MiR-223 regulates adipogenic and osteogenic differentiation of mesenchymal stem cells through a C/EBPs/miR-223/FGFR2 regulatory feedback loop

Stem Cells

Volumn 33, Issue 5, 2015, Pages 1589-1600

  Guan, Xiaohui ^a   Gao, Yifei ^a   Zhou, Jie ^a   Wang, Jun ^a   Zheng, Fang ^b   Guo, Fei ^a   Chang, Ailing ^a   Li, Xiaoxia ^a   Wang, Baoli ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b TIANJIN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

Adipocyte; CCAAT enhancer binding protein; Fibroblast growth factor receptor 2; microRNA; Osteoblast

Indexed keywords

AP2 PROTEIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; COMPLEMENT FACTOR D; FIBROBLAST GROWTH FACTOR RECEPTOR 2; LUCIFERASE; MICRORNA 223; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; UNCLASSIFIED DRUG; CCAAT ENHANCER BINDING PROTEIN; MICRORNA; MIRN223 MICRORNA, MOUSE;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; BINDING SITE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; ENZYME REPRESSION; FEEDBACK SYSTEM; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GROWTH INHIBITION; LUCIFERASE ASSAY; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOBLAST; POINT MUTATION; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; TRANSCRIPTION INITIATION;

LENTIVIRUS;

ADIPOCYTES; ADIPOGENESIS; ANIMALS; BASE SEQUENCE; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; CELL PROLIFERATION; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; OSTEOGENESIS; PROMOTER REGIONS, GENETIC; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; TRANSCRIPTIONAL ACTIVATION;

EID: 84928568039     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1947     Document Type: Article

References (49)

1. Gimble JM, Zvonic S, Floyd ZE, et al. Playing with bone and fat. J Cell Biochem 2006; 98: 251-266.
2. Gelfand IM, Hub RS, Shore EM, et al. Progressive osseous heteroplasia-like heterotopic ossification in a male infant with pseudohypoparathyroidism type Ia: A case report. Bone 2007; 40: 1425-1428.
3. Kaplan FS, Shore EM,. Progressive osseous heteroplasia. J Bone Miner Res 2000; 15: 2084-2094.
4. Kajkenova O, Lecka-Czernik B, Gubrij I, et al. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res 1997; 12: 1772-1779.
5. Rosen ED, Hsu CH, Wang X, et al. C/EBPalpha induces adipogenesis through PPARgamma: A unified pathway. Genes Dev 2002; 16: 22-26.
6. Linhart HG, Ishimura-Oka K, DeMayo F, et al. C/EBPalpha is required for differentiation of white, but not brown, adipose tissue. Proc Natl Acad Sci USA 2001; 98: 12532-12537.
7. Saraf N, Sharma PK, Mondal SC, et al. Role of PPARg2 transcription factor in thiazolidinedione-induced insulin sensitization. J Pharm Pharmacol 2012; 64: 161-171.
8. Zanotti S, Stadmeyer L, Smerdel-Ramoya A, et al. Misexpression of CCAAT/enhancer binding protein beta causes osteopenia. J Endocrinol 2009; 201: 263-274.
9. Tanaka T, Yoshida N, Kishimoto T, et al. Defective adipocyte differentiation in mice lacking the C/EBPbeta and/or C/EBPdelta gene. EMBO J 1997; 16: 7432-7443.
10. Monroe DG, McGee-Lawrence ME, Oursler MJ, et al. Update on Wnt signaling in bone cell biology and bone disease. Gene 2012; 492: 1-18.
11. 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.
12. 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: 17-29.
13. Ryoo HM, Hoffmann HM, Beumer T, et al. Stage-specific expression of Dlx-5 during osteoblast differentiation: Involvement in regulation of osteocalcin gene expression. Mol Endocrinol 1997; 11: 1681-1694.
14. Bartel DP,. MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136: 215-233.
15. Chen Y, Siegel F, Kipschull S, et al. miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat Commun 2013; 4: 1769.
16. Lee EK, Lee MJ, Abdelmohsen K, et al. miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol 2011; 31: 626-638.
17. Qin L, Chen Y, Niu Y, et al. A deep investigation into the adipogenesis mechanism: Profile of microRNAs regulating adipogenesis by modulating the canonical Wnt/beta-catenin signaling pathway. BMC Genom 2010; 11: 320.
18. Hu R, Liu W, Li H, et al. A Runx2/miR-3960/miR-2861 regulatory feedback loop during mouse osteoblast differentiation. J Biol Chem 2011; 286: 12328-12339.
19. Li H, Xie H, Liu W, et al. A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest 2009; 119: 3666-3677.
20. Jia J, Tian Q, Ling S, et al. miR-145 suppresses osteogenic differentiation by targeting Sp7. FEBS Lett 2013; 587: 3027-3031.
21. Shi K, Lu J, Zhao Y, et al. MicroRNA-214 suppresses osteogenic differentiation of C2C12 myoblast cells by targeting Osterix. Bone 2013; 55: 487-494.
22. Wang X, Guo B, Li Q, et al. miR-214 targets ATF4 to inhibit bone formation. Nat Med 2013; 19: 93-100.
23. Wang J, Guan X, Guo F, et al. miR-30e reciprocally regulates the differentiation of adipocytes and osteoblasts by directly targeting low-density lipoprotein receptor-related protein 6. Cell Death Dis 2013; 4: e845.
24. Vian L, Di Carlo M, Pelosi E, et al. Transcriptional fine-tuning of microRNA-223 levels directs lineage choice of human hematopoietic progenitors. Cell Death Differ 2014; 21: 290-301.
25. Johnnidis JB, Harris MH, Wheeler RT, et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451: 1125-1129.
26. Dong YW, Wang R, Cai QQ, et al. Sulfatide epigenetically regulates miR-223 and promotes the migration of human hepatocellular carcinoma cells. J Hepatol 2014; 60: 792-801.
27. Agatheeswaran S, Singh S, Biswas S, et al. BCR-ABL mediated repression of miR-223 results in the activation of MEF2C and PTBP2 in chronic myeloid leukemia. Leukemia 2013; 27: 1578-1580.
28. Stamatopoulos B, Meuleman N, Haibe-Kains B, et al. microRNA-29c and microRNA-223 down-regulation has in vivo significance in chronic lymphocytic leukemia and improves disease risk stratification. Blood 2009; 113: 5237-5245.
29. Liu TY, Chen SU, Kuo SH, et al. E2A-positive gastric MALT lymphoma has weaker plasmacytoid infiltrates and stronger expression of the memory B-cell-associated miR-223: Possible correlation with stage and treatment response. Mod Pathol 2010; 23: 1507-1517.
30. Laios A, O'Toole S, Flavin R, et al. Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol Cancer 2008; 7: 35.
31. Anjos-Afonso F, Bonnet D,. Isolation, culture, and differentiation potential of mouse marrow stromal cells. Curr Protoc Stem Cell Biol 2008;Chapter 2:Unit 2B 3.
32. Tsang WP, Kwok TT,. The miR-18a∗ microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 2009; 30: 953-959.
33. Fukao T, Fukuda Y, Kiga K, et al. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 2007; 129: 617-631.
34. Zhao M, Qiao M, Harris SE, et al. Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 2004; 279: 12854-12859.
35. Wang B, Jin H, Zhu M, et al. Chondrocyte beta-catenin signaling regulates postnatal bone remodeling through modulation of osteoclast formation in a murine model. Arthritis Rheumatol 2014; 66: 107-120.
36. Miraoui H, Oudina K, Petite H, et al. Fibroblast growth factor receptor 2 promotes osteogenic differentiation in mesenchymal cells via ERK1/2 and protein kinase C signaling. J Biol Chem 2009; 284: 4897-4904.
37. Sun G, Li H, Rossi JJ,. Sequence context outside the target region influences the effectiveness of miR-223 target sites in the RhoB 3'UTR. Nucleic Acids Res 2010; 38: 239-252.
38. Hong JH, Hwang ES, McManus MT, et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005; 309: 1074-1078.
39. Kanai F, Marignani PA, Sarbassova D, et al. TAZ: A novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J 2000; 19: 6778-6791.
40. Byun MR, Jeong H, Bae SJ, et al. TAZ is required for the osteogenic and anti-adipogenic activities of kaempferol. Bone 2012; 50: 364-372.
41. Cui CB, Cooper LF, Yang X, et al. Transcriptional coactivation of bone-specific transcription factor Cbfa1 by TAZ. Mol Cell Biol 2003; 23: 1004-1013.
42. Jung H, Lee MS, Jang EJ, et al. Augmentation of PPARgamma-TAZ interaction contributes to the anti-adipogenic activity of KR62980. Biochem Pharmacol 2009; 78: 1323-1329.
43. Kelleher FC, O'Sullivan H, Smyth E, et al. Fibroblast growth factor receptors, developmental corruption and malignant disease. Carcinogenesis 2013; 34: 2198-2205.
44. Eswarakumar VP, Monsonego-Ornan E, Pines M, et al. The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 2002; 129: 3783-3793.
45. Yu K, Xu J, Liu Z, et al. Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 2003; 130: 3063-3074.
46. Prendergast GC,. Actin' up: RhoB in cancer and apoptosis. Nat Rev Cancer 2001; 1: 162-168.
47. Fazi F, Rosa A, Fatica A, et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005; 123: 819-831.
48. Pulikkan JA, Dengler V, Peramangalam PS, et al. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood 2010; 115: 1768-1778.
49. Shi L, Fisslthaler B, Zippel N, et al. MicroRNA-223 antagonizes angiogenesis by targeting beta1 integrin and preventing growth factor signaling in endothelial cells. Circ Res 2013; 113: 1320-1330.