Targeting miRNAs in osteoblast differentiation and bone formation

Expert Opinion on Therapeutic Targets

Volumn 14, Issue 10, 2010, Pages 1109-1120

  Hu, Rong ^a   Li, Hui ^a   Liu, Wei ^a   Yang, Li ^a   Tan, Yan Fei ^a   Luo, Xiang Hang ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Antagomirs; Bone biology; Mesenchymal stromal cells; MiRNA; MiRNA profiling; Osteoblast differentiation; Target prediction

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; BONE MORPHOGENETIC PROTEIN 2; MESSENGER RNA; MICRORNA; SINGLE STRANDED RNA;

BONE TISSUE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DRUG TARGETING; EPIGENETICS; GENE OVEREXPRESSION; HUMAN; MESENCHYME CELL; NONHUMAN; OSSIFICATION; OSTEOBLAST; REVIEW; STROMA CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION; HUMANS; MESENCHYMAL STEM CELLS; MICE; MICRORNAS; MOLECULAR TARGETED THERAPY; OSTEOBLASTS; OSTEOGENESIS;

EID: 77957026570     PISSN: 14728222     EISSN: None     Source Type: Journal    
DOI: 10.1517/14728222.2010.512916     Document Type: Review

References (115)

1. Lakshmipathy U, Hart RP. Concise review: MicroRNA expression in multipotent mesenchymal stromal cells. Stem Cells 2008;2:356-363
2. Esau C, Kang X, Peralta E, et al. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 2004;279:52361-52365
3. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005;436(7048):214-220
4. Kuwabara T, Hsieh J, Nakashima K, et al. A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 2004;116:779-793
5. Wu L, Belasco JG. MicroRNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol 2005;25:9198-9208
6. Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010;28:357-364
7. Mizuno Y, Yagi K, Tokuzawa Y, et al. miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 2008;368:267-272
8. Li ZY, Hassan MQ, Volinia S, et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 2008;105:13906-13911
9. Suomi S, Taipaleenmaki H, Seppanen A, et al. MicroRNAs regulate osteogenesis and chondrogenesis of mouse bone marrow stromal cells. Gene Regul Syst Biol 2008;22:177-191
10. Li ZY, Hassan MQ, Jafferji M, et al. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 2009;284:15676-15684
11. Smirnova L, Grafe A, Seiler A, et al. Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005;21:1469-1477
12. Sun Q, Zhang Y, Yang G, et al. Transforming growth factor-beta-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res 2008;36:2690-2699
13. Chen JF, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006;38:228-233
14. Rao PK, Kumar RM, Farkhondeh M, et al. Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci USA 2006;103:8721-8726
15. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-297
16. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009;136:642-655
17. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat Genet 2006;38(Suppl):S31-6
18. Giraldez AJ, Mishima Y, Rihel J, et al. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006;312:75-79
19. Alvarez-Garcia I, Miska EA. MicroRNA functions in animal development and human disease. Development 2005;132:4653-4662
20. Laneve P, Di Marcotullio L, Gioia U, et al. The interplay between microRNAs and the neurotrophin receptor tropomyosin-related kinase C controls proliferation of human neuroblastoma cells. Proc Natl Acad Sci USA 2007;104:7957-7962
21. Wang X, Tang S, Le SY, et al. Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS One 2008;3:e2557
22. Song G, Zhang Y, Wang L. MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J Biol Chem 2009;284:31921-31927
23. Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006;126(4):767-774
24. Li X, Carthew RW. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 2005;123(7):1267-1277
25. Kawasaki H, Taira K. Retraction: Hes1 is a target of microRNA-23 during retinoic-acid-induced neuronal differentiation of NT2 cells. Nature 2003;426:100 (Pubitemid 37432549)
26. McGlinn E, Yekta S, Mansfield JH, et al. In ovo application of antagomiRs indicates a role for miR-196 in patterning the chick axial skeleton through Hox gene regulation. Proc Natl Acad Sci USA 2009;106:18610-18615
27. Huang TH, Zhu MJ, Li XY, Zhao SH. Discovery of porcine microRNAs and profiling from skeletal muscle tissues during development. PLoS One 2008;3:e3225
28. Foekens JA, Sieuwerts AM, Smid M, et al. Four miRNAs associated with aggressiveness of lymph node-negative, estrogen receptor-positive human breast cancer. Proc Natl Acad Sci USA 2008;105:13021-13026
29. Sun T, Wang Q, Balk S, et al. The role of microRNA-221 and microRNA-222 in androgen-independent prostate cancer cell lines. Cancer Res 2009;69:3356-3363
30. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-838
31. Voorhoeve PM, le Sage C, Schrier M, et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 2006;124:1169-1181
32. Kumar MS, Lu J, Mercer KL, et al. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007;39:673-677
33. Poy MN, Eliasson L, Krutzfeldt J, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004;432:226-230
34. Harris TA, Yamakuchi M, Ferlito M, et al. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 2008;105:1516-1521
35. Xu N, Papagiannakopoulos T, Pan G, et al. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 2009;137:647-658
36. Nahid MA, Pauley KM, Satoh M, Chan EK. miR-146a is critical for endotoxin-induced tolerance: implication in innate immunity. J Biol Chem 2009;284:34590-34599
37. Yeung ML, Bennasser Y, Le SY, Jeang KT. siRNA, miRNA and HIV: promises and challenges. Cell Res 2005;15:935-946
38. Umbach JL, Kramer MF, Jurak I, et al. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008;454:780-783
39. Bentwich I, Avniel A, Karov Y, et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 2005;37:766-770
40. Gregory RI, Yan KP, Amuthan G, et al. The microprocessor complex mediates the genesis of microRNAs. Nature 2004;432(7014):235-240
41. Tan GS, Garchow BG, Liu X, et al. Expanded RNA-binding activities of mammalian Argonaute 2. Nucleic Acids Res 2009;37:7533-7545
42. Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol 2007;17:118-126
43. Zeng Y, Yi R, Cullen BR. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci USA 2003;100:9779-9784
44. Yekta S, Shih IH, Bartel DP. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004;304:594-596
45. Krutzfeldt J, Poy MN, Stoffel M. Strategies to determine the biological function of microRNAs. Nat Genet 2006;38(Suppl):S14-19
46. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136:215-233
47. Yue D, Liu H, Huang Y. Survey of computational algorithms for microRNA target prediction. Curr Genomics 2009;10:478-492
48. Duan RH, Pak C, Jin P. Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum Mol Genet 2007;16:1124-1131
49. Jazdzewski K, Murray EL, Franssila K, et al. Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma. Proc Natl Acad Sci USA 2008;105:7269-7274
50. Li H, Xie H, Liu W, et al. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contribute to primary osteoporosis in humans. J Clin Invest 2009;119:3666-3677
51. Chen C, Ridzon DA, Broomer AJ, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005;33(20):e179
52. Liang Y, Ridzon D, Wong L, Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007;8:166
53. Raymond CJ, Roberts BS, Garrett-Engele P, et al. Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs. RNA 2005;11:1737-1744
54. Landgraf P, Rusu M, Sheridan R, et al. A mammalian microRNA expression atlas based on small library sequencing. Cell 2007;129:1401-1414
55. Porkka KP, Pfeiffer MJ, Waltering KK, et al. MicroRNA expression profiling in prostate cancer. Cancer Res 2007;67:6130-6135
56. Volinia S, Calin GA, Liu C-G, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006;103:2257-2261
57. Mattie MD, Benz CC, Bowers J, et al. Optimized high-throughput microRNA expression profiling provides novel biomarker assessment of clinical prostate and breast cancer biopsies. Mol Cancer 2006;5:24
58. Calin GA, Liu C-G, Sevignani C, et al. MicroRNA profiling reveals distinct signatures in B cell chronic lymphocytic leukemias. Proc Natl Acad Sci USA 2004;101(32):11755-11760
59. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-838
60. Oskowitz ZO, Lu J, Penfornis P, et al. Human multipotent stromal cells from bone marrow and microRNA: regulation of differentiation and leukemia inhibitory factor expression. Proc Natl Acad Sci USA 2008;105:18372-18377
61. Komori T, Yagi H, Nomura S, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997;89:755-764
62. Otto F, Thornell AP, Crompton T, et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997;89:765-771
63. Mundlos S, Otto F, Mundlos C, et al. Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 1997;89:773-779
64. Shui C, Spelsberg TC, Riggs BL, Khosla S. Changes in Runx2/Cbfa1 expression and activity during osteoblastic differentiation of human bone marrow stromal cells. J Bone Miner Res 2003;18:213-221
65. Phimphilai M, Zhao ZR, Boules H, et al. BMP signaling is required for Runx2-dependent induction of the osteoblast phenotype. J Bone Miner Res 2006;21:637-646
66. Stein GS, Lian JB, van Wijnen AJ, et al. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene 2004;23:4315-4329
67. Shalhoub V, Gerstenfeld LC, Collart D, et al. Downregulation of cell growth and cell cycle regulated genes during chick osteoblast differentiation with the reciprocal expression of histone gene variants. Biochemistry 1989;28:5318-5322
68. Winnard RG, Gerstenfeld LC, Toma CD, Franceschi RT. Fibronectin gene expression, synthesis and accumulation during in vitro differentiation of chicken osteoblasts. J Bone Miner Res 1995;10(12):1969-1977
69. Yang XB, Roach HI, Clarke NM, et al. Human osteoprogenitor growth and differentiation on synthetic biodegradable structures after surface modification. Bone 2001;29:523-531
70. Grigoriadis AE, Wang ZQ, Cecchini MG, et al. C-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling. Science 1994;266:443-448
71. Zhang Y, Feng XH, Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 1998;394(6696):909-913
72. Jensen ED, Gopalakrishnan R, Westendorf JJ. Regulation of gene expression in osteoblasts. Biofactors 2010;36:25-32
73. Kim YJ, Kim HN, Park EK, et al. The bone-related Zn finger transcription factor Osterix promotes proliferation of mesenchymal cells. Gene 2006;366:145-151
74. Lee KS, Hong SH, Bae SC. Both the Smad and p38 MAPK pathways play a crucial role in Runx2 expression following induction by transforming growth factor-beta and bone morphogenetic protein. Oncogene 2002;21:7156-7163
75. Xiao G, Jiang D, Ge C, et al. Cooperative interactions between activating transcription factor 4 and Runx2/Cbfa1 stimulate osteoblast-specific osteocalcin gene expression. J Biol Chem 2005;280:30689-30693
76. Bialek P, Kern B, Yang X, et al. A twist code determines the onset of osteoblast differentiation. Dev Cell 2004;6:423-435
77. Robledo RF, Rajan L, Li X, Lufkin T. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 2002;16:1089-1101
78. Hassan MQ, Javed A, Morasso MI, et al. Dlx3 transcriptional regulation of osteoblast differentiation: temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol Cell Biol 2004;24:9248-9261
79. Etheridge SL, Spencer GJ, Heath DJ, Genever PG. Expression profiling and functional analysis of Wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 2004;22:849-860
80. Osyczka AM, Leboy PS. Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 2005;146:3428-3437
81. Levy JB, Schindler C, Raz R, et al. Activation of the JAK-STAT signal transduction pathway by oncostatin-M cultured human and mouse osteoblastic cells. Endocrinology 1996;137:1159-1165
82. Lee KS, Hong SH, Bae SC. Both the Smad and p38 MAPK pathways play a crucial role in Runx2 expression following induction by transforming growth factor-beta and bone morphogenetic protein. Oncogene 2002;21:7156-7163
83. Luzi E, Marini F, Sala SC, et al. 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;23:287-295
84. 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;108:216-224
85. 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;284:19272-19279
86. Inose H, Ochi H, Kimura A, et al. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci USA 2009;106:20794-20799
87. Mizuno Y, Tokuzawa Y, Ninomiya Y, et al. miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 2009;583:2263-2268
88. Kim YJ, Bae SW, Yu SS, et al. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 2009;24:816-825
89. John B, Enright AJ, Aravin A, et al. Human MicroRNA targets. PLoS Biol 2004;2(11):e363
90. Rajewsky N. microRNA target predictions in animals. Nat Genet 2006;38(Supp1):S8-13
91. Lewis BP, Shih IH, Jones-Rhoades MW, et al. Prediction of mammalian microRNA targets. Cell 2003;115(7):787-798
92. Krek A, Grun D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet 2005;37:495-500
93. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20
94. Griffiths-Jones S, Grocock RJ, van Dongen S, et al. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006;34(Database issue):D140-4
95. Hsu PW, Huang HD, Hsu SD, et al. miRNAMap: genomic maps of microRNA genes and their target genes in mammalian genomes. Nucleic Acids Res 2006;34(Database issue):D135-9
96. 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(Database issue):D149-55
97. Scott GK, Goga A, Bhaumik D, et al. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 2007;282:1479-1486
98. Nasevicius A, Ekker SC. Effective targeted gene knockdown in zebrafish. Nat Genet 2000;26:216-220
99. Zellweger T, Miyake H, Cooper S, et al. 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
100. Dean NM, Bennett CF. Antisense oligonucleotide-based therapeutics for cancer. Oncogene 2003;22:9087-9096
101. Kastelein JJ, Wedel MK, Baker BF, et al. Potent reduction of apolipoprotein B and low-density lipoprotein cholesterol by short-term administration of an antisense inhibitor of apolipoprotein B. Circulation 2006;114:1729-1735
102. Krutzfeldt J, Rajewsky N, Braich R, et al. Silencing of microRNAs in vivo with antagomirs. Nature 2005;438:685-689
103. Jopling CL, Yi M, Lancaster AM, et al. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005;309:1577-1581
104. Horwich MD, Zamore PD. Design and delivery of antisense oligonucleotides to block microRNA function in cultured Drosophila and human cells. Nat Protoc 2008;3:1537-1549
105. McCaffrey AP, Meuse L, Pham TT, et al. RNA interference in adult mice. Nature 2002;418:38-39
106. de Fougerolles A, Vornlocher HP, Maraganore J, Lieberman J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Discov 2007;6:443-453
107. Jackson A, Burchard J, Schelter J, et al. Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 2006;12:1179-1187
108. Liu Z, Sall A, Yang DC. MicroRNA: an emerging therapeutic target and intervention tool. Int J Mol Sci 2008;9:978-999
109. Davis S, Lollo B, Freier S, Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res 2006;34:2294-2304
110. Elmen J, Lindow M, Schutz S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008;452:896-899
111. Leonetti C, Zupi G. Targeting different signaling pathways with antisense oligonucleotides combination for cancer therapy. Curr Pharm Des 2007;13:463-470
112. Soifer HS, Rossi JJ, Saetrom P. MicroRNAs in disease and potential therapeutic applications. Mol Ther 2007;15:2070-2079
113. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 2007;4:721-726
114. Brummelkamp T, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002;296:550-553
115. Miyagishi M, Taira K. U6 promoter-driven siRNAs with four uridine 3 overhangs efficiently suppress targeted gene expression in mammalian cells. Nat Biotechnol 2002;20:497-500