MicroRNA-23a inhibits osteogenic differentiation of human bone marrow-derived mesenchymal stem cells by targeting LRP5

International Journal of Biochemistry and Cell Biology

Volumn 72, Issue , 2016, Pages 55-62

  Li, Tao ^a   Li, Hongling ^b   Wang, Yingzhen ^a   Li, Tangping ^b   Fan, Junfen ^b   Xiao, Ke ^c   Zhao, Robert Chunhua ^b   Weng, Xisheng ^c  

^a QINGDAO UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

^c PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

Human bone marrow derived mesenchymal stem cells; LRP5; microRNA 23a; Osteogenic differentiation

Indexed keywords

LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; MICRORNA; MICRORNA 23A; UNCLASSIFIED DRUG; LRP5 PROTEIN, HUMAN; MIRN23 MICRORNA, HUMAN;

ADULT; ARTICLE; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL DIFFERENTIATION; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUCIFERASE ASSAY; MALE; MIDDLE AGED; PREDICTION; UPREGULATION; CYTOLOGY; DEFICIENCY; GENE SILENCING; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; NUCLEOTIDE SEQUENCE; PHENOTYPE; WNT SIGNALING PATHWAY;

ADULT; BASE SEQUENCE; CELL DIFFERENTIATION; DOWN-REGULATION; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-5; MALE; MESENCHYMAL STROMAL CELLS; MICRORNAS; OSTEOGENESIS; PHENOTYPE; WNT SIGNALING PATHWAY;

EID: 84955270895     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.01.004     Document Type: Article

References (39)

1. Y. Bae, T. Yang, H.C. Zeng, P.M. Campeau, Y. Chen, T. Bertin, B.C. Dawson, E. Munivez, J. Tao, and B.H. Lee miRNA-34c regulates Notch signaling during bone development Hum. Mol. Genet. 21 2012 2991 3000
2. D. Baltimore, M.P. Boldin, R.M. O'Connell, D.S. Rao, and K.D. Taganov MicroRNAs: new regulators of immune cell development and function Nat. Immunol. 9 2008 839 845
3. A. Bandyopadhyay, K. Tsuji, K. Cox, B.D. Harfe, V. Rosen, and C.J. Tabin Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis PLoS Genet. 2 2006 e216
4. L. Bao, J. Zhao, X. Dai, Y. Wang, R. Ma, Y. Su, H. Cui, J. Niu, S. Bai, Z. Xiao, H. Yuan, Z. Yang, C. Li, R. Cheng, and X. Ren Correlation between miR-23a and onset of hepatocellular carcinoma Clin. Res. Hepatol. Gastroenterol. 38 2014 318 330
5. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
6. M. Cao, M. Seike, C. Soeno, H. Mizutani, K. Kitamura, Y. Mineqishi, R. Noro, A. Yoshimura, L. Cai, and A. Gemma MiR-23a regulates TGF-β-induced epithelial-mesenchymal transition by targeting E-cadherin in lung cancer cells Int. J. Oncol. 41 2012 869 875
7. Y. Cao, Z. Sun, L. Liao, Y. Meng, Q. Han, and R.C. Zhao Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo Biochem. Biophys. Res. Commun. 332 2005 370 379
8. R. Chaturvedi, P.K. Singha, and S. Dey Water soluble bioactives of nacre mediate antioxidant activity and osteoblast differentiation PLoS One 8 2013 e84584
9. S.L. Chen, W.W. Fang, F. Ye, Y.H. Liu, J. Qian, S.J. Shan, J.J. Zhang, R.Z. Chunhua, L.M. Liao, S. Lin, and J.P. Sun Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction Am. J. Cardiol. 94 2004 92 95
10. A.M. Cheng, M.W. Byrom, J. Shelton, and L.P. Fold Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis Nucleic Acids Res. 33 2005 1290 1297
11. Y. Cui, P.J. Niziolek, B.T. MacDonald, C.R. Zylstra, N. Alenina, D.R. Robinson, Z. Zhong, S. Matthes, C.M. Jacobsen, R.A. Conlon, R. Brommage, Q. Liu, F. Mseeh, D.R. Powell, Q.M. Yang, B. Zambrowicz, H. Gerrits, J.A. Gossen, X. He, M. Bader, B.O. Williams, M.L. Warman, and A.G. Robling Lrp5 functions in bone to regulate bone mass Nat. Med. 2011 17 2011 684 691
12. S.L. Ferrari, S. Deutsch, C. Baudoin, M. Cohen-Solal, A. Ostertag, S.E. Antonarakis, R. Rizzoli, and M.C. de Vernejoul LRP5 gene polymorphisms and idiopathic osteoporosis in men Bone 37 2005 770 775
13. J.M. Hare, J.E. Fishman, G. Gerstenblith, D.L. DiFede Velazquez, J.P. Zambrano, V.Y. Suncion, M. Tracy, E. Ghersin, P.V. Johnston, J.A. Brinker, E. Breton, J. Davis-Sproul, I.H. Schulman, J. Byrnes, A.M. Mendizabal, M.H. Lowery, D. Rouy, P. Altman, C. Wong Po Foo, P. Ruiz, A. Amador, J. Da Silva, I.K. McNiece, A.W. Heldman, R. George, and A. Lardo Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial JAMA 308 2012 2369 2379
14. M.J. Hilton, X. Tu, X. Wu, S. Bai, H. Zhao, T. Kobayashi, H.M. Kronenberg, S.L. Teitelbaum, F.P. Ross, R. Kopan, and F. Long Notch signaling maintains bone marrow mesenchymal progenitors by suppressing osteoblast differentiation Nat. Med. 14 2008 306 314
15. S. Jahid, J. Sun, R.A. Edwards, D. Dizon, N.C. Panarelli, J.W. Milsom, S.S. Sikandar, Z.H. Gümüs, and S.M. Lipkin miR-23a promotes the transition from indolent to invasive colorectal cancer Cancer Discov. 2 2012 540 553
16. Y.J. Kim, S.W. Bae, S.S. Yu, Y.C. Bae, and J.S. Jung miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue J. Bone Miner. Res. 24 2009 816 825
17. W.P. Kloosterman, and R.H. Plasterk The diverse functions of microRNAs in animal development and disease Dev. Cell 11 2006 441 450
18. H. Li, T. Li, S. Wang, J. Wei, J. Fan, J. Li, Q. Han, L. Liao, C. Shao, and R.C. Zhao miR-17-5p and miR-106a are involved in the balance between osteogenic and adipogenic differentiation of adipose-derived mesenchymal stem cells Stem Cell Res. 10 2013 313 324
19. J. Li, I. Sarosi, R.C. Cattley, J. Pretorius, F. Asuncion, M. Grisanti, S. Morony, S. Adamu, Z. Geng, W. Qiu, P. Kostenuik, D.L. Lacey, W.S. Simonet, B. Bolon, X. Qian, V. Shalhoub, M.S. Ominsky, H. Zhu Ke, X. Li, and W.G. Richards Dkk1-mediated inhibition of Wnt signaling in bone results in osteopenia Bone 39 2006 754 766
20. T. Li, H.L. Li, T.P. Li, J.F. Fan, R.C. Zhao, and X.S. Weng MicroRNA expression profile of dexamethasone-induced human bone marrow-derived mesenchymal stem cells during osteogenic differentiation J. Cell Biochem. 115 2014 1683 1691
21. X. Li, P. Liu, W. Liu, P. Maye, J. Zhang, Y. Zhang, M. Hurley, C. Guo, A. Boskey, L. Sun, S.E. Harris, D.W. Rowe, H.Z. Ke, and D. Wu Dkk2 has a role in terminal osteoblast differentiation and mineralized matrix formation Nat. Genet. 37 2005 945 952
22. J. Liang, X. Li, H. Zhang, D. Wang, X. Feng, H. Wang, B. Hua, B. Liu, and L. Sun Allogeneic mesenchymal stem cells transplantation in patients with refractory RA Clin. Rheumatol. 31 2012 157 161
23. S.T. Lin, Y. Huang, L. Zhang, M.Y. Heng, L.J. Ptácek, and Y.H. Fu MicroRNA-23a promotes myelination in the central nervous system Proc. Natl. Acad. Sci. U.S.A. 110 2013 17468 17473
24. F. Long, U.I. Chung, S. Ohba, J. McMahon, H.M. Kronenberg, and A.P. McMahon Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton Development 131 2004 1309 1318
25. S. Otsuru, T.J. Hofmann, T.S. Olson, M. Dominici, and E.M. Horwitz Improved isolation and expansion of bone marrow mesenchymal stromal cells using a novel marrow filter device Cytotherapy 15 2013 146 153
26. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, and D.R. Marshak Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147
27. W. Qiu, T.E. Andersen, J. Bollerslev, S. Mandrup, B.M. Abdallah, and M. Kassem Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells J. Bone Miner. Res. 22 2007 1720 1731
28. N. Raver-Shapira, E. Marciano, E. Meiri, Y. Spector, N. Rosenfeld, N. Moskovits, Z. Bentwich, and M. Oren Transcriptional activation of miR-34a contributes to p53-mediated apoptosis Mol. Cell 26 2007 731 743
29. A. Saarinen, V.V. Välimäki, M.J. Välimäki, E. Löyttyniemi, K. Auro, P. Uusen, M. Kuris, A.E. Lehesjoki, and O. Mäkitie The A1330 V polymorphism of the low-density lipoprotein receptor-related protein 5 gene (LRP5) associates with low peak bone mass in young healthy men Bone 40 2007 1006 1012
30. C. Seeliger, K. Karpinski, A. Haug, H. Vester, A. Schmitt, J. Bauer, and M. van Griensven Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures J. Bone Miner. Res. 29 2014 1718 1728
31. G. Stefani, and F.J. Slack Small non-coding RNAs in animal devel-opment Nat. Rev. Mol. Cell Biol. 9 2008 219 230
32. M. Thomas, J. Lieberman, and A. Lal Desperately seeking microRNA targets Nat. Struct. Mol. Biol. 17 2010 1169 1174
33. J.B. van Meurs, T.A. Trikalinos, S.H. Ralston, S. Balcells, M.L. Brandi, K. Brixen, D.P. Kiel, B.L. Langdahl, P. Lips, O. Ljunggren, R. Lorenc, B. Obermayer-Pietsch, C. Ohlsson, U. Pettersson, D.M. Reid, F. Rousseau, S. Scollen, W. Van Hul, L. Agueda, K. Akesson, L.I. Benevolenskaya, S.L. Ferrari, G. Hallmans, A. Hofman, L.B. Husted, M. Kruk, S. Kaptoge, D. Karasik, M.K. Karlsson, M. Lorentzon, L. Masi, F.E. McGuigan, D. Mellström, L. Mosekilde, X. Nogues, H.A. Pols, J. Reeve, W. Renner, F. Rivadeneira, N.M. van Schoor, K. Weber, J.P. Ioannidis, A.G. Uitterlinden, and GENOMOS. Study Large-scale analysis of association between LRP5 and LRP6 variants and osteoporosis JAMA 299 2008 1277 1290
34. J. Wang, X. Guan, F. Guo, J. Zhou, A. Chang, B. Sun, Y. Cai, Z. Ma, C. Dai, X. Li, and B. Wang miR-30e reciprocally regulates the differentiation of adipocytes and osteoblasts by directly targeting low-density lipoprotein receptor-related protein 6 Cell Death Dis. 4 2013 e845
35. S. Wang, X. Qu, and R.C. Zhao Clinical applications of mesenchymal stem cells J. Hematol. Oncol. 5 2012 19
36. X. Wang, B. Guo, Q. Li, J. Peng, Z. Yang, A. Wang, D. Li, Z. Hou, K. Lv, G. Kan, H. Cao, H. Wu, J. Song, X. Pan, Q. Sun, S. Ling, Y. Li, M. Zhu, P. Zhang, S. Peng, X. Xie, T. Tang, A. Hong, Z. Bian, Y. Bai, A. Lu, Y. Li, F. He, G. Zhang, and Y. Li miR-214 targets ATF4 to inhibit bone formation Nat. Med. 19 2013 93 100
37. V.K. Yadav, J.H. Ryu, N. Suda, K.F. Tanaka, J.A. Gingrich, G. Schutz, F.H. Glorieux, C.Y. Chiang, J.D. Zajac, K.L. Insogna, J.J. Mann, R. Hen, P. Ducy, and G. Karsenty Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum Cell 135 2008 825 837
38. Z. Yang, C. Bian, H. Zhou, S. Huang, S. Wang, L. Liao, and R.C. Zhao MicroRNA hsa-miR-138 inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells through adenovirus EID-1 Stem Cells Dev. 20 2011 259 267
39. D. Zhao, D. Cui, B. Wang, F. Tian, L. Guo, L. Yang, B. Liu, and X. Yu Treatment of early stage osteonecrosis of the femoral head with autologous implantation of bone marrow-derived and cultured mesenchymal stem cells Bone 50 2012 325 330