TCF3, a novel positive regulator of osteogenesis, plays a crucial role in miR-17 modulating the diverse effect of canonical Wnt signaling in different microenvironments

Cell Death and Disease

Volumn 4, Issue 3, 2013, Pages

  Liu, W ^a   Liu, Y ^a   Guo, T ^a   Hu, C ^a   Luo, H ^a   Zhang, L ^a   Shi, S ^b   Cai, T ^c   Ding, Y ^a   Jin, Y ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Canonical Wnt signaling; Microenvironment; MiR 17; Osteogenesis; Transcription factor 3

Indexed keywords

MESSENGER RNA; MICRORNA 17; TRANSCRIPTION FACTOR 7 LIKE 1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MICRORNA; MIRN17 MICRORNA, HUMAN; TCF3 PROTEIN, HUMAN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; GENE CONTROL; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MICROENVIRONMENT; NONHUMAN; OSSIFICATION; PERIODONTAL LIGAMENT; PRIORITY JOURNAL; PROTEIN INTERACTION; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; MOUSE; MOUSE MUTANT; OSTEOBLAST; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; MICE, SCID; MICRORNAS; OSTEOBLASTS; OSTEOGENESIS; PERIODONTAL LIGAMENT; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84875879658     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.65     Document Type: Article

References (47)

1. Jensen ED, Gopalakrishnan R, Westendorf JJ. Regulation of gene expression in osteoblasts. Biofactors 2010; 36: 25-32.
2. Soltanoff CS, Yang S, Chen W, Li YP. Signaling networks that control the lineage commitment and differentiation of bone cells. Crit Rev Eukaryot Gene Expr 2009; 19: 1-46.
3. Krishnan V, Bryant HU, Macdougald OA. Regulation of bone mass by Wnt signaling. J Clin Invest 2006; 116: 1202-1209.
4. Yang F, Yang D, Tu J, Zheng Q, Cai L, Wang L. Strontium enhances osteogenic differentiation of mesenchymal stem cells and in vivo bone formation by activating Wnt/catenin signaling. Stem Cells 2011; 29: 981-991.
5. Bennett CN, Ouyang H, Ma YL, Zeng Q, Gerin I, Sousa KM et al. Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res 2007; 22: 1924-1932.
6. Guo AJ, Choi RC, Cheung AW, Chen VP, Xu SL, Dong TT et al. Baicalin, a flavone, induces the differentiation of cultured osteoblasts: An action via the Wnt/beta-catenin signaling pathway. J Biol Chem 2011; 286: 27882-27893.
7. de Boer J, Siddappa R, Gaspar C, van Apeldoorn A, Fodde R, van Blitterswijk C. Wnt signaling inhibits osteogenic differentiation of human mesenchymal stem cells. Bone 2004; 34: 818-826.
8. Liu G, Vijayakumar S, Grumolato L, Arroyave R, Qiao H, Akiri G et al. Canonical Wnts function as potent regulators of osteogenesis by human mesenchymal stem cells. J Cell Biol 2009; 185: 67-75.
9. Liu N, Shi S, Deng M, Tang L, Zhang G, Liu N et al. High levels of b-catenin signaling suppress osteogenic differentiation of periodontal ligament stem cells in inflammatory microenvironments through inhibition of the noncanonical Wnt pathway. J Bone Miner Res 2011; 26: 2082-2095.
10. Ling L, Nurcombe V, Cool SM. Wnt signaling controls the fate of mesenchymal stem cells. Gene 2009; 433: 1-7.
11. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 2004; 5: 691-701.
12. Jacques BE, Puligilla C, Weichert RM, Ferrer-Vaquer A, Hadjantonakis AK, Kelley MW et al. A dual function for canonical Wnt/b-catenin signaling in the developing mammalian cochlea. Development 2012; 139: 4395-4404.
13. Gaur T, Lengner CJ, Hovhannisyan H, Bhat RA, Bodine PV, Komm BS et al. Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J Biol Chem 2005; 280: 33132-33140.
14. McCarthy TL, Centrella M. Novel links among Wnt and TGF-beta signaling and Runx2. Mol Endocrinol 2010; 24: 587-597.
15. Kahler RA, Westendorf JJ. Lymphoid enhancer factor-1 and beta-catenin inhibit Runx2- dependent transcriptional activation of the osteocalcin promoter. J Biol Chem 2003; 278: 11937-11944.
16. Li Z, Hassan MQ, Volinia S, van Wijnen AJ, Stein JL, Croce CM et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 2008; 105: 13906-13911.
17. Du T, Zamore PD. Beginning to understand microRNA function. Cell Res 2007; 17: 661-663.
18. Neilson JR, Sharp PA. Small RNA regulators of gene expression. Cell 2008; 134: 899-902.
19. 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.
20. Tomé M, López-Romero P, Albo C, Sepúlveda JC, Fernández-Gutié rrez B, Dopazo A et al. miR-335 orchestrates cell proliferation, migration and differentiation in human mesenchymal stem cells. Cell Death Differ 2011; 18: 985-995.
21. Zhang JF, Fu WM, He ML, Xie WD, Lv Q, Wan G et al. MiRNA-20a promotes osteogenic di!erentiation of human mesenchymal stem cells by co-regulating BMP signalling. RNA Biol 2011; 8: 829-838.
22. Liu Y, Liu W, Hu C, Xue Z, Wang G, Ding B et al. MiR-17 modulates osteogenic differentiation through a coherent feed-forward loop in mesenchymal stem cells isolated from periodontal ligaments of patients with periodontitis. Stem Cells 2011; 29: 1804-1816.
23. Gregory CA, Gunn WG, Reyes E, Smolarz AJ, Munoz J, Spees JL et al. How Wnt signaling affects bone repair by mesenchymal stem cells from the bone marrow. Ann NY Acad Sci 2005; 1049: 97-106.
24. Boland GM, Perkins G, Hall DJ, Tuan RS. Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells. J Cell Biochem 2004; 93: 1210-1230.
25. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364: 149-155.
26. Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: Their biology and role in regenerative medicine. J Dent Res 2009; 88: 792-806.
27. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219: 667-676.
28. Liu Y, Wang L, Kikuiri T, Akiyama K, Chen C, Xu X et al. Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-g and TNF-a. Nat Med 2011; 17: 1594-1601.
29. Burdick JA, Vunjak-Novakovic G. Engineered microenvironments for controlled stem cell differentiation. Tissue Eng Part A 2009; 15: 205-219.
30. Yamashita A, Nishikawa S, Rancourt DE. Microenvironment modulates osteogenic cell lineage commitment in differentiated embryonic stem cells. PLoS One 2010; 5: E9663.
31. Hu Y, Cai K, Luo Z, Zhang Y, Li L, Lai M et al. Regulation of the differentiation of mesenchymal stem cells in vitro and osteogenesis in vivo by microenvironmental modification of titanium alloy surfaces. Biomaterials 2012; 33: 3515-3528.
32. Nemeth MJ, Mak KK, Yang Y, Bodine DM. Beta-catenin expression in the bone marrow microenvironment is required for long-term maintenance of primitive hematopoietic cells. Stem Cells 2009; 27: 1109-1119.
33. Edwards CM, Edwards JR, Lwin ST, Esparza J, Oyajobi BO, McCluskey B et al. Increasing Wnt signaling in the bone marrow microenvironment inhibits the development of myeloma bone disease and reduces tumor burden in bone in vivo. Blood 2008; 111: 2833-2842.
34. Cui Q, Yu Z, Purisima EO, Wang E. Principles of microRNA regulation of a human cellular signaling network. Mol Syst Biol 2006; 2: 46.
35. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell 2012; 148: 1172-1187.
36. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol 2010; 11: 252-263.
37. Liu L, Wang Y, Fan H, Zhao X, Liu D, Hu Y et al. MicroRNA-181a regulates local immune balance by inhibiting proliferation and immunosuppressive properties of mesenchymal stem cells. Stem Cells 2012; 30: 1756-1770.
38. Li Y, Vecchiarelli-Federico LM, Li YJ, Egan SE, Spaner D, Hough MR et al. The miR-17-92 cluster expands multipotent hematopoietic progenitors whereas imbalanced expression of its individual oncogenic miRNAs promotes leukemia in mice. Blood 2012; 119: 4486-4498.
39. Solberg N, Machon O, Machonova O, Krauss S. Mouse Tcf3 represses canonical Wnt signaling by either competing for b-catenin binding or through occupation of DNA-binding sites. Mol Cell Biochem 2012; 365: 53-63.
40. Andoniadou CL, Signore M, Young RM, Gaston-Massuet C, Wilson SW, Fuchs E et al. HESX1- and TCF3-mediated repression of Wnt/b-catenin targets is required for normal development of the anterior forebrain. Development 2011; 138: 4931-4942.
41. Yi F, Pereira L, Merrill BJ. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 2008; 26: 1951-1960.
42. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH et al. T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 2008; 26: 2019-2031.
43. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507.
44. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR et al. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 2011; 13: 762-770.
45. Lee E, Salic A, Kirschner MW. Physiological regulation of b-catenin stability by Tcf3 and CK1epsilon. J Cell Biol 2001; 154: 983-993.
46. Reinhold Mi, Naski MC. Direct interactions of Runx2 and canonical Wnt signaling induce FGF18. J Biol Chem 2007; 282: 3653-3663.
47. Yang ZH, Jin F, Zhang XJ, Ma DD, Han C, Huo N et al. Tissue engineering of cementum/ periodontal-ligament complex using a novel three-dimensional pellet cultivation system for human periodontal ligament stem cells. Tissue Engineering Part C 2009; 15: 571-581.