
CrossRef Pubmed Google scholar

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