MiR-497∼195 cluster micrornas regulate osteoblast differentiation by targeting BMP signaling

Journal of Bone and Mineral Research

Volumn 30, Issue 5, 2015, Pages 796-808

  Grünhagen, Johannes ^a,b   Bhushan, Raghu ^a,c   Degenkolbe, Elisa ^a   Jäger, Marten ^a   Knaus, Petra ^a,c   Mundlos, Stefan ^a,b   Robinson, Peter N ^a,b   Ott, Claus Eric ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

BMP signaling; miR 15 family; MiR 195; MiR 497; Osteoblast differentiation

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN; COLLAGENASE 3; CONNECTIVE TISSUE GROWTH FACTOR; FURIN; MICRORNA; MICRORNA 15A; MICRORNA 16; MICRORNA 195 5P; MICRORNA 497; SMAD5 PROTEIN; SMURF1 PROTEIN; TRANSCRIPTION FACTOR RUNX2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN 2; RECOMBINANT HUMAN BONE MORPHOGENETIC PROTEIN-2; RECOMBINANT PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BONE DEVELOPMENT; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; MOUSE; NONHUMAN; OSTEOBLAST; PROTEIN TARGETING; REPORTER GENE; SIGNAL TRANSDUCTION; UPREGULATION; 3T3 CELL LINE; AGING; ANIMAL; BIOLOGY; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DNA MICROARRAY; DRUG EFFECTS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEWBORN; REPRODUCIBILITY;

AGING; ANIMALS; ANIMALS, NEWBORN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPUTATIONAL BIOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICRORNAS; NIH 3T3 CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOBLASTS; RECOMBINANT PROTEINS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84927724919     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2412     Document Type: Article

References (59)

1. Komori T,. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem. 2006; 99 (5): 1233-1239.
2. Long F,. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol. 2012; 13 (1): 27-38.
3. Zheng MH, Wood DJ, Papadimitriou JM,. What's new in the role of cytokines on osteoblast proliferation and differentiation. Pathol Res Pract. 1992; 188 (8): 1104-1121.
4. Kopf J, Paarmann P, Hiepen C, Horbelt D, Knaus P,. BMP growth factor signaling in a biomechanical context. Biofactors. 2014; 40 (2): 171-187.
5. Vivekanand P, Rebay I,. Intersection of signal transduction pathways and development. Ann Rev Genet. 2006; 40: 139-157.
6. Inui M, Martello G, Piccolo S,. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol. 2010; 11 (4): 252-263.
7. Yekta S, Shih IH, Bartel DP,. MicroRNA-directed cleavage of HOXB8 mRNA. Science. 2004; 304 (5670): 594-596.
8. Chu CY, Rana TM,. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 2006; 4 (7): e210.
9. Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R,. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol. 2005; 7 (7): 719-723.
10. Ketting RF,. Semiconserved regulation of mesendoderm differentiation by microRNAs. Dev Cell. 2009; 16 (4): 487-488.
11. Hata A, Davis BN,. Regulation of pri-miRNA processing through Smads. Adv Exp Med Biol. 2010; 700: 15-27.
12. Bae Y, Yang T, Zeng HC, et al. MiRNA-34c regulates Notch signaling during bone development. Hum Mol Genet. 2012; 21 (13): 2991-3000.
13. Bhushan R, Grunhagen J, Becker J, Robinson PN, Ott CE, Knaus P,. MiR-181a promotes osteoblastic differentiation through repression of TGF-beta signaling molecules. Int J Biochem Cell Biol. 2013; 45 (3): 696-705.
14. Li Z, Hassan MQ, Volinia S, et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA. 2008; 105 (37): 13906-13911.
15. Lin EA, Kong L, Bai XH, Luan Y, Liu CJ,. MiR-199a, a bone morphogenic protein 2-responsive MicroRNA, regulates chondrogenesis via direct targeting to Smad1. J Biol Chem. 2009; 284 (17): 11326-11335.
16. Ott CE, Bauer S, Manke T, et al. Promiscuous and depolarization-induced immediate-early response genes are induced by mechanical strain of osteoblasts. J Bone Miner Res. 2009; 24 (7): 1247-1262.
17. Ott CE, Grunhagen J, Jager M, et al. MicroRNAs differentially expressed in postnatal aortic development downregulate elastin via 3' UTR and coding-sequence binding sites. PloS One. 2011; 6 (1): e16250.
18. Bauer S, Grossmann S, Vingron M, Robinson PN,. Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics. 2008; 24 (14): 1650-1651.
19. Diez-Roux G, Banfi S, Sultan M, et al. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol. 2011; 9 (1): e1000582.
20. Hwang HW, Wentzel EA, Mendell JT,. Cell-cell contact globally activates microRNA biogenesis. Proc Natl Acad Sci. 2009; 106 (17): 7016-7021.
21. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM,. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBOJ. 1998; 17 (11): 3091-3100.
22. Jonk LJ, Itoh S, Heldin CH, ten Dijke P, Kruijer P,. Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J Biol Chem. 1998; 273 (33): 21145-21152.
23. Korchynskyi O, ten Dijke P,. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem. 2002; 277 (7): 4883-4891.
24. Akiyama H, Kim JE, Nakashima K, et al. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA. 2005; 102 (41): 14665-14670.
25. Nakashima K, Zhou X, Kunkel G, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002; 108 (1): 17-29.
26. Rosa A, Ballarino M, Sorrentino A, et al. The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci USA. 2007; 104 (50): 19849-19854.
27. Sarkar S, Dey BK, Dutta A,. MiR-322/424 and -503 are induced during muscle differentiation and promote cell cycle quiescence and differentiation by down-regulation of Cdc25A. Mol Biol Cell. 2010; 21 (13): 2138-2149.
28. Kim J, Kang Y, Kojima Y, et al. An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat Med. 2013; 19 (1): 74-82.
29. Gamez B, Rodriguez-Carballo E, Ventura F,. MicroRNAs and post-transcriptional regulation of skeletal development. J Mol Endocrinol. 2014; 52 (3): R179-R197.
30. Katagiri T, Yamaguchi A, Ikeda T, et al. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commun. 1990; 172 (1): 295-299.
31. Katagiri T, Yamaguchi A, Komaki M, et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol. 1994; 127(6 Pt 1) 1755-1766.
32. 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.
33. 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 (2): 267-272.
34. Wu T, Zhou H, Hong Y, Li J, Jiang X, Huang H,. MiR-30 family members negatively regulate osteoblast differentiation. J Biol Chem. 2012; 287 (10): 7503-7511.
35. Yang L, Cheng P, Chen C, et al. MiR-93/Sp7 function loop mediates osteoblast mineralization. J Bone Miner Res. 2012; 27 (7): 1598-1606.
36. Li Z, Hassan MQ, Jafferji M, et al. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem. 2009; 284 (23): 15676-15684.
37. Wang T,. Xu Z. miR-27 promotes osteoblast differentiation by modulating Wnt signaling. Biochem Biophys Res Commun. 2010; 402 (2): 186-189.
38. Finnerty JR, Wang WX, Hebert SS, Wilfred BR, Mao G, Nelson PT,. The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J Mol Biol. 2010; 402 (3): 491-509.
39. Martello G, Zacchigna L, Inui M, et al. MicroRNA control of Nodal signalling. Nature. 2007; 449 (7159): 183-188.
40. Chamorro-Jorganes A, Araldi E, Penalva LO, Sandhu D, Fernandez-Hernando C, Suarez Y,. MicroRNA-16 and microRNA-424 regulate cell-autonomous angiogenic functions in endothelial cells via targeting vascular endothelial growth factor receptor-2 and fibroblast growth factor receptor-1. Arterioscler Thromb Vasc Biol. 2011; 31 (11): 2595-2606.
41. Chen L, Wang Q, Wang GD, et al. MiR-16 inhibits cell proliferation by targeting IGF1R and the Raf1-MEK1/2-ERK1/2 pathway in osteosarcoma. FEBS Lett. 2013; 587 (9): 1366-1372.
42. Ding J, Huang S, Wang Y, et al. Genome-wide screening reveals that miR-195 targets the TNF-alpha/NF-kappaB pathway by down-regulating IkappaB kinase alpha and TAB3 in hepatocellular carcinoma. Hepatology. 2013; 58 (2): 654-666.
43. Yang TQ, Lu XJ, Wu TF, et al. MicroRNA-16 inhibits glioma cell growth and invasion through suppression of BCL2 and the nuclear factor-kappaB1/MMP9 signaling pathway Cancer Sci. 105 3 2014; 265-271
44. Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM,. MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology. 2009; 50 (1): 113-121.
45. Ma Q, Wang X, Li Z, et al. MicroRNA-16 represses colorectal cancer cell growth in vitro by regulating the p53/survivin signaling pathway Oncol Rep. 29 4 2013; 1652-1658
46. Cao S, Xiao L, Rao JN, et al. Inhibition of Smurf2 translation by miR-322/503 modulates TGF-beta/Smad2 signaling and intestinal epithelial homeostasis. Mol Biol Cell. 2014; 25 (8): 1234-1243.
47. Parisi S, Battista M, Musto A, Navarra A, Tarantino C, Russo T,. A regulatory loop involving Dies1 and miR-125a controls BMP4 signaling in mouse embryonic stem cells FASEB J. 26 10 2012; 3957-3968
48. Ren G, Beech C, Smas CM,. The immunoglobulin superfamily protein differentiation of embryonic stem cells 1 (dies1) has a regulatory role in preadipocyte to adipocyte conversion. PloS One. 2013; 8 (6): e65531.
49. Aloia L, Parisi S, Fusco L, Pastore L, Russo T,. Differentiation of embryonic stem cells 1 (Dies1) is a component of bone morphogenetic protein 4 (BMP4) signaling pathway required for proper differentiation of mouse embryonic stem cells. J Biol Chem. 2010; 285 (10): 7776-7783.
50. Gupta RK, Arany Z, Seale P, et al. Transcriptional control of preadipocyte determination by Zfp423. Nature. 2010; 464 (7288): 619-623.
51. Masserdotti G, Badaloni A, Green YS, et al. ZFP423 coordinates Notch and bone morphogenetic protein signaling, selectively up-regulating Hes5 gene expression. J Biol Chem. 2010; 285 (40): 30814-30824.
52. Huang S, Laoukili J, Epping MT, et al. ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome. Cancer Cell. 2009; 15 (4): 328-340.
53. Melling MA, Friendship CR, Shepherd TG, Drysdale TA,. Expression of Ski can act as a negative feedback mechanism on retinoic acid signaling. Dev Dyn. 2013; 242 (6): 604-613.
54. Suzuki H, Yagi K, Kondo M, Kato M, Miyazono K, Miyazawa K,. C-Ski inhibits the TGF-beta signaling pathway through stabilization of inactive Smad complexes on Smad-binding elements. Oncogene. 2004; 23 (29): 5068-5076.
55. Luo K,. Negative regulation of BMP signaling by the ski oncoprotein. J Bone Joint Surg Am. 2003; 85-A(Suppl 3) 39-43.
56. Yamashita M, Ying SX, Zhang GM, et al. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell. 2005; 121 (1): 101-113.
57. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH,. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature. 1999; 400 (6745): 687-693.
58. Seemann P, Mundlos S, Lehmann K,. Alterations of BMP signaling pathway(s) in skeletal diseases. In Bone morphogenetic proteins: from local to systemic therapeutics. Basel, Switzerland: Birkhauser Verlag 2008; pp p. 141-p. 159.
59. Wagner DO, Sieber C, Bhushan R, Borgermann JH, Graf D, Knaus P,. From bone to body morphogenetic proteins. Sci Signal. 2010; 3 (107): mr1.