MiR-124 negatively regulates osteogenic differentiation and in vivo bone formation of mesenchymal stem cells

Journal of Cellular Biochemistry

Volumn 116, Issue 5, 2015, Pages 730-742

  Qadir, Abdul S ^a   Um, Soyoun ^a   Lee, Heesu ^b   Baek, Kyunghwa ^b   Seo, Byoung Moo ^a   Lee, Gene ^a   Kim, Gwan Shik ^a   Woo, Kyung Mi ^a   Ryoo, Hyun Mo ^a   Baek, Jeong Hwa ^a  

^a Seoul National University   (South Korea)

^b Gangneung Wonju National University   (South Korea)

Author keywords

BONE FORMATION; Dlx TRANSCRIPTION FACTORS; miR 124; OSTEOGENIC DIFFERENTIATION

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; MICRORNA 124; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR DLX3; TRANSCRIPTION FACTOR DLX5; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ANTIGEN DLX-2; BMP2 PROTEIN, HUMAN; DISTAL-LESS HOMEOBOX PROTEINS; DLX5 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MEMBRANE ANTIGEN; MICRORNA; MIRN124 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DISEASE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; C2C12 CELL LINE; CELL DIFFERENTIATION; CONTROLLED STUDY; ECTOPIC BONE FORMATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUCIFERASE ASSAY; MARKER GENE; MC3T3 E1 CELL LINE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MINERALIZATION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOGENIC DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RNA ANALYSIS; ANIMAL; BONE; BONE DEVELOPMENT; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE SILENCING; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; NUDE MOUSE; OSTEOBLAST;

MUS MUSCULUS;

3' UNTRANSLATED REGIONS; ADIPOCYTES; ANIMALS; ANTIGENS, SURFACE; BONE AND BONES; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; MICE, NUDE; MICRORNAS; OSTEOBLASTS; OSTEOGENESIS; TRANSCRIPTION FACTORS;

EID: 84924328173     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25026     Document Type: Article

References (39)

1. Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG,. 2006. Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38: 758-768.
2. Balkwill F,. 2009. Tumour necrosis factor and cancer. Nat Rev Cancer 9: 361-371.
3. Bork S, Horn P, Castoldi M, Hellwig I, Ho AD, Wagner W,. 2011. Adipogenic differentiation of human mesenchymal stromal cells is down-regulated by microRNA-369-5p and up-regulated by microRNA-371. J Cell Physiol 226: 2226-2234.
4. Cheng LC, Pastrana E, Tavazoie M, Doetsch F,. 2009. MiR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12: 399-408.
5. Cheng SL, Shao JS, Cai J, Sierra OL, Towler DA,. 2008. Msx2 exerts bone anabolism via canonical Wnt signaling. J Biol Chem 283: 20505-20522.
6. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JL,. 1999. DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414: 217-237.
7. Esau C, Kang XL, Peralta E, Hanson E, Marcusson EG, Ravichandran LV, Sun YQ, Koo S, Perera RJ, Jain R, Dean NM, Freier SM, Bennett CF, Lollo B, Griffey R,. 2004. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 279: 52361-52365.
8. Feledy JA, Morasso MI, Jang SI, Sargent TD,. 1999. Transcriptional activation by the homeodomain protein distal-less 3. Nucleic Acids Res 27: 764-770.
9. Ghanem N, Jarinova O, Amores A, Long Q, Hatch G, Park BK, Rubenstein JL, Ekker M,. 2003. Regulatory roles of conserved intergenic domains in vertebrate Dlx bigene clusters. Genome Res 13: 533-543.
10. Harris SE, Guo DY, Harris MA, Krishnaswamy A, Lichtler A,. 2003. Transcriptional regulation of BMP-2 activated genes in osteoblasts using gene expression microarray analysis: Role of DLX2 and DLX5 transcription factors. Front Biosci 8: S1249-S1265.
11. Hassan MQ, Javed A, Morasso MI, Karlin J, Montecino M, van Wijnen AJ, Stein GS, Stein JL, Lian JB,. 2004. Dlx3 transcriptional regulation of osteoblast differentiation: temporal recruitment of Msx2, Dlx3, and Dlx5 homeodomain proteins to chromatin of the osteocalcin gene. Mol Cell Biol 24: 9248-9261.
12. Hassan MQ, Tare RS, Lee SH, Mandeville M, Morasso MI, Javed A, van Wijnen AJ, Stein JL, Stein GS, Lian JB,. 2006. BMP2 commitment to the osteogenic lineage involves activation of Runx2 by DLX3 and a homeodomain transcriptional network. J Biol Chem 281: 40515-40526.
13. Huang J, Zhao L, Xing L, Chen D,. 2010. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 28: 357-364.
14. 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,. 2009. A microRNA regulatory mechanism of osteoblast differentiation. Proc Natl Acad Sci USA 106: 20794-20799.
15. Itoh T, Nozawa Y, Akao Y,. 2009. 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 284: 19272-19279.
16. Itoh T, Takeda S, Akao Y,. 2010. MicroRNA-208 modulates BMP-2-stimulated mouse preosteoblast differentiation by directly targeting V-ets erythroblastosis virus E26 oncogene homolog 1. J Biol Chem 285: 27745-27752.
17. Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany AM,. 2010. MiR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285: 25221-25231.
18. Kim SY, Kim AY, Lee HW, Son YH, Lee GY, Lee JW, Lee YS, Kim JB,. 2010. MiR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392: 323-328.
19. Kirk MD, Kahn AJ,. 1995. Extracellular matrix synthesized by clonal osteogenic cells is osteoinductive in vivo and in vitro: role of transforming growth factor-beta 1 in osteoblast cell-matrix interaction. J Bone Miner Res 10: 1203-1208.
20. Lee Y, Kim HJ, Park CK, Kim YG, Lee HJ, Kim JY, Kim HH,. 2013b. MicroRNA-124 regulates osteoclast differentiation. Bone 56: 383-389.
21. Lee MH, Kwon TG, Park HS, Wozney JM, Ryoo HM,. 2003. BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem Biophys Res Commun 309: 689-694.
22. Lee HL, Woo KM, Ryoo HM, Baek JH,. 2013a. Distal-less homeobox 5 inhibits adipogenic differentiation through the down-regulation of peroxisome proliferator-activated receptor gamma expression. J Cell Physiol 228: 87-98.
23. Luzi E, Marini F, Sala SC, Tognarini I, Galli G, Brandi ML,. 2008. 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 23: 287-295.
24. Merlo GR, Zerega B, Paleari L, Trombino S, Mantero S, Levi G,. 2000. Multiple functions of Dlx genes. Int J Dev Biol 44: 619-626.
25. 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,. 2008. MiR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 368: 267-272.
26. Nuttall ME, Gimble JM,. 2004. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol 4: 290-294.
27. Okamoto H, Matsumi Y, Hoshikawa Y, Takubo K, Ryoke K, Shiota G,. 2012. Involvement of microRNAs in regulation of osteoblastic differentiation in mouse induced pluripotent stem cells. PLoS ONE 7: e43800.
28. Panganiban G, Rubenstein JL,. 2002. Developmental functions of the Distal-less/Dlx homeobox genes. Development 129: 4371-4386.
29. Perera M, Merlo GR, Verardo S, Paleari L, Corte G, Levi G,. 2004. Defective neuronogenesis in the absence of Dlx5. Mol Cell Neurosci 25: 153-161.
30. Qadir AS, Woo KM, Ryoo HM, Baek JH,. 2013. Insulin suppresses distal-less homeobox 5 expression through the up-regulation of microRNA-124 in 3T3-L1 cells. Exp Cell Res 319: 2125-2134.
31. Qadir AS, Woo KM, Ryoo HM, Yi T, Song SU, Baek JH,. 2014. MiR-124 inhibits myogenic differentiation of mesenchymal stem cells via targeting Dlx5. J Cell Biochem 115: 1572-1581.
32. Ruan H, Hacohen N, Golub TR, Van Parijs L, Lodish HF,. 2002. Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory. Diabetes 51: 1319-1336.
33. Ryoo HM, Hoffmann HM, Beumer T, Frenkel B, Towler DA, Stein GS, Stein JL, van Wijnen AJ, Lian JB,. 1997. Stage-specific expression of Dlx-5 during osteoblast differentiation: involvement in regulation of osteocalcin gene expression. Mol Endocrinol 11: 1681-1694.
34. Ryoo HM, Lee MH, Kim YJ,. 2006. Critical molecular switches involved in BMP-2-induced osteogenic differentiation of mesenchymal cells. Gene 366: 51-57.
35. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S,. 2004. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364: 149-155.
36. Shea CM, Edgar CM, Einhorn TA, Gerstenfeld LC,. 2003. BMP treatment of C3H10T1/2 mesenchymal stem cells induces both chondrogenesis and osteogenesis. J Cell Biochem 90: 1112-1127.
37. Shirakabe K, Terasawa K, Miyama K, Shibuya H, Nishida E,. 2001. Regulation of the activity of the transcription factor Runx2 by two homeobox proteins, Msx2 and Dlx5. Genes Cells 6: 851-856.
38. Tokuzawa Y, Yagi K, Yamashita Y, Nakachi Y, Nikaido I, Bono H, Ninomiya Y, Kanesaki-Yatsuka Y, Akita M, Motegi H, Wakana S, Noda T, Sablitzky F, Arai S, Kurokawa R, Fukuda T, Katagiri T, Schonbach C, Suda T, Mizuno Y, Okazaki Y,. 2010. Id4, a new candidate gene for senile osteoporosis, acts as a molecular switch promoting osteoblast differentiation. PLoS Genet 6: e1001019.
39. Um S, Choi JR, Lee JH, Zhang Q, Seo B,. 2011. Effect of leptin on differentiation of human dental stem cells. Oral Dis 17: 662-669.